Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 5175249, 11 pages
https://doi.org/10.1155/2017/5175249
Research Article

Distinguishing the Unique Neuropathological Profile of Blast Polytrauma

1Biomedical Engineering and Mechanics, Virginia Tech, Blacksburg, VA 24061, USA
2Translational Biology, Medicine, and Health, Virginia Tech, Blacksburg, VA 24061, USA
3Department of Chemical, Biochemical and Environmental Engineering, University of Maryland, Baltimore County, Baltimore, MD 21250, USA
4Research Services, Salem VAMC, Salem, VA 24153, USA

Correspondence should be addressed to Pamela VandeVord; ude.tv@drovp

Received 20 January 2017; Accepted 28 February 2017; Published 23 March 2017

Academic Editor: Valentina Pallottini

Copyright © 2017 W. Brad Hubbard et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. P. Liao and J. B. Holcomb, “Trauma resuscitation and fluid considerations in the polytrauma patient with CNS injury,” in Neurotrauma Management for the Severely Injured Polytrauma Patient, J. M. Ecklund and L. E. Moores, Eds., pp. 51–59, Springer, Cham, Switzerland, 2017. View at Google Scholar
  2. P. A. Toyinbo, R. D. Vanderploeg, H. G. Belanger, A. M. Spehar, W. A. Lapcevic, and S. G. Scott, “A systems science approach to understanding polytrauma and blast-related injury: bayesian network model of data from a survey of the florida national guard,” American Journal of Epidemiology, vol. 185, no. 2, pp. 135–146, 2017. View at Publisher · View at Google Scholar
  3. M. Hirsch and J. Bazini, “Blast injury of the chest,” Clinical Radiology, vol. 20, no. 4, pp. 362–370, 1969. View at Publisher · View at Google Scholar · View at Scopus
  4. W. A. Hadden, W. H. Rutherford, and J. D. Merrett, “The injuries of terroist bombing: a study of 1532 consecutive patients,” British Journal of Surgery, vol. 65, no. 8, pp. 525–531, 1978. View at Publisher · View at Google Scholar · View at Scopus
  5. B. Brismar and L. Bergenwald, “The terrorist bomb explosion in Bologna, Italy, 1980: an analysis of the effects and injuries sustained,” Journal of Trauma—Injury, Infection and Critical Care, vol. 22, no. 3, pp. 216–220, 1982. View at Publisher · View at Google Scholar · View at Scopus
  6. G. J. Cooper, R. L. Maynard, N. L. Cross, and J. F. Hill, “Casualties from terrorist bombings,” Journal of Trauma, vol. 23, no. 11, pp. 955–967, 1983. View at Publisher · View at Google Scholar · View at Scopus
  7. E. R. Frykberg and J. J. Tepas III, “Terrorist bombings. Lessons learned from Belfast to Beirut,” Annals of Surgery, vol. 208, no. 5, pp. 569–576, 1988. View at Publisher · View at Google Scholar · View at Scopus
  8. E. Katz, B. Ofek, J. Adler, H. B. Abramowitz, and M. M. Krausz, “Primary blast injury after a bomb explosion in a civilian bus,” Annals of Surgery, vol. 209, no. 4, pp. 484–488, 1989. View at Publisher · View at Google Scholar · View at Scopus
  9. R. Pizov, A. Oppenheim-Eden, I. Matot et al., “Blast lung injury from an explosion on a civilian bus,” Chest, vol. 115, no. 1, pp. 165–172, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. J. M. Wightman and S. L. Gladish, “Explosions and blast injuries,” Annals of Emergency Medicine, vol. 37, no. 6, pp. 664–678, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. CDC, “Bombings: injury patterns and care. Blast curriculum: one-hour module,” 2006.
