How Reliable Is Pupillary Evaluation Following Subarachnoid Hemorrhage? Effect of Oculomotor Nerve Degeneration Secondary to Posterior Communicating Artery Vasospasm: First Experimental Study

Cengiz Ozturk; Nuriye Guzin Ozdemir; Ayhan Kanat; Mehmet Dumlu Aydin; Huseyin Findik; Nazan Aydin; Mehmet Esref Kabalar; Hizir Kazdal; Coskun Yolas; Orhan Baykal; Muhammet Calik

doi:10.1055/s-0037-1608841

Journal of Neurological Surgery Part A: Central European Neurosurgery, Inhaltsverzeichnis

J Neurol Surg A Cent Eur Neurosurg 2018; 79(04): 302-308
DOI: 10.1055/s-0037-1608841

Original Article

Georg Thieme Verlag KG Stuttgart · New York

How Reliable Is Pupillary Evaluation Following Subarachnoid Hemorrhage? Effect of Oculomotor Nerve Degeneration Secondary to Posterior Communicating Artery Vasospasm: First Experimental Study

Cengiz Ozturk

¹Family Medicine, Osmangazi Health Center, Erzurum, Turkey

,

Nuriye Guzin Ozdemir

²Department of Neurosurgery, Istanbul Training and Research Hospital, Istanbul, Turkey

,

Ayhan Kanat

³Department of Neurosurgery, Medical Faculty, Recep Tayyip Erdogan University, Rize, Turkey

,

Mehmet Dumlu Aydin

⁴Department of Neurosurgery Medical Faculty, Ataturk University, Erzurum, Turkey

,

Huseyin Findik

⁵Department of Ophthalmology, Recep Tayyip Erdogan University, Rize, Turkey

,

Nazan Aydin

⁶Psychiatry Clinic, Bakirkoy Training and Research Hospital for Psychiatry, Neurology and Neurosurgery, Istanbul, Turkey

,

Mehmet Esref Kabalar

⁷Department of Pathology Clinic, Regional Training and Research Hospital, Erzurum, Turkey

,

Hizir Kazdal

⁸Department of Anesthesiology and Reanimation, Recep Tayyip Erdogan University, Rize, Turkey

,

Coskun Yolas

⁹Department of Neurosurgery, Regional Training and Research Hospital, Erzurum, Turkey

,

Orhan Baykal

¹⁰Department of Ophthalmology, Medical Faculty, Ataturk University, Erzurum, Turkey

,

Muhammet Calik

¹¹Department of Pathology, Medical Faculty, Ataturk University, Erzurum, Turkey

› Institutsangaben

Abstract

Background and Study Aim Basic neurophysiologic principles of the light reflex are well known. However, the effects of degenerated axon densities of oculomotor nerves (OMNs) secondary to posterior communicating artery (PComA) vasospasm following subarachnoid hemorrhage (SAH) have not been investigated. Our aim was to study this subject.

Methods This study was conducted on 19 rabbits. There was a control group of five animals, a sham group of five animals in which saline was injected into the cisterna magna and a study group of nine animals in which homologous blood was injected into the cisterna magna. Pupillary diameters were measured for 1 week, then the animals were decapitated. The normal and degenerated axon densities of the OMNs were examined by stereological methods. Vasospasm indexes (VSIs) of posterior communicating arteries (PComAs) supplying OMNs were estimated and analyzed statistically.

Results The pupillary diameter was 5.439 ± 368 µm, and the mean axon density of the OMNs was 0.924 ± 324/mm³ in the control group. The pupillary diameter and degenerated axon density of the OMNs in animals of the sham group were 6.980 ± 0.370 µm and 36 ± 8/mm³, respectively. The pupillary diameter was 9.942 ± 653 µm, and degenerated axon density of the OMNs was 265 ± 57/mm³ in animals with SAH. The mean VSI values of PComAs were 0.927 ± 0.224 in the control group, 1.542 ± 0.257 in the sham group, and 2.321 ± 0.324 in the SAH group.

Conclusion We found a linear relationship between the axon density of the OMNs and pupillary diameters. High degenerated neuron density in the OMNs may be responsible for an unresponsive pupillary that has not been mentioned in the literature.

