SUBARAKNOİD KANAMANIN NEDEN OLDUĞU SEREBELLAR HASARDA UYGULANAN FARKLI TEDAVİ MODALİTELERİNİN OKSİDATİF STRES PARAMETRELERİ ÜZERİNE ETKİLERİ
Year 2021,
, 275 - 282, 15.06.2021
Ali Serdar Oğuzoğlu
,
Nilgün Şenol
,
İlter İlhan
,
Halil Aşcı
,
Mine Kaynak
,
Selçuk Çömlekci
Abstract
Amaç
Bu çalışmada, Subaraknoid Kanama (SAK) sonrasında
serebellar dokuda meydana gelen oksidatif stres
üzerinde, uygulanabilecek farklı tedavi modalitelerinin
etkilerinin değerlendirilmesi amaçlanmıştır.
Gereç-ve Yöntem
Kuyruk arterlerinden alınan 0,3 cc otolog kanın sisterna
magna bölgesine enjekte edilmesi ile SAK oluşturulan
ratlara farklı dozlarda (30-60 mg/kg Pregabalin
(PREG), Nimodipin (NİMO), Salubrinal (SLB) ve Darbeli
Elektromanyetik Alan (DEMA) uygulandı. Sakrifikasyon
sonrasında alınan serebellum dokularında
total oksidan kapasite (TOS), total antioksidan kapasite
(TAS) ve oksidatif stres indeksi (OSİ) gibi oksidatif
stres parametreleri incelendi.
Bulgular
TOS ve OSİ değerlerinde PREG30 (iki değer için de
p=0.003), PREG₆₀ (p=0.026 ve p=0.005, sırasıyla),
SLB ve DEMA uygulanan gruplarda anlamlı olarak
azalma görüldü. TAS seviyelerinde ise PREG ve
DEMA uygulanan gruplarda istatistiksel olarak anlamlı
bir değişiklik saptanmazken, SLB ve NİMO uygulanan
gruplarda anlamlı değişiklik olduğu görüldü.
NİMO uygulanan grupta OSİ değerinde de (p=0,046)
SAK grubuna göre anlamlı bir azalma saptandı.
Sonuç
PREG ve SLB SAK’ta farklı iki mekanizma üzerinden
koruyucu olabilmektedir. DEMA tedavisinin de etkinliğinden
söz edilebilir ancak etkisinin değerlendirilmesi
için farklı uygulama zamanları ve süreleri ile yeni çalışmalara
ihtiyaç vardır.
Supporting Institution
Yok
References
- 1. Özdemir M, Bozkurt M, Kahiloğulları G, Uğur HÇ, Egemen N. Subaraknoid Kanama ve Komplikasyonlarının Tedavisi. Ankara Üniversitesi Tıp Fakültesi Mecmuası 2011; 64: 52-55.
- 2. Çomoğlu S, Erdemoğlu AK. Subaraknoid Kanama ve Vazospazm. Van Tıp Dergisi: 1998;5(2):111-113.
- 3. Sen O, Caner H, Aydin MV, Ozen O, Atalay B, Altinors N, Baybek M: The effect of mexiletine on the level of lipid peroxidation and apoptosis of endothelium following experimental subarachnoid hemorrhage. Neurol Res 2006;28(8):859-863.
- 4. Tan HP, Guo Q, Hua G, Chen JX, Liang JC. Inhibition of endoplasmic reticulum stress alleviates secondary injury after traumatic brain injury. Neural Regen Res. 2018; 13(5):827-836.
- 5. Moncada S, Palmer RMJ, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacological Reviews. 1991;43(2):109–142.
- 6. Starke RM, Kim GH, Komotar RJ, et al. Endothelial nitric oxide synthase gene single-nucleotide polymorphism predicts cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Journal of Cerebral Blood Flow and Metabolism. 2008;28(6):1204–1211.
- 7. Vellimana AK, Milner E, Azad TD, et al. Endothelial nitric oxide synthase mediates endogenous protection against subarachnoid hemorrhage-induced cerebral vasospasm. Stroke. 2011;42(3):776–782.
- 8. Deslauriers AM, Afkhami-Goli A, Paul AM, Bhat RK, Acharjee S, Ellestad KK, Noorbakhsh F, Michalak M, Power C. Neuroinflammation and endoplasmic reticulum stress are coregulated by crocin to prevent demyelination and neurodegeneration. J Immunol. 2011;187:4788–4799.
