Hyperbaric oxygen therapy for traumatic brain injury

Lei Huang, Andre Obenaus, Lei Huang, Andre Obenaus

Abstract

Traumatic brain injury (TBI) is a major public health issue. The complexity of TBI has precluded the use of effective therapies. Hyperbaric oxygen therapy (HBOT) has been shown to be neuroprotective in multiple neurological disorders, but its efficacy in the management of TBI remains controversial. This review focuses on HBOT applications within the context of experimental and clinical TBI. We also discuss its potential neuroprotective mechanisms. Early or delayed multiple sessions of low atmospheric pressure HBOT can reduce intracranial pressure, improve mortality, as well as promote neurobehavioral recovery. The complimentary, synergistic actions of HBOT include improved tissue oxygenation and cellular metabolism, anti-apoptotic, and anti-inflammatory mechanisms. Thus HBOT may serve as a promising neuroprotective strategy that when combined with other therapeutic targets for TBI patients which could improve long-term outcomes.

Figures

Figure 1
Figure 1
HBO reduces rmTBI lesion volumes. Pre- and post-treatment with HBO reduces lesion volume identified from magnetic resonance imaging (MRI, T2 weighted images). Repetitive mild traumatic brain injury (rmTBI) was induced 3 days apart and resulted in ipsilateral tissue damage. On T2WI, hypointensities (white arrow) are consistent with bleeding while hyperintensities (black arrow) suggest edema formation. At 24 hrs after the rmTBI, HBO pre- or post-treatment significantly reduced the lesion size compared to untreated animals. The neuroprotective effects persisted to 14 days after the initial mTBI.
Figure 2
Figure 2
HBOT reduces extravascular blood after rmTBI. HBO pre- and post-treatment improved susceptibility weighted imaging (SWI)-identified intracerebral hemorrhage following repetitive mild traumatic brain injury (rmTBI) 3 days apart. At 24 hrs after rmTBI, HBO pre- or post-treatment significantly ameliorated the hemorrhage (hypointensity, asterisks) compared to untreated animals, which persisted to 14 days after the initial mTBI.

