Sphenopalatine ganglion stimulation for vasospasm after experimental subarachnoid hemorrhage.

OBJECT Sphenopalatine ganglion stimulation activates perivascular vasodilatory nerves in the ipsilateral anterior circle of Willis. This experiment tested whether stimulation of the ganglion could reverse vasospasm and improve cerebral perfusion after subarachnoid hemorrhage (SAH) in monkeys. METHODS Thirteen cynomolgus monkeys underwent baseline angiography followed by creation of SAH by placement of autologous blood against the right intradural internal carotid artery, the middle cerebral artery (MCA), and the anterior cerebral artery. Seven days later, angiography was repeated, and the right sphenopalatine ganglion was exposed microsurgically. Angiography was repeated 15 minutes after exposure of the ganglion. The ganglion was stimulated electrically 3 times, and angiography was repeated during and 15 and 30 minutes after stimulation. Cerebral blood flow (CBF) was monitored using laser Doppler flowmetry, and intracranial pressure (ICP) was measured throughout. The protocol was repeated again. Evans blue was injected and the animals were killed. The brains were removed for analysis of water and Evans blue content and histology. RESULTS Subarachnoid hemorrhage was associated with significant vasospasm of the ipsilateral major cerebral arteries (23% ± 10% to 39% ± 4%; p < 0.05, paired t-tests). Exposure of the ganglion and sham stimulation had no significant effects on arterial diameters, ICP, or CBF (4 monkeys, ANOVA and paired t-tests). Sphenopalatine ganglion stimulation dilated the ipsilateral extracranial and intracranial internal carotid artery, MCA, and anterior cerebral artery compared with the contralateral arteries (9 monkeys, 7% ± 9% to 15% ± 19%; p < 0.05, ANOVA). There was a significant increase in ipsilateral CBF. Stimulation had no effect on ICP or brain histology. Brain water content did not increase but Evans blue content was significantly elevated in the MCA territory of the stimulated hemisphere. CONCLUSIONS Sphenopalatine ganglion stimulation decreased vasospasm and increased CBF after SAH in monkeys. This was associated with opening of the blood-brain barrier.

[1]  R. Keep,et al.  Effect of electrical stimulation of the cervical spinal cord on blood flow following subarachnoid hemorrhage. , 2008, Journal of neurosurgery.

[2]  M. Fisher,et al.  Stimulating Circle of Willis Nerve Fibers Preserves the Diffusion-Perfusion Mismatch in Experimental Stroke , 2007, Stroke.

[3]  M. Lauritzen,et al.  Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. , 2006, Brain : a journal of neurology.

[4]  D. Graham,et al.  Thromboembolism and Delayed Cerebral Ischemia after Subarachnoid Hemorrhage: An Autopsy Study , 2006, Neurosurgery.

[5]  D. Yarnitsky,et al.  Reversal of cerebral vasospasm by sphenopalatine ganglion stimulation in a dog model of subarachnoid hemorrhage. , 2005, Surgical neurology.

[6]  H Hunt Batjer,et al.  Prediction of Cerebral Vasospasm in Patients Presenting with Aneurysmal Subarachnoid Hemorrhage: A Review , 2005, Neurosurgery.

[7]  M. Fujimiya,et al.  Increased BBB permeability by parasympathetic sphenopalatine ganglion stimulation in dogs , 2004, Brain Research.

[8]  R. Keep,et al.  Spinal cord stimulation reducing infarct volume in a model of focal cerebral ischemia in rats. , 2003, Journal of Neurosurgery.

[9]  E. Golanov,et al.  Electrical stimulation of cerebellar fastigial nucleus protects rat brain, in vitro, from staurosporine‐induced apoptosis , 2001, Journal of neurochemistry.

[10]  E. Golanov,et al.  Stimulation of the subthalamic vasodilator area and fastigial nucleus independently protects the brain against focal ischemia , 2001, Brain Research.

[11]  R. Macdonald,et al.  Vasospasm in Monkeys Resolves Because of Loss of and Encasement of Subarachnoid Blood Clot , 2001, Stroke.

[12]  N. Toda,et al.  Preganglionic and Postganglionic Neurons Responsible for Cerebral Vasodilation Mediated by Nitric Oxide in Anesthetized Dogs , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[13]  T. Tanaka,et al.  Cerebral vasodilatation induced by stimulation of the pterygopalatine ganglion and greater petrosal nerve in anesthetized monkeys , 2000, Neuroscience.

[14]  E. Golanov,et al.  Neuroprotective electrical stimulation of cerebellar fastigial nucleus attenuates expression of periinfarction depolarizing waves (PIDs) and inhibits cortical spreading depression , 1999, Brain Research.

[15]  E. Golanov,et al.  Brief electrical stimulation of cerebellar fastigial nucleus conditions long-lasting salvage from focal cerebral ischemia: conditioned central neurogenic neuroprotection , 1998, Brain Research.

[16]  P. Goadsby,et al.  Cerebral vasodilatation in the cat involves nitric oxide from parasympathetic nerves , 1996, Brain Research.

[17]  C. Owman,et al.  Origins and Pathways of Choline Acetyltransferase—Positive Parasympathetic Nerve Fibers to Cerebral Vessels in Rat , 1990, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[18]  P. Goadsby,et al.  Sphenopalatine ganglion stimulation increases regional cerebral blood flow independent of glucose utilization in the cat , 1990, Brain Research.

[19]  E. Mackenzie,et al.  Acetylcholine and Vasoactive Intestinal Peptide in Cerebral Blood Vessels: Effect of Extirpation of the Sphenopalatine Ganglion , 1989, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[20]  E. Mackenzie,et al.  Effect of Stimulation of the Sphenopalatine Ganglion on Cortical Blood Flow in the Rat , 1988, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[21]  Babak Shahian Jahromi,et al.  Magnesium and experimental vasospasm. , 2004, Journal of neurosurgery.

[22]  F. Sundler,et al.  VIP (vasoactive intestinal polypeptide)-containing nerves of intracranial arteries in mammals , 2004, Cell and Tissue Research.

[23]  F. Tomasello,et al.  Time-Course of Blood-Brain Barrier Permeability Changes After Experimental Subarachnoid Haemorrhage , 2000, Acta Neurochirurgica.

[24]  N. Toda,et al.  Impairment by damage of the pterygopalatine ganglion of nitroxidergic vasodilator nerve function in canine cerebral and retinal arteries. , 1993, Circulation research.

[25]  T. Trojanowski.  Early effects of experimental arterial subarachnoid haemorrhage on the cerebral circulation part II: Regional cerebral blood flow and cerebral microcirculation after experimental subarachnoid haemorrhage , 1984, Acta neurochirurgica.