Histopathological and ultrastructural changes in the rats brain after air shock wave impact

S.V. Kozlov; Yu.V. Kozlova; N.S.  Bondarenko; O.O.  Bondarenko

doi:10.26641/2307-0404.2024.1.300497

Авторы

S.V. Kozlov Dnipro State Medical University Volodymyra Vernadskoho str., 9, Dnipro, 49044, Ukraine https://orcid.org/0000-0002-7619-4302
Yu.V. Kozlova Dnipro State Medical University, Volodymyra Vernadskoho str., 9, Dnipro, 49044, Ukraine https://orcid.org/0000-0002-1364-1910
N.S. Bondarenko Dnipro State Medical University, Volodymyra Vernadskoho str., 9, Dnipro, 49044, Ukraine https://orcid.org/0000-0003-3933-7535
O.O. Bondarenko Dnipro State Medical University, Volodymyra Vernadskoho str., 9, Dnipro, 49044, Ukraine https://orcid.org/0000-0002-9739-9219

DOI:

https://doi.org/10.26641/2307-0404.2024.1.300497

Ключевые слова:

cerebral cortex, hippocampus, blast-induced brain injury, rats, histopathology, ultrastructure, digital morphometry, ImageJ

Аннотация

The using of explosive substances and devices can lead to brain injuries, the diagnosis of which requires the determination of primary biomarkers. Therefore, the aim was to establish and study histopathological and ultrastructural changes in the rats brain after exposure to an air blast wave. The study was carried out on 18 male Wistar rats, which were randomly divided into two groups: sham (n=9) and experimental (n=9). The animals of the experimental group were anesthetized with halothane and gently fixed in a horizontal position on the abdomen with the front part of the rat's muzzle at a distance of 5 cm from the device opening and subjected to an excess pressure of 26-36 kPa. Animals of both groups were decapitated, brains were removed, fixed, histopathological and ultrastructural analyzes were conducted using standard methods. Intergroup differences were assessed by Mann-Whitney U-test. Light microscopy revealed primary lesions in the form of small focal, multifocal hemorrhages, cerebral vessel ruptures and microscopic ruptures of the brain substance. In almost all brain samples, there is a significant saturation of the venous vessels with the presence of erythrocyte stasis. Violation of the blood-brain barrier, the presence of edema of the perivascular space, and petechial hemorrhages in the neuropil were registered ultrastructurally. Based on the study results, a morphological algorithm for assessing primary histostructural intracranial brain injuries and their consequences after exposure to an air shock wave was proposed. The injuries were found to be caused by the direct traumatic effect of the air shock wave. In the acute post-traumatic period, histopathological and ultrastructural changes in the brain can manifest as changes in neurons and in the blood-brain barrier and be accompanied by perivascular multifocal small-focal hemorrhages, neuropil ruptures, edema of pericellular and perivascular spaces, which together can be considered as biomarkers of primary traumatic changes after exposure to an air shock wave.

Библиографические ссылки

Guilhaume-Correa F, Pickrell AM, Vande Vord PJ. The imbalance of astrocytic mitochondrial dynamics following blast-induced traumatic brain injury. Biomedicines. 2023;11(2):329. doi: https://doi.org/10.3390/biomedicines11020329

Nonaka M, Taylor WW, Bukalo O, et al. Behavioral and myelin-related abnormalities after blast-induced mild traumatic brain injury in mice. J Neurotrauma. 2021;38(11):1551-71. doi: https://doi.org/10.1089/neu.2020.7254

Ou Y, Clifton BA, Li J, et al. Traumatic brain injury induced by exposure to blast overpressure via ear canal. Neural Regen Res. 2022;17(1):115-21. doi: https://doi.org/10.4103/1673-5374.314311

Huwer H, Hadizamani Y, Moehrlen U, et al. Ex Vivo pulmonary oedema after In Vivo blast-induced rat lung injury: time dependency, blast intensity and beta-2 adrenergic receptor role. Biomedicines. 2022;10(11):2930. doi: https://doi.org/10.3390/biomedicines10112930

Barnes DE, Byers AL, Gardner RC, et al. Association of mild traumatic brain injury with and without loss of consciousness with dementia in US military vete-rans. JAMA Neurol. 2018;75(9):1055-61. doi: https://doi.org/10.1001/jamaneurol.2018.0815

Griffiths DR, Law LM, Young C, et al. Chronic cognitive and cerebrovascular function after mild trau-matic brain injury in rats. J Neurotrauma. 2022t;39(19-20):1429-41. doi: https://doi.org/10.1089/neu.2022.0015

Race NS, Andrews KD, Lungwitz EA, et al. Psychosocial impairment following mild blast-induced traumatic brain injury in rats. Behav Brain Res. 2021;412:113405. doi: https://doi.org/10.1016/j.bbr.2021.113405

Shi QX, Chen B, Nie C, et al. A novel model of blast induced traumatic brain injury caused by compressed gas produced sustained cognitive deficits in rats: involvement of phosphorylation of tau at the Thr205 epitope. Brain Res Bull. 2020;157:149-61. doi: https://doi.org/10.1016/j.brainresbull.2020.02.002

Kawoos U, Abutarboush R, Gu M, et al. Blast-induced temporal alterations in blood-brain barrier properties in a rodent model. Sci Rep. 2021;11(1):5906. doi: https://doi.org/10.1038/s41598-021-84730-8

Bishop R, Won SJ, Irvine KA, et al. Blast-induced axonal degeneration in the rat cerebellum in the absence of head movement. Sci Rep. 2022;12(1):143. doi: https://doi.org/10.1038/s41598-021-03744-4

