629
Views
44
CrossRef citations to date
0
Altmetric
Review Articles

Clinical relevance of midline fluid percussion brain injury: Acute deficits, chronic morbidities and the utility of biomarkers

, , , , , & show all
Pages 1293-1301 | Received 22 Sep 2015, Accepted 07 May 2016, Published online: 11 Aug 2016

References

  • Saatman KE, Duhaime AC, Bullock R, Maas AI, Valadka A, Manley GT. Classification of traumatic brain injury for targeted therapies. Journal of Neurotrauma 2008;25:719–738.
  • O’Connor WT, Smyth A, Gilchrist MD. Animal models of traumatic brain injury: a critical evaluation. Pharmacology & Therapeutics 2011;130:106–113.
  • Walker AE. The physiological basis of concussion: 50 years later. Journal of Neurosurgery 1994;81:493–494.
  • Zweckberger K, Eros C, Zimmermann R, Kim SW, Engel D, Plesnila N. Effect of early and delayed decompressive craniectomy on secondary brain damage after controlled cortical impact in mice. Journal of Neurotrauma 2006;23:1083–1093.
  • Friess SH, Lapidus JB, Brody DL. Decompressive craniectomy reduces white matter injury after controlled cortical impact in mice. Journal of Neurotrauma 2015;32:791–800.
  • Maeda T, Lee SM, Hovda DA. Restoration of cerebral vasoreactivity by an L-type calcium channel blocker following fluid percussion brain injury. Journal of Neurotrauma 2005;22:763–71.
  • Xu Y, McArthur DL, Alger JR, Etchepare M, Hovda DA, Glenn TC, Huang S, Dinov I, Vespa PM. Early nonischemic oxidative metabolic dysfunction leads to chronic brain atrophy in traumatic brain injury. Journal of Cerebral Blood Flow & Metabolism 2010;30:883–894.
  • Wee HY, Lim SW, Chio CC, Niu KC, Wang CC, Kuo JR. Hyperbaric oxygen effects on neuronal apoptosis associations in a traumatic brain injury rat model. Journal of Surgical Research 2015;197:382–389.
  • Masel BE, DeWitt DS. Traumatic brain injury: a disease process, not an event. Journal of Neurotrauma 2010;27:1529–1540.
  • Zhang J, Yoganandan N, Pintar FA, Gennarelli TA. Brain strains in vehicle impact tests. Annual Proceedings/Association for the Advancement of Automotive Medicine 2006;50:1–12.
  • Faul M XL, Wald MM, Coronado VG. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations and Deaths 2002-2006.: Atlanta (GA): Centers for Disease Control and Prevention, National Center for Injury Prevention and Control; 2010.
  • Roozenbeek B, Maas AI, Menon DK. Changing patterns in the epidemiology of traumatic brain injury. Nature Reviews Neurology 2013;9:231–236.
  • Graham DI, Adams JH, Nicoll JA, Maxwell WL, Gennarelli TA. The nature, distribution and causes of traumatic brain injury. Brain Pathology 1995;5:397–406.
  • Levine B, Kovacevic N, Nica EI, Cheung G, Gao F, Schwartz ML, Black SE. The Toronto traumatic brain injury study: injury severity and quantified MRI. Neurology 2008;70:771–778.
  • Groat RA, Windle WF, Magoun HW. Functional and structural changes in the monkey’s brain during and after concussion. Journal of Neurosurgery 1945;2:26–35.
  • Lindgren S, Rinder L. Experimental studies in head injury. I.Some factors influencing results of model experiments. Biophysik 1965;2:320–329.
  • Sullivan HG, Martinez J, Becker DP, Miller JD, Griffith R, Wist AO. Fluid-percussion model of mechanical brain injury in the cat. Journal of Neurosurgery 1976;45:521–534.
  • Thompson HJ, Lifshitz J, Marklund N, Grady MS, Graham DI, Hovda DA, McIntosh TK. Lateral fluid percussion brain injury: a 15-year review and evaluation. Journal of Neurotrauma 2005;22:42–75.
  • McIntosh TK, Vink R, Noble L, Yamakami I, Fernyak S, Soares H, Faden AL. Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 1989;28:233–244.
  • Lifshitz J. Fluid Percussion Injury. In: J Chen ZX, Xu X-M, Zhang J, editors. Animal models of acute neurological injuries. Totowa (NJ): The Humana Press Inc.; 2008.