- 9. Deselms H, Maggio N, Rubovitch V, Chapman J, Schreiber S, Tweedie D, Kim DS, Greig NH, Pick CG. Novel pharmaceutical treatments for minimal traumatic brain injury and evaluation of animal models and methodologies supporting their development. J Neurosci Methods. 2016;272:69-76.
- 10. Sokka AL, Putkonen N, Mudo G, Pryazhnikov E, Reijonen S, Khiroug L, Belluardo N, Lindholm D, Korhonen L. Endoplasmic reticulum stress inhibition protects against excitotoxic neuronal injury in the rat brain. J Neurosci. 2007;27:901–908.
- 11. Ersahin M, Toklu HZ, Cetinel S, Yuksel M, Erzik C, Berkman MZ, Yegen BC, Sener G: Alpha lipoic acid alleviates oxidative stress and preserves blood brain permeability in rats with subarachnoid hemorrhage. Neurochem Res 2010;35:418-428.
- 12. Gilgun Sherki Y, Rosenbaum Z, Melamed E and Offen D: Antioxidant therapy in acute central nervous system injury: Current state. Pharmacol Rev 2002;54:271 284.
- 13. Pegoli M, Mandrekar J, Rabinstein AA, Lanzino G. Predictors of excellent functional outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg. 2015;122(2):414–8.
- 14. Al-Tamimi YZ, Orsi NM, Quinn AC, Homer-Vanniasinkam S, Ross SA. A review of delayed ischemic neurologic deficit following aneurysmal subarachnoid hemorrhage: historical overview, current treatment, and pathophysiology. World Neurosurg. 2010;73:654-667.
- 15. Hummig W, Kopruszinski CM, Chichorro JG. Pregabalin reduces acute inflammatory and persistent pain associated with nerve injury and cancer in rat models of orofacial pain. J Oral Facial Pain Headache. 2014 Fall;28(4):350-9.
- 16. Aswar M, Patil V. Ferulic acid ameliorates chronic constriction injury induce painful neuropathy in rats. Inflammopharmacology. 2016 Aug;24(4):181-8.
- 17. Matsuoka M, Komoike Y. Experimental evidence shows salubrinal, an eIF2alpha dephosphorylation inhibitor, reduces xenotoxicant-induced cellular damage. Int J Mol Sci. 2015;16:16275–16287.
- 18. Raghubir R, Nakka VP, Mehta SL. Endoplasmic reticulum stress in brain damage. Methods Enzymol 2011;489:259-275.
- 19. Roth TL, Nayak D, Atanasijevic T, Koretsky AP, Latour LL, McGavern DB. Transcranial amelioration of inflammation and cell death after brain injury. Nature. 2014;505:223–228.
- 20. Vergouwen MD, Vermeulen M, van Gijn J, Rinkel GJ, Wijdicks EF, Muizelaar JP, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke. 2010;41(10):2391–5.
- 21. Rubovitch V, Barak S, Rachmany L, Goldstein RB, Zilberstein Y, Pick CG. The neuroprotective effect of salubrinal in a mouse model of traumatic brain injury. Neuromolecular Med. 2015;17(1):58-70.
- 22. Hayashi T. Conversion of psychological stress into cellular stress response: roles of the sigma-1 receptor in the process. Psychiatry Clin Neurosci. 2015;69:179–191.
- 23. Hu YC, Sun Q, Li W, Zhang DD, Ma B, Li S, Li WD, Zhou ML, Hang CH. Biphasic activation of nuclear factor kappa B and expression of p65 and c-Rel after traumatic brain injury in rats. Inflamm Res. 2014;63:109–115.
- 24. Huang X, Chen Y, Zhang H, Ma Q, Zhang YW, Xu H. Salubrinal attenuates beta-amyloid-induced neuronal death and microglial activation by inhibition of the NF-kappaB pathway. Neurobiol Aging. 2012;33(1007):e1009–e1017.
- 25. Bracchi-Ricard V, Lambertsen KL, Ricard J, Nathanson L, Karmally S, Johnstone J, Ellman DG, Frydel B, McTigue DM, Bethea JR. Inhibition of astroglial NF-kappaB enhances oligodendrogenesis following spinal cord injury. J Neuroinflamm. 2013; 10:92.
