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Enduring cognitive, neurobehavioral and histopathological changes persist for up to one year following severe experimental brain injury in rats
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Clinical studies have demonstrated that patients sustain prolonged behavioral deficits following traumatic brain injury, in some cases culminating in the cognitive and histopathological hallmarks of Alzheimer's disease. However, few studies have examined the long-term consequences of experimental traumatic brain injury. In the present study, anesthetized male Sprague-Dawley rats (n = 185) were subjected to severe lateral fluid-percussion brain injury (n = 115) or sham injury (n = 70) and evaluated up to one year post-injury for cognitive and neurological deficits and histopathological changes. Compared with sham-injured controls, brain-injured animals showed a spatial learning impairment that persisted up to one year post-injury. In addition, deficits in specific neurologic motor function tasks also persisted up to one year post-injury. Immunohistochemistry using multiple antibodies to the amyloid precursor protein and/or amyloid precursor protein-like proteins revealed novel axonal degeneration in the striatum, corpus callosum and injured cortex up to one year post-injury and in the thalamus up to six months post-injury. Histologic evaluation of injured brains demonstrated a progressive expansion of the cortical cavity, enlargement of the lateral ventricles, deformation of the hippocampus, and thalamic calcifications. Taken together, these findings indicate that experimental traumatic brain injury can cause long-term cognitive and neurologic motor dysfunction accompanied by continuing neurodegeneration.
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“Many biological pathways are disrupted by experimental TBI resulting in progressive neurodegeneration including atrophy, neuronal loss, and axonal degeneration which are often associated with neuroinflammation including macrophage reactivity (82–85).”
From The Inflammatory Continuum of Traumatic Brain Injury and Alzheimer’s Disease (2018) · cites this paper as [85]
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Ertürk, A., Mentz, S., Stout, E. E., Hedehus, M., Domínguez, S. L., Neumaier, L., Krammer, F., Llovera, G., Srinivasan, K., Hansen, D. V., et al. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1898-15.2016 · Cited by 91
“Neurodegeneration can continue long after TBI, perhaps throughout a person’s remaining lifetime, albeit at a smaller scale compared with the acute cell loss (Pierce et al., 1998; Bramlett and Dietrich, 2002).”
BackgroundHuh, J. W., Widing, A. G., & Raghupathi, R. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2008.05.009 · Cited by 84
“…in the thalamus are consistent with those in other rodent models of pediatric traumatic and hypoxic-ischemic brain injury (Tong et al., 2002; Northington et al., 2001) and may be due to retrograde axonal degeneration of thalamocortical connections (Iizuka et al., 1990; Pierce et al., 1998).”
Maxwell, W., Pennington, K., MacKinnon, M., Smith, D. H., McIntosh, T., Wilson, J. T. L., & Graham, D. (2004) · Brain : a journal of neurology · doi:10.1093/brain/awh294 · Cited by 83
“However, changes in brain structure and relationships have been noted largely in terms of atrophy of the cerebrum at the site of impact and hydrocephalus of the ipsilateral, lateral ventricle (Bramlett et al., 1997; Smith et al., 1997; Pierce et al., 1998; Dixon et al., 1999).”
BackgroundInfluentialSelf-citationKharatishvili, I., & Pitkänen, A. (2010) · Epilepsy Research · doi:10.1016/j.eplepsyres.2010.03.007 · Cited by 82
Schouten, J. W., Fulp, C. T., Royo, N. C., Saatman, K. E., Watson, D. J., Snyder, E. Y., Trojanowski, J. Q., Prockop, D. J., Maas, A. I. R., & McIntosh, T. K. (2004) · Journal of Neurotrauma · doi:10.1089/neu.2004.21.1501 · Cited by 74
“Histological evaluation demonstrated ongoing axonal degeneration in the striatum, corpus callosum, and injured cortex continuing up to 1 year post-injury and for up to 6 months post-injury in the thalamus (Pierce et al., 1998).”
Self-citationFound in translation: Understanding the biology and behavior of experimental traumatic brain injury
Bondi, C. O., Semple, B. D., Noble‐Haeusslein, L. J., Osier, N. D., Carlson, S. W., Dixon, C. E., Giza, C. C., & Kline, A. E. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.12.004 · Cited by 94
“, 1999) or lateral FP brain injury (Pierce et al., 1998).”