  12. S. J. McDonald, M. Sun, D. V. Agoston, and S. R. Shultz, “The effect of concomitant peripheral injury on traumatic brain injury pathobiology and outcome,” Journal of Neuroinflammation, vol. 13, no. 1, article 90, 2016. View at Publisher · View at Google Scholar · View at Scopus
  13. D. S. Dewitt and D. S. Prough, “Blast-induced brain injury and posttraumatic hypotension and hypoxemia,” Journal of Neurotrauma, vol. 26, no. 6, pp. 877–887, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. E. Kirkman and S. Watts, “Characterization of the response to primary blast injury,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 366, no. 1562, pp. 286–290, 2010. View at Publisher · View at Google Scholar
  15. A. Chodobski, B. J. Zink, and J. Szmydynger-Chodobska, “Blood-brain barrier pathophysiology in traumatic brain injury,” Translational Stroke Research, vol. 2, no. 4, pp. 492–516, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. M. K. Başkaya, A. M. Rao, A. Doğan, D. Donaldson, and R. J. Dempsey, “The biphasic opening of the blood-brain barrier in the cortex and hippocampus after traumatic brain injury in rats,” Neuroscience Letters, vol. 226, no. 1, pp. 33–36, 1997. View at Publisher · View at Google Scholar · View at Scopus
  17. W. B. Hubbard, C. Hall, V. Siva Sai Suijith Sajja, E. Lavik, and P. VandeVord, “Examining lethality risk for rodent studies of primary blast lung injury,” Biomedical Sciences Instrumentation, vol. 50, pp. 92–99, 2014. View at Google Scholar
  18. W. B. Hubbard, M. M. Lashof-Sullivan, E. B. Lavik, and P. J. Vandevord, “Steroid-loaded hemostatic nanoparticles combat lung injury after blast trauma,” ACS Macro Letters, vol. 4, no. 4, pp. 387–391, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Huang, M. Ngo, S. Yee et al., “Repeated blast exposure alters open field behavior recorded under low illumination,” Brain Research, vol. 1529, pp. 125–133, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Darwish, A. Mahmood, T. Schallert, M. Chopp, and B. Therrien, “Simvastatin and environmental enrichment effect on recognition and temporal order memory after mild-to-moderate traumatic brain injury,” Brain Injury, vol. 28, no. 2, pp. 211–226, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. M. V. Sofroniew and H. V. Vinters, “Astrocytes: biology and pathology,” Acta Neuropathologica, vol. 119, no. 1, pp. 7–35, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Lin and M. D. Ginsberg, “Quantitative assessment of the normal cerebral microvasculature by endothelial barrier antigen (EBA) immunohistochemistry: application to focal cerebral ischemia,” Brain Research, vol. 865, no. 2, pp. 237–244, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Pelz, W. Härtig, C. Weise et al., “Endothelial barrier antigen-immunoreactivity is conversely associated with blood-brain barrier dysfunction after embolic stroke in rats,” European Journal of Histochemistry, vol. 57, no. 4, article e38, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. J. E. Westin, H. S. Lindgren, J. Gardi et al., “Endothelial proliferation and increased blood-brain barrier permeability in the basal ganglia in a rat model of 3,4-dihydroxyphenyl-L-alanine-induced dyskinesia,” Journal of Neuroscience, vol. 26, no. 37, pp. 9448–9461, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Li, M. Chavko, J. L. Slack et al., “Protective effects of decay-accelerating factor on blast-induced neurotrauma in rats,” Acta Neuropathologica Communications, vol. 1, no. 1, article 52, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. J. A. Forsythe, B.-H. Jiang, N. V. Iyer et al., “Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1,” Molecular and Cellular Biology, vol. 16, no. 9, pp. 4604–4613, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. H. Zhang, P. Zhang, Y. Gao et al., “Early VEGF inhibition attenuates blood-brain barrier disruption in ischemic rat brains by regulating the expression of MMPs,” Molecular Medicine Reports, vol. 15, no. 1, pp. 57–64, 2017. View at Publisher · View at Google Scholar