- 26. Tan HP, Guo Q, Hua G, Chen JX, Liang JC. Inhibition of endoplasmic reticulum stress alleviates secondary injury after traumatic brain injury. Neural Regen Res. 2018; 13(5):827-836.
- 27. Gaynor JS, Hagberg S, Gurfein BT. Veterinary applications of pulsed electromagnetic field therapy. Res Vet Sci. 2018;119:1‐8.
- 28. Meymandi MS, Sepehri G, Abdolsamadi M, Shaabani M, Heravi G, Yazdanpanah O, Aghtaei MM. The effects of co-administration of pregabalin and vitamin E on neuropathic pain induced by partial sciatic nerve ligation in male rats. Inflammopharmacology, 2017;25(2):237-246.
- 29. Ben‐Menachem, E. Pregabalin pharmacology and its relevance to clinical practice. Epilepsia, 2004;45:13-18.
- 30. Bragin DE, Bragina OA, Hagberg S, Nemoto EM. Pulsed Electromagnetic Field (PEMF) Mitigates High Intracranial Pressure (ICP) Induced Microvascular Shunting (MVS) in Rats. Acta Neurochir Suppl. 2018;126:93-95. doi: 10.1007/978-3-319-65798-1_20. PMID: 29492540; PMCID: PMC6340641.
- 31. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248–254.
- 32. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 2004;37:277–285.
- 33. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem 2005;38:1103–1111.
- 34. Demirbag R, Gur M, Yilmaz R, Kunt AS, Erel O, Andac MH. Influence of oxidative stress on the development of collateral circulation in total coronary occlusions. Int J Cardiol 2007;116:14–19.
- 35. Brain aneurysm foundation. Brain aneurysm statistics and facts. Available from: https://www.bafound.org/about-brain-aneurysms/. Accessed November 1, 2017.
- 36. Ekelund A, Reinstrup P, Ryding E, Andersson AM, Molund T, Kristiansson KA, Romner B, Brandt L, Säveland H. Effects of iso- and hypervolemic hemodilution on regional cerebral blood flow and oxygen delivery for patients with vasospasm after aneurysmal subarachnoid hemorrhage. Acta Neurochir (Wien) 2002;144:703–712. discussion 712-713.
- 37. Treggiari-Venzi MM, Suter PM, Romand JA. Review of medical prevention of vasospasm after aneurysmal subarachnoid hemorrhage: a problem of neurointensive care. Neurosurgery 2001; 48: 249-62.
- 38. Vergouwen MD, Ilodigwe D, Macdonald RL. Cerebral infarction after subarachnoid hemorrhage contributes to poor outcome by vasospasm-dependent and -independent effects. Stroke. 2011;42(4):924–9.
- 39. Macdonald RL, Rosengart A, Huo D, Karrison T. Factors associated with the development of vasospasm after planned surgical treatment of aneurysmal subarachnoid hemorrhage. J Neurosurg. 2003;99:644–652.
- 40. Pluta RM, Hansen-Schwartz J, Dreier J, et al. Cerebral vasospasm following subarachnoid hemorrhage: time for a new world of thought. Neurol Res 2009;31:151-8.
- 41. Crowley RW, Medel R, Dumont AS, Ilodigwe D, Kassell NF, Mayer SA, et al. Angiographic vasospasm is strongly correlated with cerebral infarction after subarachnoid hemorrhage. Stroke. 2011;42(4):919–23.
- 42. Marin J, Rodriguez-Martinez MA. Role of vascular nitric oxide in physiological and pathological conditions. Pharmacol Ther 1997; 75: 111-34.
- 43. Kiriş T, Karasu A, Yavuz C, et al. Reversal of cerebral vasospasm by the nitric oxide donor SNAP in an experimental model of subarachnoid haemorrhage. Acta Neurochir (Wien) 1999; 141: 1323-28.
- 44. Jung CS, Iuliano BA, Harvey-White J, Espey MG, Oldfield EH, Pluta RM: Association between cerebrospinal fluid levels of asymmetric dimethyl-L-arginine, an endogenous inhibitor of endothelial nitric oxide synthase, and cerebral vasospasm in a primate model of subarachnoid hemorrhage. J Neurosurg 2004; 101: 836-42.
- 45. Pickard JD, Murray GD, Illingworth R, Shaw MD, Teasdale GM, Foy PM, et al. Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. British Medical Journal, 1989;298(6674):636-642.
