Quantitative MRI predicts long-term structural and functional outcome after experimental traumatic brain injury

NeuroImage

Volumn 45, Issue 1, 2009, Pages 1-9

  Immonen, Riikka J ^a   Kharatishvili, Irina ^b   Gröhn, Heidi ^c   Pitkänen, Asla ^b,d   Gröhn, Olli H J ^a  

^a Biomedical NMR Research Group   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c NORTH KARELIA CENTRAL HOSPITAL   (Finland)

^d KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

Diffusion; Fluid percussion model; Head trauma; Long term; Outcome; Quantitative MRI; T1 ; T2; Traumatic brain injury

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; BRAIN HEMORRHAGE; BRAIN SIZE; CONTROLLED STUDY; DEPTH PERCEPTION; DIFFUSION TENSOR IMAGING; HIPPOCAMPUS; LEARNING DISORDER; LONG TERM MEMORY; MALE; MAZE TEST; MEMORY DISORDER; NERVE DEGENERATION; NEUROIMAGING; NON INVASIVE PROCEDURE; NONHUMAN; PRIORITY JOURNAL; RAT; TASK PERFORMANCE; TRAUMATIC BRAIN INJURY;

ANIMALS; BRAIN INJURIES; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY DISORDERS; PROGNOSIS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 60349125442     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2008.11.022     Document Type: Article

References (62)

