Indian Journal of Neurotrauma 2006; 03(01): 19-26
DOI: 10.1016/S0973-0508(06)80005-5
Review Article
Thieme Medical and Scientific Publishers Private Ltd.

Lasting Effects of Pediatric Traumatic Brain Injury

Christopher C. Giza

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Further Information

Publication History

Publication Date:
05 April 2017 (online)

Abstract

The number one cause of death and disability in children and teenagers is traumatic brain injury. Despite this fact, this clinical scourge receives limited research investigation. Given the remarkable recovery often seen after focal childhood brain injuries (infarction, hemorrhage, surgical excision), there is a common misconception that the younger brain is always more resilient. However, increasing evidence suggests that this assumption is incorrect. First, TBI represents a diffuse type of brain injury, and both clinical and laboratory studies suggest that the immature brain is less capable of recovering from such damage. Second, there appear to be developmental windows wherein diffuse injury can result in lost potential; at time this loss may only be detectable at a later stage of brain maturation. In addition to understanding these complex concepts of TBI sustained during development, consideration will also be given to relating these concepts to chronic sequelae of pediatric TBI, including cell death and regional brain atrophy, cognitive and behavioral deficits, and altered trajectories of brain maturation.

 
  • References

  • 1 Zwienenberg M, Muizelaar JP. Severe pediatric head injury: the role of hyperemia revisited. J Neurotrauma 16 1999; 937-943
  • 2 Suzuki K. The changes in regional cerebral blood flow with advancing age in normal children. Nagoya Med J 34 1990; 159-170
  • 3 Chugani HT, Phelps ME, Mazziotta JC. Positron emission tomography study of human brain functional development. Ann Neurol 22 1987; 487-497
  • 4 Friedman WJ, Olson L, Persson H. Cells that Express Brain-Derived Neurotrophic Factor mRNA in the Developing Postnatal Rat Brain. Eur J Neurosci 03 1991; 688-697
  • 5 Insel TR, Miller LP, Gelhard RE. The ontogeny of excitatory amino acid receptors in rat forebrain—I. N- methyl-Daspartate and quisqualate receptors. Neuroscience 35 1990; 31-43
  • 6 Miller LP, Johnson AE, Gelhard RE, Insel TR. The ontogeny of excitatory amino acid receptors in the rat forebrain—II. Kainic acid receptors. Neuroscience 35 1990; 45-51
  • 7 Annegers JF, Grabow JD, Groover RV, Laws Jr ER, Elveback LR, Kurland LT. Seizures after head trauma: a population study. Neurology 30 1980; 683-689
  • 8 Ikonomidou C, Mosinger JL, Salles KS, Labruyere J, Olney JW. Sensitivity of the developing rat brain to hypobaric/ischemic damage parallels sensitivity to N-methyl-aspartate neurotoxicity. J Neurosci 09 1989; 2809-2818
  • 9 Fineman I, Giza CC, Nahed BV, Lee SM, Hovda DA. Inhibition of neocortical plasticity during development by a moderate concussive brain injury. J Neurotrauma 17 2000; 739-749
  • 10 Giza CC, Griesbach GS, Hovda DA. Experience-dependent behavioral plasticity is disturbed following traumatic injury to the immature brain. Behav Brain Res 157 2005; 11-22
  • 11 Bittigau P, Sifringer M, Pohl D. et al Apoptotic neurodegeneration following trauma is markedly enhanced in the immature brain. Ann Neurol 45 1999; 724-735
  • 12 Pohl D, Bittigau P, Ishimaru MJ. et al N-Methyl-D-aspartate antagonists and apoptotic cell death triggered by head trauma in developing rat brain. Proc Natl Acad Sci U S A 96 1999; 2508-2513
  • 13 Katayama Y, Becker DP, Tamura T, Hovda DA. Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg 73 1990; 889-900
  • 14 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 Res 561 1991; 106-119
  • 15 Hovda DA. In, Narayan RK, Wilberger JE, Povlishock JT. (Eds) Neurotrauma. 1996. McGraw-Hill; San Francisco: 1459-1478
