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Published in: Acta Neurochirurgica 5/2014

01-05-2014 | Experimental Research - Vascular

The comparative effects of recombinant human erythropoietin and darbepoetin-alpha on cerebral vasospasm following experimental subarachnoid hemorrhage in the rabbit

Authors: Hayri Kertmen, Bora Gürer, Erdal Resit Yilmaz, Ata Türker Arikok, Mehmet Ali Kanat, Berrin Imge Ergüder, Zeki Sekerci

Published in: Acta Neurochirurgica | Issue 5/2014

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Abstract

Background

Darbepoetin alpha is a hypersialylated analogue of erythropoietin effective for activating erythropoietin-receptors. This study investigated the vasodilator and neuroprotective effects of darbepoetin alpha on an experimental subarachnoid hemorrhage model and compared it with erythropoietin.

Methods

Forty adult male New Zealand white rabbits were randomly divided into four groups of ten rabbits each: group 1 (control), group 2 (subarachnoid hemorrhage), group 3 (erythropoietin), and group 4 (darbepoetin alpha). Recombinant human erythropoietin was administered at a dose of 1,000 U/kg intraperitoneally after the induction of subarachnoid hemorrhage and continued every 8 h up to 72 h. Darbepoetin alpha was administered at a single intraperitoneal dose of 30 μg/kg. Animals were killed 72 h after subarachnoid hemorrhage. Basilar artery cross-sectional areas, arterial wall thicknesses, hippocampal degeneration scores and biochemical analyses were measured in all groups.

Results

Both erythropoietin and darbepoetin alpha treatments were found to attenuate cerebral vasospasm and provide neuroprotection after subarachnoid hemorrhage in rabbits. Darbepoetin alpha revealed better morphometric and histopathological results than erythropoietin among experimental subarachnoid hemorrhage-induced vasospasm.

Conclusions

Our findings, for the first time, showed that darbepoetin alpha can prevent vasospasm and provides neuroprotection following experimental subarachnoid hemorrhage. Moreover, darbepoetin alpha showed better results when compared with erythropoietin.
Literature
2.
go back to reference Aladag MA, Turkoz Y, Parlakpinar H, Ozen H, Egri M, Unal SC (2009) Melatonin ameliorates cerebral vasospasm after experimental subarachnoidal haemorrhage correcting imbalance of nitric oxide levels in rats. Neurochem Res 34:1935–1944PubMedCrossRef Aladag MA, Turkoz Y, Parlakpinar H, Ozen H, Egri M, Unal SC (2009) Melatonin ameliorates cerebral vasospasm after experimental subarachnoidal haemorrhage correcting imbalance of nitric oxide levels in rats. Neurochem Res 34:1935–1944PubMedCrossRef
3.
go back to reference Alafaci C, Salpietro F, Grasso G, Sfacteria A, Passalacqua M, Morabito A, Tripodo E, Calapai G, Buemi M, Tomasello F (2000) Effect of recombinant human erythropoietin on cerebral ischemia following experimental subarachnoid hemorrhage. Eur J Pharmacol 406:219–225PubMedCrossRef Alafaci C, Salpietro F, Grasso G, Sfacteria A, Passalacqua M, Morabito A, Tripodo E, Calapai G, Buemi M, Tomasello F (2000) Effect of recombinant human erythropoietin on cerebral ischemia following experimental subarachnoid hemorrhage. Eur J Pharmacol 406:219–225PubMedCrossRef
4.
go back to reference Ayer RE, Zhang JH (2008) Oxidative stress in subarachnoid haemorrhage: significance in acute brain injury and vasospasm. Acta Neurochir Suppl 104:33–41PubMedCentralPubMedCrossRef Ayer RE, Zhang JH (2008) Oxidative stress in subarachnoid haemorrhage: significance in acute brain injury and vasospasm. Acta Neurochir Suppl 104:33–41PubMedCentralPubMedCrossRef
5.
go back to reference Banerjee D, Rodriguez M, Nag M, Adamson JW (2000) Exposure of endothelial cells to recombinant human erythropoietin induces nitric oxide synthase activity. Kidney Int 57:1895–1904PubMedCrossRef Banerjee D, Rodriguez M, Nag M, Adamson JW (2000) Exposure of endothelial cells to recombinant human erythropoietin induces nitric oxide synthase activity. Kidney Int 57:1895–1904PubMedCrossRef
6.