  28. W.-L. Yeh, D.-Y. Lu, C.-J. Lin, H.-C. Liou, and W.-M. Fu, “Inhibition of hypoxia-induced increase of blood-brain barrier permeability by YC-1 through the antagonism of HIF-1α accumulation and VEGF expression,” Molecular Pharmacology, vol. 72, no. 2, pp. 440–449, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. M. K. Sköld, C. Von Gertten, A.-C. Sandberg-Nordqvist, T. Mathiesen, and S. Holmin, “VEGF and VEGF receptor expression after experimental brain contusion in rat,” Journal of Neurotrauma, vol. 22, no. 3, pp. 353–367, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Skotak, F. Wang, A. Alai et al., “Rat injury model under controlled field-relevant primary blast conditions: acute response to a wide range of peak overpressures,” Journal of Neurotrauma, vol. 30, no. 13, pp. 1147–1160, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. V. Mishra, M. Skotak, H. Schuetz, A. Heller, J. Haorah, and N. Chandra, “Primary blast causes mild, moderate, severe and lethal TBI with increasing blast overpressures: experimental rat injury model,” Scientific Reports, vol. 6, Article ID 26992, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. S. T. Ahlers, E. Vasserman-Stokes, M. C. Shaughness et al., “Assessment of the effects of acute and repeated exposure to blast overpressure in rodents: toward a greater understanding of blast and the potential ramifications for injury in humans exposed to blast,” Frontiers in Neurology, vol. 3, article 32, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. J. M. Simard, A. Pampori, K. Keledjian et al., “Exposure of the thorax to a sublethal blast wave causes a hydrodynamic pulse that leads to perivenular inflammation in the brain,” Journal of Neurotrauma, vol. 31, no. 14, pp. 1292–1304, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. L. Prut and C. Belzung, “The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review,” European Journal of Pharmacology, vol. 463, no. 1–3, pp. 3–33, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. V. S. Sajja, W. B. Hubbard, and P. J. VandeVord, “Subacute oxidative stress and glial reactivity in the amygdala are associated with increased anxiety following blast neurotrauma,” Shock, vol. 44, supplement 1, pp. 71–78, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. H. O. Awwad, L. P. Gonzalez, P. Tompkins et al., “Blast overpressure waves induce transient anxiety and regional changes in cerebral glucose metabolism and delayed hyperarousal in rats,” Frontiers in Neurology, vol. 6, article 132, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. S. A. Heldt, A. J. Elberger, Y. Deng et al., “A novel closed-head model of mild traumatic brain injury caused by primary overpressure blast to the cranium produces sustained emotional deficits in mice,” Frontiers in Neurology, vol. 5, article 2, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Kovesdi, A. Kamnaksh, D. Wingo et al., “Acute minocycline treatment mitigates the symptoms of mild blast-induced traumatic brain injury,” Frontiers in Neurology, vol. 3, article 111, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Kamnaksh, E. Kovesdi, S.-K. Kwon et al., “Factors affecting blast traumatic brain injury,” Journal of Neurotrauma, vol. 28, no. 10, pp. 2145–2153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. P. J. VandeVord, R. Bolander, V. S. Sajja, K. Hay, and C. A. Bir, “Mild neurotrauma indicates a range-specific pressure response to low level shock wave exposure,” Annals of Biomedical Engineering, vol. 40, no. 1, pp. 227–236, 2012. View at Publisher · View at Google Scholar
  41. B. R. Huber, J. S. Meabon, Z. S. Hoffer et al., “Blast exposure causes dynamic microglial/macrophage responses and microdomains of brain microvessel dysfunction,” Neuroscience, vol. 319, pp. 206–220, 2016. View at Publisher · View at Google Scholar · View at Scopus
