J Neurol Surg A Cent Eur Neurosurg 2019; 80(06): 430-440
DOI: 10.1055/s-0039-1685186
Original Article
Georg Thieme Verlag KG Stuttgart · New York

Describing a New Mechanism of Retinal Detachment Secondary to Ophthalmic Artery Vasospasm Following Subarachnoid Hemorrhage: An Experimental Study

Huseyin Findik
1   Department of Ophthalmology, Recep Tayyip Erdogan University, Medical Faculty, Rize, Turkey
,
Ayhan Kanat
2   Department of Neurosurgery, Recep Tayyip Erdogan University, Rize, Turkey
,
Mehmet Dumlu Aydin
3   Department of Neurosurgery, Ataturk University Medical Faculty, Erzurum, Turkey
,
Murteza Cakir
3   Department of Neurosurgery, Ataturk University Medical Faculty, Erzurum, Turkey
,
Sevilay Akalp Ozmen
4   Department of Pathology, Erzurum Research-Training Hospital, Erzurum, Turkey
,
Murat Okutucu
1   Department of Ophthalmology, Recep Tayyip Erdogan University, Medical Faculty, Rize, Turkey
,
Orhan Baykal
5   Department of Ophthalmology, Ataturk University Medical Faculty, Erzurum, Turkey
,
Sare Sipal
6   Department of Pathology, Ataturk University Medical Faculty, Erzurum, Turkey
› Institutsangaben
Weitere Informationen

Publikationsverlauf

30. August 2018

19. November 2018

Publikationsdatum:
20. August 2019 (online)

Abstract

Background The pterygopalatine ganglion (PPG) and ophthalmic arteries (OpAs) have important roles in ocular autoregulation and retinal and visual functions. The relationship between PPG neuron density, OpA vasospasm, and retinal detachment in subarachnoid hemorrhage (SAH) has never been studied.

Methods This study was conducted on 25 rabbits. Five animals were in the control group (GI; n = 5), five in the sham group (GII; n = 5), and 15 in the study group (GIII; n = 15). After injection of 1 cc serum saline into the cisterna magna in the sham group, and autologous blood in the SAH group, the animals were followed for 3 weeks. All animals underwent a retinal examination five times a week for 3 weeks before and after the experiment. After the experiment, the neuron density of PPGs of the facial nerves, vasospasm index (VSI) of OpAs, and total basal surface values of the detached retinal parts (DRPs) were calculated.

Results In the funduscopic examination, intravitreous hemorrhage ( Terson's syndrome) was detected in four animals in the SAH group. In the control groups, neuron density was 12,000 ± 1,240/mm3, VSI = 0.345 ± 0.076, and DRP = 0 to 1.5 mm2. Mean neuron density was 9,450 ± 940/mm3, VSI = 1.645 ± 0.940, and DRP = 6.23 ± 1.61 mm2 in the sham group (p < 0.05). Neuron density was 6,890 ± 932/mm3, VSI = 2.92 ± 0.97, and DRP = 9.43 ± 2.54 mm2 in SAH group.

Conclusion Mean neuron density, VSI of OpAs, and DRP values differed statistically significant between the SAH group and other groups (p < 0.005). There is an inverse relationship between PPG neurons and DRP. However, a direct relationship was observed between the mean VSI and DRP values.

Animal Experiments

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.