go back to reference Banks WA, Jumbe NL, Farrell CL, Niehoff ML, Heatherington AC (2004) Passage of erythropoietic agents across the blood-brain barrier: a comparison of human and murine erythropoietin and the analog darbepoetin alfa. Eur J Pharmacol 505:93–101PubMedCrossRef Banks WA, Jumbe NL, Farrell CL, Niehoff ML, Heatherington AC (2004) Passage of erythropoietic agents across the blood-brain barrier: a comparison of human and murine erythropoietin and the analog darbepoetin alfa. Eur J Pharmacol 505:93–101PubMedCrossRef
7.
go back to reference Belen D, Besalti O, Yiğitkanli K, Kösemehmetoğlu K, Simşek S, Bolay H (2007) Leflunomide prevents vasospasm secondary to subarachnoid haemorrhage. Acta Neurochir 149:1041–1047PubMedCrossRef Belen D, Besalti O, Yiğitkanli K, Kösemehmetoğlu K, Simşek S, Bolay H (2007) Leflunomide prevents vasospasm secondary to subarachnoid haemorrhage. Acta Neurochir 149:1041–1047PubMedCrossRef
8.
go back to reference Beleslin-Cokic BB, Cokic VP, Yu X, Weksler BB, Schechter AN, Noguchi CT (2004) Erythropoietin and hypoxia stimulate erythropoietin receptor and nitric oxide production by endothelial cells. Blood 104:2073–2080PubMedCrossRef Beleslin-Cokic BB, Cokic VP, Yu X, Weksler BB, Schechter AN, Noguchi CT (2004) Erythropoietin and hypoxia stimulate erythropoietin receptor and nitric oxide production by endothelial cells. Blood 104:2073–2080PubMedCrossRef
9.
go back to reference Braissant O, Gotoh T, Loup M, Mori M, Bachmann C (1999) L-arginine uptake, the citrulline-NO cycle and arginase II in the rat brain: an in situ hybridization study. Brain Res Mol Brain Res 70:231–241PubMedCrossRef Braissant O, Gotoh T, Loup M, Mori M, Bachmann C (1999) L-arginine uptake, the citrulline-NO cycle and arginase II in the rat brain: an in situ hybridization study. Brain Res Mol Brain Res 70:231–241PubMedCrossRef
10.
go back to reference Buemi M, Allegra A, Squadrito F, Buemi AL, Laganà A, Aloisi C, Frisina N (1993) Effects of intravenous administration of recombinant human erythropoietin in rats subject to hemorrhagic shock. Nephron 65:440–443PubMedCrossRef Buemi M, Allegra A, Squadrito F, Buemi AL, Laganà A, Aloisi C, Frisina N (1993) Effects of intravenous administration of recombinant human erythropoietin in rats subject to hemorrhagic shock. Nephron 65:440–443PubMedCrossRef
11.
go back to reference Buemi M, Grasso G, Corica F, Calapai G, Salpietro FM, Casuscelli T, Sfacteria A, Aloisi C, Alafaci C, Sturiale A, Frisina N, Tomasello F (2000) In vivo evidence that erythropoietin has a neuroprotective effect during subarachnoid hemorrhage. Eur J Pharmacol 392:31–34PubMedCrossRef Buemi M, Grasso G, Corica F, Calapai G, Salpietro FM, Casuscelli T, Sfacteria A, Aloisi C, Alafaci C, Sturiale A, Frisina N, Tomasello F (2000) In vivo evidence that erythropoietin has a neuroprotective effect during subarachnoid hemorrhage. Eur J Pharmacol 392:31–34PubMedCrossRef
12.
go back to reference Buga GM, Singh R, Pervin S, Rogers NE, Schmitz DA, Jenkinson CP, Cederbaum SD, Ignarro LJ (1996) Arginase activity in endothelial cells: inhibition by NG-hydroxy-L-arginine during high-output NO production. Am J Physiol 271:H1988–H19998PubMed Buga GM, Singh R, Pervin S, Rogers NE, Schmitz DA, Jenkinson CP, Cederbaum SD, Ignarro LJ (1996) Arginase activity in endothelial cells: inhibition by NG-hydroxy-L-arginine during high-output NO production. Am J Physiol 271:H1988–H19998PubMed
13.