References

    1. Gill AL, Bell CN. Hyperbaric Oxygen: Its Uses, Mechanisms of Action and Outcomes. QJM. 2004;97:385–395. doi: 10.1093/qjmed/hch074.
    1. Zhou Z, Daugherty WP, Sun D, Levasseur JE, Altememi N, Hamm RJ. et al.Protection of Mitochondrial Function and Improvement in Cognitive Recovery in Rats Treated with Hyperbaric Oxygen Following Lateral Fluid-Percussion Injury. J Neurosurg. 2007;106:687–694. doi: 10.3171/jns.2007.106.4.687.
    1. Daugherty WP, Levasseur JE, Sun D, Rockswold GL, Bullock MR. Effects of Hyperbaric Oxygen Therapy on Cerebral Oxygenation and Mitochondrial Function Following Moderate Lateral Fluid-Percussion Injury in Rats. J Neurosurg. 2004;101:499–504. doi: 10.3171/jns.2004.101.3.0499.
    1. Tolias CM, Reinert M, Seiler R, Gilman C, Scharf A, Bullock MR. Normobaric Hyperoxia--Induced Improvement in Cerebral Metabolism and Reduction in Intracranial Pressure in Patients with Severe Head Injury: A Prospective Historical Cohort-Matched Study. J Neurosurg. 2004;101:435–444. doi: 10.3171/jns.2004.101.3.0435.
    1. Rockswold SB, Rockswold GL, Vargo JM, Erickson CA, Sutton RL, Bergman TA. et al.Effects of Hyperbaric Oxygenation Therapy on Cerebral Metabolism and Intracranial Pressure in Severely Brain Injured Patients. J Neurosurg. 2001;94:403–411. doi: 10.3171/jns.2001.94.3.0403.
    1. Palzur E, Zaaroor M, Vlodavsky E, Milman F, Soustiel JF. Neuroprotective Effect of Hyperbaric Oxygen Therapy in Brain Injury Is Mediated by Preservation of Mitochondrial Membrane Properties. Brain Res. 2008;1221:126–133.
    1. Jain KK. Origin of Textbook of Hyperbaric Medicine. Cambrige, MA: Hogrefe & Huber; 2004.
    1. van Hulst RA, Haitsma JJ, Klein J, Lachmann B. Oxygen Tension under Hyperbaric Conditions in Healthy Pig Brain. Clin Physiol Funct Imaging. 2003;23:143–148. doi: 10.1046/j.1475-097X.2003.00485.x.
    1. Calvert JW, Cahill J, Zhang JH. Hyperbaric Oxygen and Cerebral Physiology. Neurol Res. 2007;29:132–141. doi: 10.1179/016164107X174156.
    1. Miller JD, Ledingham IM. Reduction of Increased Intracranial Pressure. Comparison between Hyperbaric Oxygen and Hyperventilation. Arch Neurol. 1971;24:210–216.
    1. Lambertsen CJ, Dough RH, Cooper DY, Emmel GL, Loeschcke HH, Schmidt CF. Oxygen Toxicity; Effects in Man of Oxygen Inhalation at 1 and 3.5 Atmospheres Upon Blood Gas Transport, Cerebral Circulation and Cerebral Metabolism. J Appl Physiol. 1953;5:471–486.
    1. Sukoff MH, Ragatz RE. Hyperbaric Oxygenation for the Treatment of Acute Cerebral Edema. Neurosurgery. 1982;10:29–38. doi: 10.1227/00006123-198201000-00006.
    1. Kohshi K, Yokota A, Konda N, Kinoshita Y, Kajiwara H. Intracranial Pressure Responses During Hyperbaric Oxygen Therapy. Neurol Med Chir (Tokyo) 1991;31:575–581. doi: 10.2176/nmc.31.575.
    1. Rockswold SB, Rockswold GL, Zaun DA, Zhang X, Cerra CE, Bergman TA. et al.A Prospective, Randomized Clinical Trial to Compare the Effect of Hyperbaric to Normobaric Hyperoxia on Cerebral Metabolism, Intracranial Pressure, and Oxygen Toxicity in Severe Traumatic Brain Injury. J Neurosurg. 2010;112:1080–1094. doi: 10.3171/2009.7.JNS09363.
    1. Edwards ML. Hyperbaric Oxygen Therapy. Part 2: Application in Disease. J Vet Emerg Crit Care (San Antonio) 2010;20:289–297. doi: 10.1111/j.1476-4431.2010.00535_1.x.
    1. Mandal NG, White N, Wee MY. Carbon Monoxide Poisoning in a Parturient and the Use of Hyperbaric Oxygen for Treatment. Int J Obstet Anesth. 2001;10:71–74. doi: 10.1054/ijoa.2000.0492.
