Experimental diffuse brain injury results in regional alteration of gross vascular morphology independent of neuropathology

References

• Langlois JA, Rutland-Brown W, Wald MM. The epidemiology and impact of traumatic brain injury: a brief overview. Journal of Head Trauma Rehabilitation 2006;21:375–378.
   PubMed Web of Science ®Google Scholar
• Reilly P. The impact of neurotrauma on society: an international perspective. Progress in Brain Research 2007;161:3–9.
   PubMed Web of Science ®Google Scholar
• Albensi BC, Janigro D. Traumatic brain injury and its effects on synaptic plasticity. Brain Injury 2003;17:653–663.
   PubMed Web of Science ®Google Scholar
• Masel BE, DeWitt DS. Traumatic brain injury: a disease process, not an event. Journal of Neurotrauma 2010;27:1529–1540.
   PubMed Web of Science ®Google Scholar
• Yeates KO, Taylor HG, Wade SL, Drotar D, Stancin T, Minich N. A prospective study of short- and long-term neuropsychological outcomes after traumatic brain injury in children. Neuropsychology 2002;16:514–523.
   PubMed Web of Science ®Google Scholar
• Yeates KO, Taylor HG, Woodrome SE, Wade SL, Stancin T, Drotar D. Race as a moderator of parent and family outcomes following pediatric traumatic brain injury. Journal of Pediatric Psychology 2002;27:393–403.
   PubMed Web of Science ®Google Scholar
• Stanimirovic DB, Friedman A. Pathophysiology of the neurovascular unit: disease cause or consequence? Journal of Cerebral Blood Flow & Metabolism 2012;32:1207–1221.
   PubMed Web of Science ®Google Scholar
• Thornton E, Ziebell JM, Leonard AV, Vink R. Kinin receptor antagonists as potential neuroprotective agents in central nervous system injury. Molecules 2010;15:6598–6618.
   PubMed Web of Science ®Google Scholar
• Turner RJ, Dasilva KW, O’Connor C, van den Heuvel C, Vink R. Magnesium gluconate offers no more protection than magnesium sulphate following diffuse traumatic brain injury in rats. Journal of the American College of Nutrition 2004;23:541S–544S.
   PubMed Web of Science ®Google Scholar
• Vink R, Nimmo AJ. Multifunctional drugs for head injury. Neurotherapeutics 2009;6:28–42.
   PubMed Web of Science ®Google Scholar
• Vink R, van den Heuvel C. Substance P antagonists as a therapeutic approach to improving outcome following traumatic brain injury. Neurotherapeutics 2010;7:74–80.
   PubMed Web of Science ®Google Scholar
• Ziebell JM, Bye N, Semple BD, Kossmann T, Morganti-Kossmann MC. Attenuated neurological deficit, cell death and lesion volume in Fas-mutant mice is associated with altered neuroinflammation following traumatic brain injury. Brain Research 2011;1414:94–105.
   PubMed Web of Science ®Google Scholar
• Werner C, Engelhard K. Pathophysiology of traumatic brain injury. British Journal of Anaesthesia 2007;99:4–9.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Yuan XQ, Prough DS, Smith TL, Dewitt DS. The effects of traumatic brain injury on regional cerebral blood flow in rats. Journal of Neurotrauma 1988;5:289–301.
   PubMed Web of Science ®Google Scholar
• Unterberg AW, Stover J, Kress B, Kiening KL. Edema and brain trauma. Neuroscience 2004;129:1021–1029.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Barzo P, Marmarou A, Fatouros P, Corwin F, Dunbar J. Magnetic resonance imaging-monitored acute blood-brain barrier changes in experimental traumatic brain injury. Journal of Neurosurgery 1996;85):1113–1121.
   PubMed Web of Science ®Google Scholar
• Povlishock JT, Becker DP, Sullivan HG, Miller JD. Vascular permeability alterations to horseradish peroxidase in experimental brain injury. Brain Research 1978;153:223–239.