BackgroundChronic ibuprofen administration worsens cognitive outcome following traumatic brain injury in rats.
Browne, K., Iwata, A., Putt, M., & Smith, D. H. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.04.008 · Cited by 80
Self-citationOLIGODENDROCYTE VULNERABILITY FOLLOWING TRAUMATIC BRAIN INJURY IN RATS
Lotocki, G., Vaccari, J. P. D. R., Alonso, O., Molano, J. S., Nixon, R., Safavi, P., Dietrich, W., & Bramlett, H. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.05.056 · Cited by 79
Association of Chronic Vascular Changes with Functional Outcome after Traumatic Brain Injury in Rats
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“…from a combination of immediate mechanical disruption of tissue and a delayed secondary injury, which is mediated by a series of events leading to progressive neurodegeneration as shown both in humans and in rodents (Bigler et al., 1992; Mantyla, 1981; McAllister, 1992; Pierce et al., 1998).”
Pre-Clinical Testing of Therapies for Traumatic Brain Injury
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“The total volume of the brain lesion was calculated as described previously (Raghupathi et al., 1998) by integrating the lesion area obtained from each section calculated as (contralateral hemisphere area ) ipsilateral hemisphere area) with the distance between each level, and expressed as mean ±…”
MethodInfluentialSelf-citationReactive gliosis in traumatic brain injury: a comprehensive review
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“Considering the increasing cell and tissue loss that occurs after lateral FP brain injury (Smith et al., 1997; Bramlett et al., 1997b,c; Pierce et al., 1998), multiple doses over the 2-week evaluation period may have greater therapeutic effects in the attenuation of this progressive cell and tissue…”
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“Using experimental models of brain injury, many studies have reported hippocampal-dependent learning deficits lasting for weeks to months [20–26].”
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“…the mechanisms and pathological and functional neurological consequences of TBI and to develop new therapeutic strategies (Conti et al., 1998; Pierce et al., 1998; Bram-lett et al., 1995; Smith et al., 1991; Yamakami and McIn-tosh 1991; McIntosh et al., 1989; Cortez et al., 1989; Dixon et…”
Models of Traumatic Brain Injury
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Fedor, M., Berman, R. F., Muizelaar, J. P., & Lyeth, B. G. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2010.1370 · Cited by 77
“Some studies have documented that such deficits in rodents can persist even months after the initial injury, mirroring the long-term cognitive deficits seen after human TBI (Pierce et al., 1998).”
Mäkinen, S., van Groen, T., Clarke, J., Thornell, A., Corbett, D., Hiltunen, M. O., Soininen, H. S., & Jolkkonen, J. (2007) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600529 · Cited by 64
“Interestingly, thalamic calcification also occurs following brain trauma and global ischemia and seizures (Kato et al, 1995; Pierce et al, 1998), indicating that focal cortical damage per se is not needed for deposition.”
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“Nonetheless, thalamic expansion following brain injury has been reported previously in conjunction with acute and secondary delayed processes triggered by brain injury (Osteen et al., 2001; Pierce et al., 1998).”
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Smith, F. M., Raghupathi, R., MacKinnon, M., McIntosh, T., Saatman, K., Meaney, D., & Graham, D. (2000) · Acta Neuropathologica · doi:10.1007/s004010000222 · Cited by 70
“More recently, it was reported that after fluid percussioninduced brain injury in the rat, the volume of cortical contusion increased with prolonged survival [8, 35, 38 , 44].”
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“logical damage depends on the initial injury severity [25,26].”
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Self-citationDopaminergic abnormalities following traumatic brain injury
Jenkins, P., Simoni, S. D., Bourke, N., Fleminger, J., Scott, G. P. T., Towey, D., Svensson, W., Khan, S., Patel, M. C., Greenwood, R., et al. (2018) · Brain : a journal of neurology · doi:10.1093/brain/awx357 · Cited by 64
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Traumatic brain injury induces biphasic upregulation of ApoE and ApoJ protein in rats
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“Although the injured animals seemed generally normal, we have observed previously that mild neurologic motor dysfunction and moderate cognitive deficits persist for up to 1 yr after FP injury (Leoni et al., 2000; Pierce et al., 1998; Browne et al., 2004).”