  • 16 Thomas S, Prins ML, Samii M, Hovda DA. Cerebral metabolic response to traumatic brain injury sustained early in development: a 2-deoxy-D-glucose autoradiographic study. J Neurotrauma 17 2000; 649-665
  • 17 Prins ML, Hovda DA. Traumatic brain injury in the developing rat: effects of maturation on Morris water maze acquisition. J Neurotrauma 15 1998; 799-811
  • 18 Prins ML, Hovda DA. Mapping cerebral glucose metabolism during spatial learning: interactions of development and traumatic brain injury. J Neurotrauma 18 2001; 31-46
  • 19 Osteen CL, Moore AH, Prins ML, Hovda DA. Age-dependency of 45calcium accumulation following lateral fluid percussion: acute and delayed patterns. J Neurotrauma 18 2001; 141-162
  • 20 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 Res Dev Brain Res 95 1996; 272-282
  • 21 Gurkoff G, Hoffmann JR, Giza CC, Hovda DA. Injury severity does not predict outcome in a model of developmental lateral fluid percussion. J Neurotrauma 20 2003; 2003 (Abstract)
  • 22 Adelson PD, Jenkins LW, Hamilton RL, Robichaud P, Tran MP, Kochanek PM. Histopathologic response of the immature rat to diffuse traumatic brain injury. J Neurotrauma 18 2001; 967-976
  • 23 Conti AC, Raghupathi R, Trojanowski JQ, McIntosh TK. Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period. J Neurosci 18 1998; 5663-5672
  • 24 Tong W, Igarashi T, Ferriero DM, Noble LJ. Traumatic brain injury in the immature mouse brain: characterization of regional vulnerability. Exp Neurol 176 2002; 105-116
  • 25 Prins ML, Hovda DA. Developing experimental models to address traumatic brain injury in children. J Neurotrauma 20 2003; 123-137
  • 26 Ikonomidou C, Qin Y, Labruyere J, Kirby C, Olney JW. Prevention of trauma-induced neurodegeneration in infant rat brain. Pediatr Res 39 1996; 1020-1027
  • 27 Ikonomidou C, Turski L. Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injury?. Lancet Neurol 01 2002; 383-386
  • 28 Bigler ED, Johnson SC, Blatter DD. Head trauma and intellectual status: relation to quantitative magnetic resonance imaging findings. Appl Neuropsychol 06 1999; 217-225
  • 29 Verger K, Junque C, Levin HS. et al Correlation of atrophy measures on MRI with neuropsychological sequelae in children and adolescents with traumatic brain injury. Brain Inj 15 2001; 211-221
  • 30 Levin HS, Benavidez DA, Verger-Maestre K. et al Reduction of corpus callosum growth after severe traumatic brain injury in children. Neurology 54 2000; 647-653
  • 31 Wilde EA. et al Frontal and temporal morphometric findings on MRI in children after moderate to severe traumatic brain injury. J Neurotrauma 22 2005; 333-344
  • 32 Adelson PD, Dixon CE, Robichaud P, Kochanek PM. Motor and cognitive functional deficits following diffuse traumatic brain injury in the immature rat. J Neurotrauma 14 1997; 99-108
  • 33 Adelson PD, Dixon CE, Kochanek PM. Long-term dysfunction following diffuse traumatic brain injury in the immature rat. J Neurotrauma 17 2000; 273-282
  • 34 DeFord SM, Wilson MS, Rice AC. et al Repeated mild brain injuries result in cognitive impairment in B6C3F1 mice. J Neurotrauma 19 2002; 427-438
  • 35 Collins MW, Lovell MR, Iverson GL, Cantu RC, Maroon JC, Field M. Cumulative Effects of Concussion in High School Athletes. Neurosurgery 51 2002; 1175-1181
  • 36 Collins MW, Grindel SH, Lovell MR. et al Relationship between concussion and neuropsychological performance in college football players. JAMA 282 1999; 964-970
  • 37 Field M, Collins MW, Lovell MR, Maroon J. Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. J Pediat 142 2003; 546-553
  • 38 Matser EJ, Kessels AG, Lezak MD, Jordan BD, Troost J. Neuropsychological impairment in amateur soccer players. JAMA 282 1999; 971-973