   PubMed Web of Science ®Google Scholar
• Park E, Bell JD, Siddiq IP, Baker AJ. An analysis of regional microvascular loss and recovery following two grades of fluid percussion trauma: a role for hypoxia-inducible factors in traumatic brain injury. Journal of Cerebral Blood Flow & Metabolism 2009;29:575–584.
   PubMed Web of Science ®Google Scholar
• Busl KM, Greer DM. Hypoxic-ischemic brain injury: pathophysiology, neuropathology and mechanisms. NeuroRehabilitation 2010;26:5–13.
   PubMed Web of Science ®Google Scholar
• Kelley BJ, Farkas O, Lifshitz J, Povlishock JT. Traumatic axonal injury in the perisomatic domain triggers ultrarapid secondary axotomy and Wallerian degeneration. Experimental Neurology 2006;198:350–360.
   PubMed Web of Science ®Google Scholar
• Lifshitz J, Kelley BJ, Povlishock JT. Perisomatic thalamic axotomy after diffuse traumatic brain injury is associated with atrophy rather than cell death. Journal of Neuropathology & Experiemental Neurology 2007;66:218–229.
   PubMed Web of Science ®Google Scholar
• Singleton RH, Zhu J, Stone JR, Povlishock JT. Traumatically induced axotomy adjacent to the soma does not result in acute neuronal death. Journal of Neuroscience 2002;22:791–802.
   PubMed Web of Science ®Google Scholar
• Learoyd AE, Lifshitz J. Comparison of rat sensory behavioral tasks to detect somatosensory morbidity after diffuse brain-injury. Behavioural Brain Research 2012;226:197–204.
   PubMed Web of Science ®Google Scholar
• Lifshitz J, Lisembee AM. Neurodegeneration in the somatosensory cortex after experimental diffuse brain injury. Brain Structure & Function 2012;217:49–61.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Taylor SE, Morganti-Kossmann C, Lifshitz J, Ziebell JM. Rod microglia: a morphological definition. PLoS One 2014;9:e97096.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ziebell JM, Taylor SE, Cao T, Harrison JL, Lifshitz J. Rod microglia: elongation, alignment, and coupling to form trains across the somatosensory cortex after experimental diffuse brain injury. Journal of Neuroinflammation 2012;9:247.
   PubMed Web of Science ®Google Scholar
• Dietrich WD, Ginsberg MD, Busto R, Smith DW. Metabolic alterations in rat somatosensory cortex following unilateral vibrissal removal. Journal of Neuroscience 1985;5:874–880.
   PubMed Web of Science ®Google Scholar
• Petersen CC. Cortical control of whisker movement. Annual Review of Neuroscience 2014;37:183–203.
   PubMed Web of Science ®Google Scholar
• Hall KD, Lifshitz J. Diffuse traumatic brain injury initially attenuates and later expands activation of the rat somatosensory whisker circuit concomitant with neuroplastic responses. Brain Research 2010;1323:161–173.
   PubMed Web of Science ®Google Scholar
• Cao T, Thomas TC, Ziebell JM, Pauly JR, Lifshitz J. Morphological and genetic activation of microglia after diffuse traumatic brain injury in the rat. Neuroscience 2012;225:65–75.
   PubMed Web of Science ®Google Scholar
• Hosseini AH, Lifshitz J. Brain injury forces of moderate magnitude elicit the fencing response. Medicine & Science in Sports & Exercise 2009;41:1687–1697.
   PubMed Web of Science ®Google Scholar
• Kelley BJ, Lifshitz J, Povlishock JT. Neuroinflammatory responses after experimental diffuse traumatic brain injury. Journal of Neuropathology & Experimental Neurology 2007;66:989–1001.
   PubMed Web of Science ®Google Scholar
• de Olmos JS, Beltramino CA, de Olmos de Lorenzo S. Use of an amino-cupric-silver technique for the detection of early and semiacute neuronal degeneration caused by neurotoxicants, hypoxia, and physical trauma. Neurotoxicology Teratology 1994;16:545–561.
   Google Scholar
• Switzer RC, 3rd. Application of silver degeneration stains for neurotoxicity testing. Toxicologic Pathology 2000;28:70–83.
