Stimulation of the sphenopalatine Ganglion induces reperfusion and blood-brain barrier protection in the Photothrombotic stroke model

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Levi, Haviv ^a   Schoknecht, Karl ^b   Prager, Ofer ^a   Chassidim, Yoash ^a   Weissberg, Itai ^a   Serlin, Yonatan ^a   Friedman, Alon ^a,b  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; BRAIN ISCHEMIA; CONTROLLED STUDY; ELECTROCORTICOGRAPHY; ELECTRODE; FLUORESCENCE ANGIOGRAPHY; GANGLION; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LASER DOPPLER FLOWMETRY; MALE; NONHUMAN; PTERYGOPALATINE GANGLION; QUANTITATIVE ANALYSIS; RAT; REPERFUSION; SENSORIMOTOR CORTEX; STROKE; VASODILATATION;

ANIMALS; BLOOD-BRAIN BARRIER; ELECTRIC STIMULATION; GANGLIA, PARASYMPATHETIC; MALE; RATS; RATS, SPRAGUE-DAWLEY; STROKE;

EID: 84862665619     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039636     Document Type: Article

References (42)

1. Ginsberg MD, (1997) The new language of cerebral ischemia. Ajnr American Journal Of Neuroradiology 18: 1435-1445.
2. Dirnagl U, Iadecola C, Moskowitz MA, (1999) Pathobiology of ischaemic stroke: an integrated view. Trends in Neurosciences 22: 391-397. Available http://www.ncbi.nlm.nih.gov/pubmed/10441299.
3. Kastrup A, Engelhorn T, Beaulieu C, de Crespigny A, Moseley ME, (1999) Dynamics of cerebral injury, perfusion, and blood-brain barrier changes after temporary and permanent middle cerebral artery occlusion in the rat. Journal of the neurological sciences 166: 91-99. Available:http://www.jns-journal.com/article/S0022-510X(99)00121-5/abstract. Accessed 21 February 2012.
4. Shlosberg D, Benifla M, Kaufer D, Friedman A, (2010) Blood-brain barrier breakdown as a therapeutic target in traumatic brain injury. Nature reviews Neurology 6: 393-403. Available http://www.ncbi.nlm.nih.gov/pubmed/20551947.
5. Smith WS, Sung G, Starkman S, Saver JL, Kidwell CS, et al. (2005) Safety and efficacy of mechanical embolectomy in acute ischemic stroke: results of the MERCI trial. Stroke 36: 1432-1438. Available http://www.ncbi.nlm.nih.gov/pubmed/15961709.
6. Zauner A, Daugherty WP, Bullock MR, Warner DS, (2002) Brain oxygenation and energy metabolism: part I-biological function and pathophysiology. Neurosurgery 51: 289-301; discussion 302.
7. Reeves MJ, Arora S, Broderick JP, Frankel M, Heinrich JP, et al. (2005) Acute stroke care in the US: results from 4 pilot prototypes of the Paul Coverdell National Acute Stroke Registry. Stroke: A Journal of Cerebral Circulation 36: 1232-1240. Available http://www.ncbi.nlm.nih.gov/pubmed/15890989.
8. Khurana D, Kaul S, Bornstein NM, (2009) Implant for augmentation of cerebral blood flow trial 1: a pilot study evaluating the safety and effectiveness of the Ischaemic Stroke System for treatment of acute ischaemic stroke. International journal of stroke?: official journal of the International Stroke Society 4: 480-485. Available:http://www.ncbi.nlm.nih.gov/pubmed/19930060. Accessed 11 May 2012.
9. Ayajiki K, Fujioka H, Shinozaki K, Okamura T, (2005) Effects of capsaicin and nitric oxide synthase inhibitor on increase in cerebral blood flow induced by sensory and parasympathetic nerve stimulation in the rat. Journal of Applied Physiology 98: 1792-1798. Available http://www.ncbi.nlm.nih.gov/pubmed/15626754.
10. Seylaz J, Hara H, Pinard E, Mraovitch S, MacKenzie ET, et al. (1988) Effect of stimulation of the sphenopalatine ganglion on cortical blood flow in the rat. Journal of cerebral blood flow and metabolism official journal of the International Society of Cerebral Blood Flow and Metabolism 8: 875-878.
11. Suzuki N, Hardebo JE, Kåhrström J, Owman C, (1990) Selective electrical stimulation of postganglionic cerebrovascular parasympathetic nerve fibers originating from the sphenopalatine ganglion enhances cortical blood flow in the rat. Journal of cerebral blood flow and metabolism official journal of the International Society of Cerebral Blood Flow and Metabolism 10: 383-391.
12. Toda N, Tanaka T, Ayajiki K, Okamura T, (2000) Cerebral vasodilatation induced by stimulation of the pterygopalatine ganglion and greater petrosal nerve in anesthetized monkeys. Neuroscience 96: 393-398. Available http://www.ncbi.nlm.nih.gov/pubmed/10683579.