go back to reference Chen G, Zhang S, Shi J, Ai J, Hang C (2009) Effects of recombinant human erythropoietin (rhEPO) on JAK2/STAT3 pathway and endothelial apoptosis in the rabbit basilar artery after subarachnoid hemorrhage. Cytokine 45:162–168PubMedCrossRef Chen G, Zhang S, Shi J, Ai J, Hang C (2009) Effects of recombinant human erythropoietin (rhEPO) on JAK2/STAT3 pathway and endothelial apoptosis in the rabbit basilar artery after subarachnoid hemorrhage. Cytokine 45:162–168PubMedCrossRef
14.
go back to reference Chinard FP (1952) Photometric estimation of proline and ornithine. J Biol Chem 199:91–95PubMed Chinard FP (1952) Photometric estimation of proline and ornithine. J Biol Chem 199:91–95PubMed
15.
go back to reference Clatterbuck RE, Gailloud P, Tierney T, Clatterbuck VM, Murphy KJ, Tamargo RJ (2005) Controlled release of a nitric oxide donor for the prevention of delayed cerebral vasospasm following experimental subarachnoid hemorrhage in nonhuman primates. J Neurosurg 103:745–751PubMedCrossRef Clatterbuck RE, Gailloud P, Tierney T, Clatterbuck VM, Murphy KJ, Tamargo RJ (2005) Controlled release of a nitric oxide donor for the prevention of delayed cerebral vasospasm following experimental subarachnoid hemorrhage in nonhuman primates. J Neurosurg 103:745–751PubMedCrossRef
16.
go back to reference Dahle LK, Hill EG, Holman RT (1962) The thiobarbituric acid reaction and the autoxidations of polyunsaturated fatty acid methyl esters. Arch Biochem Biophys 98:253–261PubMedCrossRef Dahle LK, Hill EG, Holman RT (1962) The thiobarbituric acid reaction and the autoxidations of polyunsaturated fatty acid methyl esters. Arch Biochem Biophys 98:253–261PubMedCrossRef
17.
go back to reference Durak I, Kavutcu M, Kaçmaz M, Avci A, Horasanli E, Dikmen B, Cimen MY, Oztürk HS (2001) Effects of isoflurane on nitric oxide metabolism and oxidant status of guinea pig myocardium. Acta Anaesthesiol Scand 45:119–122PubMedCrossRef Durak I, Kavutcu M, Kaçmaz M, Avci A, Horasanli E, Dikmen B, Cimen MY, Oztürk HS (2001) Effects of isoflurane on nitric oxide metabolism and oxidant status of guinea pig myocardium. Acta Anaesthesiol Scand 45:119–122PubMedCrossRef
18.
go back to reference Echigo R, Shimohata N, Karatsu K, Yano F, Kayasuga-Kariya Y, Fujisawa A, Ohto T, Kita Y, Nakamura M, Suzuki S, Mochizuki M, Shimizu T, Chung UI, Sasaki N (2012) Trehalose treatment suppresses inflammation, oxidative stress, and vasospasm induced by experimental subarachnoid hemorrhage. J Transl Med 10:80PubMedCentralPubMedCrossRef Echigo R, Shimohata N, Karatsu K, Yano F, Kayasuga-Kariya Y, Fujisawa A, Ohto T, Kita Y, Nakamura M, Suzuki S, Mochizuki M, Shimizu T, Chung UI, Sasaki N (2012) Trehalose treatment suppresses inflammation, oxidative stress, and vasospasm induced by experimental subarachnoid hemorrhage. J Transl Med 10:80PubMedCentralPubMedCrossRef
19.
go back to reference Edwards DH, Byrne JV, Griffith TM (1992) The effect of chronic subarachnoid hemorrhage on basal endothelium-derived relaxing factor activity in intrathecal cerebral arteries. J Neurosurg 76:830–837PubMedCrossRef Edwards DH, Byrne JV, Griffith TM (1992) The effect of chronic subarachnoid hemorrhage on basal endothelium-derived relaxing factor activity in intrathecal cerebral arteries. J Neurosurg 76:830–837PubMedCrossRef
21.
