Repeat traumatic brain injury in the developing brain

International Journal of Developmental Neuroscience

Volumn 30, Issue 3, 2012, Pages 185-190

  Prins, M L ^a,d   Giza, C C ^a,b,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MATTEL CHILDREN S HOSPITAL   (United States)

^c Interdepartmental Program for Neuroscience   (United States)

^d Interdepartmental Program for Biomedical Engineering   (United States)

Author keywords

Experimental models; Pediatric; Repeat traumatic brain injury; Vulnerability

Indexed keywords

BEHAVIOR; BRAIN DEVELOPMENT; COGNITION; DEVELOPMENTAL STAGE; EPIDEMIOLOGICAL DATA; GENETIC SUSCEPTIBILITY; GROUPS BY AGE; HUMAN; INCIDENCE; NATURAL SELECTION; NONHUMAN; PRACTICE GUIDELINE; PRIORITY JOURNAL; REVIEW; TRAUMATIC BRAIN INJURY;

AGING; BRAIN; BRAIN INJURIES; HUMANS; MODELS, NEUROLOGICAL; RECURRENCE;

EID: 84859427148     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2011.05.009     Document Type: Review

References (77)

1. Adelson P.D., Jenkins L.W., Hamilton R.L., Robichaud P., Tran M.P., Kochanek P.M. Histopathologic response of the immature rat to diffuse traumatic brain injury. J. Neurotrauma 2001, 18:967-976.
2. American Academy of Neurology Practice parameter: the management of concussion in sports (summary statement). Report of the Quality Standards Subcommittee. Neurology 1997, 48.
3. Anderson V., Catroppa C., Morse S., Haritou F., Rosenfeld J. Functional plasticity or vulnerability after early brain injury?. Pediatrics 2005, 116:1374-1382.
4. Babikian T., Asarnow R. Neurocognitive outcomes and recovery after pediatric TBI: meta-analytic review of the literature. Neuropsychiatrie 2009, 23:283-296.
5. Babikian T., Prins M.L., Cai Y., Barkhoudarian G., Hartonian I., Hovda D.A., Giza C.C. Molecular and physiological responses to juvenile traumatic brain injury focus on growth and metabolism. Dev. Neurosci. 2010.
6. Barlow K.M., Thomson E., Johnson D., Minns R.A. Late neurologic and cognitive sequelae of inflicted traumatic brain injury in infancy. Pediatrics 2005, 116:e174-e185.
7. Bittigau P., et al. Apoptotic neurodegeneration following trauma is markedly enhanced in the immature brain. Ann. Neurol. 1999, 45:724-735.
8. Bonnier C., Mesples B., Carpentier S., Henin D., Gressens P. Delayed white matter injury in a murine model of shaken baby syndrome. Br. Pathol. 2002, 12:320-328.
9. Cantu R.C., Gean A.D. Second-impact syndrome and a small subdural hematoma: an uncommon catastrophic result of repetitive head injury with a characteristic imaging appearance. J. Neurotrauma 2010, 27:1557-1564.
10. Chugani H.T., Phelps M.E., Mazziotta J.C. Positron emission tomography study of human brain functional development. Ann. Neurol. 1987, 22:487-497.
11. Collins M., Grindel S., Lovell M., Dede D., Moser D., Phalin B., Nogle S., Wasik M., Cordry D., Daugherty M., Sears S., Nicolette G., Indelicato P., McKeag D. Relationship between concussions and neurophsychological performance in college football players. JAMA 1999, 282:964-970.
12. Collins M.W., Lovell M.R., Iverson G.L., Cantu R.C., Maroon J.C., Field M. Cumulative effects of concussion in high school athletes. Neurosurgery 2002, 51:1175-1179.
13. de Beaumont L., Brisson B., Lassonde M., Jolicoeur P. Long-term electrophysiological changes in athletes with a history of multiple concussions. Br. Inj. 2007, 21:631-644.
14. de Beaumont L., Theoret H., Mongeon D., Messier J., Leclerc S., Tremblay S., Ellemberg D., Lassonde M. Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain 2009, 132:695-708.
15. Faul M., Xu L., Wald M.M., Coronado V.G. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations and Deaths 2002-2006 Atlanta (GA) 2010, Center for Disease Control and Prevention.