13. Yarnitsky D, Lorian A, Shalev A, Zhang Z-D, Takahashi M, et al. (2005) Reversal of cerebral vasospasm by sphenopalatine ganglion stimulation in a dog model of subarachnoid hemorrhage. Surgical Neurology 64: 5-11; discussion 11. Available http://www.ncbi.nlm.nih.gov/pubmed/15993169.
14. Yarnitsky D, Gross Y, Lorian A, Shalev A, Lamensdorf I, et al. (2004) Blood-brain barrier opened by stimulation of the parasympathetic sphenopalatine ganglion: a new method for macromolecule delivery to the brain. Journal Of Neurosurgery 101: 303-309. Available http://www.ncbi.nlm.nih.gov/pubmed/15309923.
15. Henninger N, Fisher M, (2007) Stimulating circle of Willis nerve fibers preserves the diffusion-perfusion mismatch in experimental stroke. Stroke: A Journal of Cerebral Circulation 38: 2779-2786. Available http://www.ncbi.nlm.nih.gov/pubmed/17761922.
16. Diansan S, Shifen Z, Zhen G, Heming W, Xiangrui W, (2010) Resection of the nerves bundle from the sphenopalatine ganglia tend to increase the infarction volume following middle cerebral artery occlusion. Neurological sciences official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology 31: 431-435.
17. Seiffert E, Dreier JP, Ivens S, Bechmann I, Tomkins O, et al. (2004) Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. Journal of Neuroscience 24: 7829-7836. Available http://www.ncbi.nlm.nih.gov/pubmed/15356194.
18. Watson BD, Dietrich WD, Busto R, Wachtel MS, Ginsberg MD, (1985) Induction of reproducible brain infarction by photochemically initiated thrombosis. Annals of Neurology 17: 497-504. Available http://www.ncbi.nlm.nih.gov/pubmed/4004172.
19. Dirnagl U, Kaplan B, Jacewicz M, Pulsinelli W, (1989) Continuous measurement of cerebral cortical blood flow by laser-Doppler flowmetry in a rat stroke model. Journal of cerebral blood flow and metabolism official journal of the International Society of Cerebral Blood Flow and Metabolism 9: 589-596. Available http://www.ncbi.nlm.nih.gov/pubmed/2674168.
20. Prager O, Chassidim Y, Klein C, Levi H, Shelef I, et al. (2010) Dynamic in vivo imaging of cerebral blood flow and blood-brain barrier permeability. NeuroImage 49: 337-344. Available http://www.ncbi.nlm.nih.gov/pubmed/19682584.
21. Williams P, White A, Ferraro D, Clark S, Staley K, et al. (2006) The use of radiotelemetry to evaluate electrographic seizures in rats with kainate-induced epilepsy. Journal of Neuroscience Methods 155: 39-48. Available http://www.ncbi.nlm.nih.gov/pubmed/16564574.
22. Ivens S, Kaufer D, Flores LP, Bechmann I, Zumsteg D, et al. (2007) TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain: A journal of neurology 130: 535-547. Available http://www.ncbi.nlm.nih.gov/pubmed/17121744.
23. O'Donnell ME, Lam TI, Tran L, Anderson SE, (2004) The role of the blood-brain barrier Na-K-2Cl cotransporter in stroke. Adamantiades Behcet'S Disease 559: 67-75. Available http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18727228.
24. Stoll G, Kleinschnitz C, Meuth SG, Braeuninger S, Ip CW, et al. (2009) Transient widespread blood-brain barrier alterations after cerebral photothrombosis as revealed by gadofluorine M-enhanced magnetic resonance imaging. Journal of cerebral blood flow and metabolism official journal of the International Society of Cerebral Blood Flow and Metabolism 29: 331-341. Available http://www.ncbi.nlm.nih.gov/pubmed/18957988.
25. Marchi N, Angelov L, Masaryk T, Fazio V, Granata T, et al. (2007) Seizure-promoting effect of blood-brain barrier disruption. Epilepsia 48: 732-742. Available http://www.ncbi.nlm.nih.gov/pubmed/17319915.
26. Friedman A, Kaufer D, Heinemann U, (2009) Blood-brain barrier breakdown-inducing astrocytic transformation: Novel targets for the prevention of epilepsy. Epilepsy Research. Available http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19362806.