  • Dixon CE, Lyeth BG, Povlishock JT, Findling RL, Hamm RJ, Marmarou A, Young HF, Hayes RL. A fluid percussion model of experimental brain injury in the rat. Journal of Neurosurgery 1987;67:110–119.
  • McIntosh TK, Noble L, Andrews B, Faden AI. Traumatic brain injury in the rat: characterization of a midline fluid-percussion model. Central Nervous System Trauma 1987;4:119–134.
  • Vink R, Mullins PG, Temple MD, Bao W, Faden AI. Small shifts in craniotomy position in the lateral fluid percussion injury model are associated with differential lesion development. Journal of Neurotrauma 2001;18:839–847.
  • Floyd CL, Golden KM, Black RT, Hamm RJ, Lyeth BG. Craniectomy position affects morris water maze performance and hippocampal cell loss after parasagittal fluid percussion. Journal of Neurotrauma 2002;19:303–316.
  • Pierce JE, Smith DH, Trojanowski JQ, McIntosh TK. Enduring cognitive, neurobehavioral and histopathological changes persist for up to one year following severe experimental brain injury in rats. Neuroscience 1998;87:359–369.
  • Smith DH, Chen XH, Pierce JE, Wolf JA, Trojanowski JQ, Graham DI, McIntosh TK. Progressive atrophy and neuron death for one year following brain trauma in the rat. Journal of Neurotrauma 1997;14:715–727.
  • Stein DG. Sex differences in brain damage and recovery of function: experimental and clinical findings. Progress in Brain Research 2007;161:339–351.
  • Naderi V, Khaksari M, Abbasi R, Maghool F. Estrogen provides neuroprotection against brain edema and blood brain barrier disruption through both estrogen receptors alpha and beta following traumatic brain injury. Iranian Journal of Basic Medical Sciences 2015;18:138–144.
  • Maghool F, Khaksari M, Siahposht Khachki A. Differences in brain edema and intracranial pressure following traumatic brain injury across the estrous cycle: involvement of female sex steroid hormones. Brain Research 2013;1497:61–72.
  • Soltani Z, Khaksari M, Shahrokhi N, Mohammadi G, Mofid B, Vaziri A, Amiresmaili S. Effect of estrogen and/or progesterone administration on traumatic brain injury-caused brain edema: the changes of aquaporin-4 and interleukin-6. Journal of Physiology & Biochemistry 2015; SD. Journal of Physiology & Biochemistry 2016;72(1):33–44.
  • Khaksari M, Abbasloo E, Dehghan F, Soltani Z, Asadikaram G. The brain cytokine levels are modulated by estrogen following traumatic brain injury: Which estrogen receptor serves as modulator? International Immunopharmacology 2015;28:279–287.
  • Prins ML, Hovda DA. Developing experimental models to address traumatic brain injury in children. Journal of Neurotrauma 2003;20:123–137.
  • Prins ML, Lee SM, Cheng CL, Becker DP, Hovda DA. Fluid percussion brain injury in the developing and adult rat: a comparative study of mortality, morphology, intracranial pressure and mean arterial blood pressure. Brain Research Development Brain Research 1996;95:272–282.
  • Dixon CE, Lighthall JW, Anderson TE. Physiologic, histopathologic, and cineradiographic characterization of a new fluid-percussion model of experimental brain injury in the rat. Journal of Neurotrauma 1988;5:91–104.
  • Hosseini AH, Lifshitz J. Brain injury forces of moderate magnitude elicit the fencing response. Medicine & Science in Sports & Exercise 2009;41:1687–1697.
  • Lafrenaye AD, McGinn MJ, Povlishock JT. Increased intracranial pressure after diffuse traumatic brain injury exacerbates neuronal somatic membrane poration but not axonal injury: evidence for primary intracranial pressure-induced neuronal perturbation. Journal of Cerebral Blood Flow & Metabolism 2012;32:1919–1932.
  • Hillered L, Vespa PM, Hovda DA. Translational neurochemical research in acute human brain injury: the current status and potential future for cerebral microdialysis. Journal of Neurotrauma 2005;22:3–41.
  • Schmidt RH, Grady MS. Regional patterns of blood-brain barrier breakdown following central and lateral fluid percussion injury in rodents. Journal of Neurotrauma 1993;10:415–430.