Keywords

oculomotor nerve - pupillary diameter - subarachnoid hemorrhage

Volltext

Referenzen

References
1 Akca N, Ozdemir B, Kanat A, Batcik OE, Yazar U, Zorba OU. Describing a new syndrome in L5-S1 disc herniation: sexual and sphincter dysfunction without pain and muscle weakness. J Craniovertebr Junction Spine 2014; 5 (04) 146-150
2 Kanat A, Yazar U, Ozdemir B, Coskun ZO, Erdivanli O. Frontal sinus asymmetry: is it an effect of cranial asymmetry? X-ray analysis of 469 normal adult human frontal sinus. J Neurosci Rural Pract 2015; 6 (04) 511-514
3 Balik MS, Kanat A, Erkut A, Ozdemir B, Batcik OE. Inequality in leg length is important for the understanding of the pathophysiology of lumbar disc herniation. J Craniovertebr Junction Spine 2016; 7 (02) 87-90
4 Ozdemir B, Kanat A, Batcik OE, Gucer H, Yolas C. Ligamentum flavum hematomas: why does it mostly occur in old Asian males? Interesting point of reported cases: review and case report. J Craniovertebr Junction Spine 2016; 7 (01) 7-12
5 Ozturk C, Kanat A, Aydin MD. , et al. The impact of L5 dorsal root ganglion degeneration and Adamkiewicz artery vasospasm on descending colon dilatation following spinal subarachnoid hemorrhage: An experimental study; first report. J Craniovertebr Junction Spine 2015; 6 (02) 69-75
6 Yolas C, Kanat A, Aydin MD. , et al. Unraveling of the effect of nodose ganglion degeneration on the coronary artery vasospasm after subarachnoid hemorrhage: an experimental study. World Neurosurg 2016; 86: 79-87
7 Kanat A, Turkmenoglu O, Aydin MD. , et al. Toward changing of the pathophysiologic basis of acute hydrocephalus after subarachnoid hemorrhage: a preliminary experimental study. World Neurosurg 2013; 80 (3–4): 390-395
8 Onen MR, Yilmaz I, Ramazanoglu L. , et al. Rational roots of sympathetic overactivity by neurogenic pulmonary edema modeling arising from sympathyco-vagal imbalance in subarachnoid hemorrhage: an experimental study. World Neurosurg 2016; 92: 463-470
9 Sarmiento JM, Mukherjee D, Nosova K. , et al. Predictors of treatment delay in aneurysmal subarachnoid hemorrhage patients. J Neurol Surg A Cent Eur Neurosurg 2015; 76 (01) 46-55
10 Yolas C, Kanat A, Aydin MD, Turkmenoglu ON, Gundogdu C. Important casual association of carotid body and glossopharyngeal nerve and lung following experimental subarachnoid hemorrhage in rabbits. First report. J Neurol Sci 2014; 336 (1–2): 220-226
11 Yolas C, Ozdemir NG, Kanat A. , et al. Uncovering a new cause of obstructive hydrocephalus following subarachnoid hemorrhage: choroidal artery vasospasm-related ependymal cell degeneration and aqueductal stenosis—first experimental study. World Neurosurg 2016; 90: 484-491
12 Aydin MD, Akyol-Salman I, Sahin O. Histopathological changes in ciliary ganglion of rabbits with subarachnoid hemorrhage. Int J Neurosci 2005; 115 (11) 1595-1602
13 Kanat A, Yilmaz A, Aydin MD, Musluman M, Altas S, Gursan N. Role of degenerated neuron density of dorsal root ganglion on anterior spinal artery vasospasm in subarachnoid hemorrhage: experimental study. Acta Neurochir (Wien) 2010; 152 (12) 2167-2172
14 Kayaci S, Kanat A, Aydin MD. , et al. Role of neuron density of the stellate ganglion on regulation of the basilar artery volume in subarachnoid hemorrhage: an experimental study. Auton Neurosci 2011; 165 (02) 163-167
15 Aydin MD, Kanat A, Yilmaz A. , et al. The role of ischemic neurodegeneration of the nodose ganglia on cardiac arrest after subarachnoid hemorrhage: an experimental study. Exp Neurol 2011; 230 (01) 90-95
16 Aydin MD, Serarslan Y, Gundogdu C. et al. The relationship between the neuron density of the trigeminal ganglion and the posterior communicating artery vasospasm in subarachnoid hemorrhage: an experimental study. Neurosurg Q 2012; 22: 1-6
17 Aydin MD, Kanat A, Turkmenoglu ON, Yolas C, Gundogdu C, Aydın N. Changes in number of water-filled vesicles of choroid plexus in early and late phase of experimental rabbit subarachnoid hemorrhage model: the role of petrous ganglion of glossopharyngeal nerve. Acta Neurochir (Wien) 2014; 156 (07) 1311-1317
18 Turkmenoglu ON, Kanat A, Yolas C, Aydin MD, Ezirmik N, Gundogdu C. First report of important causal relationship between the Adamkiewicz artery vasospasm and dorsal root ganglion cell degeneration in spinal subarachnoid hemorrhage: an experimental study using a rabbit model. Asian J Neurosurg 2017; 12 (01) 22-27
19 Sterio DC. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 1984; 134 (Pt 2): 127-136
