Is there a role for vagus nerve stimulation therapy as a treatment of traumatic brain injury?

British Journal of Neurosurgery

Volumn 26, Issue 3, 2012, Pages 316-320

  Kumaria, Ashwin ^a   Tolias, Christos M ^b  

^a SOUTHAMPTON GENERAL HOSPITAL   (United Kingdom)

^b KING S COLLEGE HOSPITAL   (United Kingdom)

Author keywords

Neuromodulation; Neuroprotection; Neurosurgery; Neurotrauma; Traumatic brain injury; Vagus nerve stimulation

Indexed keywords

GLUTAMIC ACID;

ANTIINFLAMMATORY ACTIVITY; BRAIN CORTEX; BRAIN EDEMA; COGNITION; DEPOLARIZATION; DISEASE MODEL; EXCITOTOXICITY; EXPERIMENTAL RAT; HIPPOCAMPUS; INTRACRANIAL PRESSURE; MEDLINE; MOTOR PERFORMANCE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; REVIEW; SEIZURE; TRAUMATIC BRAIN INJURY; UPREGULATION; VAGUS NERVE STIMULATION;

ANIMALS; BRAIN INJURIES; ENCEPHALITIS; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; INTRACRANIAL HYPERTENSION; NEURAL STEM CELLS; NEURONAL PLASTICITY; NOREPINEPHRINE; RATS; SYNAPSES; VAGUS NERVE STIMULATION;

EID: 84861643497     PISSN: 02688697     EISSN: 1360046X     Source Type: Journal    
DOI: 10.3109/02688697.2012.663517     Document Type: Review

References (70)

