Synthesis of Findings, Current Investigations, and Future Directions: Operation Brain Trauma Therapy

Journal of Neurotrauma

Volumn 33, Issue 6, 2016, Pages 606-614

  Kochanek, Patrick M ^a   Bramlett, Helen M ^b,c   Shear, Deborah A ^d   Dixon, C Edward ^e   Mondello, Stefania ^f   Dietrich, W Dalton ^b   Hayes, Ronald L ^g   Wang, Kevin K W ^g   Poloyac, Samuel M ^h   Empey, Philip E ^h   Povlishock, John T ⁱ   Mountney, Andrea ^d   Browning, Megan ^a   Deng Bryant, Ying ^d   Yan, Hong Q ^e   Jackson, Travis C ^a   Catania, Michael ^j   Glushakova, Olena ^j   Richieri, Steven P ^j   Tortella, Frank C ^d  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF MESSINA   (Italy)

^g UNIVERSITY OF FLORIDA HEALTH   (United States)

^h UNIVERSITY OF PITTSBURGH   (United States)

ⁱ VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^j Banyan Biomarkers ^*  (United States)

more..

Author keywords

biomarker; controlled cortical impact; drug; fluid percussion; micropig; penetrating ballistic like brain injury; pre clinical modeling; rat; reproducibility; therapy; traumatic brain injury

Indexed keywords

AER 271; BIOLOGICAL MARKER; CYCLOSPORIN A; ERYTHROPOIETIN; ETIRACETAM; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIBENCLAMIDE; METHYLPREDNISOLONE; NICOTINAMIDE; POVIDONE; SIMVASTATIN; UNCLASSIFIED DRUG; NEUROPROTECTIVE AGENT;

ARTICLE; BATTLE INJURY; DEGENERATIVE DISEASE; NONHUMAN; RIGOR; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN INJURIES, TRAUMATIC; DISEASE MODEL; MALE; NEUROLOGY; PRECLINICAL STUDY; PROCEDURES; RAT; SPRAGUE DAWLEY RAT; TRENDS;

ANIMALS; BRAIN INJURIES, TRAUMATIC; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; MALE; NEUROLOGY; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84962283654     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2015.4133     Document Type: Article

References (52)