go back to reference Egrie JC, Dwyer E, Browne JK, Hitz A, Lykos MA (2003) Darbepoetin alfa has a longer circulating half-life and greater in vivo potency than recombinant human erythropoietin. Exp Hematol 31:290–299PubMedCrossRef Egrie JC, Dwyer E, Browne JK, Hitz A, Lykos MA (2003) Darbepoetin alfa has a longer circulating half-life and greater in vivo potency than recombinant human erythropoietin. Exp Hematol 31:290–299PubMedCrossRef
22.
go back to reference Grasso G, Buemi M, Alafaci C, Sfacteria A, Passalacqua M, Sturiale A, Calapai G, De Vico G, Piedimonte G, Salpietro FM, Tomasello F (2002) Beneficial effects of systemic administration of recombinant human erythropoietin in rabbits subjected to subarachnoid hemorrhage. Proc Natl Acad Sci U S A 99:5627–5631PubMedCentralPubMedCrossRef Grasso G, Buemi M, Alafaci C, Sfacteria A, Passalacqua M, Sturiale A, Calapai G, De Vico G, Piedimonte G, Salpietro FM, Tomasello F (2002) Beneficial effects of systemic administration of recombinant human erythropoietin in rabbits subjected to subarachnoid hemorrhage. Proc Natl Acad Sci U S A 99:5627–5631PubMedCentralPubMedCrossRef
23.
go back to reference Grasso G, Passalacqua M, Sfacteria A, Conti A, Morabito A, Mazzullo G, De VG, Buemi M, Macrì B, Tomasello F (2002) Does administration of recombinant human erythropoietin attenuate the increase of S-100 protein observed in cerebrospinal fluid after experimental subarachnoid hemorrhage? J Neurosurg 96:565–570PubMedCrossRef Grasso G, Passalacqua M, Sfacteria A, Conti A, Morabito A, Mazzullo G, De VG, Buemi M, Macrì B, Tomasello F (2002) Does administration of recombinant human erythropoietin attenuate the increase of S-100 protein observed in cerebrospinal fluid after experimental subarachnoid hemorrhage? J Neurosurg 96:565–570PubMedCrossRef
24.
25.
go back to reference Grasso G (2004) An overview of new pharmacological treatments for cerebrovascular dysfunction after experimental subarachnoid hemorrhage. Brain Res Brain Res Rev 44:49–63PubMedCrossRef Grasso G (2004) An overview of new pharmacological treatments for cerebrovascular dysfunction after experimental subarachnoid hemorrhage. Brain Res Brain Res Rev 44:49–63PubMedCrossRef
26.
go back to reference Grasso G (2001) Neuroprotective effect of recombinant human erythropoietin in experimental subarachnoid hemorrhage. J Neurosurg Sci 45:7–14PubMed Grasso G (2001) Neuroprotective effect of recombinant human erythropoietin in experimental subarachnoid hemorrhage. J Neurosurg Sci 45:7–14PubMed
27.
go back to reference Helbok R, Shaker E, Beer R, Chemelli A, Sojer M, Sohm F, Broessner G, Lackner P, Beck M, Zangerle A, Pfausler B, Thome C, Schmutzhard E (2012) High dose erythropoietin increases brain tissue oxygen tension in severe vasospasm after subarachnoid hemorrhage. BMC Neurol 12:32PubMedCentralPubMedCrossRef Helbok R, Shaker E, Beer R, Chemelli A, Sojer M, Sohm F, Broessner G, Lackner P, Beck M, Zangerle A, Pfausler B, Thome C, Schmutzhard E (2012) High dose erythropoietin increases brain tissue oxygen tension in severe vasospasm after subarachnoid hemorrhage. BMC Neurol 12:32PubMedCentralPubMedCrossRef
28.
go back to reference Hino A, Tokuyama Y, Weir B, Takeda J, Yano H, Bell GI, Macdonald RL (1996) Changes in endothelial nitric oxide synthase mRNA during vasospasm after subarachnoid hemorrhage in monkeys. Neurosurgery 39:562–567PubMed Hino A, Tokuyama Y, Weir B, Takeda J, Yano H, Bell GI, Macdonald RL (1996) Changes in endothelial nitric oxide synthase mRNA during vasospasm after subarachnoid hemorrhage in monkeys. Neurosurgery 39:562–567PubMed
29.