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“This paradigm has been used successfully to demonstrate impaired learning ability up to 12 months following traumatic brain injury in adult rats (Pierce et al., 1998) and to demonstrate the effect of post-traumatic intervention (Saatman et al., 1997).”
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“Although most investigations of posttraumatic learning deficits employ multiple-day tests (Hamm et al., 1996; Pierce et al., 1998), single-day procedures have been shown to be adequate to distinguish the effects of controlled cortical impact of varying severity (Scheff et al., 1997).”
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Gaulke, L. J., Horner, P. J., Fink, A. J. P., McNamara, C. L., & Hicks, R. R. (2005) · Molecular Brain Research · doi:10.1016/j.molbrainres.2005.08.011 · Cited by 59
“TBI, including the lateral fluid percussion (FP) brain injury model also produce persistent impairments in learning and memory [61], which have been attributed to neuronal injury and dysfunction in the hippocampus [11,27,33,47].”
BackgroundCheng, W. H., Martens, K. M., Bashir, A., Cheung, H., Stukas, S. K., Gibbs, E., Namjoshi, D., Button, E. B., Wilkinson, A., Barrón, C., et al. (2019) · Alzheimer s Research & Therapy · doi:10.1186/s13195-018-0461-0 · Cited by 63
“, corpus callosum and external capsule) [7, 10, 27, 74, 79, 88].”
Briones, T. L., Woods, J., & Rogozinska, M. (2013) · Acta Neuropathologica Communications · doi:10.1186/2051-5960-1-57 · Cited by 58
“The persistent neuroinflammation seen in the mTBI control group is similar to reports from clinical and experimental studies that neuroinflammation resulting from mTBI can last from months to years after injury [14,38,39].”
ResultRetractedKharatishvili, I., Sierra, A., Immonen, R., Gröhn, O., & Pitkänen, A. (2009) · Experimental Neurology · doi:10.1016/j.expneurol.2009.01.026 · Cited by 58
Maegele, M., Lippert-Gruener, M., Ester-Bode, T., Garbe, J., Bouillon, B., Neugebauer, E., Klug, N., Lefering, R., Neiss, W., & Angelov, D. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04070.x · Cited by 58
Hoover, R., Motta, M., Davis, J. E., Saatman, K., Fujimoto, S. T., Thompson, H., Stover, J. F., Dichter, M., Twyman, R., White, H., et al. (2004) · Journal of Neurotrauma · doi:10.1089/089771504774129847 · Cited by 58
“Neurologic motor dysfunction, cognitive impairment and alterations in regional cerebral blood flow (rCBF) persist for up to one year after severe FP brain injury in the rat (Pierce et al., 1998; Kochanek et al., 2002).”
Self-citationMuir, J. K., Raghupathi, R., Saatman, K., Wilson, C. A., Lee, V., Trojanowski, J., Philips, M. F., & McIntosh, T. K. (1999) · Journal of Neurotrauma · doi:10.1089/neu.1999.16.403 · Cited by 58
“Lateral FP brain injury can cause profound and persistent motor and cognitive dysfunction (Mclntosh et al., 1989; Smith et al., 1991; Pierce et al., 1998), which may be, in part, due to loss of cortical, thalamic, and hippocampal neurons (Hicks et al., 1993, Bramlett et al., 1997).”
Self-citationKasturi, B. S., & Stein, D. G. (2009) · Journal of Neurotrauma · doi:10.1089/neu.2008.0751 · Cited by 57
“…the HP axis at 2 months post-injury, since persistence and progression of inflammatory and atrophic changes previously reported (Bramlett et al., 1997; Smith et al., 1997; Pierce et al., 1998; Holmin and Mathiesen, 1999) were evident one month post-injury (Smith et al., 1997; Pierce et al., 1998).”
Astrocyte Hypertrophy Contributes to Aberrant Neurogenesis after Traumatic Brain Injury
Robinson, C., Apgar, C. J., & Shapiro, L. A. (2016) · Neural Plasticity · doi:10.1155/2016/1347987 · Cited by 72
Traumatic brain injury and its effects on synaptic plasticity
Albensi, B. C., & Janigro, D. (2003) · Brain Injury · doi:10.1080/0269905031000107142 · Cited by 51
“Animal models have been further utilized to explore specific mechanisms of how trauma affects synaptic plasticity [4, 9–13] and cognition [14].”