20 Gundersen HJ, Bendtsen TF, Korbo L. , et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 1988; 96 (05) 379-394
21 Özdemir NG, Aydin MD, Yolaş C. , et al. Predictive role of external carotid artery vasospasm on cerebral ischemia in subarachnoid hemorrhage: experimental study. Turk Neurosurg 2016; April 26 (Epub ahead of print)
22 McDougal DH, Gamlin PD. Autonomic control of the eye. Compr Physiol 2015; 5 (01) 439-473
23 Bertinotti L, Pietrini U, Del Rosso A. , et al. The use of pupillometry in joint and connective tissue diseases. Ann N Y Acad Sci 2002; 966: 446-455
24 Currie J, Lessell S. Tonic pupil with giant cell arteritis. Br J Ophthalmol 1984; 68 (02) 135-138
25 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 (02) 107-110
26 Kazdal H, Kanat A, Aydin MD. , et al. Sudden death and cervical spine: a new contribution to pathogenesis for sudden death in critical care unit from subarachnoid hemorrhage. First report—an experimental study. J Craniovertebr Junction Spine 2017; 8 (01) 33-38
27 Plata Bello J, Acosta-Lopez S, Garcia-Marin V. Clinical features and complications in idiopathic subarachnoid hemorrhage: case studies. J Neurol Surg A Cent Eur Neurosurg 2016; 77 (03) 222-228
28 Firsching R, Woischneck D, Langejürgen A. , et al. Clinical, radiologic, and legal significance of “extensor response” in posttraumatic coma. J Neurol Surg A Cent Eur Neurosurg 2015; 76 (06) 456-465
29 Tokuda Y, Nakazato N, Stein GH. Pupillary evaluation for differential diagnosis of coma. Postgrad Med J 2003; 79 (927) 49-51
30 Kanat A. Science in neurosurgery: the importance of the scientific method. Neurosurgery 1998; 43 (06) 1497
31 Silva MD, Brazis P, Miller D, Wharen R, Smith CC, Freeman WD. True- true- unrelated? A delayed onset, complete third-nerve palsy after traumatic subarachnoid hemorrhage. J Vasc Interv Neurol 2013; 6 (01) 22-25
32 Fairbanks C, White JB. Oculomotor nerve palsy in the setting of an anterior cerebral A2 segment aneurysm. J Neurointerv Surg 2011; 3 (01) 74-76
33 Giombini S, Ferraresi S, Pluchino F. Reversal of oculomotor disorders after intracranial aneurysm surgery. Acta Neurochir (Wien) 1991; 112 (1–2): 19-24
34 Kanat A, Kayaci S, Yazar U, Sahin Y, Yaman O, Guvercin AR. One of the giants of neurological surgery left us more than a decade ago, and neurosurgical literature did not show much interest. Neurol Neurochir Pol 2011; 45 (01) 63-67
35 Ko JH, Kim YJ. Oculomotor nerve palsy caused by posterior communicating artery aneurysm: evaluation of symptoms after endovascular treatment. Interv Neuroradiol 2011; 17 (04) 415-419
36 McCracken DJ, Lovasik BP, McCracken CE. , et al. Resolution of oculomotor nerve palsy secondary to posterior communicating artery aneurysms: comparison of clipping and coiling. Neurosurgery 2015; 77 (06) 931-939 ; discussion 939
37 Kanat A, Aydin Y. Selection of cerebral aneurysms for treatment using Guglielmi detachable coils: the preliminary University of Illinois at Chicago experience. Neurosurgery 1999; 45 (03) 670-674
38 Lagares A, Jiménez-Roldán L, Gomez PA. , et al. Prognostic value of the amount of bleeding after aneurysmal subarachnoid hemorrhage: a quantitative volumetric study. Neurosurgery 2015; 77 (06) 898-907 ; discussion 907
39 Klooster J, Beckers HJ, Vrensen GFJ, van der Want JJ. The peripheral and central projections of the Edinger-Westphal nucleus in the rat. A light and electron microscopic tracing study. Brain Res 1993; 632 (1–2): 260-273
40 Kanat A. Pathophysiology of acute hydrocephalus after subarachnoid hemorrhage. World Neurosurg 2014; 82 (1–2): e386-e387
41 Kazdal H, Kanat A, Sen A. , et al. A novel clinical observation in neuroleptic malignant-like syndrome: first demonstration of early progression of hydrocephalus. J Clin Psychopharmacol 2015; 35 (02) 211-212
42 Kazdal H, Kanat A, Findik H. , et al. Transorbital ultrasonographic measurement of optic nerve sheath diameter for intracranial midline shift in patients with head trauma. World Neurosurg 2016; 85: 292-297
43 Kanat A, Aydin MD, Bayram E. , et al. A new determinant of poor outcome after spontaneous subarachnoid hemorrhage; blood pH and the disruption of glossopharyngeal nerve-carotid body network: first experimental study. World Neurosurg 2017; April 26 (Epub ahead of print)
44 Kanat A, Ozdemir B. In reply to the letter to the editor regarding “Restoration of Anterior Vertebral Height by Short-Segment Pedicle Screw Fixation with Screwing of Fractured Vertebra for the Treatment of Unstable Thoracolumbar Fractures.”. World Neurosurg 2017; 101: 793