  • 39 Ewing-Cobbs L, Fletcher JM, Levin HS, Iovino I, Miner ME. Academic achievement and academic placement following traumatic brain injury in children and adolescents: a two-year longitudinal study. J Clin Exp Neuropsychol 20 1998; 769-781
  • 40 Levin HS, Eisenberg HM, Wigg NR, Kobayashi K. Memory and intellectual ability after head injury in children and adolescents. Neurosurgery 11 1982; 668-673
  • 41 Taylor HG, Alden J. Age-related differences in outcomes following childhood brain insults: an introduction and overview. J Int Neuropsychol Soc 03 1997; 555-567
  • 42 Ewing-Cobbs L, Prasad MR, Landry SH, Kramer L, DeLeon R. Executive functions following traumatic brain injury in young children: a preliminary analysis. Dev Neuropsychol 26 2004; 487-512
  • 43 Jaffe KM, Polissar NL, Fay GC, Liao S. Recovery trends over three years following pediatric traumatic brain injury. Arch Phys Med Rehabil 76 1995; 17-26
  • 44 Levin HS, Hanten G, Chang CC. et al Working memory after traumatic brain injury in children. Ann Neurol 52 2002; 82-88
  • 45 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 16 2002; 514-523
  • 46 Giza CC, Li HH, Prins ML, Hovda DA. Gene expression profiling after lateral fluid percussion injury in the immature rat suggests multiple mechanisms of neural dysfunction. J Neurotrauma 20 2003; 1101 (Abstract)
  • 47 Giza CC, Cai Y, Prins ML, Hovda DA. Lateral fluid percussion injury in the developing rat triggers expression changes in multiple families of cell cycle, developmental and cytoskeletal genes. Restorative Neurol and Neurosci 23 3,4 2004; 209-210 (Abstract)
  • 48 Griesbach GS, Hovda DA, Molteni R, Gomez-Pinilla F. Alterations in BDNF and synapsin I within the occipital cortex and hippocampus after mild traumatic brain injury in the developing rat: reflections of injury-induced neuroplasticity. J Neurotrauma 19 2002; 803-814
  • 49 Prins ML, Povlishock JT, Phillips LL. The effects of combined fluid percussion traumatic brain injury and unilateral entorhinal deafferentation on the juvenile rat brain. Brain Res Dev Brain Res 140 2003; 93-104
  • 50 Giza CC, Santamaria NS, Hovda DA. N-methyl-D-aspartate receptor subunit changes following traumatic injury to the developing brain. J Neurotrauma, in press 2006.
  • 51 Santamaria NS, Hovda DA, Giza CC. Alteration in N-methyl-D-aspartate subunit composition and impaired neuroplasticity after fluid percussion injury in the developing rat. J Neurotrauma 21 2004; 1329 (Abstract)
  • 52 D'Ambrosio R, Maris DO, Grady MS, Winn HR, Janigro D. Selective loss of hippocampal long-term potentiation, but not depression, following fluid percussion injury. Brain Res 786 1998; 64-79
  • 53 Dietrich WD, Alonso O, Busto R, Ginsberg MD. Widespread metabolic depression and reduced somatosensory circuit activation following traumatic brain injury in rats. J Neurotrauma 11 1994; 629-640
  • 54 Sick TJ, Perez-Pinzon MA, Feng ZZ. Impaired expression of long-term potentiation in hippocampal slices 4 and 48 h following mild fluid-percussion brain injury in vivo. Brain Res 785 1998; 287-292
  • 55 Osteen CL, Giza CC, Hovda DA. Injury-induced alterations in N-methyl-D-aspartate receptor subunit composition contribute to prolonged (45)calcium accumulation following lateral fluid percussion. Neuroscience 128 2004; 305-322
  • 56 Biegon A, Fry PA, Paden CM, Alexandrovich A, Tsenter J, Shohami E. Dynamic changes in N-methyl-D-aspartate receptors after closed head injury in mi Implications for treatment of neurological and cognitive deficits. Proc Natl Acad Sci U S A 101 2004; 5117-5122
  • 57 Raghupathi R, Mehr MF, Helfaer MA, Margulies SS. Traumatic axonal injury is exacerbated following repetitive closed head injury in the neonatal pig. J Neurotrauma 21 2004; 307-316
  • 58 Tong KA, Ashwal S, Holshouser BA. et al Hemorrhagic shearing lesions in children and adolescents with posttraumatic diffuse axonal injury: improved detection and initial results. Radiology 227 2003; 332-339