BackgroundWahl, F., Piot, O., Bareyre, F. M., Uzan, A., & Stutzmann, J. M. (2000) · Journal of Neurotrauma · doi:10.1089/neu.2000.17.1055 · Cited by 54
“(# )p < 0.05, <**)p < 0.01, <***>p < 0.001 versus TBI vehicle at the same time point. tusional lesion is a more delayed, slowly evolving over several days (Toulmond et al., 1993) or months, at which time neurodegenerative changes are involved in the neuronal loss (Pierce et al., 1998).”
InfluentialAzim, A., & Joseph, B. (2018) · Springer eBooks · doi:10.1007/978-3-319-71712-8_1 · Cited by 54
Bregy, A., Nixon, R. A., Lotocki, G., Alonso, O. F., Atkins, C. M., Tsoulfas, P., Bramlett, H. M., & Dietrich, W. D. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.12.008 · Cited by 53
“TBI produces long-term neurodegenerative changes and a spectrum of behavioral abnormalities resulting from regional patterns of cell death and circuit dysfunction (Bramlett et al., 1997b; Dixon et al., 1999; Pierce et al., 1998; Smith et al., 1997).”
Lifshitz, J., Witgen, B. M., & Grady, M. S. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.11.014 · Cited by 58
“In the laboratory, the Morris water maze (MWM) and radial arm maze routinely demonstrate injury-related cognitive deficits [37,54,63,67].”
BackgroundMethodMarklund, N., Fulp, C. T., Shimizu, S., Puri, R., McMillan, A., Strittmatter, S., & McIntosh, T. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2005.08.029 · Cited by 54
“These observations of progressive brain atrophy have been replicated in experimental TBI models (Smith et al., 1997; Pierce et al., 1998; Bramlett and Dietrich, 2002; Bramlett et al., 1997).”
BackgroundSelf-citationZhang, C., Saatman, K., Royo, N., Soltesz, K. M., Millard, M., Schouten, J., Motta, M., Hoover, R., McMillan, A., Watson, D., et al. (2005) · Journal of Neurotrauma · doi:10.1089/neu.2005.22.1456 · Cited by 53
“Lateral FP brain injury can cause profound and persistent motor and cognitive dysfunction (Mclntosh et al., 1989; Smith et al., 1997; Pierce et al., 1998) which may be, in part, due to loss of cortical, thalamic and hippocampal neurons (Hicks et al., 1993; Bramlett, et al., 1997).”
Self-citationSmith, D. C., Tan, A., Duke, A., Neese, S., Clough, R., Browning, R., & Jensen, R. A. (2006) · Journal of Neurotrauma · doi:10.1089/neu.2006.23.1549 · Cited by 52
“It is also possible that this single time point may be too late or too early after FPI (Bramlett and Dietrich, 2002; Hicks et al., 1993, 1996; Pierce et al., 1998; Smith et al., 1997) to observe significant differences.”
Self-citationDeficits in Novelty Exploration after Controlled Cortical Impact
Wagner, A. K., Postal, B. A., Darrah, S. D., Chen, X., & Khan, A. S. (2007) · Journal of Neurotrauma · doi:10.1089/neu.2007.0274 · Cited by 45
“…experimental TBI also produces spatial learning acquisition deficits in adult rats tested using the Morris water maze (MWM) (Smith et al., 1991; Hoffman et al., 1994; Bramlett et al., 1997; Scheff et al., 1997; Pierce et al., 1998; Dixon et al., 1999a,b; Sanders et al., 1999; Kline et al., 2000).”
