Predictive Role of Posterior Communicating Artery Spasm on Axonal Degeneration in Oculomotor Nerve Root Following Subarachnoid Hemorrhage: Experimental Study

Year 2023, , 73 - 82, 26.05.2023

Mete Zeynal , Mehmet Hakan Şahin

https://doi.org/10.56766/ntms.1277530

Abstract

Background: The oculomotor nerve root's medial aspect in the cisternal space is closely associated with the posterior communicating artery and receives blood supply from it. This study investigates whether ischemic damage to oculomotor nerve roots results from posterior communicating artery spasm in subarachnoid hemorrhages.
Methods: A total of 18 rabbits participated in this study. Baseline pupil diameters were measured using sunlight and ocular tomography. Rabbits were divided into control (GI, n=5), SHAM (GII, n=5; 0.75 cc serum physiologic injection), and subarachnoid hemorrhage-induced groups (GIII, n=8; 0.75 cc autolog blood injection). Pupil diameters were re-measured after the experiment and daily for three weeks. The animals were observed for one week before euthanasia. The posterior communicating artery vasospasm index (VSI) was determined using the wall surface/lumen surface ratio. Stereological methods were employed to examine the normal and degenerated axon densities of the oculomotor nerves. The Kruskal-Wallis and Mann-Whitney U tests were used to evaluate degenerated axon density (n/mm2) and VSI values. A p-value of less than 0.005 was considered significant.
Results: Degenerated axon numbers (n/mm2) and VSI values of the posterior communicating artery were as follows: 3±1/0.936±0.212 in GI; 18±4/1.578±0.235 in GII; and 212±34/2.515±0.347 in GIII. The p-values were p<0.005 for GI/GII, p<0.0005 for GII/GIII, and p<0.00001 for GI/GIII.
Conclusion: The posterior communicating artery vasospasm plays a significant role in oculomotor nerve root injury.

Keywords

Subarachnoid hemorrhage, oculomotor nerve, vasospasm, ischemic demage

References

• 1. Zhang WG, Zhang SX, Wu BH. A study on the sectional anatomy of the oculomotor nerve and its related blood vessels with plastination and MRI. Surg Radiol Anat. 2002; 24(5):277-84.
• 2. Marinković S, Gibo H. The neurovascular relationships and the blood supply of the oculomotor nerve: the microsurgical anatomy of its cisternal segment. Surg Neurol Dec. 1994; 42(6):505-16.
• 3. Wong GK, Ng SC, Tsang PK, Poon WS. Clipping vs coiling of posterior communicating artery aneurysms with third nerve palsy. Neurology. 2006; 66(12):1959-60.
• 4. Renowden SA, Harris KM, Hourihan MD. Isolated atraumatic third nerve palsy: clinical features and imaging techniques. Br J Radiol. 1993; 66(792):1111-17.
• 5. Yamada S, Mizutani T, Nagura H, Yamanouchi H, Matsuo Y. A case of closed head injury with diffuse axonal injury, and oculomotor nerve avulsion and midbrain infarction. Rinsho Shinkeigaku. 1995;35(3):267-71.
• 6. Shih TY. Delayed oculomotor palsy from focal subarachnoid hematoma. J Clin Neuroophthalmol. 1993; 13(3):218-19.
• 7. Tanriverdi O, Aydin MD, Onen MR, et al. Understanding of Dry Eye in Subarachnoid Hemorrhage: An Experimental Study on the Role of Facial Nerve Ischemia. Turk Neurosurg. 2019; 29(3):362-68.
• 8. Onen MR, Yilmaz I, Ramazanoglu L, et al. Uncovering the Forgotten Effect of Superior Cervical Ganglia on Pupil Diameter in Subarachnoid Hemorrhage: An Experimental Study. Turk Neurosurg. 2018; 28(1):48-55.
• 9. Aydin MD, Onder S, Ulvi H, Onder A, Baykal O. Histopathological alterations in ciliary ganglions in meningitis: an experimental study. Minim Invasive Neurosurg. 2005; 48(5):297-301.
• 10. Aydin MD, Akyol-Salman I, Sahin O. Histopathological changes in ciliary ganglion of rabbits with subarachnoid hemorrhage. Int J Neurosci. 2005; 115(11):1595-602.
• 11. Ozkan U, Aydin MD, Gündoğdu C, Onder A. Histopathologic changes in oculomotor nerve and ciliary ganglion in aneurysmatic compression injuries of oculomotor nerve. Minim Invasive Neurosurg. 2004; 47(2):107-10.
• 12. Cruz-Orive LM, Weibel ER. Recent stereological methods for cell biology: a brief survey. Am J Physiol. 1990; 258(4 Pt 1):L148-56.
• 13. Lanzino G, Andreoli A, Limoni P, Tognetti F, Testa C. Vertebro-basilar aneurysms: does delayed surgery represent the best surgical strategy? Acta Neurochir (Wien). 1993; 125(1-4):5-8.
• 14. Bogousslavsky J, Regli F. Intra-axial involvement of the common oculomotor nerve in mesencephalic infarctions. Rev Neurol (Paris). 1984; 140(4):263-70.
• 15. Mehta S, Bathini A, Dubey A, et al. Isolated oculomotor nerve palsy secondary to non-aneurysmal subarachnoid hemorrhage. J Cerebrovasc Endovasc Neurosurg. 2022; 24(3):267-75.
• 16. Reynolds MR, Vega RA, Murphy RK, Miller-Thomas MM, Zipfel GJ. Perimesencephalic subarachnoid hemorrhage associated with a painless, pupillary-involving third cranial nerve palsy: case report and literature review. Clin Neurol Neurosurg. 2012; 114(8):1168-71.
• 17. Meyer YJ, Paine JT, Batjer HH. Focal subarachnoid hematoma: an unusual cause of delayed third cranial nerve paralysis. Surg Neurol. 1990; 34(3):169-72.
• 18. Aydin N, Kotan D, Keles S, et al. An experimental study of the neurophysical mechanisms of photophobia induced by subarachnoid hemorrhage. Neurosci Lett. 2016; 630:93-100.
• 19. Westheimer G, Blair SM. The parasympathetic pathways to internal eye muscles. Invest Ophthalmol. 1973; 12(3):193-97.
• 20. Heermann S. Neuroanatomy of the Oculomotor System. Klin Monbl Augenheilkd. 2017; 234(11):1334-43.
• 21. Levy NS, Kramer SG, de Barros T. Pupillary and accommodative abnormalities in the Vogt-Koyanagi-Harada syndrome. Am J Ophthalmol. 1970; 69(4):582-88.