  42. R. D. Readnower, M. Chavko, S. Adeeb et al., “Increase in blood-brain barrier permeability, oxidative stress, and activated microglia in a rat model of blast-induced traumatic brain injury,” Journal of Neuroscience Research, vol. 88, no. 16, pp. 3530–3539, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. P. M. Abdul-Muneer, H. Schuetz, F. Wang et al., “Induction of oxidative and nitrosative damage leads to cerebrovascular inflammation in an animal model of mild traumatic brain injury induced by primary blast,” Free Radical Biology and Medicine, vol. 60, pp. 282–291, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. C. D. Hue, F. S. Cho, S. Cao et al., “Time course and size of blood-brain barrier opening in a mouse model of blast-induced traumatic brain injury,” Journal of Neurotrauma, vol. 33, no. 13, pp. 1202–1211, 2016. View at Publisher · View at Google Scholar · View at Scopus
  45. J. R. Perez-Polo, H. C. Rea, K. M. Johnson et al., “A rodent model of mild traumatic brain blast injury,” Journal of Neuroscience Research, vol. 93, no. 4, pp. 549–561, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. U. Kawoos, M. Gu, J. Lankasky, R. M. McCarron, M. Chavko, and M. A. Deli, “Effects of exposure to blast overpressure on intracranial pressure and blood-brain barrier permeability in a rat model,” PLoS ONE, vol. 11, no. 12, Article ID e0167510, 2016. View at Publisher · View at Google Scholar
  47. C. Kaur and E. A. Ling, “Blood brain barrier in hypoxic-ischemic conditions,” Current Neurovascular Research, vol. 5, no. 1, pp. 71–81, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. G. Rajkowska, J. Hughes, C. A. Stockmeier, J. Javier Miguel-Hidalgo, and D. Maciag, “Coverage of blood vessels by astrocytic endfeet is reduced in major depressive disorder,” Biological Psychiatry, vol. 73, no. 7, pp. 613–621, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Yeoh, E. D. Bell, and K. L. Monson, “Distribution of blood-brain barrier disruption in primary blast injury,” Annals of Biomedical Engineering, vol. 41, no. 10, pp. 2206–2214, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. G. Mohaddes, J. Abdolalizadeh, S. Babri, and F. Hossienzadeh, “Ghrelin ameliorates blood-brain barrier disruption during systemic hypoxia,” Experimental Physiology, vol. 102, no. 3, pp. 376–382, 2017. View at Publisher · View at Google Scholar
  51. A. Li, X. Sun, Y. Ni, X. Chen, and A. Guo, “HIF-1α involves in neuronal apoptosis after traumatic brain injury in adult rats,” Journal of Molecular Neuroscience, vol. 51, no. 3, pp. 1052–1062, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. F. Ahmed, I. Cernak, S. Plantman, and D. V. Agoston, “The temporal pattern of changes in serum biomarker levels reveal complex and dynamically changing pathologies after exposure to a single low-intensity blast in mice,” Frontiers in Neurology, vol. 6, article 114, 2015. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Liu, C. Zhang, W. Liu et al., “A novel rat model of blast-induced traumatic brain injury simulating different damage degree: implications for morphological, neurological, and biomarker changes,” Frontiers in Cellular Neuroscience, vol. 9, article 168, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Engelhardt, A. J. Al-Ahmad, M. Gassmann, and O. O. Ogunshola, “Hypoxia selectively disrupts brain microvascular endothelial tight junction complexes through a hypoxia-inducible factor-1 (HIF-1) dependent mechanism,” Journal of Cellular Physiology, vol. 229, no. 8, pp. 1096–1105, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. O. O. Ogunshola and A. Al-Ahmad, “HIF-1 at the blood-brain barrier: a mediator of permeability?” High Altitude Medicine and Biology, vol. 13, no. 3, pp. 153–161, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. C. Chen, Q. Hu, J. Yan et al., “Early inhibition of HIF-1α with small interfering RNA reduces ischemic-reperfused brain injury in rats,” Neurobiology of Disease, vol. 33, no. 3, pp. 509–517, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Okada, R. Okeda, S. Matsushita, and A. Kawano, “Histopathological and morphometric study of the late effects of heavy- ion irradiation on the spinal cord of the rat,” Radiation Research, vol. 150, no. 3, pp. 304–315, 1998. