Neuropathological Protection after Traumatic Brain Injury in Intact Female Rats Versus Males or Ovariectomized Females
Abstract
An important consideration in traumatic brain injury (TBI) in females is the influence of hormones on recovery. Recent studies in both cerebral ischemia and TBI have demonstrated an attenuation in both damage and neurologic recovery following hormonal treatment. However, the ability of endogenous hormone levels to provide neuropathological protection after fluid percussion (FP) brain injury has not been studied. The purpose of this experiment was to determine whether endogenous circulating hormones in the female rat could provide neuroprotection compared to males and ovariectomized female animals. Sixty-four Sprague-Dawley rats underwent a moderate (1.7-2.2 atm) right parasagittal FP injury. Intact females (i.e., nonovariectomized) were subjected to injury either during the proestrous (TBI-FP, n = 18) phase of their cycle or nonproestrous (TBI-FNP, n = 19) phase. A separate group of females were ovariectomized (TBI-OVX, n = 10) 10 days prior to FP injury in order to reduce hormone levels. Male animals were also traumatized (TBI-M, n = 17). Appropriate sham controls (Sham-FP, n = 2; Sham-FNP, n = 2; Sham-OVX, n = 2; Sham-M, n = 2) also underwent all aspects of surgery except for the actual FP injury. All groups were sacrificed 3 days following TBI for analysis. Both intact female groups had significantly (p < 0.05) smaller cortical contusions compared to male animals. In addition to this finding, the TBI-FNP group was significantly (p < 0.04) different from the ovariectomized female animals. Ovariectomized rats had larger areas of damage compared to intact females. The TBI-OVX group's cortical contusion volume was similar to male animals. These results provide evidence for endogenous hormonal histopathological protection following parasagittal FP brain injury. The use of hormone therapy after TBI warrants continued exploration.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Estrous stage at injury did not influence contusion volumes or behavioral outcomes in female rats.
“Estrous stage at injury did not influence contusion volumes or behavioral outcomes in female rats. 38,61”
From Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know (2019) · cites this paper as [61]
Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
The Role of Excitatory Amino Acids and NMDA Receptors in Traumatic Brain Injury
Faden, A. I., Demediuk, P., Panter, S. S., & Vink, R. (1989) · Science · doi:10.1126/science.2567056 · Cited by 1,508 · see citing works
A fluid percussion model of experimental brain injury in the rat
Dixon, C. E., Lyeth, B. G., Povlishock, J. T., Findling, R. L., Hamm, R. J., Marmarou, A., Young, H. F., & Hayes, R. L. (1987) · Journal of neurosurgery · doi:10.3171/jns.1987.67.1.0110 · Cited by 1,038 · see citing works
Goodman, Y., Bruce‐Keller, A. J., Cheng, B., & Mattson, M. P. (1996) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1996.66051836.x · Cited by 830 · see citing works
Zilles, K. (1985) · Springer eBooks · doi:10.1007/978-3-642-70573-1 · Cited by 756 · see citing works
Gender-Linked Brain Injury in Experimental Stroke
Alkayed, N. J., Harukuni, I., Kimes, A. S., London, E. D., Traystman, R. J., & Hurn, P. D. (1998) · Stroke · doi:10.1161/01.str.29.1.159 · Cited by 754 · see citing works
The Cortex of the Rat: A Stereotaxic Atlas
Zilles, K. (1985) · Medical Entomology and Zoology · Cited by 657 · see citing works
Roof, R. L., & Hall, E. D. (2000) · Journal of Neurotrauma · doi:10.1089/neu.2000.17.367 · Cited by 652 · see citing works
17-β Estradiol Protects Neurons from Oxidative Stress-Induced Cell Death in Vitro
Behl, C., Widmann, M., Trapp, T., & Holsboer, F. (1995) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1995.2647 · Cited by 608 · see citing works
Globus, M. Y. ‐., Alonso, O. F., Dietrich, W. D., Busto, R., & Ginsberg, M. D. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.65041704.x · Cited by 607 · see citing works
Self-citationRoberts, G. W., Gentleman, S. M., Lynch, A., Murray, L., Landon, M., & Graham, D. I. (1994) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.57.4.419 · Cited by 569 · see citing works
Estradiol Protects against Ischemic Injury
Dubal, D. B., Kashon, M. L., Pettigrew, L. C., Ren, J. M., Finklestein, S. P., Rau, S. W., & Wise, P. M. (1998) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199811000-00012 · Cited by 554 · see citing works
Nilsson, P., Hillered, L., Pontén, U., & Ungerstedt, U. (1990) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1990.115 · Cited by 519 · see citing works
Experimental fluid percussion brain injury: vascular disruption and neuronal and glial alterations.