1. Kochanek, P.M., Bramlett, H.M., Dixon, C.E., Shear, D.A., Dietrich, W.D., Schmid, K.E., Mondello, S., Wang, K.K., Hayes, R.L., Povlishock, J.T., and Tortella, F.C. (2016). Approach to modeling, therapy evaluation, drug selection, and biomarker assessments, for a multicenter pre-clinical drug screening consortium for acute therapies in severe traumatic brain injury: Operation brain trauma therapy. J. Neurotrauma 33, 513-522.
2. Shear, D.A., Dixon, C.E., Bramlett, H.M., Mondello, S., Dietrich, W.D., Deng-Bryant, Y., Schmid, K.E., Wang, K.K., Hayes, R.L., Povlishock, J.T., Kochanek, P.M., and Tortella, F.C. (2016). Nicotinamide treatment in traumatic brain injury: Operation brain trauma therapy. J. Neurotrauma 33, 523-537.
3. Bramlett, H.M., Dietrich, W.D., Dixon, C.E., Shear, D.A., Schmid, K.E., Mondello, S., Wang, K.K., Hayes, R.L., Povlishock, J.T., Tortella, F.C., and Kochanek, P.M. (2016). Erythropoietin treatment in traumatic brain injury: Operation brain trauma therapy. J. Neurotrauma 33, 538-552.
4. Dixon, C.E., Bramlett, H.M., Dietrich, W.D., Shear, D.A., Yan, H.Q., Deng-Bryant, Y., Mondello, S., Wang, K.K., Hayes, R.L., Empey, P.E., Povlishock, J.T., Tortella, F.C., and Kochanek, P.M. (2016). Cyclosporine treatment in traumatic brain injury: Operation brain trauma therapy. J. Neurotrauma 33, 553-566.
5. Mountney, A., Bramlett, H.M., Dixon, C.E., Mondello, S., Dietrich, W.D., Wang, K.K.W., Hayes, R.L., Schmid, K.E., Povlishock, J.T., Tortella, F.C., Kochanek, P.M., and Shear, D.A. (2015). Simvastatin treatment in traumatic brain injury: Operation brain trauma therapy. J. Neurotrauma 33, 567-580.
6. Browning, M., Shear, D.A., Bramlett, H.M., Dixon, C.E., Mondello, S., Schmid, K.E., Poloyac, S.M., Dietrich, W.D., Hayes, R.L., Wang, K.K., Povlishock, J.T., Tortella, F.C., and Kochanek, P.M. (2016). Levetiracetam treatment in traumatic brain injury: Operation brain trauma therapy. J. Neurotrauma 33, 581-594.
7. Mondello, S., Shear, D.A., Bramlett, H.M., Dixon, C.E., Schmid, K.E., Dietrich, W.D., Wang, K. K., Hayes, R.L., Glushakova, O., Catania, M., Richieri, S., Povlishock, J.T., Tortella, F.C., and Kochanek, P.M. (2016). Insight into pre-clinical models of traumatic brain injury using circulating brain damage biomarkers: Operation brain trauma therapy. J. Neurotrauma 33, 595-605.
8. Basso, D.M., Beattie, M.S., Bresnahan, J.C., Anderson, D.K., Faden, A.I., Gruner, J.A., Holford, T.R., Hsu, C.Y., Noble, L.J., Nockels, R., Perot, P.L., Salzman, S.K., and Young, W. (1996). MASCIS evaluation of open field locomotor scores: effects of experience and teamwork on reliability. Multicenter Animal Spinal Cord Injury Study. J. Neurotrauma 13, 343-359.
9. Beattie, M.S., Bresnahan, J.C., Komon, J., Tovar, C.A., Van Meter, M., Anderson, D.K., Faden, A.I., Hsu, C.Y., Noble, L.J., Salzman, S., and Young, W. (1997). Endogenous repair after spinal cord contusion injuries in the rat. Exp. Neurol. 148, 453-463.
10. Bigler, E.D. (2014). Comment: Importance of cognitive reserve in traumatic brain injury. Neurology 82, 1641.
11. Saatman, K.E., Duhaime, A.C., Bullock, R., Maas, A.I., Valadka, A., and Manley, G.T. (2008). Classification of traumatic brain injury for targeted therapies. J. Neurotrauma 25, 719-738.
12. Hawryluk, G.W.J., and Manley, G.T. (2015). Classification of traumatic brain injury: past, present, and future. Handb. Clin. Neurol. 127, 15-21.