1. Tolias CM. In vitro models of neurotrauma. B r J Neurosurg 2008;22:200-6.
2. A rundine M, Aarts M, Lau A, Tymianski M. Vulnerability of central neurons to secondary insults after in vitro mechanical stretch . J Neurosci 2004;24:8106-23.
3. B en-Menachem E. Vagus-nerve stimulation for the treatment of epilepsy. Lancet Neurol 2002;1:477-82.
4. Koo B. EEG changes with vagus nerve stimulation. J Clin Neurophysiol 2001;18:434-41.
5. Hammond EJ, Uthman BM, Wilder BJ, Ben-Menachem E, Hamberger A, Hedner T, Ekman R. Neurochemical eff ects of vagus nerve stimulation in humans. Brain Res 1992;583:300-3.
6. Ben-Menachem E, Hamberger A, Hedner T, e t al . Eff ects of vagus nerve stimulation on amino acids and other metabolites in the CSF of patients with partial seizures. Epilepsy Res 1995;20:221-7.
7. M arangell LB, Martinez M, Jurdi RA, Zboyan H. Neurostimulation therapies in depression: a review of new modalities. Acta Psychiatr Scand 2007;116:174-81.
8. P ark MC, Goldman MA, Carpenter LL, Price LH, Friehs GM. Vagus nerve stimulation for depression: rationale, anatomical and physiological basis of effi cacy and future prospects. Acta Neurochir Suppl 2007;97:407-16.
9. Sjögren MJ, Hellström PT, Jonsson MA, Runnerstam M, Silander HC, Ben-Menachem E. Cognition-enhancing eff ect of vagus nerve stimulation in patients with Alzheimer's disease: a pilot study. J Clin Psychiatry 2002;63:972-80.
10. M errill CA, Jonsson MA, Minthon L, e t al. Vagus nerve stimulation in patients with Alzheimer's disease: Additional follow-up results of a pilot study through 1 year. J Clin Psychiatry 2006;67:1171-8.
11. Smith DC, Modglin AA, Roosevelt RW, Neese SL, Jensen RA, Browning RA, Clough RW. Electrical stimulation of the vagus nerve enhances cognitive and motor recovery following moderate fl uid percussion injury in the rat. J Neurotrauma 2005;22: 1485-502.
12. Smith DC, Tan AA, Duke A, Neese SL, Clough RW, Browning RA, Jensen RA. Recovery of function after vagus nerve stimulation initiated 24 hours after fl uid percussion brain injury. J Neurotrauma 2006;23:1549-60.
13. Neese SL, Sherill LK, Tan AA, Roosevelt RW, Browning RA, Smith DC, Duke A, Clough RW. Vagus nerve stimulation may protect GABAergic neurons following traumatic brain injury in rats: An immunocytochemical study. Brain Res 2007;1128:157-63.
14. Clough RW, Neese SL, Sherill LK, Tan AA, Duke A, Roosevelt RW, Browning RA, Smith DC. Cortical edema in moderate fl uid percussion brain injury is attenuated by vagus nerve stimulation. Neuroscience 2007;147:286-93.
15. T akigawa M, Mogenson GJ. A study of inputs to antidromically identifi ed neurons of the locus coeruleus. Brain Res 1977;135: 217-30.
16. G roves DA, Brown VJ. Vagal nerve stimulation: a review of its applications and potential mechanisms that mediate its clinical eff ects. Neurosci Biobehav Rev 2005;29:493-500.
17. R oosevelt RW, Smith DC, Clough RW, Jensen RA, Browning RA. Increased extracellular concentrations of norepinephrine in cortex and hippocampus following vagus nerve stimulation in the rat. Brain Res 2006;1119:124-32.
18. N aritoku DK, Terry WJ, Helfert RH. Regional induction of fos immunoreactivity in the brain by anticonvulsant stimulation of the vagus nerve. Epilepsy Res 1995;22:53-62.
19. K rahl SE, Clark KB, Smith DC, Browning RA. Locus coeruleus lesions suppress the seizure-attenuating eff ects of vagus nerve stimulation. Epilepsia 1998;39:709-14.
20. F eeney DM, Sutton RL. Pharmacotherapy for recovery of function after brain injury. Crit Rev Neurobiol 1987;3:135-97.
21. G ladstone DJ, Black SE. Enhancing recovery after stroke with noradrenergic pharmacotherapy: a new frontier? Can J Neurol Sci 2000;27:97-105.
22. M cIntosh TK. Novel pharmacologic therapies in the treatment of experimental traumatic brain injury: a review. J Neurotrauma 1993;10:215-61.
23. F eeney DM, Hovda DA. Reinstatement of binocular depth perception by amphetamine and visual experience after visual cortex ablation. Brain Res 1985;342:352-6.
24. F eeney DM, Hovda DA. Amphetamine and apomorphine restore tactile placing after motor cortex injury in the cat. Psychopharmacology (Berl) 1983;79:67-71.
25. S utton RL, Hovda DA, Feeney DM. Amphetamine accelerates recovery of locomotor function following bilateral frontal cortex ablation in cats. Behav Neurosci 1989;103:837-41.
26. H ovda DA, Fenney DM. Amphetamine wiThexperience promotes recovery of locomotor function after unilateral frontal cortex injury in the cat. Brain Res 1984;298:358-61.
27. B oyeson MG, Feeney DM. Intraventricular norepinephrine facilitates motor recovery following sensorimotor cortex injury. Pharmacol Biochem Behav 1990;35:497-501.
28. F eeney DM, Westerberg VS. Norepinephrine and brain damage: alpha noradrenergic pharmacology alters functional recovery after cortical trauma. Can J Psychol 1990;44:233-52.
29. K asamatsu T, Pettigrew JD. Depletion of brain catecholamines: failure of ocular dominance shift after monocular occlusion in kittens. Science 1976;194:206-09.
30. K ikuchi K, Nishino K, Ohyu H. Increasing CNS norepinephrine levels by the precursor L-DOPS facilitates beam-walking recovery after sensorimotor cortex ablation in rats. Brain Res 2000;860: 130-5.
31. C risostomo EA, Duncan PW, Propst M, Dawson DV, Davis JN. Evidence that amphetamine with physical therapy promotes recovery of motor function in stroke patients. Ann Neurol 1988;23:94-7.