go back to reference Jelkmann W (1992) Erythropoietin: structure, control of production, and function. Physiol Rev 72:449–489PubMed Jelkmann W (1992) Erythropoietin: structure, control of production, and function. Physiol Rev 72:449–489PubMed
30.
go back to reference Kassell NF, Sasaki T, Colohan AR, Nazar G (1985) Cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Stroke 16:562–572PubMedCrossRef Kassell NF, Sasaki T, Colohan AR, Nazar G (1985) Cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Stroke 16:562–572PubMedCrossRef
31.
go back to reference Kertmen H, Gürer B, Yilmaz ER, Arikok AT, Demirci A, Gökyaprak SM, Sekerci Z (2012) The effect of thiocolchicoside on cerebral vasospasm following experimental subarachnoid hemorrhage in the rabbit. Acta Neurochir 154:1431–1436PubMedCrossRef Kertmen H, Gürer B, Yilmaz ER, Arikok AT, Demirci A, Gökyaprak SM, Sekerci Z (2012) The effect of thiocolchicoside on cerebral vasospasm following experimental subarachnoid hemorrhage in the rabbit. Acta Neurochir 154:1431–1436PubMedCrossRef
32.
go back to reference Kobayashi H, Hayashi M, Kobayashi S, Kabuto M, Handa Y, Kawano H, Ide H (1991) Cerebral vasospasm and vasoconstriction caused by endothelin. Neurosurgery 28:673–678PubMedCrossRef Kobayashi H, Hayashi M, Kobayashi S, Kabuto M, Handa Y, Kawano H, Ide H (1991) Cerebral vasospasm and vasoconstriction caused by endothelin. Neurosurgery 28:673–678PubMedCrossRef
33.
go back to reference Kolias AG, Sen J, Belli A (2009) Pathogenesis of cerebral vasospasm following aneurysmal subarachnoid hemorrhage: putative mechanisms and novel approaches. J Neurosci Res 87:1–11PubMedCrossRef Kolias AG, Sen J, Belli A (2009) Pathogenesis of cerebral vasospasm following aneurysmal subarachnoid hemorrhage: putative mechanisms and novel approaches. J Neurosci Res 87:1–11PubMedCrossRef
35.
go back to reference Li H, Meininger CJ, Hawker JR Jr, Haynes TE, Kepka-Lenhart D, Mistry SK, Morris SM Jr, Wu G (2001) Regulatory role of arginase I and II in nitric oxide, polyamine, and proline syntheses in endothelial cells. Am J Physiol Endocrinol Metab 280:E75–E82PubMed Li H, Meininger CJ, Hawker JR Jr, Haynes TE, Kepka-Lenhart D, Mistry SK, Morris SM Jr, Wu G (2001) Regulatory role of arginase I and II in nitric oxide, polyamine, and proline syntheses in endothelial cells. Am J Physiol Endocrinol Metab 280:E75–E82PubMed
36.
go back to reference Marbacher S, Fandino J, Kitchen ND (2010) Standard intracranial in vivo animal models of delayed cerebral vasospasm. Br J Neurosurg 24:415–434PubMedCrossRef Marbacher S, Fandino J, Kitchen ND (2010) Standard intracranial in vivo animal models of delayed cerebral vasospasm. Br J Neurosurg 24:415–434PubMedCrossRef
37.
go back to reference Markham A, Bryson HM (1995) Epoetin alfa. A review of its pharmacodynamic and pharmacokinetic properties and therapeutic use in nonrenal applications. Drugs 49:232–254PubMedCrossRef Markham A, Bryson HM (1995) Epoetin alfa. A review of its pharmacodynamic and pharmacokinetic properties and therapeutic use in nonrenal applications. Drugs 49:232–254PubMedCrossRef
38.