  • Yoshino A, Hovda DA, Kawamata T, Katayama Y, Becker DP. Dynamic changes in local cerebral glucose utilization following cerebral conclusion in rats: evidence of a hyper- and subsequent hypometabolic state. Brain Reseearch 1991;561:106–119.
  • Giza CC, Hovda DA. The new neurometabolic cascade of concussion. Neurosurgery 2014;75(Suppl 4):S24–33.
  • Bergsneider M, Hovda DA, Lee SM, Kelly DF, McArthur DL, Vespa PM, Lee JH, Huang SC, Martin NA, Phelps ME, et al. Dissociation of cerebral glucose metabolism and level of consciousness during the period of metabolic depression following human traumatic brain injury. Journal of Neurotrauma 2000;17:389–401.
  • Ip EY, Zanier ER, Moore AH, Lee SM, Hovda DA. Metabolic, neurochemical, and histologic responses to vibrissa motor cortex stimulation after traumatic brain injury. Journal of Cerebral Blood Flow & Metabolism 2003;23:900–910.
  • Barkhoudarian G, Hovda DA, Giza CC. The molecular pathophysiology of concussive brain injury. Clinical Sports Medicine 2011;30:33–48, vii–iii.
  • Prins ML, Alexander D, Giza CC, Hovda DA. Repeated mild traumatic brain injury: mechanisms of cerebral vulnerability. Journal of Neurotrauma 2013;30:30–38.
  • Rowe RK, Striz M, Bachstetter AD, Van Eldik LJ, Donohue KD, O’Hara BF, Lifshitz J. Diffuse brain injury induces acute post-traumatic sleep. PLoS One 2014;9:e82507.
  • Raghupathi R, McIntosh TK, Smith DH. Cellular responses to experimental brain injury. Brain Pathology 1995;5:437–442.
  • Krueger JM, Rector DM, Churchill L. Sleep and cytokines. Sleep Medicine Clinics 2007;2:161–169.
  • Thompson HJ, Hoover RC, Tkacs NC, Saatman KE, McIntosh TK. Development of posttraumatic hyperthermia after traumatic brain injury in rats is associated with increased periventricular inflammation. Journal of Cerebral Blood Flow & Metabolism 2005;25:163–176.
  • Thompson HJ, Tkacs NC, Saatman KE, Raghupathi R, McIntosh TK. Hyperthermia following traumatic brain injury: a critical evaluation. Neurobiology of Disease 2003;12:163–173.
  • Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Medicine Reviews 2006;10:49–62.
  • Fenn AM, Gensel JC, Huang Y, Popovich PG, Lifshitz J, Godbout JP. Immune activation promotes depression 1 month after diffuse brain injury: a role for primed microglia. Biological Psychiatry 2014;76:575–584.
  • Rowe RK, Harrison JL, O’Hara BF, Lifshitz J. Diffuse brain injury does not affect chronic sleep patterns in the mouse. Brain Injury 2014;28:504–510.
  • Hamm RJ. Neurobehavioral assessment of outcome following traumatic brain injury in rats: an evaluation of selected measures. Journal of Neurotrauma 2001 ;18):1207–1216.
  • Bachstetter AD, Rowe RK, Kaneko M, Goulding D, Lifshitz J, Van Eldik LJ. The p38alpha MAPK regulates microglial responsiveness to diffuse traumatic brain injury. Journal of Neuroscience 2013;33:6143–6153.
  • Harrison JL, Rowe RK, Ellis TW, Yee NS, O’Hara BF, Adelson PD, Lifshitz J. Resolvins AT-D1 and E1 differentially impact functional outcome, post-traumatic sleep, and microglial activation following diffuse brain injury in the mouse. Brain, Behavior & Immunity 2015;47:131–140.
  • Morales DM, Marklund N, Lebold D, Thompson HJ, Pitkanen A, Maxwell WL, Longhi L, Laurer H, Maegele M, Neugebauer E, et al. Experimental models of traumatic brain injury: do we really need to build a better mousetrap? Neuroscience 2005;136:971–989.
  • Chen AJ, D’Esposito M. Traumatic brain injury: from bench to bedside to society. Neuron 2010;66:11–14.
  • McAllister TW. Neuropsychiatric sequelae of head injuries. Psychiatrics Clinics of North America 1992;15:395–413.
