A model for mild traumatic brain injury that induces limited transient memory impairment and increased levels of axon related serum biomarkers

Frontiers in Neurology

Volumn JUL, Issue , 2012, Pages

  Rostami, Elham ^a   Davidsson, Johan ^b   Chye Ng, Kian ^c   Lu, Jia ^c   Gyorgy, Andrea ^d   Walker, John ^d   Wingo, Daniel ^d   Plantman, Stefan ^a   Bellander, Bo Michael ^e   Agoston, Denes V ^d   Risling, Mårten ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^c DSO NATIONAL LABORATORIES   (Singapore)

^d UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^e KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

APP; Behavioral outcome; Brain trauma model; DAI; Mild traumatic brain injury; NF H; S100B; Serum biomarker

Indexed keywords

EID: 84865987823     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2012.00115     Document Type: Article

References (46)

1. Anderson, K. J., Scheff, S. W., Miller, K. M., Roberts, K. N., Gilmer, L. K., Yang, C., and Shaw, G. (2008). The phosphorylated axonal form of the neurofilament subunit NF-H (pNF-H) as a blood biomarker of traumatic brain injury. J. Neurotrauma 25,1079-1085.
2. Bazarian, J. J., and Atabaki, S. (2001). Predicting postconcussion syndrome after minor traumatic brain injury. Acad. Emerg. Med. 8, 788-795.
3. Bazarian, J. J., Blyth, B., and Cimpello, L. (2006). Bench to bedside: evidence for brain injury after concussion - lo oking beyond the computed tomography scan. Acad. Emerg. Med. 13,199-214.
4. Bazarian, J. J., Wong, T., Harris, M., Lea-hey, N., Mookerjee, S., and Dom-bovy, M. (1999). Epidemiology and predictors of post-concussive syndrome after minor head injury in an emergency population. Brain Inj. 13, 173-189.
5. Berger, R. P., Adelson, P. D., Pierce, M. C., Dulani, T., Cassidy, L. D., and Kochanek, P. M. (2005). Serum neuron-specific enolase, S100B, and myelin basic protein concentrations after inflicted and noninflicted traumatic brain injury in children. J. Neurosurg. 103, 61-68.
6. Binder, L. I., Frankfurter, A., and Reb-hun, L. I. (1985). The distribution of tau in the mammalian central nervous system. J. Cell Biol. 101, 1371-1378.
7. Blumbergs, P. C., Scott, G., Manavis, J., Wainwright, H., Simpson, D. A., andMclean,A. J. (1994). Staining of amyloid precursor protein to study axonal damage in mild head injury. Lancet 344, 1055-1056.
8. Blumbergs, P. C., Scott, G., Manavis, J., Wainwright, H., Simpson, D. A., and Mclean, A. J. (1995). Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury. J. Neurotrauma 12,565-572.
9. Bulut, M., Koksal, O., Dogan, S., Bolca, N., Ozguc, H., Korfali, E., Ilcol, Y. O., and Parklak, M. (2006). Tau protein as a serum marker of brain damage in mild traumatic brain injury: preliminary results. Adv. Ther. 23, 12-22.
10. Cernak, I. (2005). Animal models of head trauma. NeuroRx 2, 410-422.
11. Cernak, I., Vink, R., Zapple, D. N., Cruz, M. I., Ahmed, F., Chang, T., Fricke, S. T., and Faden, A. I. (2004). The pathobiology of moderate diffuse traumatic brain injury as identified using a new experimental model of injury in rats. Neurobiol Dis. 17, 29-43.
12. Chu, Z., Wilde, E. A., Hunter, J. V., Mccauley, S. R., Bigler, E. D., Troy-anskaya, M., Yallampalli, R., Chia, J. M., and Levin, H. S. (2010). Voxel-based analysis of diffusion tensor imaging in mild traumatic brain injury in adolescents. AJNR Am. J. Neuroradiol. 31, 340-346.
13. Davidsson, J., and Risling, M. (2011). A new model to produce sagittal plane rotational induced diffuse axonal injuries. Front. Neurol. 2:41. doi:10.3389/fneur.2011.00041
14. Donato, R. (1999). Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim. Biophys. Acta 1450, 191-231.