- 46. Biondi A, Ricciardi GK, Puybasset L, Abdennour L, Longo M, Chiras J, van Effenterre R. Intra-arterial nimodipine for the treatment of symptomatic cerebral vasospasm after aneurysmal subarachnoid hemorrhage: preliminary results. AJNR Am J Neuroradiol. 2004;25:1067–1076.
- 47. Hui C, Lau KP. Efficacy of intra-arterial nimodipine in the treatment of cerebral vasospasm complicating subarachnoid haemorrhage. Clin Radiol. 2005;60:1030–1036.
- 48. Friedrich V, Flores R, Sehba FA. Cell death starts early after subarachnoid hemorrhage. Neurosci Lett. 2012b; 512:6–11.
- 49. Bannister JP, Adebiyi A, Zhao G, Narayanan D, Thomas CM, Feng JY, Jaggar JH. Smooth muscle cell alpha2delta-1 subunits are essential for vasoregulation by CaV1.2 channels. Circ Res. 2009 Nov 6;105(10):948-55.
- 50. Hummig W, Kopruszinski CM, Chichorro JG. Pregabalin reduces acute inflammatory and persistent pain associated with nerve injury and cancer in rat models of orofacial pain. J Oral Facial Pain Headache. 2014 Fall;28(4):350-9.
- 51. Aswar M, Patil V. Ferulic acid ameliorates chronic constriction injury induce painful neuropathy in rats. Inflammopharmacology. 2016 Aug;24(4):181-8.
- 52. Aşcı S, Demirci S, Aşcı H, Doğuç DK, Onaran İ. Neuroprotective Effects of Pregabalin on Cerebral Ischemia and Reperfusion. Balkan Med J. 2016 Mar;33(2):221-7.
- 53. Allen GS, Ahn HS, Presozi TJ ve ark: Cerebral arterial spasm-a controlled trial of nimodipine in patients with subarachnoid hemorrhage. N Engl J Med, 1983;308:619-24.
- 54. Kim CH, Wheatley-Guy CM, Stewart GM, Yeo D, Shen WK, Johnson BD. The impact of pulsed electromagnetic field therapy on blood pressure and circulating nitric oxide levels: a double blind, randomizedstudy in subjects with metabolic syndrome. BVlood Pressure 2020;29:1, 47–54.
- 55. Bragin DE, Statom GL, Hagberg S, Nemoto EM. Increased in microvascular perfusion and tissue oxygenation via pulsed electromagnetic fields in the healty rat brain. J Neurosurg. 2015;122(5):1239-47.
THE EFFECTS OF DIFFERENT TREATMENT MODALITIES ON OXIDATIVE STRESS MARKERS FOR CEREBELLAR INJURY SECONDARY TO SUBARACHNOID HEMORRHAGE
Year 2021,
, 275 - 282, 15.06.2021
Ali Serdar Oğuzoğlu
,
Nilgün Şenol
,
İlter İlhan
,
Halil Aşcı
,
Mine Kaynak
,
Selçuk Çömlekci
Abstract
Objective
In this study, we aimed to evaluate the effects of different
treatment modalities on oxidative stress occured in
cerebellar tissue after subarachnoid hemorrhage (SAH).
Materials and Methods
Different doses of Pregabaline (30-60 mg/kg Pregabalin
(PREG), and Nimodipine (NIMO), Salubrinal
(SLB), Pulsed ElectromagneticFfield (PEMF) was
used in the rats, that SAH was comprised via 0,3cc
otolog blood injection into the cisterna magna. After
sacrification oxidative stress parameters like Total Antioxidant
Status (TAS), Total Oxidant Status (TOS),
and Oxidative Stress Index (OSI) were evaluated in
the cerellum tissues.
Results
Significant decrease was seen in the TOS and OSI
values of the groups that PREG30 (p=0.003 for both),
PREG₆₀ (p=0.026 and p=0.005, respectively), SLB
and PEMF were used. Although there was no statistically
difference in the TAS values of the PREG and
DEMA groups, significant difference was seen in the
SLB and NIMO groups. In the NIMO group there was
a significant decrease (p=0,046) in the OSI values
according to the SAH group.
Conclusion
PREG and SLB can be protective in SAH via two different
mechanisms, PEMF treatment can be effective
but new studies with different application periods and
doses are needed to evaluate the effects.