  • Behan LA, Phillips J, Thompson CJ, Agha A. Neuroendocrine disorders after traumatic brain injury. Journal of Neurology, Neurosurgery & Psychiatry 2008;79:753–759.
  • Dusick JR, Wang C, Cohan P, Swerdloff R, Kelly DF. Pathophysiology of hypopituitarism in the setting of brain injury. Pituitary 2012;15:2–9.
  • Grundy PL, Harbuz MS, Jessop DS, Lightman SL, Sharples PM. The hypothalamo-pituitary-adrenal axis response to experimental traumatic brain injury. Journal of Neurotrauma 2001;18):1373–1381.
  • Griesbach GS, Hovda DA, Tio DL, Taylor AN. Heightening of the stress response during the first weeks after a mild traumatic brain injury. Neuroscience 2011;178:147–58.
  • Griesbach GS, Tio DL, Vincelli J, McArthur DL, Taylor AN. Differential effects of voluntary and forced exercise on stress responses after traumatic brain injury. Journal of Neurotrauma 2012;29:1426–1433.
  • Griesbach GS, Tio DL, Nair S, Hovda DA. Recovery of stress response coincides with responsiveness to voluntary exercise after traumatic brain injury. Journal of Neurotrauma 2014;31:674–682.
  • Yeh CC, Chen TL, Hu CJ, Chiu WT, Liao CC. Risk of epilepsy after traumatic brain injury: a retrospective population-based cohort study. Journal of Neurology, Neurosurgery & Psychiatry 2013;84:441–445.
  • Pitkanen A, Bolkvadze T. Head trauma and epilepsy. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado–Escueta AV, editors. Jasper’s Basic Mechanisms of the Epilepsies. 4th ed. Bethesda, MD: Oxford University Press; 2012.
  • D’Ambrosio R, Fairbanks JP, Fender JS, Born DE, Doyle DL, Miller JW. Post-traumatic epilepsy following fluid percussion injury in the rat. Brain 2004;127:304–314.
  • Pitkanen A, McIntosh TK. Animal models of post-traumatic epilepsy. Journal of Neurotrauma 2006;23:241–261.
  • Johnstone VP, Yan EB, Alwis DS, Rajan R. Cortical hypoexcitation defines neuronal responses in the immediate aftermath of traumatic brain injury. PLoS One 2013;8:e63454.
  • Alwis DS, Yan EB, Morganti-Kossmann MC, Rajan R. Sensory cortex underpinnings of traumatic brain injury deficits. PLoS One 2012;7:e52169.
  • McNamara KC, Lisembee AM, Lifshitz J. The whisker nuisance task identifies a late-onset, persistent sensory sensitivity in diffuse brain-injured rats. Journal of Neurotrauma 2010;27:695–706.
  • Learoyd AE, Lifshitz J. Comparison of rat sensory behavioral tasks to detect somatosensory morbidity after diffuse brain-injury. Behavior & Brain Research 2012;226:197–204.
  • Thomas TC, Hinzman JM, Gerhardt GA, Lifshitz J. Hypersensitive glutamate signaling correlates with the development of late-onset behavioral morbidity in diffuse brain-injured circuitry. Journal of Neurotrauma 2012;29:187–200.
  • Adams JH, Jennett B, Murray LS, Teasdale GM, Gennarelli TA, Graham DI. Neuropathological findings in disabled survivors of a head injury. Journal of Neurotrauma 2011;28:701–709.
  • Mez J, Stern RA, McKee AC. Chronic traumatic encephalopathy: where are we and where are we going? Current Neurology & Neuroscience Reports 2013;13:407.
  • Mondello S, Tortella FC. Brain injury markers: where are we? Frontiers in Neurology 2014;5:145.
  • Papa L, Ramia MM, Edwards D, Johnson BD, Slobounov SM. Systematic review of clinical studies examining biomarkers of brain injury in athletes after sports-related concussion. Journal of Neurotrauma 2015;32:661–673.
  • Forde CT, Karri SK, Young AM, Ogilvy CS. Predictive markers in traumatic brain injury: opportunities for a serum biosignature. British Journal of Neurosurgery 2014;28:8–15.
  • Jeter CB, Hergenroeder GW, Hylin MJ, Redell JB, Moore AN, Dash PK. Biomarkers for the diagnosis and prognosis of mild traumatic brain injury/concussion. Journal of Neurotrauma 2013;30:657–670.