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Kamnaksh, S.-K. Kwon, E. Kovesdi et al., “Neurobehavioral, cellular, and molecular consequences of single and multiple mild blast exposure,” Electrophoresis, vol. 33, no. 24, pp. 3680–3692, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. F. A. Ahmed, A. Kamnaksh, E. Kovesdi, J. B. Long, and D. V. Agoston, “Long-term consequences of single and multiple mild blast exposure on select physiological parameters and blood-based biomarkers,” Electrophoresis, vol. 34, no. 15, pp. 2229–2233, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. E. P. Thelin, A. Frostell, J. Mulder et al., “Lesion size is exacerbated in hypoxic rats whereas hypoxia-inducible factor-1 alpha and vascular endothelial growth factor increase in injured normoxic rats: a prospective cohort study of secondary hypoxia in focal traumatic brain injury,” Frontiers in Neurology, vol. 7, article 23, 2016. View at Publisher · View at Google Scholar · View at Scopus
  61. T. Higashida, C. W. Kreipke, J. A. Rafols et al., “The role of hypoxia-inducible factor-1α, aquaporin-4, and matrix metalloproteinase-9 in blood-brain barrier disruption and brain edema after traumatic brain injury,” Journal of Neurosurgery, vol. 114, no. 1, pp. 92–101, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. R. Bolander, B. Mathie, C. Bir, D. Ritzel, and P. Vandevord, “Skull flexure as a contributing factor in the mechanism of injury in the rat when exposed to a shock wave,” Annals of Biomedical Engineering, vol. 39, no. 10, pp. 2550–2559, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Dal Cengio Leonardi, N. J. Keane, C. A. Bir, A. G. Ryan, L. Xu, and P. J. VandeVord, “Head orientation affects the intracranial pressure response resulting from shock wave loading in the rat,” Journal of Biomechanics, vol. 45, no. 15, pp. 2595–2602, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. A. D. C. Leonardi, C. A. Bir, D. V. Ritzel, and P. J. VandeVord, “Intracranial pressure increases during exposure to a shock wave,” Journal of Neurotrauma, vol. 28, no. 1, pp. 85–94, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. C. E. Hampton and P. J. VandeVord, “Vibrational frequency response to impact loading of skull models,” Biomedical Sciences Instrumentation, vol. 48, pp. 157–164, 2012. View at Google Scholar · View at Scopus
  66. A. D. Gean, Brain Injury: Applications from War and Terrorism, Wolters Kluwer, 2014.
  67. W. C. Moss, M. J. King, and E. G. Blackman, “Skull flexure from blast waves: a mechanism for brain injury with implications for helmet design,” Physical Review Letters, vol. 103, no. 10, Article ID 108702, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. R. A. Bauman, G. Ling, L. Tong et al., “An introductory characterization of a combat-casualty-care relevant swine model of closed head injury resulting from exposure to explosive blast,” Journal of Neurotrauma, vol. 26, no. 6, pp. 841–860, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. R. Kuehn, P. F. Simard, I. Driscoll et al., “Rodent model of direct cranial blast injury,” Journal of Neurotrauma, vol. 28, no. 10, pp. 2155–2169, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. F. Adhami, G. Liao, Y. M. Morozov et al., “Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy,” The American Journal of Pathology, vol. 169, no. 2, pp. 566–583, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. G. N. Neigh, M. J. Owens, W. R. Taylor, and C. B. Nemeroff, “Changes in the vascular area fraction of the hippocampus and amygdala are induced by prenatal dexamethasone and/or adult stress,” Journal of Cerebral Blood Flow and Metabolism, vol. 30, no. 6, pp. 1100–1104, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. V. S. S. S. Sajja, W. B. Hubbard, C. S. Hall, F. Ghoddoussi, M. P. Galloway, and P. J. VandeVord, “Enduring deficits in memory and neuronal pathology after blast-induced traumatic brain injury,” Scientific Reports, vol. 5, Article ID 15075, 2015. View at Publisher · View at Google Scholar · View at Scopus