13. Papa, L., Lewis, L.M., Silvestri, S., Falk, J.L., Giordano, P., Brophy, G.M., Demery, J.A., Liu, M.C., Mo, J., Akinyi, L., Mondello, S., Schmid, K., Robertson, C.S., Tortella, F.C., Hayes, R.L., and Wang, K.K. (2012). Serum levels of ubiquitin C-terminal hydrolase distinguish mild traumatic brain injury from trauma controls and are elevated in mild and moderate traumatic brain injury patients with intracranial lesions and neurosurgical intervention. J. Trauma Acute Care Surg. 72, 1335-1344.
14. Plog, B.A., Dashnaw, M.L., Hitomi, E., Peng, W., Liao, Y., Lou, N., Deane, R., and Nedergaard, M. (2015). Biomarkers of traumatic injury are transported from brain to blood via the glymphatic system. J. Neurosci. 35, 518-526.
15. Wang, H., Gao, J., Lassiter, T.F., McDonagh, D.L., Sheng, H., Warner, D.S., Lynch, J.R., and Laskowitz, D.T. (2006). Levetiracetam is neuroprotective in murine models of closed head injury and subarachnoid hemorrhage. Neurocrit. Care 5, 71-78.
16. Hoane, M.R., Tan, A.A., Pierce, J.L., Anderson, G.D., and Smith, D.C. (2006). Nicotinamide treatment reduces behavioral impairments and provides cortical protection after fluid percussion injury in the rat. J. Neurotrauma 23, 1535-1548.
17. Hemerka, J.N., Wu, X., Dixon, C.E., Garman, R.H., Exo, J.L., Shellington, D.K., Blasiole, B., Vagni, V.A., Janesko-Feldman, K., Xu, M., Wisniewski, S.R., Bayir, H., Jenkins, L.W., Clark, R.S., Tisherman, S.A., and Kochanek, P.M. (2012). Severe brief pressure-controlled hemorrhagic shock after traumatic brain injury exacerbates functional deficits and long-term neuropathological damage in mice. J. Neurotrauma 29, 2192-2208.
18. Diaz-Arrastia, R., Kochanek, P.M., Bergold, P., Kenney, K., Marx, C.E., Grimes, C.J.B., Loh, L.T., Adam, L.T., Oskvig, D., Curley, K.C., and Salzer,W. (2014). Pharmacotherapy of traumatic brain injury: state of the science and the road forward: report of the Department of Defense Neurotrauma Pharmacology Workgroup. J. Neurotrauma 31, 135-158.
19. Robertson, C.S., Hannay, H.J., Yamal, J.-M., Gopinath, S., Goodman, J.C., Tilley, B.C.; Epo Severe TBI Investigators, Baldwin, A., Rivera Lara, L., Saucedo-Crespo, H., Ahmed, O., Sadasivan, S., Ponce, L., Cruz-Navarro, J., Shahin, H., Aisiku, I.P., Doshi, P., Valadka, A., Neipert, L., Waguspack, J.M., Rubin, M.L., Benoit, J.S., and Swank, P. (2014). Effect of erythropoietin and transfusion threshold on neurological recovery after traumatic brain injury: a randomized clinical trial. JAMA 312, 36-47.
20. Ehrenreich, H., Weissenborn, K., Prange, H., Schneider, D., Weimar, C., Wartenberg, K., Schellinger, P.D., Bohn, M., Becker, H., Wegrzyn, M., Jähnig, P., Herrmann, M., Knauth, M., Bähr, M., Heide, W., Wagner, A., Schwab, S., Reichmann, H., Schwendemann, G., Dengler, R., Kastrup, A., and Bartels, C. (2009). Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke 40, e647-e656.
21. Begley, C.G., and Ellis, L.M. (2012). Drug development: Raise standards for preclinical cancer research. Nature 483, 531-533.
22. Begley, C.G., and Ioannidis, J.P. (2015). Reproducibility in science: improving the standard for basic and preclinical research. Circ. Res. 116, 116-126.
23. Lapchak, P.A., Zhang, J.H., and Noble-Haeusslein, L.J. (2013). RIGOR guidelines: escalating STAIR and STEPS for effective translational research. Transl. Stroke Res. 4, 279-285.
24. Reier, P.J., Lane, M.A., Hall, E.D., Teng, Y.D., and Howland, D.R. (2012). Translational spinal cord injury research: preclinical guidelines and challenges. Handb. Clin. Neurol. 109, 411-433.
25. Warner, D.S., James, M.L., Laskowitz, D.T., and Wijdicks, E.F. (2014). Translational research in acute central nervous system injury: lessons learned and the future. JAMA Neurol. 71, 1311-1318.