15. Folkerts, M. M., Berman, R. F., Muize-laar, J. P., and Rafols, J. A. (1998). Disruption of MAP-2 immunostain-ing in rat hippocampus after traumatic brain injury. J. Neurotrauma 15, 349-363.
16. Goldstein, L. B., and Davis, J. N. (1990). Beam-walking in rats: studies towards developing an animal model of functional recovery after brain injury.J. Neurosci. Methods31, 101-107.
17. Gyorgy, A., Ling, G., Wingo, D., Walker, J., Tong, L., Parks, S., Januszkiewicz, A., Baumann, R., and Agoston, D. V. (2011). Time-dependent changes in serum biomarker levels after blast traumatic brain injury. J. Neurotrauma 28, 1121-1126.
18. Gyorgy, A. B., Walker, J., Wingo, D., Eidelman, O., Pollard, H. B., Mol-nar, A., and Agoston, D. V. (2010). Reverse phase protein microar-ray technology in traumatic brain injury. J. Neurosci. Methods 192, 96-101.
19. Julien, J. P., and Mushynski, W E. (1998). Neurofilaments in health and disease. Prog. Nucleic Acid Res. Mol. Biol. 61,1-23.
20. Kavalci, C., Pekdemir, M., Durukan, P., Ilhan, N., Yildiz, M., Serhatlioglu, S., and Seckin, D. (2007). The value of serum tau protein for the diagnosis of intracranial injury in minor head trauma. Am. J. Emerg. Med. 25, 391-395.
21. King, N. S., Crawford, S., Wenden, F. J., Caldwell, F. E., and Wade, D. T. (1999). Early prediction of persisting post-concussion symptoms following mild and mo derate head injuries. Br.J. Clin. Psychol. 38(Pt 1), 15-25.
22. Kovesdi, E., Luckl, J., Bukovics, P., Farkas, O., Pal, J., Czeiter, E., Szel-lar, D., Doczi, T., Komoly, S., and Buki, A. (2010). Update on protein biomarkers in traumatic brain injury with emphasis on clinical use in adults and pediatrics. Acta Neu-rochir. (Wien) 152,1-17.
23. Lau, A. A., Crawley, A. C., Hopwood, J. J., and Hemsley, K. M. (2008). Open field locomotor activity and anxiety-related behaviors in mucopolysac-charidosis type IIIA mice. Behav. Brain Res. 191, 130-136.
24. Liliang, P. C., Liang, C. L., Lu, K., Wang, K.W.,Weng,H.C.,Hsieh,C.H.,Tsai, Y. D., and Chen, H. J. (2010). Relationship between injury severity and serum tau protein levels in traumatic brain injured rats. Resuscitation 81, 1205-1208.
25. Liu, M. C., Akle, V., Zheng, W., Kitlen, J., O'steen, B., Larner, S. F., Dave, J. R., Tortella, F. C., Hayes, R. L., and Wang, K. K. (2006). Extensive degradation of myelin basic protein isoforms by calpain following traumatic brain injury. J. Neurochem. 98, 700-712.
26. Lyeth, B. G., Jenkins, L. W., Hamm, R. J., Dixon, C. E., Phillips, L. L., Clifton, G. L., Young, H. F., and Hayes, R. L. (1990). Prolonged memory impairment in the absence of hippocam-pal cell death following traumatic brain injury in the rat. Brain Res. 526, 249-258.
27. Marmarou, A., Foda, M. A., Van Den Brink, W., Campbell, J., Kita, H., and Demetriadou, K. (1994). A new model of diffuse brain injury in rats. Part I: pathophysiology and biomechanics. J. Neurosurg. 80, 291-300.
28. Maruichi, K., Kuroda, S., Chiba, Y., Hokari, M., Shichinohe, H., Hida, K., and Iwasaki, Y. (2009). Graded model of diffuse axonal injury for studying head injury-induced cognitive dysfunction in rats. Neuropathology 29, 132-139.
29. Mayer, A. R., Ling, J., Mannell, M. V., Gasparovic, C., Phillips, J. P., Doezema, D., Reichard, R., and Yeo, R. A. (2010). A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 74, 643-650.
30. Middleboe, T., Andersen, H. S., Birket-Smith, M., and Friis, M. L. (1992). Minor head injury: impact on general health after 1 year. A prospective follow-up study. Acta Neurol. Scand. 85, 5-9.