Pavlovic D, Pekic S, Stojanovic M, Popovic V. Traumatic brain injury: neuropathological, neurocognitive and neurobehavioral sequelae. Pituitary. 2019;22(3):270-82. doi: https://doi.org/10.1007/s11102-019-00957-9

Kuriakose M, Younger D, Ravula AR, et al. Synergistic role of oxidative stress and blood-brain barrier permeability as injury mechanisms in the acute patho-physiology of blast-induced neurotrauma. Sci Rep. 2019;9(1):7717. doi: https://doi.org/10.1038/s41598-019-44147-w

Schwab N, Leung E, Hazrati LN. Cellular senescence in traumatic brain injury: evidence and perspectives. Front Aging Neurosci. 2021;13:742632. doi: https://doi.org/10.3389/fnagi.2021.742632

Yalciner BZ, Kandemir M, Taskale S, et al. Modified visual magnetic resonance rating scale for evaluation of patients with forgetfulness. Can J Neurol Sci. 2019;46(1):71-8. doi: https://doi.org/10.1017/cjn.2018.333

Sparks P, Lawrence T, Hinze S. Neuroimaging in the diagnosis of chronic traumatic encephalopathy: A systematic review. Clin J Sport Med. 2020;30,1:S1-S10. doi: https://doi.org/10.1097/JSM.0000000000000541

National Advisory Committee for Laboratory Animal Research. Guidelines on the care and use of animals for scientific purpose. Singapore; 2022. 145 p.

Percie du Sert N, Hurst V, Ahluwalia A, et al. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biol. 2020;18(7):e3000410. doi: https://doi.org/10.1371/journal.pbio.3000410

Kozlova YuV, Abdul-Ohly LV, Kosharnyi AV, Kytova IV, Korzachenko MA, inventors. [Device for studying the effect of the shock wave of an explosion on the body]. Patent Ukraine U202100358. 2021 Mar 24. Ukrainian.

Elder GA, Gama Sosa MA, De Gasperi R, et al. The neurovascular unit as a locus of injury in low-level blast-induced neurotrauma. Int J Mol Sci. 2024;25(2):1150. doi: https://doi.org/10.3390/ijms25021150

Bagriy MM, Dibrova VA, Popadynets OG, Grischuk MI. [Methods of morphological research]. Vinnytsia: Nova knyha; 2016. 328 р. Ukranian.

Danilov VY. [Statistical data processing: tutorial]. Kyiv; 2019. 156 p. Ukranian.

Logsdon AF, Lucke-Wold BP, Turner RC, et al. Low-intensity blast wave model for preclinical assessment of closed-head mild traumatic brain injury in rodents. J Vis Exp. 2020;165:10.3791/61244. doi: https://doi.org/10.3791/61244

Gama Sosa MA, De Gasperi R, Pryor D, et al. Late chronic local inflammation, synaptic alterations, vascular remodeling and arteriovenous malformations in the brains of male rats exposed to repetitive low-level blast overpressures. Acta Neuropathol Commun. 2023;11(1):81. doi: https://doi.org/10.1186/s40478-023-01553-6

Ma X, Aravind A, Pfister BJ, et al. Animal models of traumatic brain injury and assessment of injury severity. Mol Neurobiol. 2019;56(8):5332-45. doi: https://doi.org/10.1007/s12035-018-1454-5

Przekwas A, Garimella HT, Tan XG, et al. Biome-chanics of blast TBI with time-resolved consecutive pri-mary, secondary, and tertiary loads. Mil Med. 2019;184:195-205. doi: https://doi.org/10.1093/milmed/usy344

Chen B, Tjahja J, Malla S, et al. Astrocyte viability and functionality in spatially confined microcavitation zone. ACS Appl Mater Interfaces. 2019;11(5):4889-99. doi: https://doi.org/10.1021/acsami.8b21410

Fievisohn E, Bailey Z, Guettler A, VandeVord P. Primary blast brain injury mechanisms: current knowledge, limitations, and future directions. J Biomech Eng. 2018;140(2). doi: https://doi.org/10.1115/1.4038710

Russell AL, Richardson MR, Bauman BM, et al. Differential responses of the HPA axis to mild blast traumatic brain injury in male and female mice. Endocrinology. 2018;159(6):2363-75. doi: https://doi.org/10.1210/en.2018-00203

Belding JN, Englert RM, Fitzmaurice SJ, et al. Potential health and performance effects of high-level and low-level blast: a scoping review of two decades of research. Front Neurol. 2021;12:628782. doi: https://doi.org/10.3389/fneur.2021.628782

1.Friedman L, Peng H, Zeman R. Cannabidiol reduces lesion volume and restores vestibulomotor and cognitive function following moderately severe traumatic brain injury. Experimental Neurology [Internet]. 2021Dec.1;346:113844. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0014488621002521

Gallo V, Motley K, Kemp SPT, et al. Concussion and long-term cognitive impairment among professional or elite sport-persons: a systematic review. J Neurol Neurosurg Psychiatry. 2020;91(5):455-68. doi: https://doi.org/10.1136/jnnp-2019-321170

Ratliff WA, Mervis RF, Citron BA, et al. Effect of mild blast-induced TBI on dendritic architecture of the cortex and hippocampus in the mouse. Sci Rep. 2020;10(1):2206. doi: https://doi.org/10.1038/s41598-020-59252-4

Han EX, Fernandez JM, Swanberg C, et al. Lon-gitudinal auditory pathophysiology following mild blast-induced trauma. J Neurophysiol. 2021;126(4):1172-89. doi: https://doi.org/10.1152/jn.00039.2021

Marsh JL, Bentil SA. Cerebrospinal fluid cavita-tion as a mechanism of blast-induced traumatic brain injury: a review of current debates, methods, and findings. Front Neurol. 2021;12:626393. doi: https://doi.org/10.3389/fneur.2021.626393