   PubMed Web of Science ®Google Scholar
• Paxinos G, Watson C. The rat brain in stereotaxic coordinates. Amsterdam: Academic Press/Elsevier; 2007.
   Google Scholar
• Hattori N, Huang SC, Wu HM, Liao W, Glenn TC, Vespa PM, Phelps ME, Hovda DA, Bergsneider M. PET investigation of post-traumatic cerebral blood volume and blood flow. Acta Neurochirurgica Supplement 2003;86:49–52.
   PubMedGoogle Scholar
• Hellewell SC, Yan EB, Agyapomaa DA, Bye N, Morganti-Kossmann MC. Post-traumatic hypoxia exacerbates brain tissue damage: analysis of axonal injury and glial responses. Journal of Neurotrauma 2010;27:1997–2010.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Vink R, Young A, Bennett CJ, Hu X, Connor CO, Cernak I, Nimmo AJ. Neuropeptide release influences brain edema formation after diffuse traumatic brain injury. Acta Neurochirurgica Supplement 2003;86:257–260.
   PubMedGoogle Scholar
• Ziebell JM, Morganti-Kossmann MC. Involvement of pro- and anti-inflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury. Neurotherapeutics 2010;7:22–30.
   PubMed Web of Science ®Google Scholar
• Giza CC, Hovda DA. The Neurometabolic Cascade of Concussion. Journal of Athletic Training 2001;36:228–235.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Baeza A, Reina-de la Torre F, Poca A, Marti M, Garnacho A. Morphological features in human cortical brain microvessels after head injury: a three-dimensional and immunocytochemical study. Anatomical Record Part A: Discoveries in Molecular, Cellular & Evolutionary Biology 2003;273:583–593.
   Google Scholar
• Hall ED, Bryant YD, Cho W, Sullivan PG. Evolution of post-traumatic neurodegeneration after controlled cortical impact traumatic brain injury in mice and rats as assessed by the de Olmos silver and fluorojade staining methods. Journal of Neurotrauma 2008;25:235–247.
   PubMed Web of Science ®Google Scholar
• Scremin OU. Cerebral vascular system. In: Paxinos G, editor. The rat nervous system. San Diego, CA: Elsevier Academic Press; 2004. p 1165–1202.
   Google Scholar
• Kontos HA, Wei EP, Ellis EF, Dietrich WD, Povlishock JT. Prostaglandins in physiological and in certain pathological responses of the cerebral circulation. Federal Proceedings 1981;40:2326–2330.
   PubMedGoogle Scholar
• Wei EP, Dietrich WD, Povlishock JT, Navari RM, Kontos HA. Functional, morphological, and metabolic abnormalities of the cerebral microcirculation after concussive brain injury in cats. Circulation Research 1980;46:37–47.
   PubMed Web of Science ®Google Scholar
• Yamakami I, McIntosh TK. Effects of traumatic brain injury on regional cerebral blood flow in rats as measured with radiolabeled microspheres. Journal of Cerebral Blood Flow & Metabolism 1989;9:117–124.
   PubMed Web of Science ®Google Scholar
• Povlishock JT, Kontos HA. Continuing axonal and vascular change following experimental brain trauma. Central Nervous System Trauma 1985;2:285–298.
   PubMedGoogle Scholar
• Baranova AI, Wei EP, Ueda Y, Sholley MM, Kontos HA, Povlishock JT. Cerebral vascular responsiveness after experimental traumatic brain injury: the beneficial effects of delayed hypothermia combined with superoxide dismutase administration. Journal of Neurosurgery 2008;109:502–509.
   PubMed Web of Science ®Google Scholar
• Wei EP, Hamm RJ, Baranova AI, Povlishock JT. The long-term microvascular and behavioral consequences of experimental traumatic brain injury after hypothermic intervention. Journal of Neurotrauma 2009;26:527–537.
   PubMed Web of Science ®Google Scholar
• Meier TB, Bellgowan PS, Singh R, Kuplicki R, Polanski DW, Mayer AR. Recovery of cerebral blood flow following sports-related concussion. JAMA Neurology 2015;72:530–538.
   Google Scholar