References
- 1. Özdemir M, Bozkurt M, Kahiloğulları G, Uğur HÇ, Egemen N. Subaraknoid Kanama ve Komplikasyonlarının Tedavisi. Ankara Üniversitesi Tıp Fakültesi Mecmuası 2011; 64: 52-55.
- 2. Çomoğlu S, Erdemoğlu AK. Subaraknoid Kanama ve Vazospazm. Van Tıp Dergisi: 1998;5(2):111-113.
- 3. Sen O, Caner H, Aydin MV, Ozen O, Atalay B, Altinors N, Baybek M: The effect of mexiletine on the level of lipid peroxidation and apoptosis of endothelium following experimental subarachnoid hemorrhage. Neurol Res 2006;28(8):859-863.
- 4. Tan HP, Guo Q, Hua G, Chen JX, Liang JC. Inhibition of endoplasmic reticulum stress alleviates secondary injury after traumatic brain injury. Neural Regen Res. 2018; 13(5):827-836.
- 5. Moncada S, Palmer RMJ, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacological Reviews. 1991;43(2):109–142.
- 6. Starke RM, Kim GH, Komotar RJ, et al. Endothelial nitric oxide synthase gene single-nucleotide polymorphism predicts cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Journal of Cerebral Blood Flow and Metabolism. 2008;28(6):1204–1211.
- 7. Vellimana AK, Milner E, Azad TD, et al. Endothelial nitric oxide synthase mediates endogenous protection against subarachnoid hemorrhage-induced cerebral vasospasm. Stroke. 2011;42(3):776–782.
- 8. Deslauriers AM, Afkhami-Goli A, Paul AM, Bhat RK, Acharjee S, Ellestad KK, Noorbakhsh F, Michalak M, Power C. Neuroinflammation and endoplasmic reticulum stress are coregulated by crocin to prevent demyelination and neurodegeneration. J Immunol. 2011;187:4788–4799.
- 9. Deselms H, Maggio N, Rubovitch V, Chapman J, Schreiber S, Tweedie D, Kim DS, Greig NH, Pick CG. Novel pharmaceutical treatments for minimal traumatic brain injury and evaluation of animal models and methodologies supporting their development. J Neurosci Methods. 2016;272:69-76.
- 10. Sokka AL, Putkonen N, Mudo G, Pryazhnikov E, Reijonen S, Khiroug L, Belluardo N, Lindholm D, Korhonen L. Endoplasmic reticulum stress inhibition protects against excitotoxic neuronal injury in the rat brain. J Neurosci. 2007;27:901–908.
- 11. Ersahin M, Toklu HZ, Cetinel S, Yuksel M, Erzik C, Berkman MZ, Yegen BC, Sener G: Alpha lipoic acid alleviates oxidative stress and preserves blood brain permeability in rats with subarachnoid hemorrhage. Neurochem Res 2010;35:418-428.
- 12. Gilgun Sherki Y, Rosenbaum Z, Melamed E and Offen D: Antioxidant therapy in acute central nervous system injury: Current state. Pharmacol Rev 2002;54:271 284.
- 13. Pegoli M, Mandrekar J, Rabinstein AA, Lanzino G. Predictors of excellent functional outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg. 2015;122(2):414–8.
- 14. Al-Tamimi YZ, Orsi NM, Quinn AC, Homer-Vanniasinkam S, Ross SA. A review of delayed ischemic neurologic deficit following aneurysmal subarachnoid hemorrhage: historical overview, current treatment, and pathophysiology. World Neurosurg. 2010;73:654-667.
- 15. Hummig W, Kopruszinski CM, Chichorro JG. Pregabalin reduces acute inflammatory and persistent pain associated with nerve injury and cancer in rat models of orofacial pain. J Oral Facial Pain Headache. 2014 Fall;28(4):350-9.
- 16. Aswar M, Patil V. Ferulic acid ameliorates chronic constriction injury induce painful neuropathy in rats. Inflammopharmacology. 2016 Aug;24(4):181-8.
- 17. Matsuoka M, Komoike Y. Experimental evidence shows salubrinal, an eIF2alpha dephosphorylation inhibitor, reduces xenotoxicant-induced cellular damage. Int J Mol Sci. 2015;16:16275–16287.
- 18. Raghubir R, Nakka VP, Mehta SL. Endoplasmic reticulum stress in brain damage. Methods Enzymol 2011;489:259-275.