1. Albensi B.C., Knoblach S.M., Chew B.G., O'Reilly M.P., Faden A.I., and Pekar J.J. Diffusion and high resolution MRI of traumatic brain injury in rats: time course and correlation with histology. Exp. Neurol. 162 1 (2000) 61-72
2. Ashwal S., Babikian T., Gardner-Nichols J., Freier M.C., Tong K.A., and Holshouser B.A. Susceptibility-weighted imaging and proton magnetic resonance spectroscopy in assessment of outcome after pediatric traumatic brain injury. Arch. Phys. Med. Rehabil. 87 12 Suppl. 2 (2006) S50-S58
3. Belanger H.G., Vanderploeg R.D., Curtiss G., and Warden D.L. Recent neuroimaging techniques in mild traumatic brain injury. J. Neuropsychiatry Clin. Neurosci. 19 1 (2007) 5-20
4. Bigler E.D., Blatter D.D., Anderson C.V., Johnson S.C., Gale S.D., Hopkins R.O., and Burnett B. Hippocampal volume in normal aging and traumatic brain injury. AJNR. Am. J. Neuroradiol. 18 1 (1997) 11-23
5. Bramlett H.M., and Dietrich W.D. Quantitative structural changes in white and gray matter 1 year following traumatic brain injury in rats. Acta Neuropathol. (Berl) 103 (2002) 607-614
6. Bramlett H.M., Kraydieh S., Green E.J., and Dietrich W.D. Temporal and regional patterns of axonal damage following traumatic brain injury: a beta-amyloid precursor protein immunocytochemical study in rats. J. Neuropathol. Exp. Neurol. 56 10 (1997) 1132-1141
7. Carbonell W.S., and Grady M.S. Evidence disputing the importance of excitotoxicity in hippocampal neuron death after experimental traumatic brain injury. Ann. N.Y. Acad. Sci. 890 (1999) 287-298
8. Caroli M., Locatelli M., Campanella R., Balbi S., Martinelli F., and Arienta C. Multiple intracranial lesions in head injury: clinical considerations, prognostic factors, management, and results in 95 patients. Surg. Neurol. 56 2 (2001) 82-88
9. Catroppa C., Anderson V., Ditchfield M., and Coleman L. Using magnetic resonance imaging to predict new learning outcome at 5 years after childhood traumatic brain injury. J. Child Neurol. 23 5 (2008) 486-496
10. Cernak I., Vink R., Zapple D.N., Cruz M.I., Ahmed F., Chang T., Fricke S.T., and Faden A.I. The pathobiology of moderate diffuse traumatic brain injury as identified using a new experimental model of injury in rats. Neurobiol. Dis. 17 1 (2004) 29-43
11. Chieregato A., Fainardi E., Morselli-Labate A.M., Antonelli V., Compagnone C., Targa L., Kraus J., and Servadei F. Factors associated with neurological outcome and lesion progression in traumatic subarachnoid hemorrhage patients. Neurosurgery 56 4 (2005) 671-680 discussion 671-80
12. Conti A.C., Raghupathi R., Trojanowski J.Q., and McIntosh T.K. Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period. J. Neurosci.: Off. J. Soc. Neurosci. 18 15 (1998) 5663-5672
13. Cortez S.C., McIntosh T.K., and Noble L.J. Experimental fluid percussion brain injury: Vascular disruption and neuronal and glial alterations. Brain Res. 482 (1989) 271-282
14. Dubreuil C.I., Marklund N., Deschamps K., McIntosh T.K., and McKerracher L. Activation of rho after traumatic brain injury and seizure in rats. Exp. Neurol. 198 2 (2006) 361-369
15. Freund T.F., Ylinen A., Miettinen R., Pitkänen A., Lahtinen H., Baimbridge K.G., and Riekkinen P.J. Pattern of neuronal death in the rat hippocampus after status epilepticus. Relationship to calcium binding protein content and ischemic vulnerability. Brain Res. Bull. 28 1 (1992) 27-38 Jan
16. Gallagher C.N., Hutchinson P.J., and Pickard J.D. Neuroimaging in trauma. Curr. Opin. Neurol. 20 4 (2007) 403-409
17. Gentry L.R., Godersky J.C., and Thompson B. MR imaging of head trauma: review of the distribution and radiopathologic features of traumatic lesions. Am. J. Roentgenol. 150 3 (1988) 663-672
18. Gerber D.J., Weintraub A.H., Cusick C.P., Ricci P.E., and Whiteneck G.G. Magnetic resonance imaging of traumatic brain injury: relationship of T2*SE and T2GE to clinical severity and outcome. Brain Inj.: [BI] 18 11 (2004) 1083-1097
19. Graham D.I., McIntosh T.K., Maxwell W.L., and Nicoll J.A. Recent advances in neurotrauma. J. Neuropathol. Exp. Neurol. 59 8 (2000) 641-651
20. Graham D.I., Raghupathi R., Saatman K.E., Meaney D., and McIntosh T.K. Tissue tears in the white matter after lateral fluid percussion brain injury in the rat: relevance to human brain injury. Acta Neuropathol. 99 2 (2000) 117-124
21. Grohn O.H., Lukkarinen J.A., Silvennoinen M.J., Pitkanen A., van Zijl P.C., and Kauppinen R.A. Quantitative magnetic resonance imaging assessment of cerebral ischemia in rat using on-resonance T(1) in the rotating frame. Magn. Reson. Med. Off. J. Soc. Magn. Reson. Med. / Soc. Magn. Reson. Med. 42 2 (1999) 268-276