go back to reference Morishita E, Masuda S, Nagao M, Yasuda Y, Sasaki R (1997) Erythropoietin receptor is expressed in rat hippocampal and cerebral cortical neurons, and erythropoietin prevents in vitro glutamate-induced neuronal death. Neuroscience 76:105–116PubMedCrossRef Morishita E, Masuda S, Nagao M, Yasuda Y, Sasaki R (1997) Erythropoietin receptor is expressed in rat hippocampal and cerebral cortical neurons, and erythropoietin prevents in vitro glutamate-induced neuronal death. Neuroscience 76:105–116PubMedCrossRef
39.
go back to reference Murphy AM, Xenocostas A, Pakkiri P, Lee TY (2008) Hemodynamic effects of recombinant human erythropoietin on the central nervous system after subarachnoid hemorrhage: reduction of microcirculatory impairment and functional deficits in a rabbit model. J Neurosurg 109:1155–1164PubMedCrossRef Murphy AM, Xenocostas A, Pakkiri P, Lee TY (2008) Hemodynamic effects of recombinant human erythropoietin on the central nervous system after subarachnoid hemorrhage: reduction of microcirculatory impairment and functional deficits in a rabbit model. J Neurosurg 109:1155–1164PubMedCrossRef
40.
go back to reference Onoue H, Kaito N, Akiyama M, Tomii M, Tokudome S, Abe T (1995) Altered reactivity of human cerebral arteries after subarachnoid hemorrhage. J Neurosurg 83:510–515PubMedCrossRef Onoue H, Kaito N, Akiyama M, Tomii M, Tokudome S, Abe T (1995) Altered reactivity of human cerebral arteries after subarachnoid hemorrhage. J Neurosurg 83:510–515PubMedCrossRef
41.
go back to reference Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169PubMed Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169PubMed
42.
go back to reference Polin RS, Bavbek M, Shaffrey ME, Billups K, Bogaev CA, Kassell NF, Lee KS (1998) Detection of soluble E-selectin, ICAM-1, VCAM-1, and L-selectin in the cerebrospinal fluid of patients after subarachnoid hemorrhage. J Neurosurg 89:559–567PubMedCrossRef Polin RS, Bavbek M, Shaffrey ME, Billups K, Bogaev CA, Kassell NF, Lee KS (1998) Detection of soluble E-selectin, ICAM-1, VCAM-1, and L-selectin in the cerebrospinal fluid of patients after subarachnoid hemorrhage. J Neurosurg 89:559–567PubMedCrossRef
43.
go back to reference Ridnour LA, Sim JE, Hayward MA, Wink DA, Martin SM, Buettner GR, Spitz DR (2000) A spectrophotometric method for the direct detection and quantitation of nitric oxide, nitrite, and nitrate in cell culture media. Anal Biochem 281:223–229PubMedCrossRef Ridnour LA, Sim JE, Hayward MA, Wink DA, Martin SM, Buettner GR, Spitz DR (2000) A spectrophotometric method for the direct detection and quantitation of nitric oxide, nitrite, and nitrate in cell culture media. Anal Biochem 281:223–229PubMedCrossRef
44.
go back to reference Sadamoto Y, Igase K, Sakanaka M, Sato K, Otsuka H, Sakaki S, Masuda S, Sasaki R (1998) Erythropoietin prevents place navigation disability and cortical infarction in rats with permanent occlusion of the middle cerebral artery. Biochem Biophys Res Commun 253:26–32PubMedCrossRef Sadamoto Y, Igase K, Sakanaka M, Sato K, Otsuka H, Sakaki S, Masuda S, Sasaki R (1998) Erythropoietin prevents place navigation disability and cortical infarction in rats with permanent occlusion of the middle cerebral artery. Biochem Biophys Res Commun 253:26–32PubMedCrossRef
45.
go back to reference Sakanaka M, Wen TC, Matsuda S, Masuda S, Morishita E, Nagao M, Sasaki R (1998) In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci U S A 95:4635–4640PubMedCentralPubMedCrossRef Sakanaka M, Wen TC, Matsuda S, Masuda S, Morishita E, Nagao M, Sasaki R (1998) In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci U S A 95:4635–4640PubMedCentralPubMedCrossRef
46.