  • Raad M, Nohra E, Chams N, Itani M, Talih F, Mondello S, Kobeissy F. Autoantibodies in traumatic brain injury and central nervous system trauma. Neuroscience 2014;281c:16–23.
  • McCrory P, Meeuwisse WH, Aubry M, Cantu RC, Dvorak J, Echemendia RJ, Engebretsen L, Johnston K, Kutcher JS, Raftery M, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport, Zurich, November 2012. J Athl Train 2013;48(4):554–75.
  • Carpenter KL, Czosnyka M, Jalloh I, Newcombe VF, Helmy A, Shannon RJ, Budohoski KP, Kolias AG, Kirkpatrick PJ, Carpenter TA, et al. Systemic, local, and imaging biomarkers of brain injury: more needed, and better use of those already established? Frontiers in Neurology 2015;6:26.
  • Smitherman E, Hernandez A, Stavinoha PL, Huang R, Kernie SG, Diaz-Arrastia R, Miles DK. Predicting outcome after pediatric traumatic brain injury by early magnetic resonance imaging lesion location and volume. Journal of Neurotrauma 2016;33:35–48.
  • Sharp DJ, Scott G, Leech R. Network dysfunction after traumatic brain injury. Nature Reviews Neurology 2014;10:156–166.
  • Lew HL, Poole JH, Guillory SB, Salerno RM, Leskin G, Sigford B. Persistent problems after traumatic brain injury: the need for long-term follow-up and coordinated care. Journal of Rehabilitation Research & Development 2006;43:vii–x.
  • Rowe RK, Harrison JL, Thomas TC, Pauly JR, Adelson PD, Lifshitz J. Using anesthetics and analgesics in experimental traumatic brain injury. Lab Animal (NY) 2013;42:286–291.
  • Shultz SR, Sun M, Wright DK, Brady RD, Liu S, Beynon S, Schmidt SF, Kaye AH, Hamilton JA, O’Brien TJ, et al. Tibial fracture exacerbates traumatic brain injury outcomes and neuroinflammation in a novel mouse model of multitrauma. Journal of Cerebral Blood Flow & Metabolism 2015;35:1339–1347.
  • Maegele M, Sauerland S, Bouillon B, Schafer U, Trubel H, Riess P, Neugebauer EA. Differential immunoresponses following experimental traumatic brain injury, bone fracture and “two-hit”-combined neurotrauma. Inflammation Research 2007;56:318–323.
  • Chen B, Mutschler M, Yuan Y, Neugebauer E, Huang Q, Maegele M. Superimposed traumatic brain injury modulates vasomotor responses in third-order vessels after hemorrhagic shock. Scandinavian Journal of Trauma, Resuscitation & Emergency Medicine 2013;21:77.
  • DeRoss AL, Adams JE, Vane DW, Russell SJ, Terella AM, Wald SL. Multiple head injuries in rats: effects on behavior. Journal of Trauma 2002;52:708–714.
  • Shultz SR, Bao F, Weaver LC, Cain DP, Brown A. Treatment with an anti-CD11d integrin antibody reduces neuroinflammation and improves outcome in a rat model of repeated concussion. Journal of Neuroinflammation 2013;10:26.
  • Shultz SR, Bao F, Omana V, Chiu C, Brown A, Cain DP. Repeated mild lateral fluid percussion brain injury in the rat causes cumulative long-term behavioral impairments, neuroinflammation, and cortical loss in an animal model of repeated concussion. Journal of Neurotrauma 2012;29:281–294.
  • Wang T, Van KC, Gavitt BJ, Grayson JK, Lu YC, Lyeth BG, Pichakron KO. Effect of fish oil supplementation in a rat model of multiple mild traumatic brain injuries. Restorative Neurology & Neuroscience 2013;31:647–659.
  • Aungst SL, Kabadi SV, Thompson SM, Stoica BA, Faden AI. Repeated mild traumatic brain injury causes chronic neuroinflammation, changes in hippocampal synaptic plasticity, and associated cognitive deficits. Journal of Cereb Blood Flow & Metabolism 2014;34:1223–1232.
  • Hawkins BE, Cowart JC, Parsley MA, Capra BA, Eidson KA, Hellmich HL, Dewitt DS, Prough DS. Effects of trauma, hemorrhage and resuscitation in aged rats. Brain Research 2013;1496:28–35.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.