16. Field M., Collins M.W., Lovell M.R., Maroon J. Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. J. Pediatr. 2003, 142:546-553.
17. Fineman I., Giza C.C., Nahed B.V., Lee S.M., Hovda D.A. Inhibition of neocortical plasticity during development by a moderate concussive brain injury. J. Neurotrauma 2000, 17:739-749.
18. Friess S.H., Ichord R.N., Ralston J., Ryall K., Helfaer M.A., Smith C., Margulies S.S. Repeated traumatic brain injury affects composite cognitive function in piglets. J. Neurotrauma 2009, 26:1111-1121.
19. Gavett B.E., Stern R.A., McKee A.C. Chronic traumatic encephalopathy: a potential late effect of sport-related concussive and subconcussive head trauma. Clin. Sports Med. 2011, 30:179-188.
20. Giedd J.N. The teen brain: insights from neuroimaging. J. Adolesc. Health 2008, 42:335-343.
21. Gioia G.A., Schneider J.C., Vaughan C.G., Isquith P.K. Which symptom assessments and approaches are uniquely appropriate for paediatric concussion?. Br. J. Sports Med. 2009, 43(Suppl. 1):i13-i22.
22. Giza C.C., Griesbach G.S., Hovda D.A. Experience-dependent behavioral plasticity is disturbed following traumatic injury to the immature brain. Behav. Br. Res. 2005, 157:11-22.
23. Giza C.C., Hovda D.A. The neurometabolic cascade of concussion. J. Athl. Train. 2001, 36:228-235.
24. Giza C.C., Kolb B., Harris N.G., Asarnow R.F., Prins M.L. Hitting a moving target: basic mechanisms of recovery from acquired developmental brain injury. Dev. Neurorehabil. 2009, 12:255-268.
25. Giza C.C., Prins M.L. Is being plastic fantastic? Mechanisms of altered plasticity after developmental traumatic brain injury. Dev. Neurosci. 2006, 28:364-379.
26. Griesbach G.S., Gomez-Pinilla F., Hovda D.A. Time window for voluntary exercise-induced increases in hippocampal neuroplasticity molecules after traumatic brain injury is severity dependent. J. Neurotrauma 2007, 24:1161-1171.
27. Gurkoff G.G., Giza C.C., Hovda D.A. Lateral fluid percussion injury in the developing rat causes an acute, mild behavioral dysfunction in the absence of significant cell death. Br. Res. 2006, 1077:24-36.
28. Guskiewicz K.M., McCrea M., Marshall S.W., Cantu R.C., Randolph C., Barr W., Onate J.A., Kelly J.P. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA 2003, 290:2549-2555.
29. Guskiewicz K.M., Marshall S.W., Bailes J., McCrea M., Cantu R.C.C., Randolph B, Jordan D. Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery 2005, 57:719-726.
30. Guskiewicz K.M., Marshall S.W., Bailes J., McCrea M., Harding H.P., Matthews A., Mihalik J.R., Cantu R.C. Recurrent concussion and risk of depression in retired professional football players. Med. Sci. Sports Exerc. 2007, 39:903-909.
31. Hariri A.R., Goldberg T.E., Mattay V.S., Kolachana B.S., Callicott J.H., Egan M.F., Weinberger D.R. Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J. Neurosci. 2003, 23:6690-6694.
32. Huang M., et al. Integrated imaging approach with MEG and DTI to detect mild traumatic brain injury in military and civilian patients. J. Neurotrauma 2009, 229:64-75.
33. Huh J.W., Widing A.G., Raghupathi R. Basic science; repetitive mild non-contusive brain trauma in immature rats exacerbates traumatic axonal injury and axonal calpain activation: a preliminary report. J. Neurotrauma 2007, 24:15-27.
34. Ikonomidou C., Mosinger J.L., Salles K.S., Labruyere J., Olney J.W. Sensitivity of the developing rat brain to hypobaric/ischemic damage parallels sensitivity to N-methyl-aspartate neurotoxicity. J. Neurosci. 1989, 9:2809-2818.
35. Johnson C.P., Juranek J., Kramer L.A., Prasad M.R., Swank P.R., Ewing-Cobbs L. Predicting behavioral deficits in pediatric traumatic brain injury through uncinate fasciculus integrity. J. Int. Neuropsychol. Soc. 2011, 2011:1-11.