go back to reference Santhanam AV, Smith LA, Akiyama M, Rosales AG, Bailey KR, Katusic ZS (2005) Role of endothelial NO synthase phosphorylation in cerebrovascular protective effect of recombinant erythropoietin during subarachnoid hemorrhage-induced cerebral vasospasm. Stroke 36:2731–2737PubMedCrossRef Santhanam AV, Smith LA, Akiyama M, Rosales AG, Bailey KR, Katusic ZS (2005) Role of endothelial NO synthase phosphorylation in cerebrovascular protective effect of recombinant erythropoietin during subarachnoid hemorrhage-induced cerebral vasospasm. Stroke 36:2731–2737PubMedCrossRef
47.
go back to reference Seçkin H, Yigitkanli K, Besalti O, Kosemehmetoglu K, Ozturk E, Simsek S, Belen D, Bavbek M (2008) Lamotrigine attenuates cerebral vasospasm after experimental subarachnoid hemorrhage in rabbits. Surg Neurol 70:344–351PubMedCrossRef Seçkin H, Yigitkanli K, Besalti O, Kosemehmetoglu K, Ozturk E, Simsek S, Belen D, Bavbek M (2008) Lamotrigine attenuates cerebral vasospasm after experimental subarachnoid hemorrhage in rabbits. Surg Neurol 70:344–351PubMedCrossRef
48.
go back to reference Sirén AL, Fratelli M, Brines M, Goemans C, Casagrande S, Lewczuk P, Keenan S, Gleiter C, Pasquali C, Capobianco A, Mennini T, Heumann R, Cerami A, Ehrenreich H, Ghezzi P (2001) Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci U S A 98:4044–4049PubMedCentralPubMedCrossRef Sirén AL, Fratelli M, Brines M, Goemans C, Casagrande S, Lewczuk P, Keenan S, Gleiter C, Pasquali C, Capobianco A, Mennini T, Heumann R, Cerami A, Ehrenreich H, Ghezzi P (2001) Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci U S A 98:4044–4049PubMedCentralPubMedCrossRef
49.
go back to reference Springborg JB, Ma X, Rochat P, Knudsen GM, Amtorp O, Paulson OB, Juhler M, Olsen NV (2002) A single subcutaneous bolus of erythropoietin normalizes cerebral blood flow autoregulation after subarachnoid haemorrhage in rats. Br J Pharmacol 135:823–829PubMedCentralPubMedCrossRef Springborg JB, Ma X, Rochat P, Knudsen GM, Amtorp O, Paulson OB, Juhler M, Olsen NV (2002) A single subcutaneous bolus of erythropoietin normalizes cerebral blood flow autoregulation after subarachnoid haemorrhage in rats. Br J Pharmacol 135:823–829PubMedCentralPubMedCrossRef
50.
go back to reference Springborg JB, Møller C, Gideon P, Jørgensen OS, Juhler M, Olsen NV (2007) Erythropoietin in patients with aneurysmal subarachnoid haemorrhage: a double blind randomised clinical trial. Acta Neurochir 149:1089–1101PubMedCrossRef Springborg JB, Møller C, Gideon P, Jørgensen OS, Juhler M, Olsen NV (2007) Erythropoietin in patients with aneurysmal subarachnoid haemorrhage: a double blind randomised clinical trial. Acta Neurochir 149:1089–1101PubMedCrossRef
51.
go back to reference Tseng MY, Hutchinson PJ, Richards HK, Czosnyka M, Pickard JD, Erber WN, Brown S, Kirkpatrick PJ (2009) Acute systemic erythropoietin therapy to reduce delayed ischemic deficits following aneurysmal subarachnoid hemorrhage: a phase II randomized, double-blind, placebo-controlled trial. Clinical article. J Neurosurg 111:171–180PubMedCrossRef Tseng MY, Hutchinson PJ, Richards HK, Czosnyka M, Pickard JD, Erber WN, Brown S, Kirkpatrick PJ (2009) Acute systemic erythropoietin therapy to reduce delayed ischemic deficits following aneurysmal subarachnoid hemorrhage: a phase II randomized, double-blind, placebo-controlled trial. Clinical article. J Neurosurg 111:171–180PubMedCrossRef
52.
go back to reference Turner JD, Mammis A, Prestigiacomo CJ (2010) Erythropoietin for the treatment of subarachnoid hemorrhage: a review. World Neurosurg 73:500–507PubMedCrossRef Turner JD, Mammis A, Prestigiacomo CJ (2010) Erythropoietin for the treatment of subarachnoid hemorrhage: a review. World Neurosurg 73:500–507PubMedCrossRef
53.