31. Morales, D. M., Marklund, N., Lebold, D., Thompson, H. J., Pitkanen, A., Maxwell, W. L., Longhi, L., Lau-rer, H., Maegele, M., Neugebauer, E., Graham, D. I., Stocchetti, N., and Mcintosh, T. K. (2005). Experimental models of traumatic brain injury: do we really need to build a better mousetrap? Neuroscience 136, 971-989.
32. Ng, H. K., Mahaliyana, R. D., and Poon, W. S. (1994). The pathological spectrum of diffuse axonal injury in blunt head trauma: assessment with axon and myelin strains. Clin. Neurol. Neurosurg. 96,24-31.
33. Niogi, S. N., Mukherjee, P., Ghajar, J., Johnson, C., Kolster, R. A., Sarkar, R., Lee, H., Meeker, M., Zimmerman, R. D., Manley, G. T., and Mccandliss, B. D. (2008a). Extent of microstruc-tural white matter injury in post-concussive syndrome correlates with impaired cognitive reaction time: a 3T diffusion tensor imaging study of mild traumatic brain injury. AJNR Am. I Neuroradiol. 29, 967-973.
34. Niogi, S. N., Mukherjee, P., Ghajar, J., Johnson, C. E., Kolster, R., Lee, H., Suh, M., Zimmerman, R. D., Manley, G. T., and Mccandliss, B. D. (2008b). Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. Brain 131, 3209-3221.
35. Nishizuka, S., Charboneau, L.,Young, L., Major, S., Reinhold, W. C., Waltham, M., Kouros-Mehr, H., Bussey, K. J., Lee, J. K., Espina, V., Munson, P. J., Petricoin, E. III., Liotta, L. A., and Weinstein, J. N. (2003). Proteomic profiling of the NCI-60 cancer cell lines usingnew high-density reverse-phase lysate microarrays. Proc. Natl. Acad. Sci. U.S.A. 100, 14229-14234.
36. Pierce, J. E., Smith, D. H., Trojanowski, J. Q., and Mcintosh, T. K. (1998). Enduring cognitive, neurobehav-ioral and histopathological changes persist for up to one year following severe experimental brain injury in rats. Neuroscience 87, 359-369.
37. Plantman, S., Ng, K. C., Lu, J., Davids-son, J., and Risling, M. (2012). Characterization of a novel rat model of penetrating traumatic brain injury. J. Neurotrauma 29, 1219-1232.
38. Risling, M., Plantman, S., Angeria, M., Rostami, E., Bellander, B. M., Kirkegaard, M., Arborelius, U., and Davidsson, J. (2011). Mechanisms of blast induced brain injuries, experimental studies in rats. Neuroimage 54(Suppl. 1),S89-S97.
39. Scheff, S. W., Baldwin, S. A., Brown, R. W., and Kraemer, P. J. (1997). Morris water maze deficits in rats following traumatic brain injury: lateral controlled cortical impact. J. Neurotrauma 14,615-627.
40. Shaw, G., Yang, C., Ellis, R., Anderson, K., Parker Mickle, J., Scheff, S., Pike, B., Anderson, D. K., and Howland, D. R. (2005). Hyperphos-phorylated neurofilament NF-H is a serum biomarker of axonal injury. Biochem. Biophys. Res. Commun. 336, 1268-1277.
41. Spurrier, B., Ramalingam, S., and Nishizuka, S. (2008). Reverse-phase protein lysate microarrays for cell signaling analysis. Nat. Protoc. 3, 1796-1808.
42. Thomas, D. G., Palfreyman, J. W., and Ratcliffe, J. G. (1978). Serum-myelin-basic-protein assay in diagnosis and prognosis of patients with head injury. Lancet 1, 113-115.
43. Unden, J., and Romner, B. (2010). Can low serum levels of S100B predict normal CT findings after minor head injury in adults?: an evidence-based review and meta-analysis. J. Head Trauma Rehabil. 25, 228-240.
44. Walf, A. A., and Frye, C. A. (2007). The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat. Protoc. 2, 322-328.
45. Watson, M. R., Fenton, G. W., Mcclel-land, R. J., Lumsden, J., Headley, M., and Rutherford, W H. (1995). The post-concussional state: neurophysi-ological aspects. Br.J. Psychiatry 167, 514-521.
46. Wilde, E. A., Mccauley, S. R., Hunter, J. V., Bigler, E. D., Chu, Z., Wang, Z. J., Hanten, G. R., Troyanskaya, M., Yallampalli, R., Li, X., Chia, J., and Levin, H. S. (2008). Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology 70, 948-955.