32. V espa PM, McArthur DL, Xu Y, e t al. Nonconvulsive seizures after traumatic brain injury are associated with hippocampal atrophy. Neurology 2010;75:792-8.
33. L auritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ. Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab 2011;31:17-35.
34. S trong AJ, Dardis R. Depolarisation phenomena in traumatic and ischaemic brain injury. Adv Tech Stand Neurosurg 2005;30:3-49.
35. S trong AJ, Hartings JA, Dreier JP. Cortical spreading depression: an adverse but treatable factor in intensive care? Curr Opin Crit Care 2007;13:126-33.
36. T akano T, Tian GF, Peng W, e t al. Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 2007;10:754-62.
37. K umaria A, Tolias CM. Normobaric hyperoxia therapy for traumatic brain injury and stroke: a review. Br J Neurosurg 2009;23:576-84.
38. F abricius M, Fuhr S, Willumsen L, e t al. Association of seizures with cortical spreading depression and peri-infarct depolarisations in the acutely injured human brain. Clin Neurophysiol 2008;119:1973-84.
39. W illmore LJ. Antiepileptic drugs and neuroprotection: current status and future roles. Epilepsy Behav 2005;7:S25-8.
40. M artins-Ferreira H, Nedergaard M, Nicholson C. Perspectives on spreading depression. Brain Res Brain Res Rev 2000;32:215-34.
41. S omjen GG. Mechanisms of spreading depression and hypoxic spread ing depression-like depolarization. Physiol Rev 2001;81:1065-96.
42. Tian GF, Azmi H, Takano T, et al. . An astrocytic basis of epilepsy. Nat Med 2005;11:973-81.
43. Guthrie PB, Knappenberger J, Segal M, Bennett MV, Charles AC, Kater SB. ATP released from astrocytes mediates glial calcium waves. J Neurosci 1999;19:520-8.
44. Kumaria A, Tolias CM, Burnstock G. ATP signalling in epilepsy. Purinergic Signal 2008;4:339-46.
45. R aghupathi R. Cell death mechanisms following traumatic brain injury. Brain Pathol 2004;14:215-22.
46. Ikonomidou C, Turski L. Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injury? Lancet Neurol 2002;1:383-6.
47. Kalia LV, Kalia SK, Salter MW. NMDA receptors in clinical neurology: excitatory times ahead. Lancet Neurol 2008;7:742-55.
48. Grady MS, Jane JA, Steward O. Synaptic reorganization within the human central nervous system following injury. J Neurosurg 1989;71:534-7.
49. Scheff SW, Price DA, Hicks RR, Baldwin SA, Robinson S, Brackney C. Synaptogenesis in the hippocampal CA1 field following traumatic brain injury. J Neurotrauma 2005;22:719-32.
50. Carmichael ST. Plasticity of cortical projections after stroke. Neuroscientist 2003;9:64-75.
51. M uller D, Nikonenko I, Jourdain P, Alberi S. LTP, memory and structural plasticity. Curr Mol Med 2002;2:605-11.
52. Zuo Y, Smith DC, Jensen RA. Vagus nerve stimulation potentiates hippocampal LTP in freely-moving rats. Physiol Behav 2007;90:583-9.
53. Eriksson PS, Perfi lieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. Neurogenesis in the adult human hippocampus. Nat Med 1998;4:1313-17.
54. Sanai N, Tramontin AD, Quiñones-Hinojosa A, e t al . Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004;427:740-4.
55. C urtis MA, Kam M, Nannmark U, e t al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007;315:1243-9.
56. D ash PK, Mach SA, Moore AN. Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury. J Neurosci Res 2001;63:313-19.
57. L indvall O, Kokaia Z. Stem cells for the treatment of neurological disorders. Nature 2006;441:1094-6.
58. Revesz D, Tjernstrom M, Ben-Menachem E, Th orlin T. Eff ects of vagus nerve stimulation on rat hippocampal progenitor proliferation. Exp Neurol 2008;214:259-65.
59. Toda H, Hamani C, Fawcett AP, Hutchison WD, Lozano AM. The regulation of adult rodent hippocampal neurogenesis by deep brain stimulation. J Neurosurg 2008;108:132-8.
60. Tubbs RS, Wellons JC 3rd, Blount JP, Oakes WJ. Left-sided vagus nerve stimulation decreases intracranial pressure without resultant bradycardia in the pig: a potential therapeutic modality for humans. Childs Nerv Syst 2004;20:309-12.
61. Pettorossi VE, Di Rocco C, Caldarelli M, Mancinelli R, Velardi F. Infl uences of phasic changes in systemic blood pressure on intracranial pressure. Eur Neurol 1978;17:216-25.
62. P avlov VA, Tracey KJ. The cholinergic anti-infl ammatory pathway. Brain Behav Immun 2005;19:493-9.
63. Wang H, Yu M, Ochani M, e t al Nicotinic acetylcholine receptor alph 7 subunit is an essential regulator of infl ammation. Nature 2003 ;421 :384-8.
64. Rothwell N. Interleukin-1 and neuronal injury: mechanisms, modifi cation, and therapeutic potential. Brain Behav Immun 2003;17:152-7.
65. B ansal V, Ryu SY, Lopez N, e t al . Vagal stimulation modulates infl ammation through a ghrelin mediated mechanism in traumatic brain injury. Infl ammation 2012;35:214-20.
66. Bansal V, Costantini T, Ryu SY, et al. . Stimulating the central nervous system to prevent intestinal dysfunction after traumatic brain injury. J Trauma 2010;68:1059-64.
67. K ox M, Pompe JC, Pickkers P, Hoedemaekers CW, van Vugt AB, van der Hoeven Jg. Increased vagal tone accounts for the observed immune paralysis in patients with traumatic brain injury. Neurology 2008;70:480-5.
68. Unterberg AW, Stover J, Kress B, Kiening KL. Edema and brain trauma. Neuroscience 2004;129:1021-9.
69. Ay I, Lu J, Ay H, Gregory Sorensen A. Vagus nerve stimulation reduces infarct size in rat focal cerebral ischemia. Neurosci Lett 2009;459:147-51.
70. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 1999;22:391-7.