    1. Rockswold GL, Ford SE, Anderson DC, Bergman TA, Sherman RE. Results of a Prospective Randomized Trial for Treatment of Severely Brain-Injured Patients with Hyperbaric Oxygen. J Neurosurg. 1992;76:929–934. doi: 10.3171/jns.1992.76.6.0929.
    1. Dunn JE, Lawson DD. In: Origins of Hyperbaric Medicine. Brown IW, Cox BGs, editor. Washington, DC: National Research Council; 1966. Effects of Hypobaric and Hyperbaric Oxygen on Experimental Brain Injury; pp. 447–454.
    1. Miller JD, Fitch W, Ledingham IM, Jennett WB. The Effect of Hyperbaric Oxygen on Experimentally Increased Intracranial Pressure. J Neurosurg. 1970;33:287–296. doi: 10.3171/jns.1970.33.3.0287.
    1. Hollin SA, Sukoff MH, Jacobson JH. The Protective Effect of Hyperbaric Oxygenation in Experimentally Produced Cerebral Edema and Compression. Prog Brain Res. 1968;30:479–489.
    1. Sukoff MH, Hollin SA, Espinosa OE, Jacobson JH. The Protective Effect of Hyperbaric Oxygenation in Experimental Cerebral Edema. J Neurosurg. 1968;29:236–241. doi: 10.3171/jns.1968.29.3.0236.
    1. Moody RA, Mead CO, Ruamsuke S, Mullan S. Therapeutic Value of Oxygen at Normal and Hyperbaric Pressure in Experimental Head Injury. J Neurosurg. 1970;32:51–54. doi: 10.3171/jns.1970.32.1.0051.
    1. Hayakawa T, Kanai N, Kuroda R, Yamada R, Mogami H. Response of Cereborspinal Fluid Pressure to Hyperbaric Oxygenation. J Neurol Neurosurg Psychiatry. 1971;34:580–586. doi: 10.1136/jnnp.34.5.580.
    1. Mink RB, Dutka AJ. Hyperbaric Oxygen after Global Cerebral Ischemia in Rabbits Does Not Promote Brain Lipid Peroxidation. Crit Care Med. 1995;23:1398–1404. doi: 10.1097/00003246-199508000-00014.
    1. Harch PG, Kriedt GL, Weisand MP, Van Meter KW, Sutherland RJ. Low Pressure Hyperbaric Oxygen Therapy Induces Cerebrovascular Changes and Improves Complex Learning/Memory in a Rat Open Head Bonk Chronic Brain Contusion Model. Undersea Hyperb Med. 1996;23
    1. Harch PG, Kriedt C, Van Meter KW, Sutherland RJ. Hyperbaric Oxygen Therapy Improves Spatial Learning and Memory in a Rat Model of Chronic Traumatic Brain Injury. Brain Res. 2007;1174:120–129.
    1. Wang GH, Zhang XG, Jiang ZL, Li X, Peng LL, Li YC. et al.Neuroprotective Effects of Hyperbaric Oxygen Treatment on Traumatic Brain Injury in the Rat. J Neurotrauma. 2010;27:1733–1743. doi: 10.1089/neu.2009.1175.
    1. Marx RE, Ehler WJ, Tayapongsak P, Pierce LW. Relationship of Oxygen Dose to Angiogenesis Induction in Irradiated Tissue. Am J Surg. 1990;160:519–524. doi: 10.1016/S0002-9610(05)81019-0.
    1. Myers RA, Marx RE. Use of Hyperbaric Oxygen in Postradiation Head and Neck Surgery. NCI Monogr. 1990. pp. 151–157.
    1. Golden ZL, Neubauer R, Golden CJ, Greene L, Marsh J, Mleko A. Improvement in Cerebral Metabolism in Chronic Brain Injury after Hyperbaric Oxygen Therapy. Int J Neurosci. 2002;112:119–131. doi: 10.1080/00207450212027.
    1. Neubauer RA, Gottlieb SF, Miale A Jr. Identification of Hypometabolic Areas in the Brain Using Brain Imaging and Hyperbaric Oxygen. Clin Nucl Med. 1992;17:477–481. doi: 10.1097/00003072-199206000-00010.
    1. Giza CC, Hovda DA. The Neurometabolic Cascade of Concussion. J Athl Train. 2001;36:228–235.
    1. Bennett MH, Trytko B, Jonker B. Hyperbaric Oxygen Therapy for the Adjunctive Treatment of Traumatic Brain Injury. Cochrane Database Syst Rev. 2004. p. CD004609.
    1. Kumaria A, Tolias CM. Normobaric Hyperoxia Therapy for Traumatic Brain Injury and Stroke: A Review. Br J Neurosurg. 2009;23:576–584. doi: 10.3109/02688690903050352.
    1. Narotam PK, Morrison JF, Nathoo N. Brain Tissue Oxygen Monitoring in Traumatic Brain Injury and Major Trauma: Outcome Analysis of a Brain Tissue Oxygen-Directed Therapy. J Neurosurg. 2009;111:672–682. doi: 10.3171/2009.4.JNS081150.