Clarke, J., Thornell, A., Corbett, D., Soininen, H., Hiltunen, M., & Jolkkonen, J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05807.x · Cited by 50
“…of the accumulated protein disappears over time (Uryu et al., 2003), APP ⁄Ab has been detected in various brain areas for up to 1 year after injury (Pierce et al., 1998), and a recent study showed that Ab forms plaque-like deposits in thalamic nuclei months after cerebral ischaemia in rats (van…”
BackgroundMarklund, N., Bareyre, F., Royo, N., Thompson, H., Mir, A., Grady, M., Schwab, M., & McIntosh, T. (2007) · Journal of Neurosurgery · doi:10.3171/jns-07/10/0844 · Cited by 50
Self-citationBrambrink, A., Ichord, R., Martin, L. J., Koehler, R., & Traystman, R. (1999) · Experimental and Toxicological Pathology · doi:10.1016/s0940-2993(99)80089-x · Cited by 50
White, E. R., Pinar, C., Bostrom, C. A., Meconi, A., & Christie, B. R. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2016.4638 · Cited by 49
“32,33 It has been suggested that models that directly impact the brain may be better classified as either moderate or severe TBI, to reflect the invasive nature of the procedure, and the actual degree of damage produced.”
Kokiko-Cochran, O., Ransohoff, L., Veenstra, M., Lee, S., Saber, M., Sikora, M., Teknipp, R., Xu, G., Bemiller, S., Wilson, G., et al. (2016) · Journal of Neurotrauma · doi:10.1089/neu.2015.3970 · Cited by 49
Chronic motor performance following different traumatic brain injury severity—A systematic review
Corrigan, F., Wee, I. C., & Collins‐Praino, L. E. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1180353 · Cited by 56
“Nonetheless, in studies utilizing focal or mixed moderate (30, 81, 87), moderate–severe (90, 91), and severe TBI models (82–85, 92), a consistent impairment was found in neuroscore, regardless of the scoring system implemented, out to 8 months post-injury, with no further deficits noted in the one study that included…”
BackgroundInfluentialDetecting Behavioral Deficits in Rats After Traumatic Brain Injury
Hausser, N., Johnson, K. M., Parsley, M. A., Guptarak, J., Spratt, H. M., & Sell, S. L. (2018) · Journal of Visualized Experiments · doi:10.3791/56044 · Cited by 48
Lipponen, A., El-Osta, A., Kaspi, A., Ziemann, M., Khurana, I., KN, H., Navarro-Ferrandis, V., Puhakka, N., Paananen, J., & Pitkänen, A. (2018) · Acta Neuropathologica Communications · doi:10.1186/s40478-018-0519-z · Cited by 47
“These pathologies progress in parallel and serial time windows over weeks to months in experimental models [7, 46, 91, 112] and humans [36, 49, 98].”
BackgroundTraumatic brain injury induces long-lasting changes in immune and regenerative signaling
Boone, D. R., Weisz, H. A., Willey, H. E., Torres, K. E. O., Falduto, M. T., Sinha, M., Spratt, H. M., Bolding, I. J., Johnson, K. M., Parsley, M. A., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0214741 · Cited by 52
Huh, J. W., & Raghupathi, R. (2007) · Journal of Neurotrauma · doi:10.1089/neu.2006.3787 · Cited by 43
“This paradigm has been used successfully to demonstrate impaired learning ability up to 12 months following TBI in adult rats (Pierce et al., 1998) and to demonstrate the effect of post-traumatic intervention (Saatman et al., 1997).”
Thompson, H., Hoover, R., Tkacs, N., Saatman, K., & McIntosh, T. (2005) · Journal of Cerebral Blood Flow and Metabolism · doi:10.1038/sj.jcbfm.9600008 · Cited by 46
“After lateral FP brain injury, there is evidence of histopathologic damage in the cortex, thalamus, and hippocampal regions (Soares et al, 1995; Hicks et al, 1996; Bramlett et al, 1997; Pierce et al, 1998; Bramlett and Dietrich, 2002), and regional inflammatory changes including”
BackgroundSelf-citationZhang, B., Chen, X., Lin, Y., Tan, T., Yang, Z. R., Dayao, C., Liu, L., Jiang, R., & Zhang, J. (2011) · Brain Research · doi:10.1016/j.brainres.2011.01.065 · Cited by 45
PKC activator therapeutic for mild traumatic brain injury in mice
Zohar, O., Lavy, R., Zi, X., Nelson, T. J., Hongpaisan, J., Pick, C. G., & Alkon, D. L. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.10.001 · Cited by 53
“…causes secondary damage by activating endogenous autodestructive biochemical processes which can last many years (Berger et al., 1999; Waxweiler et al., 1995; Assaf et al., 1999; Shapira et al., 1993; Gorrie et al., 2002; Graham et al., 2000; Albensi, 2001; Pierce et al., 1996, 1998; Reilly, 2001).”