Cortez, S., McIntosh, T., & Noble, L. (1989) · Brain Research · doi:10.1016/0006-8993(89)91190-6 · Cited by 481 · see citing works
Estradiol Modulates bcl-2 in Cerebral Ischemia: A Potential Role for Estrogen Receptors
Dubal, D. B., Shughrue, P. J., Wilson, M. E., Merchenthaler, I. J., & Wise, P. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-15-06385.1999 · Cited by 449 · see citing works
Estrogen-Mediated Neuroprotection After Experimental Stroke in Male Rats
Toung, T. J. K., Traystman, R. J., & Hurn, P. D. (1998) · Stroke · doi:10.1161/01.str.29.8.1666 · Cited by 364 · see citing works
Dietrich, W. D., Alonso, O. F., & Halley, M. (1994) · Journal of Neurotrauma · doi:10.1089/neu.1994.11.289 · Cited by 354 · see citing works
Self-citationNeuroprotective Effects of Female Gonadal Steroids in Reproductively Senescent Female Rats
Alkayed, N. J., Murphy, S. J., Traystman, R. J., & Hurn, P. D. (2000) · Stroke · doi:10.1161/01.str.31.1.161 · Cited by 335 · see citing works
Recent advances in neurotrauma
Graham, D. I., McIntosh, T. K., Maxwell, W. L., & Nicoll, J. A. R. (2000) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/59.8.641 · Cited by 328 · see citing works
Gender influences outcome of brain injury: progesterone plays a protective role
Roof, R. L., Duvdevani, R., & Stein, D. G. (1993) · Brain Research · doi:10.1016/0006-8993(93)91526-x · Cited by 327 · see citing works
Roof, R. L., Duvdevani, R., Braswell, L., & Stein, D. G. (1994) · Experimental Neurology · doi:10.1006/exnr.1994.1147 · Cited by 322 · see citing works
Estrogen protects primary cortical neurons from glutamate toxicity
Singer, C. A., Rogers, K. L., Strickland, T. M., & Dorsa, D. M. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)12760-9 · Cited by 322 · see citing works
Dietrich, W. D., Alonso, O. F., Busto, R., Globus, M. Y. ‐., & Ginsberg, M. D. (1994) · Acta Neuropathologica · doi:10.1007/bf00296740 · Cited by 321 · see citing works
Self-citationEffect of 17 beta-estradiol on endothelium-dependent responses in the rabbit.
Gisclard, V., Miller, V. M., & Vanhoutte, P. M. (1988) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)24250-1 · Cited by 320 · see citing works
Progesterone protects against lipid peroxidation following traumatic brain injury in rats
Roof, R. L., Hoffman, S. W., & Stein, D. G. (1997) · Molecular and Chemical Neuropathology · doi:10.1007/bf02815156 · Cited by 317 · see citing works
17β-Estradiol Reduces Stroke Injury in Estrogen-Deficient Female Animals
Rusa, R., Alkayed, N. J., Crain, B. J., Traystman, R. J., Kimes, A. S., London, E. D., Klaus, J. A., & Hurn, P. D. (1999) · Stroke · doi:10.1161/01.str.30.8.1665 · Cited by 304 · see citing works
EPIDEMIOLOGIC ASPECTS OF BRAIN INJURY
Kraus, J. F., & McArthur, D. L. (1996) · Neurologic Clinics · doi:10.1016/s0733-8619(05)70266-8 · Cited by 304 · see citing works
17β-Estradiol protects against NMDA-induced excitotoxicity by direct inhibition of NMDA receptors
Weaver, C. E., Park-Chung, M., Gibbs, T. T., & Farb, D. H. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00449-6 · Cited by 274 · see citing works
Progesterone Rapidly Decreases Brain Edema: Treatment Delayed up to 24 Hours Is Still Effective
Roof, R. L., Duvdevani, R., Heyburn, J. W., & Stein, D. G. (1996) · Experimental Neurology · doi:10.1006/exnr.1996.0063 · Cited by 244 · see citing works
Pierce, J., Trojanowski, J., Graham, D., Smith, D., & McIntosh, T. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-03-01083.1996 · Cited by 239 · cited 1× · see citing works
“Various laboratories have reported increases in b -APP immunoreactivity after clinical and experimental brain injury (Bramlett et al., 1997; Pierce et al., 1996; Roberts et al., 1994).”