 
  • References

  • 1 Kanat A, Aydin Y. Asymptomatic familial cerebral aneurysms. Neurosurgery 1999; 44 (06) 1364-1365
  • 2 Musluman AM, Aydin MD, Yilmaz A. , et al. The effect of degenerated neuron density of petrosal ganglion on the development of blood pressure variabilities after subarachnoid hemorrhage in a rabbit model: an experimental study. Turk Neurosurg 2011; 21 (04) 559-566
  • 3 Ozdemir NG, Aydin MD, Yolas C. , et al. Predictive role of external carotid artery vasospasm on cerebral ischemia after subarachnoid hemorrhage: experimental study. Turk Neurosurg 2017; 27 (06) 874-883
  • 4 Gasenzer ER, Kanat A, Neugebauer E. The unforgettable neurosurgical operations of musicians in the last century. World Neurosurg 2017; 101 (05) 444-450
  • 5 Gasenzer ER, Kanat A, Neugebauer E. Neurosurgery and music; effect of Wolfgang Amadeus Mozart. World Neurosurg 2017; 102: 313-319
  • 6 Gasenzer ER, Kanat A, Neugebauer EAM. First report of awake craniotomy of a famous musician: suprasellar tumor surgery of pianist Clara Haskil in 1942. J Neurol Surg A Cent Eur Neurosurg 2017; 78 (03) 260-268
  • 7 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; 104: 333-338
  • 8 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
  • 9 Ďuriš K, Neuman E, Vybíhal V. , et al. Early dynamics of interleukin-6 in cerebrospinal fluid after aneurysmal subarachnoid hemorrhage. J Neurol Surg A Cent Eur Neurosurg 2018; 79 (02) 145-151
  • 10 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
  • 11 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
  • 12 Skevas C, Czorlich P, Knospe V. , et al. Terson's syndrome—rate and surgical approach in patients with subarachnoid hemorrhage: a prospective interdisciplinary study. Ophthalmology 2014; 121 (08) 1628-1633
  • 13 Kanat A. Brain oxygenation and energy metabolism: Part 1—Biological function and pathophysiology. Neurosurgery 2003; 52 (06) 1508-1509 ; author reply 1509
  • 14 Cuthbertson S, Jackson B, Toledo C. , et al. Innervation of orbital and choroidal blood vessels by the pterygopalatine ganglion in pigeons. J Comp Neurol 1997; 386 (03) 422-442
  • 15 Toda N, Tanaka T, Ayajiki K, Okamura T. Cerebral vasodilatation induced by stimulation of the pterygopalatine ganglion and greater petrosal nerve in anesthetized monkeys. Neuroscience 2000; 96 (02) 393-398
  • 16 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
  • 17 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
  • 18 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
  • 19 Yolas C, Kanat A, Aydin MD. , et al. The important liaison between Onuf nucleus-pudendal nerve ganglia complex degeneration and urinary retention in spinal subarachnoid hemorrhage: an experimental study. World Neurosurg 2016; 89: 208-214
  • 20 Kilic M, Aydin MD, Demirci E. , et al. Unpublished neuropathologic mechanism behind the muscle weakness/paralysis and gait disturbances induced by sciatic nerve degeneration after spinal subarachnoid hemorrhage: an experimental study. World Neurosurg 2018; 119: e1029-e1034
  • 21 Yilmaz A, Aydin MD, Kanat A. , et al. The effect of choroidal artery vasospasm on choroid plexus injury in subarachnoid hemorrhage: experimental study. Turk Neurosurg 2011; 21 (04) 477-482
  • 22 Sabanci PA, Omay B, Aras Y. , et al. Effect of visible light on vasospasticity of post-subarachnoid hemorrhage cerebrospinal fluid. J Neurol Surg A Cent Eur Neurosurg 2017; 78 (06) 548-555
  • 23 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
  • 24 Ozturk C, Ozdemir NG, Kanat A. , et al. How reliable is pupillary evaluation following subarachnoid hemorrhage? Effect of oculomotor nerve degeneration secondary to posterior communicating artery vasospasm: first experimental study. j Neurol Surg A Cent Eur Neurosurg 2018; 79 (04) 302-308
  • 25 McDougal DH, Gamlin PD. Autonomic control of the eye. Compr Physiol 2015; 5 (01) 439-473
  • 26 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
  • 27 Eliott D, Papakostas TD. Traumatic chorioretinopathies. In: Schachat A, Wilkinson C, Hinton D, Sadda SV, Wiedemann P. , eds. Ryan's Retina. 6th ed. Philadelphia, PA: Elsevier; 2017
  • 28 Kapoor S. Terson syndrome: an often overlooked complication of subarachnoid hemorrhage. World Neurosurg 2014; 81 (01) e4
  • 29 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
  • 30 Yarnitsky D, Lorian A, Shalev A. , et al. Reversal of cerebral vasospasm by sphenopalatine ganglion stimulation in a dog model of subarachnoid hemorrhage. Surg Neurol 2005; 64 (01) 5-11 ; discussion 11