BackgroundMattiasson, G., Philips, M., Tomasevic, G., Johansson, B., Wieloch, T., & McIntosh, T. (2000) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(99)00162-4 · Cited by 45
Self-citationBird, S., Sohrabi, H. R., Sutton, T. A., Weinborn, M., Rainey‐Smith, S. R., Brown, B. M., Patterson, L. C., Taddei, K., Gupta, V. B., Carruthers, M. E., et al. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.01.004 · Cited by 46
Neuroinflammation and the plasticity-related immediate-early gene Arc
Rosi, S. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.02.003 · Cited by 40
“Traumatic brain injury results in both acute and chronic disruption of cognitive processes, which may be mediated through a disruption of hippocampal circuitry and activation of the innate immune system (Dixon et al., 1999; Pierce et al., 1998; Rosi et al., 2010).”
BackgroundThompson, H., Marklund, N., Lebold, D., Morales, D. M., Keck, C. A., Vinson, M., Royo, N., Grundy, R., & McIntosh, T. K. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05197.x · Cited by 44
“Similar to human TBI, over time there is a progressive development of the injury cavity and hydrocephalus seen with the lateral FP model (Bramlett et al., 1997; Pierce et al., 1998).”
BackgroundSelf-citationLozada, A. F., Maegele, M., Stark, H., Neugebauer, E., & Panula, P. (2005) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2004.00622.x · Cited by 44
Haar, C. V., Lam, F. C. W., Adams, W. K., Riparip, L., Kaur, S., Muthukrishna, M., Rosi, S., & Winstanley, C. A. (2016) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.6b00166 · Cited by 45
Detection of Calcifications In Vivo and Ex Vivo After Brain Injury in Rat Using SWIFT
Lehto, L., Sierra, A., Corum, C. A., Zhang, J., Idiyatullin, D., Pitkänen, A., Garwood, M., & Gröhn, O. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.03.002 · Cited by 43
“Therefore, they are more commonly detected in the chronic phase of the disease, that is, several months after TBI (Pierce et al., 1998) or brain ischemic insult (Mäkinen et al., 2007).”
BackgroundDose-dependent neuronal injury after traumatic brain injury.
Hellmich, H. L., Capra, B. A., Eidson, K. A., Garcia, J. M., Kennedy, D., Uchida, T., Parsley, M. O., Cowart, J. C., Dewitt, D., & Prough, D. (2005) · Brain Research · doi:10.1016/j.brainres.2005.02.054 · Cited by 43
Abdul-Muneer, P. M., Conte, A. A., Haldar, D., Long, M., Patel, R. K., Santhakumar, V., Overall, C., & Pfister, B. J. (2017) · Brain, behavior, and immunity · doi:10.1016/j.bbi.2016.09.002 · Cited by 43
“Over time, neurons and their axons can degenerate which can be evident months to years after injury (Pierce et al., 1998; Povlishock, 1993; Povlishock and Pettus, 1996; Sherriff et al., 1994).”
BackgroundO'Connor, C. A., Heath, D. L., Černak, I., Nimmo, A. J., & Vink, R. (2003) · Journal of Neurotrauma · doi:10.1089/089771503770195830 · Cited by 41
“In those studies that were able to demonstrate persistent functional deficits after injury, periodic testing was used in untrained animals (Pierce et al., 1998; Dixon et al., 1999).”
InfluentialMuir, J. K., Raghupathi, R., Emery, D. L., Bareyre, F., & McIntosh, T. (1999) · Experimental Neurology · doi:10.1006/exnr.1999.7187 · Cited by 42
Self-citationRoadmap for Advancing Pre-Clinical Science in Traumatic Brain Injury
Smith, D. H., Kochanek, P. M., Rosi, S., Meyer, R., Ferland‐Beckham, C., Prager, E. M., Ahlers, S. T., & Crawford, F. (2021) · Journal of Neurotrauma · doi:10.1089/neu.2021.0094 · Cited by 46
Self-citationHyperbaric oxygen effects on neuronal apoptosis associations in a traumatic brain injury rat model.