- 19. Roth TL, Nayak D, Atanasijevic T, Koretsky AP, Latour LL, McGavern DB. Transcranial amelioration of inflammation and cell death after brain injury. Nature. 2014;505:223–228.
- 20. Vergouwen MD, Vermeulen M, van Gijn J, Rinkel GJ, Wijdicks EF, Muizelaar JP, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke. 2010;41(10):2391–5.
- 21. Rubovitch V, Barak S, Rachmany L, Goldstein RB, Zilberstein Y, Pick CG. The neuroprotective effect of salubrinal in a mouse model of traumatic brain injury. Neuromolecular Med. 2015;17(1):58-70.
- 22. Hayashi T. Conversion of psychological stress into cellular stress response: roles of the sigma-1 receptor in the process. Psychiatry Clin Neurosci. 2015;69:179–191.
- 23. Hu YC, Sun Q, Li W, Zhang DD, Ma B, Li S, Li WD, Zhou ML, Hang CH. Biphasic activation of nuclear factor kappa B and expression of p65 and c-Rel after traumatic brain injury in rats. Inflamm Res. 2014;63:109–115.
- 24. Huang X, Chen Y, Zhang H, Ma Q, Zhang YW, Xu H. Salubrinal attenuates beta-amyloid-induced neuronal death and microglial activation by inhibition of the NF-kappaB pathway. Neurobiol Aging. 2012;33(1007):e1009–e1017.
- 25. Bracchi-Ricard V, Lambertsen KL, Ricard J, Nathanson L, Karmally S, Johnstone J, Ellman DG, Frydel B, McTigue DM, Bethea JR. Inhibition of astroglial NF-kappaB enhances oligodendrogenesis following spinal cord injury. J Neuroinflamm. 2013; 10:92.
- 26. Tan HP, Guo Q, Hua G, Chen JX, Liang JC. Inhibition of endoplasmic reticulum stress alleviates secondary injury after traumatic brain injury. Neural Regen Res. 2018; 13(5):827-836.
- 27. Gaynor JS, Hagberg S, Gurfein BT. Veterinary applications of pulsed electromagnetic field therapy. Res Vet Sci. 2018;119:1‐8.
- 28. Meymandi MS, Sepehri G, Abdolsamadi M, Shaabani M, Heravi G, Yazdanpanah O, Aghtaei MM. The effects of co-administration of pregabalin and vitamin E on neuropathic pain induced by partial sciatic nerve ligation in male rats. Inflammopharmacology, 2017;25(2):237-246.
- 29. Ben‐Menachem, E. Pregabalin pharmacology and its relevance to clinical practice. Epilepsia, 2004;45:13-18.
- 30. Bragin DE, Bragina OA, Hagberg S, Nemoto EM. Pulsed Electromagnetic Field (PEMF) Mitigates High Intracranial Pressure (ICP) Induced Microvascular Shunting (MVS) in Rats. Acta Neurochir Suppl. 2018;126:93-95. doi: 10.1007/978-3-319-65798-1_20. PMID: 29492540; PMCID: PMC6340641.
- 31. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248–254.
- 32. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 2004;37:277–285.
- 33. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem 2005;38:1103–1111.
- 34. Demirbag R, Gur M, Yilmaz R, Kunt AS, Erel O, Andac MH. Influence of oxidative stress on the development of collateral circulation in total coronary occlusions. Int J Cardiol 2007;116:14–19.
- 35. Brain aneurysm foundation. Brain aneurysm statistics and facts. Available from: https://www.bafound.org/about-brain-aneurysms/. Accessed November 1, 2017.
- 36. Ekelund A, Reinstrup P, Ryding E, Andersson AM, Molund T, Kristiansson KA, Romner B, Brandt L, Säveland H. Effects of iso- and hypervolemic hemodilution on regional cerebral blood flow and oxygen delivery for patients with vasospasm after aneurysmal subarachnoid hemorrhage. Acta Neurochir (Wien) 2002;144:703–712. discussion 712-713.
- 37. Treggiari-Venzi MM, Suter PM, Romand JA. Review of medical prevention of vasospasm after aneurysmal subarachnoid hemorrhage: a problem of neurointensive care. Neurosurgery 2001; 48: 249-62.
- 38. Vergouwen MD, Ilodigwe D, Macdonald RL. Cerebral infarction after subarachnoid hemorrhage contributes to poor outcome by vasospasm-dependent and -independent effects. Stroke. 2011;42(4):924–9.