36. Juraska J.M., Markham J.A. The cellular basis for volume changes in the rat cortex during puberty: white-gray matter. Ann. N.Y. Acad. Sci. 2004, 1021:431-435.
37. Katayama Y., Becker D.P., Tamura T., Hovda D.A. Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J. Neurosurg. 1990, 73:889-900.
38. Keenan H.T., Runyan D.K., Nocera M. Child outcomes and family characteristics 1 year after severe inflicted or noninflicted traumatic brain injury. Pediatrics 2006, 117:317-324.
39. Kochanek P.M., et al. Adenosine A1 receptor knockout mice develop lethal status epilepticus after experimental traumatic brain injury. J. Cereb. Blood Flow Metab. 2006, 26:565-575.
40. Kolb B., Forgie M., Gibb R., Gorny G., Rowntree S. Age, experience and the changing brain. Neurosci. Biobehav. Rev. 1998, 22:143-159.
41. Kolb B., Gibb R., Gorny G. Experience-dependent changes in dendritic arbor and spine density in neocortex vary qualitatively with age and sex. Neurobiol. Learn. Mem. 2003, 79:1-10.
42. Kors E.E., et al. Delayed cerebral edema and fatal coma after minor head trauma: role of the CACNA1A calcium channel subunit gene and relationship with familial hemiplegic migraine. Ann. Neurol. 2001, 49:753-760.
43. Kraus M.F., Susmaras T., Caughlin B.P., Walker C.J., Sweeney J.A., Little D.M. White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain 2007, 130:2508-2519.
44. Langburt W., Cohen B., Akhthar N., apos O., Neill K., Lee J.C. Incidence of concussion in high school football players of Ohio and Pennsylvania. J. Child Neurol. 2001, 16:83-85.
45. Laviola G., Macri S., Morley-Fletcher S., Adriani W. Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci. Biobehav. Rev. 2003, 27:19-31.
46. Leao A.A. Further observations on the spreading depression of activity in the cerebral cortex. J. Neurophysiol. 1947, 10:409-414.
47. McCrory P., Collie A., Anderson V., Davis G. Can we manage sport related concussion in children the same as in adults?. Br. J. Sports Med. 2004, 38:516-519.
48. McCrory P., Meeuwisse W., Johnston K., Dvorak J., Aubry M., Molloy M., Cantu R. Consensus statement on concussion in sport. Br. J. Sports Med. 2009, 43:i76-i90.
49. McCrory P.R., Berkovic S.F. Second impact syndrome. Neurology 1998, 50:677-683.
50. McKee A.C., et al. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J. Neuropathol. Exp. Neurol. 2009, 68:709-735.
51. Moser R.S., Schatz P., Jordan B.D. Prolonged effects of concussion in high school athletes. Neurosurgery 2005, 57:300-306.
52. Nacajauskaite O., Endziniene M., Jureniene K., Schrader H. The validity of post-concussion syndrome in children: a controlled historical cohort study. Br. Dev. 2006, 28:507-514.
53. Nehlig A., de Vasconcelos A.P., Boyet S. Quantitative autoradiographic measurement of local cerebral glucose utilization in freely moving rats during postnatal development. J. Neurosci. 1988, 8:2321-2333.
54. Niogi S.N., Mukherjee P., Ghajar J., Johnson C.E., Kolster R., Lee H., Suh M., Zimmerman R.D., Manley G.T., McCandliss B.D. Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. Brain 2008, 131:3209-3221.
55. Niogi S.N., Mukherjee P. Diffusion tensor imaging of mild traumatic brain injury. J. Head Trauma Rehabil. 2010, 25:241-255.
56. Omalu B.I., DeKosky S.T., Minster R.L., Kamboh M.I., Hamilton R.L., Wecht C.H. Chronic traumatic encephalopathy in a National Football League player. Neurosurgery 2005, 57:128-134.
57. Oni M.B., Wilde E.A., Bigler E.D., McCauley S.R., Wu T.C., Yallampalli R., Chu Z., Hunter J.V., Vasquez A.C., Levin H.S. Diffusion tensor imaging analysis of frontal lobes in pediatric traumatic brain injury. J. Child Neurol. 2010, 25(8):976-984.