Wee, H.-Y., Lim, S.-W., Chio, C., Niu, K.-C., Wang, C.-C., & Kuo, J.-R. (2015) · Journal of Surgical Research · doi:10.1016/j.jss.2015.04.052 · Cited by 41
Inflammaging, cellular senescence, and cognitive aging after traumatic brain injury
Lu, Y., Jarrahi, A., Moore, N. D., Bartoli, M., Brann, D. W., Baban, B., & Dhandapani, K. M. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106090 · Cited by 52
“…the placebo arm (Roberts et al., 2004), supporting the notion that inflammation is a double-edged sword after injury (Bramlett and Dietrich, 2002; Pierce et al., 1998; Johnson et al., 2013a; Ramlackhansingh et al., 2011; Buki and Povlishock, 2006; Green et al., 2014; Gale et al., 1995; Johnson…”
BackgroundHistorical Review of the Fluid-Percussion TBI Model
Lyeth, B. G. (2016) · Frontiers in Neurology · doi:10.3389/fneur.2016.00217 · Cited by 41
“The extent of histological pathology was associated with injury severity (51, 55, 56) and the contusion cavity progressively expanded for up to 1 year post-TBI (57, 58).”
BackgroundKuo, J., Cheng, Y.-H., Chen, Y.-S., Chio, C., & Gean, P. (2013) · Journal of Neurotrauma · doi:10.1089/neu.2012.2689 · Cited by 41
“11 Each is intended to mimic certain components of clinical TBI, although it is difficult to establish consistent models that include most or all of the factors that contribute to post-trauma tissue damage.”
Christidi, F., Bigler, E., McCauley, S., Schnelle, K. P., Merkley, T. L., Mors, M. B., Li, X.-Q., Macleod, M. C., Chu, Z., Hunter, J., et al. (2011) · Journal of Neurotrauma · doi:10.1089/neu.2010.1644 · Cited by 40
“Similarly, there is an extensive experimental animal literature that shows cell loss or damage in the hippocampus following TBI (Carbonell and Grady, 1999; Geddes et al., 2003; Hicks et al., 1996; Pierce et al., 1998; Sick et al., 1998; Taft et al., 1992).”
InfluentialWang, H.-C., Duan, Z.-X., Wu, F.-F., Xie, L., Zhang, H., & Ma, Y.-B. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2009.1071 · Cited by 40
“Rather, axonal pathology has been shown to develop over the course of hours to days after injury (Adams et al., 1982; Pierce et al., 1998; D.H. Smith et al., 2003).”
Churn, S. B., Campbell, J. N., Gandhi, A., & Singh, B. (2014) · International Journal of Neurology and Brain Disorders · doi:10.15436/2377-1348.14.002 · Cited by 47
“Lateral fluid percussion TBI causes progressive degeneration of ipsilateral cortex over the course of a year[31], and the degeneration of certain cortical regions correlates with the incidence of late spontaneous seizures[26].”
BackgroundWilson, S., Raghupathi, R., Saatman, K. E., MacKinnon, M.-A., McIntosh, T. K., & Graham, D. I. (2004) · Journal of Neurotrauma · doi:10.1089/089771504322972031 · Cited by 38
“There is experimental evidence after fluid percussion-induced brain injury (Bramlett et al., 1997; Smith et al., 1997; McIntosh et al., 1998; Pierce et al., 1998), and controlled cortical impact (Dixon et al., 1999) in the rat that the volume of the cortical contusion and the ventricles increase…”
Self-citationEarly electroacupuncture treatment ameliorates neuroinflammation in rats with traumatic brain injury
Tang, W., Hsu, Y., Wang, C.-C., Hu, C.-Y., Chio, C., & Kuo, J.-R. (2016) · BMC Complementary and Alternative Medicine · doi:10.1186/s12906-016-1457-6 · Cited by 38
Ansari, M. A., Roberts, K. N., & Scheff, S. W. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.08.025 · Cited by 41
“[11], neuronal circuitry failure [72,73] and eventually behavioral problems after TBI [23,49,74-76].”