26. Smith, D.H., Hicks, R.R., Johnson, V.E., Bergstrom, D.A., Cummings, D.M., Noble, L.J., Hovda, D., Whalen, M.J., Ahlers, S.T., LaPlaca, M., Tortella, F.C., Duhaime, A.C., and Dixon, C.E. (2015). Preclinical traumatic brain injury common data elements: toward a common language across laboratories. J. Neurotrauma 32, 1725-1735.
27. Garman, R.H., Jenkins, L.W., Switzer, R.C., 3rd, Bauman, R.A., Tong, L.C., Swauger, P. V, Parks, S.A., Ritzel, D. V, Dixon, C.E., Clark, R.S., Bayir, H., Kagan, V., Jackson, E.K., and Kochanek, P.M. (2011). Blast exposure in rats with body shielding is characterized primarily by diffuse axonal injury. J. Neurotrauma 28, 947-959.
28. DeWitt, D.S., and Prough, D.S. (2009). Blast-induced brain injury and posttraumatic hypotension and hypoxemia. J. Neurotrauma 26, 877-887.
29. Shein, S.L., Shellington, D.K., Exo, J.L., Jackson, T.C., Wisniewski, S.R., Jackson, E.K., Vagni, V.A., Bayir, H., Clark, R.S., Dixon, C.E., Janesko-Feldman, K.L., and Kochanek, P.M. (2014). Hemorrhagic shock shifts the serum cytokine profile from pro-to anti-inflammatory after experimental traumatic brain injury in mice. J. Neurotrauma 31, 1386-1395.
30. Morganti-Kossmann, M.C., Yan, E., and Bye, N. (2010). Animal models of traumatic brain injury: is there an optimal model to reproduce human brain injury in the laboratory? Injury 41, Suppl 1, S10-S13.
31. Foda, M.A., and Marmarou, A. (1994). A new model of diffuse brain injury in rats. Part II: morphological characterization. J. Neurosurg. 80, 301-313.
32. Goldstein, L.E., Fisher, A.M., Tagge, C.A., Zhang, X.-L., Velisek, L., Sullivan, J.A., Upreti, C., Kracht, J.M., Ericsson, M., Wojnarowicz, M.W., Goletiani, C.J., Maglakelidze, G.M., Casey, N., Moncaster, J.A., Minaeva, O., Moir, R.D., Nowinski, C.J., Stern, R.A., Cantu, R.C., Geiling, J., Blusztajn, J.K., Wolozin, B.L., Ikezu, T., Stein, T.D., Budson, A.E., Kowall, N.W., Chargin, D., Sharon, A., Saman, S., Hall, G.F., Moss, W.C., Cleveland, R.O., Tanzi, R.E., Stanton, P.K., and McKee, A.C. (2012). Chronic traumatic encephalopathy in blastexposed military veterans and a blast neurotrauma mouse model. Sci. Transl. Med. 4, 134ra60.
33. Statler, K.D., Jenkins, L.W., Dixon, C.E., Clark, R.S., Marion, D.W., and Kochanek, P.M. (2001). The simple model versus the super model: translating experimental traumatic brain injury research to the bedside. J. Neurotrauma 18, 1195-1206.
34. Wright, D.W., Yeatts, S.D., Silbergleit, R., Palesch, Y.Y., Hertzberg, V.S., Frankel, M., Goldstein, F.C., Caveney, A.F., Howlett-Smith, H., Bengelink, E.M., Manley, G.T., Merck, L.H., Janis, L.S., Barsan, W.G., and NETT Investigators. (2014). Very early administration of progesterone for acute traumatic brain injury. N. Engl. J. Med. 371, 2457-2466.
35. Bullock, M.R., Lyeth, B.G., and Muizelaar, J.P. (1999). Current status of neuroprotection trials for traumatic brain injury: lessons from animal models and clinical studies. Neurosurgery 45, 207-220.
36. Tolias, C.M., and Bullock, M.R. (2004). Critical appraisal of neuroprotection trials in head injury: what have we learned? NeuroRx 1, 71-79.
37. Darrah, S.D., Chuang, J., Mohler, L.M., Chen, X., Cummings, E.E., Burnett, T., Reyes-Littaua, M.C., Galang, G.N., and Wagner, A.K. (2011). Dilantin therapy in an experimental model of traumatic brain injury: effects of limited versus daily treatment on neurological and behavioral recovery. J. Neurotrauma 28, 43-55.
38. Simard, J.M., Tsymbalyuk, N., Tsymbalyuk, O., Ivanova, S., Yurovsky, V., and Gerzanich, V. (2010). Glibenclamide is superior to decompressive craniectomy in a rat model of malignant stroke. Stroke. 41, 531-537.