Estradiol Exerts Neuroprotective Effects When Administered After Ischemic Insult
Yang, S.-H., Shi, J., Day, A. L., & Simpkins, J. W. (2000) · Stroke · doi:10.1161/01.str.31.3.745 · Cited by 236 · see citing works
Estradiol protects against β-amyloid (25–35)-induced toxicity in SK-N-SH human neuroblastoma cells
Green, P. S., Gridley, K. E., & Simpkins, J. W. (1996) · Neuroscience Letters · doi:10.1016/s0304-3940(96)13148-7 · Cited by 230 · see citing works
Estrogen-Binding Sites in Endothelial Cell Cultures
Colburn, P., & Buonassisi, V. (1978) · Science · doi:10.1126/science.684408 · Cited by 229 · see citing works
BRAMLETT, H. M., KRAYDIEH, S., GREEN, E. J., & DIETRICH, W. D. (1997) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-199710000-00007 · Cited by 225 · see citing works
Self-citationSmith, S. S., Waterhouse, B. D., Chapin, J. K., & Woodward, D. J. (1987) · Brain Research · doi:10.1016/0006-8993(87)90634-2 · Cited by 222 · see citing works
Yamakami, I., & McIntosh, T. K. (1989) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1989.16 · Cited by 215 · see citing works
Hayes, R. L., Jenkins, L. W., & Lyeth, B. G. (1992) · Journal of Neurotrauma · doi:10.1177/089771519200901s16 · Cited by 214 · see citing works
Hall, E. D. (1992) · Journal of Neurotrauma · doi:10.1089/neu.1992.9.173 · Cited by 192 · see citing works
Tanno, H., Nockels, R. P., Pitts, L. H., & Noble‐Haeusslein, L. J. (1992) · Journal of Neurotrauma · doi:10.1089/neu.1992.9.21 · Cited by 184 · see citing works
Smith, S. S. (1994) · Progress in Neurobiology · doi:10.1016/0301-0082(94)90057-4 · Cited by 181 · see citing works
Estrogen Receptor Is Expressed in Different Types of Glial Cells in Culture
Santagati, S., Melcangi, R. C., Celotti, F., Martini, L., & Maggi, A. C. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.63062058.x · Cited by 159 · see citing works
Emerson, C. S., Headrick, J. P., & Vink, R. (1993) · Brain Research · doi:10.1016/0006-8993(93)90778-l · Cited by 154 · see citing works
Postischemic Cerebral Blood Flow Recovery in the Female: Effect of 17β-Estradiol
Hurn, P. D., Littleton‐Kearney, M. T., Kirsch, J. R., Dharmarajan, A., & Traystman, R. J. (1995) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1995.82 · Cited by 150 · see citing works
Progesterone treatment attenuates brain edema following contusion injury in male and female rats
Roof, R. L., Duvdevani, R., & Stein, D. G. (1992) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-1992-4608 · Cited by 147 · see citing works
Regan, R. F., & Guo, Y. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00437-x · Cited by 138 · see citing works
Hormonal state affects recovery from frontal cortex lesions in adult female rats
Attella, M. J., Nattinville, A., & Stein, D. G. (1987) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(87)90918-6 · Cited by 138 · see citing works
Progesterone administration attenuates excitatory amino acid responses of cerebellar Purkinje cells
Smith, S. S. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90377-z · Cited by 130 · see citing works
Soares, H. D., Thomas, M. J., Cloherty, K., & McIntosh, T. K. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb10061.x · Cited by 115 · see citing works
Fukuda, K., Yao, H., Ibayashi, S., Nakahara, T., Uchimura, H., & Fujishima, M. (2000) · Stroke · doi:10.1161/01.str.31.1.155 · Cited by 111 · see citing works
Ginsberg, M. D., Zhao, W., Alonso, O. F., Loor, J. Y., Dietrich, W. D., & Busto, R. (1997) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1997.272.6.h2859 · Cited by 107 · see citing works