  • 31 Takahashi M, Zhang Z-D, Macdonald RL. Sphenopalatine ganglion stimulation for vasospasm after experimental subarachnoid hemorrhage. J Neurosurg 2011; 114 (04) 1104-1109
  • 32 Korinek AM. ; Service Epidémiologie Hygiène et Prévention. Risk factors for neurosurgical site infections after craniotomy: a prospective multicenter study of 2944 patients. The French Study Group of Neurosurgical Infections, the SEHP, and the C-CLIN Paris-Nord. Neurosurgery 1997; 41 (05) 1073-1079 ; discussion 1079–1081
  • 33 Gasenzer ER, Kanat A, Ozdemir V, Neugebauer E. Analyzing of dark past and bright present of neurosurgical history with a picture of musicians. Br J Neurosurg 2018; 32 (03) 303-304
  • 34 Kanat A. Science in neurosurgery: the importance of the scientific method. Neurosurgery 1998; 43 (06) 1497
  • 35 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
  • 36 Aydın MD, Aydın N, Kanat A. , et al. The sooth beneath the taste roseas in the urethra and first description of neuro-morpho-chemical mechanism of penile erectile posture in males: an experimental study. Int J Neurosci 2018; 128 (07) 663-669
  • 37 Ehlert A, Budde U, Middendorff R, Manthei G, Kemmling A, Tiemann B. Reintroduction of the rat for experimental subarachnoid hemorrhage with accelerated clot formation: a low mortality model with persistent clots as a precondition for studies in vasospasm. J Neurol Surg A Cent Eur Neurosurg 2018; 79 (05) 424-433
  • 38 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
  • 39 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
  • 40 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
  • 41 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
  • 42 Aydın MD, Kanat A, Aydın N. , et al. New evidence for causal central mechanism of hyperglycemia in subarachnoid hemorrhage secondary to ischemic degenerative disruption of circuitry among insular cortex, nodose ganglion, and pancreas: experimental study. World Neurosurg 2017; 106: 570-577
  • 43 Kanat A, Balik MS, Kirbas S. , et al. Paradox in the cubital tunnel syndrome—frequent involvement of left elbow: first report. Acta Neurochir (Wien) 2014; 156 (01) 165-168
  • 44 Ozdemir B, Kanat A, Batcik OE. , et al. First report of perforation of ligamentum flavum by sequestrated lumbar intervertebral disc. J Craniovertebr Junction Spine 2017; 8 (01) 70-73
  • 45 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
  • 46 Ehrenberg M, Thresher RJ, Machemer R. Vitreous hemorrhage nontoxic to retina as a stimulator of glial and fibrous proliferation. Am J Ophthalmol 1984; 97 (05) 611-626
  • 47 Stiebel-Kalish H, Turtel LS, Kupersmith MJ. The natural history of nontraumatic subarachnoid hemorrhage-related intraocular hemorrhages. Retina 2004; 24 (01) 36-40
  • 48 Fisher SK, Lewis GP. Cellular effects of detachment and reattachment on the neural retina and the retinal pigment epithelium. In: Ryan SJ, Hinton DR. , eds. Retinal Reattachments: Surgical Principles and Techniques. 6th ed. Philadelphia, PA: Elsevier; 2006: 1991-2012
  • 49 Cook B, Lewis GP, Fisher SK, Adler R. Apoptotic photoreceptor degeneration in experimental retinal detachment. Invest Ophthalmol Vis Sci 1995; 36 (06) 990-996
  • 50 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
  • 51 Laslo AM, Eastwood JD, Pakkiri P, Chen F, Lee TY. CT perfusion-derived mean transit time predicts early mortality and delayed vasospasm after experimental subarachnoid hemorrhage. AJNR Am J Neuroradiol 2008; 29 (01) 79-85
  • 52 Kanat A. Pathophysiology of acute hydrocephalus after subarachnoid hemorrhage. World Neurosurg 2014; 82 (1–2): e386-e387
  • 53 Kanat A. Letter to the editor regarding “Predictors of shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage? A systematic review and meta-analysis.”. World Neurosurg 2017; 108: 963
  • 54 Charan J, Kantharia ND. How to calculate sample size in animal studies?. J Pharmacol Pharmacother 2013; 4 (04) 303-306 10.4103/0976-500X.119726
  • 55 Bostan H, Cabalar M, Altinay S. , et al. A histopathological examination: the sciatic nerve injury following analgesic drug injection in rats. North Clin Istanb 2018 Doi: 10.14744/nci.2017.28190
  • 56 Kanat A, Aydin Y. Prognostic value and determinants of ultra-early angiographic vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery 2000; 46 (02) 505-507
  • 57 Garfinkle AM, Danys IR, Nicolle DA, Colohan AR, Brem S. Terson's syndrome: a reversible cause of blindness following subarachnoid hemorrhage. J Neurosurg 1992; 76 (05) 766-771
  • 58 Karadžić J, Kovačević I, Stefanović I, Risimić D. Terson's syndrome—a report of two cases. Srp Arh Celok Lek 2015; 143 (9–10): 595-598