    1. Nortje J, Coles JP, Timofeev I, Fryer TD, Aigbirhio FI, Smielewski P. et al.Effect of Hyperoxia on Regional Oxygenation and Metabolism after Severe Traumatic Brain Injury: Preliminary Findings. Crit Care Med. 2008;36:273–281. doi: 10.1097/01.CCM.0000292014.60835.15.
    1. Rockswold SB, Rockswold GL, Defillo A. Hyperbaric Oxygen in Traumatic Brain Injury. Neurol Res. 2007;29:162–172. doi: 10.1179/016164107X181798.
    1. Contreras FL, Kadekaro M, Eisenberg HM. The Effect of Hyperbaric Oxygen on Glucose Utilization in a Freeze-Traumatized Rat Brain. J Neurosurg. 1988;68:137–141. doi: 10.3171/jns.1988.68.1.0137.
    1. Azbill RD, Mu X, Bruce-Keller AJ, Mattson MP, Springer JE. Impaired Mitochondrial Function, Oxidative Stress and Altered Antioxidant Enzyme Activities Following Traumatic Spinal Cord Injury. Brain Res. 1997;765:283–290. doi: 10.1016/S0006-8993(97)00573-8.
    1. Springer JE, Azbill RD, Carlson SL. A Rapid and Sensitive Assay for Measuring Mitochondrial Metabolic Activity in Isolated Neural Tissue. Brain Res Brain Res Protoc. 1998;2:259–263. doi: 10.1016/S1385-299X(97)00045-7.
    1. Vlodavsky E, Palzur E, Feinsod M, Soustiel JF. Evaluation of the Apoptosis-Related Proteins of the Bcl-2 Family in the Traumatic Penumbra Area of the Rat Model of Cerebral Contusion, Treated by Hyperbaric Oxygen Therapy: A Quantitative Immunohistochemical Study. Acta Neuropathol. 2005;110:120–126. doi: 10.1007/s00401-004-0946-8.
    1. Vlodavsky E, Palzur E, Soustiel JF. Hyperbaric Oxygen Therapy Reduces Neuroinflammation and Expression of Matrix Metalloproteinase-9 in the Rat Model of Traumatic Brain Injury. Neuropathol Appl Neurobiol. 2006;32:40–50. doi: 10.1111/j.1365-2990.2005.00698.x.
    1. Palzur E, Vlodavsky E, Mulla H, Arieli R, Feinsod M, Soustiel JF. Hyperbaric Oxygen Therapy for Reduction of Secondary Brain Damage in Head Injury: An Animal Model of Brain Contusion. J Neurotrauma. 2004;21:41–48. doi: 10.1089/089771504772695931.
    1. Korsmeyer SJ, Shutter JR, Veis DJ, Merry DE, Oltvai ZN. Bcl-2/Bax: A Rheostat That Regulates an Anti-Oxidant Pathway and Cell Death. Semin Cancer Biol. 1993;4:327–332.
    1. Sharpe JC, Arnoult D, Youle RJ. Control of Mitochondrial Permeability by Bcl-2 Family Members. Biochim Biophys Acta. 2004;1644:107–113. doi: 10.1016/j.bbamcr.2003.10.016.
    1. Shimizu S, Narita M, Tsujimoto Y. Bcl-2 Family Proteins Regulate the Release of Apoptogenic Cytochrome C by the Mitochondrial Channel Vdac. Nature. 1999;399:483–487. doi: 10.1038/20959.
    1. Calvert JW, Zhou C, Nanda A, Zhang JH. Effect of Hyperbaric Oxygen on Apoptosis in Neonatal Hypoxia-Ischemia Rat Model. J Appl Physiol. 2003;95:2072–2080.
    1. Yin D, Zhou C, Kusaka I, Calvert JW, Parent AD, Nanda A. et al.Inhibition of Apoptosis by Hyperbaric Oxygen in a Rat Focal Cerebral Ischemic Model. J Cereb Blood Flow Metab. 2003;23:855–864.
    1. Cuzner ML, Opdenakker G. Plasminogen Activators and Matrix Metalloproteases, Mediators of Extracellular Proteolysis in Inflammatory Demyelination of the Central Nervous System. J Neuroimmunol. 1999;94:1–14. doi: 10.1016/S0165-5728(98)00241-0.
    1. Wennersten A, Holmin S, Mathiesen T. Characterization of Bax and Bcl-2 in Apoptosis after Experimental Traumatic Brain Injury in the Rat. Acta Neuropathol. 2003;105:281–288.
    1. Hu SL, Hu R, Li F, Liu Z, Xia YZ, Cui GY. et al.Hyperbaric Oxygen Preconditioning Protects against Traumatic Brain Injury at High Altitude. Acta Neurochir Suppl. 2008;105:191–196. doi: 10.1007/978-3-211-09469-3_37.

Source: PubMed

3
Subskrybuj