go back to reference Ulusal I, Tari R, Ozturk G, Aycicek E, Aktar F, Kotil K, Bilge T, Kiriş T (2010) Dose-dependent ultrastructural and morphometric alterations after erythropoietin treatment in rat femoral artery vasospasm model. Acta Neurochir 152:2161–2166PubMedCrossRef Ulusal I, Tari R, Ozturk G, Aycicek E, Aktar F, Kotil K, Bilge T, Kiriş T (2010) Dose-dependent ultrastructural and morphometric alterations after erythropoietin treatment in rat femoral artery vasospasm model. Acta Neurochir 152:2161–2166PubMedCrossRef
54.
go back to reference Ustün ME, Duman A, Oğun CO, Vatansev H, Ak A (2001) Effects of nimodipine and magnesium sulfate on endogenous antioxidant levels in brain tissue after experimental head trauma. J Neurosurg Anesthesiol 13:227–232PubMedCrossRef Ustün ME, Duman A, Oğun CO, Vatansev H, Ak A (2001) Effects of nimodipine and magnesium sulfate on endogenous antioxidant levels in brain tissue after experimental head trauma. J Neurosurg Anesthesiol 13:227–232PubMedCrossRef
55.
go back to reference Vorkapic P, Bevan JA, Bevan RD (1991) Two indices of functional damage of the artery wall parallel the time course of irreversible narrowing in experimental vasospasm in the rabbit. Blood Vessels 28:179–182PubMed Vorkapic P, Bevan JA, Bevan RD (1991) Two indices of functional damage of the artery wall parallel the time course of irreversible narrowing in experimental vasospasm in the rabbit. Blood Vessels 28:179–182PubMed
56.
go back to reference Yilmaz ER, Kertmen H, Dolgun H, Gürer B, Sanli AM, Kanat MA, Arikok AT, Bahsi SY, Ergüder BI, Sekerci Z (2012) Effects of darbepoetin-α in spinal cord ischemia-reperfusion injury in the rabbit. Acta Neurochir 154:1037–1043PubMedCrossRef Yilmaz ER, Kertmen H, Dolgun H, Gürer B, Sanli AM, Kanat MA, Arikok AT, Bahsi SY, Ergüder BI, Sekerci Z (2012) Effects of darbepoetin-α in spinal cord ischemia-reperfusion injury in the rabbit. Acta Neurochir 154:1037–1043PubMedCrossRef
57.
go back to reference Zhang C, Hein TW, Wang W, Chang CI, Kuo L (2001) Constitutive expression of arginase in microvascular endothelial cells counteracts nitric oxide-mediated vasodilatory function. FASEB J 15:1264–1266PubMedCrossRef Zhang C, Hein TW, Wang W, Chang CI, Kuo L (2001) Constitutive expression of arginase in microvascular endothelial cells counteracts nitric oxide-mediated vasodilatory function. FASEB J 15:1264–1266PubMedCrossRef
58.
go back to reference Zhang J, Zhu Y, Zhou D, Wang Z, Chen G (2010) Recombinant human erythropoietin (rhEPO) alleviates early brain injury following subarachnoid hemorrhage in rats: possible involvement of Nrf2-ARE pathway. Cytokine 52:252–257PubMedCrossRef Zhang J, Zhu Y, Zhou D, Wang Z, Chen G (2010) Recombinant human erythropoietin (rhEPO) alleviates early brain injury following subarachnoid hemorrhage in rats: possible involvement of Nrf2-ARE pathway. Cytokine 52:252–257PubMedCrossRef
Metadata
Title
The comparative effects of recombinant human erythropoietin and darbepoetin-alpha on cerebral vasospasm following experimental subarachnoid hemorrhage in the rabbit
Authors
Hayri Kertmen
Bora Gürer
Erdal Resit Yilmaz
Ata Türker Arikok
Mehmet Ali Kanat
Berrin Imge Ergüder
Zeki Sekerci
Publication date
01-05-2014
Publisher
Springer Vienna
Published in
Acta Neurochirurgica / Issue 5/2014
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-014-2008-x

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