58. Prins M.L., Hovda D.A. Traumatic brain injury in the developing rat: effects of maturation on Morris water maze acquisition. J. Neurotrauma 1998, 15:799-811.
59. Prins M.L., Lee S.M., Cheng C.L., Becker D.P., Hovda D.A. Fluid percussion brain injury in the developing and adult rat: a comparative study of mortality, morphology, intracranial pressure and mean arterial blood pressure. Br. Res. Dev. Br. Res. 1996, 95:272-282.
60. Prins M.L., Hales A., Reger M., Giza C.C., Hovda D.A. Repeat traumatic brain injury in the juvenile rat is associated with increased axonal injury and cognitive impairments. Dev. Neurosci. 2010, 32:510-518.
61. Reeves T.M., Phillips L.L., Povlishock J.T. Myelinated and unmyelinated axons of the corpus callosum differ in vulnerability and functional recovery following traumatic brain injury. Exp. Neurol. 2005, 196:126-137.
62. Raghupathi R., Margulies S.S. Traumatic axonal injury after closed head injury in the neonatal pig. J. Neurotrauma 2002, 19:843-853.
63. Raghupathi R., Mehr M.F., Helfaer M.A., Margulies S.S. Traumatic axonal injury is exacerbated following repetitive closed head injury in the neonatal pig. J. Neurotrauma 2004, 23:307-316.
64. Reger M.L., Hovda D.A., Giza C.C. Ontogeny of rat recognition memory measured by the novel object recognition task. Dev. Psychobiol. 2009, 51:672-678.
65. Romijn H.J., Hofman M.A., Gramsbergen A. At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby?. Early Human Dev. 1991, 26:61-67.
66. Rubenstein J.L. Annual research review: development of the cerebral cortex: implications for neurodevelopmental disorders. J. Child Psychol. Psychiatry 2011, 52(4):339-355.
67. Sim A., Terryberry-Spohr L., Wilson K.R. Prolonged recovery of memory functioning after mild traumatic brain injury in adolescent athletes. J. Neurosurg. 2008, 108:511-516.
68. Slobounov S., Slobounov E., Sebastianelli W., Cao C., Newell K. Differential rate of recovery in athletes after first and second concussion episodes. Neurosurgery 2007, 61:338-344.
69. Smith S.L., Andrus P.K., Gleason D.D., Hall E.D. Infant rat model of the shaken baby syndrome: preliminary characterization and evidence for the role of free radicals in cortical hemorrhaging and progressive neuronal degeneration. J. Neurotrauma 1998, 15:693-705.
70. Smith S.L., Hall E.D. Tirilazad widens the therapeutic window for riluzole-induced attenuation of progressive cortical degeneration in an infant rat model of the shaken baby syndrome. J. Neurotrauma 1998, 15:707-719.
71. Sowell E.R., Thompson K.D., Toga A.W. Mapping changes in the human cortex throughout the span of life. Neuroscientist 2004, 10:372-392.
72. Sowell E.R., Thompson P.M., Tessner K.D., Toga A.W. Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: inverse relationships during postadolescent brain maturation. J. Neurosci. 2001, 21:8819-8829.
73. Stansfield K.H., Kirstein C.L. Effects of novelty on behavior in the adolescent and adult rat. Dev. Psychobiol. 2006, 48:10-15.
74. Talavage T.M., Nauman E., Breedlove E.L., Yoruk U., Dye A.E., Morigaki K., Feuer H., Leverenz L.J. Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. J. Neurotrauma 2010.
75. Wagner A.K., Miller M.A., Scanlon J., Ren D., Kochanek P.M., Conley Y.P. Adenosine A1 receptor gene variants associated with post-traumatic seizures after severe TBI. Epilepsy Res. 2010, 90:259-272.
76. Wilde E.A., et al. Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology 2008, 70:948-955.
77. Zhang L., Heier L.A., Zimmerman R.D., Jordan B., Ulug A.M. Diffusion anisotropy changes in the brains of professional boxers. Am. J. Neuroradiol. 2006, 27:2000-2004.