27. Seylaz J, Hara H, Pinard E, Mraovitch S, MacKenzie ET, et al. (1988) Effect of stimulation of the sphenopalatine ganglion on cortical blood flow in the rat. Journal of cerebral blood flow and metabolism?: official journal of the International Society of Cerebral Blood Flow and Metabolism 8: 875-878. Available:http://www.ncbi.nlm.nih.gov/pubmed/3192652. Accessed 11 May 2012.
28. Bar-Shir A, Shemesh N, Nossin-Manor R, Cohen Y, (2010) Late stimulation of the sphenopalatine-ganglion in ischemic rats: improvement in N-acetyl-aspartate levels and diffusion weighted imaging characteristics as seen by MR. Journal of Magnetic Resonance Imaging 31: 1355-1363. Available http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=20512887.
29. Matta BF, Heath KJ, Tipping K, Summors AC, (1999) Direct cerebral vasodilatory effects of sevoflurane and isoflurane. Anesthesiology 91: 677-680. Available:http://www.ncbi.nlm.nih.gov/pubmed/10485778. Accessed 11 May 2012.
30. Takahashi M, Zhang Z-D, Macdonald RL, (2011) Sphenopalatine ganglion stimulation for vasospasm after experimental subarachnoid hemorrhage. Journal of neurosurgery 114: 1104-1109. Available:http://thejns.org/doi/full/10.3171/2010.6.JNS091525. Accessed 11 May 2012.
31. Vasquez J, Purves MJ, (1979) The cholinergic pathway to cerebral blood vessels. I. Morphological studies. Pflügers Archiv?: European journal of physiology 379: 157-163. Available:http://www.ncbi.nlm.nih.gov/pubmed/571110. Accessed 11 May 2012.
32. Yarnitsky D, Gross Y, Lorian A, Shalev A, Shorer S, et al. (2004) Increased BBB permeability by parasympathetic sphenopalatine ganglion stimulation in dogs. Brain research 1018: 236-240. Available:http://dx.doi.org/10.1016/j.brainres.2004.05.103. Accessed 11 May 2012.
33. Tétrault S, Chever O, Sik A, Amzica F, (2008) Opening of the blood-brain barrier during isoflurane anaesthesia. The European journal of neuroscience 28: 1330-1341. Available:http://www.ncbi.nlm.nih.gov/pubmed/18973560. Accessed 20 April 2012.
34. Cacheaux LP, Ivens S, David Y, Lakhter AJ, Bar-Klein G, et al. (2009) Transcriptome profiling reveals TGF-beta signaling involvement in epileptogenesis. Journal of Neuroscience 29: 8927-8935. Available http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2875073&tool=pmcentrez&rendertype=abstract.
35. David Y, Cacheaux LP, Ivens S, Lapilover E, Heinemann U, et al. (2009) Astrocytic dysfunction in epileptogenesis: consequence of altered potassium and glutamate homeostasis? Journal of Neuroscience 29: 10588-10599.
36. Tomkins O, Friedman O, Ivens S, Reiffurth C, Major S, et al. (2007) Blood-brain barrier disruption results in delayed functional and structural alterations in the rat neocortex. Neurobiology of Disease 25: 367-377. Available http://www.ncbi.nlm.nih.gov/pubmed/17188501.
37. Zlokovic BV, (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57: 178-201. Available http://www.ncbi.nlm.nih.gov/pubmed/18215617.
38. Bang OY, Buck BH, Saver JL, Alger JR, Yoon SR, et al. (2007) Prediction of hemorrhagic transformation after recanalization therapy using T2*-permeability magnetic resonance imaging. Annals of Neurology 62: 170-176. Available http://www.ncbi.nlm.nih.gov/pubmed/17683090.
39. Dohmen C, Sakowitz OW, Fabricius M, Bosche B, Reithmeier T, et al. (2008) Spreading depolarizations occur in human ischemic stroke with high incidence. Annals of neurology 63: 720-728. Available:http://www.ncbi.nlm.nih.gov/pubmed/18496842. Accessed 1 March 2012.
40. Dreier JP, (2011) The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nature medicine 17: 439-447. Available:http://dx.doi.org/10.1038/nm.2333. Accessed 9 March 2012.
41. Dreier JP, Major S, Pannek H-W, Woitzik J, Scheel M, et al. (2012) Spreading convulsions, spreading depolarization and epileptogenesis in human cerebral cortex. Brain?: a journal of neurology 135: 259-275. Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3267981&tool=pmcentrez&rendertype=abstract. Accessed 1 April 2012.
42. Drenckhahn C, Winkler MKL, Major S, Scheel M, Kang E-J, et al. (2012) Correlates of spreading depolarization in human scalp electroencephalography. Brain?: a journal of neurology 135: 853-868. Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3286336&tool=pmcentrez&rendertype=abstract. Accessed 15 March 2012.