22. Grohn O.H.J., Kettunen M.I., Makela H.I., Penttonen M., Pitkanen A., Lukkarinen J.A., and Kauppinen R.A. Early detection of irreversible cerebral ischemia in the rat using dispersion of the magnetic resonance imaging relaxation time, T1rho. J. Cereb. Blood Flow Metab. Off. J. Int. Soc. Cereb. Blood Flow Metab. 20 10 (2000) 1457-1466
23. Hadley D.M., Teasdale G.M., Jenkins A., Condon B., MacPherson P., Patterson J., and Rowan J.O. Magnetic resonance imaging in acute head injury. Clin. Radiol. 39 2 (1988) 131-139
24. Hatashita S., and Hoff J.T. Brain edema and cerebrovascular permeability during cerebral ischemia in rats. Stroke; J. Cereb. Circ. 21 4 (1990) 582-588
25. Hicks R., Soares H., Smith D., and McIntosh T. Temporal and spatial characterization of neuronal injury following lateral fluid-percussion brain injury in the rat. Acta Neuropathol. (Berl) 91 (1996) 236-246
26. Immonen R., Kharatishvili I., Niskanen J.P., Gröhn H., Pitkänen A., and Gröhn O. Distinct MRI pattern in lesional and perilesional area after traumatic brain injury in rat - 11 months follow-up. Exp. Neurol. 215 (2009) 29-40
27. Ito U., Ohno K., Nakamura R., Suganuma F., and Inaba Y. Brain edema during ischemia and after restoration of blood flow. measurement of water, sodium, potassium content and plasma protein permeability. Stroke; J. Cereb. Circ. 10 5 (1979) 542-547
28. Iwamoto Y., Yamaki T., Murakami N., Umeda M., Tanaka C., Higuchi T., Aoki I., Naruse S., and Ueda S. Investigation of morphological change of lateral and midline fluid percussion injury in rats, using magnetic resonance imaging. Neurosurgery 40 1 (1997) 163-167
29. Karhunen H., Pitkanen A., Virtanen T., Gureviciene I., Pussinen R., Ylinen A., Sivenius J., Nissinen J., and Jolkkonen J. Long-term functional consequences of transient occlusion of the middle cerebral artery in rats: a 1-year follow-up of the development of epileptogenesis and memory impairment in relation to sensorimotor deficits. Epilepsy Res. 54 1 (2003) 1-10
30. Kharatishvili I., Nissinen J.P., McIntosh T.K., and Pitkanen A. A model of posttraumatic epilepsy induced by lateral fluid-percussion brain injury in rats. Neuroscience 140 2 (2006) 685-697
31. Kharatishvili I., Immonen R., Grohn O., and Pitkanen A. Quantitative diffusion MRI of hippocampus as a surrogate marker for post-traumatic epileptogenesis. Brain J. Neurol. 130 Pt 12 (2007) 3155-3168
32. Kinoshita K., Chatzipanteli K., Alonso O.F., Howard M., and Dietrich W.D. The effect of brain temperature on hemoglobin extravasation after traumatic brain injury. J. Neurosurg. 97 4 (2002) 945-953
33. Kurth S.M., Bigler E.D., and Blatter D.D. Neuropsychological outcome and quantitative image analysis of acute haemorrhage in traumatic brain injury: preliminary findings. Brain Inj.: [BI] 8 6 (1994) 489-500
34. Lenzlinger P.M., Morganti-Kossmann M.C., Laurer H.L., and McIntosh T.K. The duality of the inflammatory response to traumatic brain injury. Mol. Neurobiol. 24 1-3 (2001) 169-181
35. Leon-Carrion J., Dominguez-Morales, Mdel R., Barroso y Martin J.M., and Murillo-Cabezas F. Epidemiology of traumatic brain injury and subarachnoid hemorrhage. Pituitary 8 3-4 (2005) 197-202
36. Lewine J.D., Davis J.T., Bigler E.D., Thoma R., Hill D., Funke M., Sloan J.H., Hall S., and Orrison W.W. Objective documentation of traumatic brain injury subsequent to mild head trauma: multimodal brain imaging with MEG, SPECT, and MRI. J. Head Trauma Rehabil. 22 3 (2007) 141-155
37. Lowenstein D.H., Thomas M.J., Smith D.H., and McIntosh T.K. Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J. Neurosci. 12 1 (1992) 4846-4853
38. Mac Donald C.L., Dikranian K., Song S.K., Bayly P.V., Holtzman D.M., and Brody D.L. Detection of traumatic axonal injury with diffusion tensor imaging in a mouse model of traumatic brain injury. Exp. Neurol. 205 1 (2007) 116-131
39. Makela H.I., Grohn O.H., Kettunen M.I., and Kauppinen R.A. Proton exchange as a relaxation mechanism for T1 in the rotating frame in native and immobilized protein solutions. Biochem. Biophys. Res. Commun. 289 4 (2001) 813-818
40. McIntosh T.K., Vink R., Noble L., Yamakami I., Fernyak S., Soares H., and Faden A.L. Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28 (1989) 233-244
41. Metting Z., Rodiger L.A., De Keyser J., and van der Naalt J. Structural and functional neuroimaging in mild-to-moderate head injury. Lancet Neurol. 6 8 (2007) 699-710
42. Morais D.F., Spotti A.R., Tognola W.A., Gaia F.F., and Andrade A.F. Clinical application of magnetic resonance in acute traumatic brain injury. Arq. Neuro-Psiquiatr. 66 1 (2008) 53-58