BackgroundGrossman, R., Shohami, E., Alexandrovich, A., Yatsiv, I., Kloog, Y., & Biegon, A. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.06.003 · Cited by 38
Shishido, H., Kishimoto, Y., Kawai, N., Toyota, Y., Ueno, M., Kubota, T., Kirino, Y., & Tamiya, T. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.06.066 · Cited by 38
Animal Models of Posttraumatic Seizures and Epilepsy
Glushakov, A. V., Glushakova, O. Y., Doré, S., Carney, P. R., & Hayes, R. L. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3816-2_27 · Cited by 40
Chen, S.-H., Wang, J., Chen, C., Chang, H.-K., Lin, M., Chang, F., & Chio, C. (2013) · Cell Transplantation · doi:10.3727/096368913x667006 · Cited by 34
“Long-term investigations have detected persistent neurological motor function impairment up to 1 year after severe lateral FPI (52).”
BackgroundSchütz, C., Stover, J., Thompson, H., Hoover, R., Morales, D., Schouten, J., McMillan, A., Soltesz, K. M., Motta, M., Spangler, Z. P., et al. (2006) · Critical Care Medicine · doi:10.1097/01.ccm.0000198326.32049.7f · Cited by 36
“Over time, the observed neurologic deficit shows a slight improvement, with the contralateral forelimb showing the most prolonged injury-induced deficit, up to 12 wks postinjury, similar to previously published results (30).”
MethodResultSelf-citationPharmacological blockers of CCR5 and CXCR4 improve recovery after traumatic brain injury.
Friedman-Levi, Y., Liraz-zaltsman, S., Shemesh, C., Rosenblatt, K., Kesner, E. L., Gincberg, G., Carmichael, S., Silva, A. J., & Shohami, E. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113604 · Cited by 35
Mammalian Models of Traumatic Brain Injury and a Place for Drosophila in TBI Research
Shah, E. J., Gurdziel, K., & Ruden, D. M. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00409 · Cited by 45
Pöttker, B., Stöber, F., Hummel, R., Angenstein, F., Radyushkin, K., Goldschmidt, J., & Schäfer, M. K. E. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1452-9 · Cited by 35
“Neurological deficits, motor deficits, impaired cognitive functions as well as anxiety-related behavior have been reported (Lindner et al. 1998; Pierce et al. 1998; Dixon et al. 1999; Jones et al. 2008).”
BackgroundA novel apparatus for lateral fluid percussion injury in the rat
Frey, L., Hellier, J. L., Unkart, C., Lepkin, A., Howard, A., Hasebroock, K., Serkova, N., Liang, L.-P., Patel, M. N., Soltesz, I., et al. (2008) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2008.10.022 · Cited by 35
Sanders, M. J., Dietrich, W., & Green, E. J. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02424-6 · Cited by 35
Metadata
- Authors
- Pierce, J. E. S., Smith, D. H., Trojanowski, J. Q., & McIntosh, T. K.
- Affiliations
- UConn Health (US)
- University of Pennsylvania (US)
- Corresponding author
- Smith, D.H
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 1998-07
- Volume
- 87
- Issue
- 2
- Pages
- 359-369
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2019544787
- Cited by
- 385
- References
- 61
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 9 · 2023: 10 · 2022: 10 · 2021: 11 · 2020: 16 · 2019: 16 · 2018: 16 · 2017: 11 · 2016: 21 · 2015: 15 · 2014: 15 · 2013: 22 · 2012: 14
- FWCI
- 11.56
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Neuroscience (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging (AG12527, R01AG012527)
- National Institute of Neurological Disorders and Stroke (NS-08803, NS26818)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury Research
- Physical Sciences › Engineering › Biomedical Engineering › Automotive and Human Injury Biomechanics
- Keywords
- traumatic brain injury, fluid percussion injury, long-term cognitive deficits, spatial learning impairment, motor impairment, axonal degeneration, amyloid precursor protein, neurodegeneration, thalamic calcification, ventriculomegaly, Alzheimer's disease
- MeSH terms
- Animals, Behavior, Animal, Brain, Brain Chemistry, Brain Injuries, Cognition Disorders, Forelimb, Male, Psychomotor Performance, Amyloid beta-Peptides, Amyloid beta-Protein Precursor, Rats, Sprague-Dawley, Maze Learning, Rats
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