  • 59 Tong KA, Ashwal S, Holshouser BA. et al Diffuse axonal injury in children: clinical correlation with hemorrhagic lesions. Ann Neurol 56 2004; 36-50
  • 60 Bennett EL, Diamond MC, Krech D, Rosenzweig MR. Chemical and anatomical plasticity of brain. Science 164 1964; 610-619
  • 61 Diamond MC, Krech D, Rosenzweig MR. The effects of an enriched environment on the histology of the rat cerebral cortex. J Comp Neurol 123 1964; 111-120
  • 62 Greenough WT, Volkmar FR, Juraska JM. Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. Exp Neurol 41 1973; 371-378
  • 63 Rampon C, Jiang CH, Dong H. et al Effects of environmental enrichment on gene expression in the brain. Proc Natl Acad Sci U S A 97 2000; 12880-12884
  • 64 Rosenzweig MR, Bennett EL. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78 1996; 57-65
  • 65 Tang YP, Wang H, Feng R, Kyin M, Tsien JZ. Differential effects of enrichment on learning and memory function in NR2B transgenic mice. Neuropharmacology 41 2001; 779-790
  • 66 Tees RC, Buhrmann K, Hanley J. The effect of early experience on water maze spatial learning and memory in rats. Dev Psychobiol 23 1990; 427-439
  • 67 Venable N, Pinto-Hamuy T, Arraztoa JA. et al Greater efficacy of preweaning than postweaning environmental enrichment on maze learning in adult rats. Behav Brain Res 31 1988; 89-92
  • 68 Marin-Padilla M, Parisi JE, Armstrong DL, Sargent SK, Kaplan JA. Shaken infant syndrome: developmental neuropathology, progressive cortical dysplasia, and epilepsy. Acta Neuropathol (Berl) 103 2002; 321-332
  • 69 Lombroso CT. Can early postnatal closed head injury induce cortical dysplasia. Epilepsia 41 2000; 245-253
  • 70 Ip EY, Giza CC, Griesbach GS, Hovda DA. Effects of enriched environment and fluid percussion injury on dendritic arborization within the cerebral cortex of the developing rat. J Neurotrauma 19 2002; 573-585
  • 71 Miller LP, Lyeth BG, Jenkins LW. et al Excitatory amino acid receptor subtype binding following traumatic brain injury. Brain Res 526 1990; 103-107
  • 72 Ashwal S, Holshouser B, Tong K. et al Proton MR spectroscopy detected glutamate/glutamine is increased in children with traumatic brain injury. J Neurotrauma 21 2004; 1539-1552
  • 73 Hawley CA, Ward AB, Magnay AR, Long J. Outcomes following childhood head injury: a population study. J Neurol Neurosurg Psychiat 75 2004; 737-742
  • 74 Taylor HG. et al A prospective study of short- and long-term outcomes after traumatic brain injury in children: behavior and achievement. Neuropsychology 16 2002; 15-27
  • 75 Griesbach GS, Hovda DA, Molteni R, Wu A, Gomez-Pinilla F. Voluntary exercise following traumatic brain injury: brainderived neurotrophic factor upregulation and recovery of function. Neuroscience 125 2004; 129-139
  • 76 Ip EY, Zanier ER, Moore AH, Lee SM, Hovda DA. Metabolic, neurochemical, and histologic responses to vibrissa motor cortex stimulation after traumatic brain injury. J Cereb Blood Flow Metab 23 2003; 900-910
  • 77 Jantzen KJ, Anderson B, Steinberg FL, Kelso JA. A prospective functional MR imaging study of mild traumatic brain injury in college football players. AJNR 25 2004; 738-745
  • 78 McAllister TW, Saykin AJ, Flashman LA. et al Brain activation during working memory 1 month after mild traumatic brain injury: a functional MRI study. Neurology 53 1999; 1300-1308
  • 79 Humm JL, Kozlowski DA, Bland ST, James DC, Schallert T. Use-dependent exaggeration of brain injury: is glutamate involved?. Exp Neurol 157 1999; 349-358
  • 80 Kozlowski DA, James DC, Schallert T. Use-dependent exaggeration of neuronal injury after unilateral sensorimotor cortex lesions. J Neurosci 16 1996; 4776-4786
  • 81 Leasure JL, Schallert T. Consequences of forced disuse of the impaired forelimb after unilateral cortical injury. Behav Brain Res 150 2004; 83-91