39. Bye, N., Habgood, M.D., Callaway, J.K., Malakooti, N., Potter, A., Kossmann, T., and Morganti-Kossmann, M.C. (2007). Transient neuroprotection by minocycline following traumatic brain injury is associated with attenuated microglial activation but no changes in cell apoptosis or neutrophil infiltration. Exp. Neurol. 204, 220-233.
40. Haber, M., Abdel Baki, S.G., Grin'kina, N.M., Irizarry, R., Ershova, A., Orsi, S., Grill, R.J., Dash, P., and Bergold, P.J. (2013). Minocycline plus N-acetylcysteine synergize to modulate inflammation and prevent cognitive and memory deficits in a rat model of mild traumatic brain injury. Exp. Neurol. 249, 169-177.
41. Dixon, C.E., Kraus,M.F., Kline, A.E.,Ma, X., Yan, H.Q., Griffith, R.G., Wolfson, B.M., and Marion, D.W. (1999). Amantadine improves water maze performance without affecting motor behavior following traumatic brain injury in rats. Restor. Neurol. Neurosci. 14, 285-294.
42. Wang, T., Huang, X.J., Van, K.C., Went, G.T., Nguyen, J.T., and Lyeth, B.G. (2014). Amantadine improves cognitive outcome and increases neuronal survival after fluid percussion traumatic brain injury in rats. J. Neurotrauma 31, 370-377.
43. Giacino, J.T., Whyte, J., Bagiella, E., Kalmar, K., Childs, N., Khademi, A., Eifert, B., Long, D., Katz, D.I., Cho, S., Yablon, S.A., Luther, M., Hammond, F.M., Nordenbo, A., Novak, P., Mercer, W., Maurer-Karattup, P., and Sherer, M. (2012). Placebo-controlled trial of amantadine for severe traumatic brain injury. N. Engl. J. Med. 366, 819-826.
44. Kochanek, P.M., Jackson, T.C., Ferguson, N.M., Carlson, S.W., Simon, D.W., Brockman, E.C., Ji, J., Bayir, H., Poloyac, S.M., Wagner, A.K., Kline, A.E., Empey, P.E., Clark, R.S., Jackson, E.K., and Dixon, C.E. (2015). Emerging therapies in traumatic brain injury. Semin. Neurol. 35, 83-100.
45. Liao, G.P., Harting, M.T., Hetz, R.A., Walker, P.A., Shah, S.K., Corkins, C.J., Hughes, T.G., Jimenez, F., Kosmach, S.C., Day, M.C., Tsao, K., Lee, D.A., Worth, L.L., Baumgartner, J.E., and Cox, C.S., Jr. (2015). Autologous bone marrow mononuclear cells reduce therapeutic intensity for severe traumatic brain injury in children. Pediatr. Crit. Care Med. 16, 245-255.
46. Kernie, S.G. (2015). Cell-based therapy for pediatric traumatic brain injury: not (yet) an update to the traumatic brain injury guidelines. Pediatr. Crit. Care Med. 16, 294-295.
47. Khuman, J., Zhang, J., Park, J., Carroll, J.D., Donahue, C., and Whalen, M.J. (2012). Low-level laser light therapy improves cognitive deficits and inhibits microglial activation after controlled cortical impact in mice. J. Neurotrauma 29, 408-417.
48. Loane, D.J., Kumar, A., Stoica, B.A., Cabatbat, R., and Faden, A.I. (2014). Progressive neurodegeneration after experimental brain trauma: association with chronic microglial activation. J. Neuropathol. Exp. Neurol. 73, 14-29.
49. Kovesdi, E., Kamnaksh, A., Wingo, D., Ahmed, F., Grunberg, N.E., Long, J.B., Kasper, C.E., and Agoston, D.V. (2012). Acute minocycline treatment mitigates the symptoms of mild blast-induced traumatic brain injury. Front. Neurol. 3, 111.
50. Dixon, C.E., Kochanek, P.M., Yan, H.Q., Schiding, J.K., Griffith, R.G., Baum, E., Marion, D.W., and DeKosky, S.T. (1999). One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J. Neurotrauma 16, 109-122.
51. Bramlett, H.M., and Dietrich, W.D. (2002). Quantitative structural changes in white and gray matter 1 year following traumatic brain injury in rats. Acta Neuropathol. 103, 607-614.
52. Bramlett, H.M., and Dietrich, W.D. (2014). Long-term consequences of traumatic brain injury: current status of potential mechanisms of injury and neurological outcomes. J. Neurotrauma. 32, 1834-1848.