43. Nairismagi J., Grohn O.H., Kettunen M.I., Nissinen J., Kauppinen R.A., and Pitkanen A. Progression of brain damage after status epilepticus and its association with epileptogenesis: A quantitative MRI study in a rat model of temporal lobe epilepsy. Epilepsia 45 9 (2004) 1024-1034
44. Nimmo A.J., Cernak I., Heath D.L., Hu X., Bennett C.J., and Vink R. Neurogenic inflammation is associated with development of edema and functional deficits following traumatic brain injury in rats. Neuropeptides 38 1 (2004) 40-47
45. Obenaus A., Robbins M., Blanco G., Galloway N.R., Snissarenko E., Gillard E., Lee S., and Curras-Collazo M. Multi-modal magnetic resonance imaging alterations in two rat models of mild neurotrauma. J. Neurotrauma 24 7 (2007) 1147-1160
46. Oh H.S., Seo W.S., Lee S., and Song H. Comparisons of the prognostic predictors of traumatic brain injury according to admission glasgow coma scale scores-based on 1- and 6-month assessments. Taehan Kanho Hakhoe Chi 36 4 (2006) 621-629
47. Onyszchuk G., Al-Hafez B., He Y.Y., Bilgen M., Berman N.E., and Brooks W.M. A mouse model of sensorimotor controlled cortical impact: characterization using longitudinal magnetic resonance imaging, behavioral assessments and histology. J. Neurosci. Methods 160 2 (2007) 187-196
48. In: Paxinos G., and Watson C. (Eds). The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, New York
49. Philips M.F., Mattiasson G., Wieloch T., Bjorklund A., Johansson B.B., Tomasevic G., Martinez-Serrano A., Lenzlinger P.M., Sinson G., Grady M.S., et al. Neuroprotective and behavioral efficacy of nerve growth factor-transfected hippocampal progenitor cell transplants after experimental traumatic brain injury. J. Neurosurg. 94 5 (2001) 765-774
50. Pierce J.E., Smith D.H., Trojanowski J.Q., and McIntosh T.K. Enduring cognitive, neurobehavioral and histopathological changes persist for up to one year following severe experimental brain injury in rats. Neuroscience 87 2 (1998) 359-369
51. Salmond C.H., Menon D.K., Chatfield D.A., Williams G.B., Pena A., Sahakian B.J., and Pickard J.D. Diffusion tensor imaging in chronic head injury survivors: correlations with learning and memory indices. NeuroImage 29 1 (2006) 117-124
52. Scheid R., Ott D.V., Roth H., Schroeter M.L., and von Cramon D.Y. Comparative magnetic resonance imaging at 1.5 and 3 tesla for the evaluation of traumatic microbleeds. J. Neurotrauma 24 12 (2007) 1811-1816
53. Schmidt R.H., and Grady M.S. Regional patterns of blood-brain barrier breakdown following central and lateral fluid percussion injury in rodents. J. Neurotrauma 10 4 (1993) 415-430
54. Sepponen R.E., Pohjonen J.A., Sipponen J.T., and Tanttu J.I. A method for T1 rho imaging. J. Comput. Assist. Tomogr. 9 6 (1985) 1007-1011
55. Smith D.H., Okiyama K., Thomas M.J., Claussen B., and McIntosh T.K. Evaluation of memory dysfunction following experimental brain injury using the morris water maze. J. Neurotrauma 8 4 (1991) 259-269
56. Smith D.H., Chen X.H., Pierce J.E., Wolf J.A., Trojanowski J.Q., Graham D.I., and McIntosh T.K. Progressive atrophy and neuron death for one year following brain trauma in the rat. J. Neurotrauma 14 1 (1997) 715-727
57. Soares H.D., Hicks R.R., Smith D., and McIntosh T.K. Inflammatory leukocytic recruitment and diffuse neuronal degeneration are separate pathological processes resulting from traumatic brain injury. J. Neurosci. Off. J. Soc. Neurosci. 15 12 (1995) 8223-8233
58. Tagliaferri F., Compagnone C., Korsic M., Servadei F., and Kraus J. A systematic review of brain injury epidemiology in europe. Acta Neurochir. 148 3 (2006) 255-268 discussion 268
59. Thompson H.J., Lifshitz J., Marklund N., Grady M.S., Graham D.I., Hovda D.A., and McIntosh T.K. Lateral fluid percussion brain injury: a 15-year review and evaluation. J. Neurotrauma 22 1 (2005) 42-75
60. Van Putten H.P., Bouwhuis M.G., Muizelaar J.P., Lyeth B.G., and Berman R.F. Diffusion-weighted imaging of edema following traumatic brain injury in rats: effects of secondary hypoxia. J. Neurotrauma 22 8 (2005) 857-872
61. Vink R., Mullins P.G., Temple M.D., Bao W., and Faden A.I. Small shifts in craniotomy position in the lateral fluid percussion injury model are associated with differential lesion development. J. Neurotrauma 18 8 (2001) 839-847
62. Wilde E.A., Bigler E.D., Hunter J.V., Fearing M.A., Scheibel R.S., Newsome M.R., Johnson J.L., Bachevalier J., Li X., and Levin H.S. Hippocampus, amygdala, and basal ganglia morphometrics in children after moderate-to-severe traumatic brain injury. Dev. Med. Child Neurol. 49 4 (2007) 294-299