- 39. Macdonald RL, Rosengart A, Huo D, Karrison T. Factors associated with the development of vasospasm after planned surgical treatment of aneurysmal subarachnoid hemorrhage. J Neurosurg. 2003;99:644–652.
- 40. Pluta RM, Hansen-Schwartz J, Dreier J, et al. Cerebral vasospasm following subarachnoid hemorrhage: time for a new world of thought. Neurol Res 2009;31:151-8.
- 41. Crowley RW, Medel R, Dumont AS, Ilodigwe D, Kassell NF, Mayer SA, et al. Angiographic vasospasm is strongly correlated with cerebral infarction after subarachnoid hemorrhage. Stroke. 2011;42(4):919–23.
- 42. Marin J, Rodriguez-Martinez MA. Role of vascular nitric oxide in physiological and pathological conditions. Pharmacol Ther 1997; 75: 111-34.
- 43. Kiriş T, Karasu A, Yavuz C, et al. Reversal of cerebral vasospasm by the nitric oxide donor SNAP in an experimental model of subarachnoid haemorrhage. Acta Neurochir (Wien) 1999; 141: 1323-28.
- 44. Jung CS, Iuliano BA, Harvey-White J, Espey MG, Oldfield EH, Pluta RM: Association between cerebrospinal fluid levels of asymmetric dimethyl-L-arginine, an endogenous inhibitor of endothelial nitric oxide synthase, and cerebral vasospasm in a primate model of subarachnoid hemorrhage. J Neurosurg 2004; 101: 836-42.
- 45. Pickard JD, Murray GD, Illingworth R, Shaw MD, Teasdale GM, Foy PM, et al. Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. British Medical Journal, 1989;298(6674):636-642.
- 46. Biondi A, Ricciardi GK, Puybasset L, Abdennour L, Longo M, Chiras J, van Effenterre R. Intra-arterial nimodipine for the treatment of symptomatic cerebral vasospasm after aneurysmal subarachnoid hemorrhage: preliminary results. AJNR Am J Neuroradiol. 2004;25:1067–1076.
- 47. Hui C, Lau KP. Efficacy of intra-arterial nimodipine in the treatment of cerebral vasospasm complicating subarachnoid haemorrhage. Clin Radiol. 2005;60:1030–1036.
- 48. Friedrich V, Flores R, Sehba FA. Cell death starts early after subarachnoid hemorrhage. Neurosci Lett. 2012b; 512:6–11.
- 49. Bannister JP, Adebiyi A, Zhao G, Narayanan D, Thomas CM, Feng JY, Jaggar JH. Smooth muscle cell alpha2delta-1 subunits are essential for vasoregulation by CaV1.2 channels. Circ Res. 2009 Nov 6;105(10):948-55.
- 50. Hummig W, Kopruszinski CM, Chichorro JG. Pregabalin reduces acute inflammatory and persistent pain associated with nerve injury and cancer in rat models of orofacial pain. J Oral Facial Pain Headache. 2014 Fall;28(4):350-9.
- 51. Aswar M, Patil V. Ferulic acid ameliorates chronic constriction injury induce painful neuropathy in rats. Inflammopharmacology. 2016 Aug;24(4):181-8.
- 52. Aşcı S, Demirci S, Aşcı H, Doğuç DK, Onaran İ. Neuroprotective Effects of Pregabalin on Cerebral Ischemia and Reperfusion. Balkan Med J. 2016 Mar;33(2):221-7.
- 53. Allen GS, Ahn HS, Presozi TJ ve ark: Cerebral arterial spasm-a controlled trial of nimodipine in patients with subarachnoid hemorrhage. N Engl J Med, 1983;308:619-24.
- 54. Kim CH, Wheatley-Guy CM, Stewart GM, Yeo D, Shen WK, Johnson BD. The impact of pulsed electromagnetic field therapy on blood pressure and circulating nitric oxide levels: a double blind, randomizedstudy in subjects with metabolic syndrome. BVlood Pressure 2020;29:1, 47–54.
- 55. Bragin DE, Statom GL, Hagberg S, Nemoto EM. Increased in microvascular perfusion and tissue oxygenation via pulsed electromagnetic fields in the healty rat brain. J Neurosurg. 2015;122(5):1239-47.