Self-citationDietrich, W. D., Alonso, O. F., Busto, R., Prado, R., Zhao, W., Dewanjee, M. K., & Ginsberg, M. D. (1998) · Neurosurgery · doi:10.1097/00006123-199809000-00105 · Cited by 105 · see citing works
Self-citationDietrich, W. D., Alonso, O. F., Busto, R., Prado, R., Dewanjee, S., Dewanjee, M. K., & Ginsberg, M. D. (1996) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199605000-00015 · Cited by 98 · see citing works
Self-citationShi, J., Panickar, K. S., Yang, S.-H., Rabbani, O., Day, A. L., & Simpkins, J. W. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00888-9 · Cited by 95 · see citing works
Non-genomic effects of estrogen and the vessel wall
Farhat, M. Y., Abi-Younes, S., & Ramwell, P. W. (1996) · Biochemical Pharmacology · doi:10.1016/s0006-2952(95)02159-0 · Cited by 91 · see citing works
Gentleman, S. M., Graham, D. I., & Roberts, G. W. (1993) · Progress in brain research · doi:10.1016/s0079-6123(08)63270-7 · Cited by 87 · see citing works
Role of Excitatory Amino Acid‐Mediated Ionic Fluxes in Traumatic Brain Injury
Katayama, Y., Maeda, T., Koshinaga, M., Kawamata, T., & Tsubokawa, T. (1995) · Brain Pathology · doi:10.1111/j.1750-3639.1995.tb00621.x · Cited by 81 · see citing works
Regional cerebrovascular responses to progressive hypotension after traumatic brain injury in cats
DeWitt, D. S., Prough, D. S., Taylor, C. L., Whitley, J. M., Deal, D. D., & Vines, S. M. (1992) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1992.263.4.h1276 · Cited by 67 · see citing works
Dietrich, W. D., Alonso, O. F., Busto, R., et al. (1994) · Acta Neuropathologica · doi:10.1007/s004010050083 · Cited by 57 · see citing works
Self-citationDevelopment of Brain Edema Following Fluid Percussion Injury
Marmarou, A., Nakamura, T., Sakamoto, H., Jenkins, L., & Becker, D. P. (1985) · Springer eBooks · doi:10.1007/978-3-642-70696-7_11 · Cited by 10 · see citing works
The bioelectric parameters of the vagina during the oestrous cycle of the rat.
Edwards, D., & Levin, R. J. (1975) · The Journal of Physiology · doi:10.1113/jphysiol.1975.sp010975 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Sex bias in neuroscience and biomedical research
Beery, A. K., & Zucker, I. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.07.002 · Cited by 1,763 · see citing works
Fleminger, S. (2003) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.74.7.857 · Cited by 719 · see citing works
Pathophysiology of Cerebral Ischemia and Brain Trauma: Similarities and Differences
Bramlett, H., & Dietrich, W. (2004) · Journal of Cerebral Blood Flow and Metabolism · doi:10.1097/01.wcb.0000111614.19196.04 · Cited by 622 · see citing works
Self-citationSex Differences in Traumatic Brain Injury: What We Know and What We Should Know
Gupte, R. P., Brooks, W. M., Vukas, R. R., Pierce, J. D., & Harris, J. L. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6171 · Cited by 533 · see citing works
Lateral Fluid Percussion Brain Injury: A 15-Year Review and Evaluation
Thompson, H., Lifshitz, J., Marklund, N., Grady, M., Graham, D., Hovda, D., & McIntosh, T. (2005) · Journal of Neurotrauma · doi:10.1089/neu.2005.22.42 · Cited by 545 · see citing works
Sex Differences in Outcome after Mild Traumatic Brain Injury
Bazarian, J. J., Blyth, B. J., Mookerjee, S., He, H., & McDermott, M. (2009) · Journal of Neurotrauma · doi:10.1089/neu.2009.1068 · Cited by 375 · see citing works
Experimental models of traumatic brain injury: do we really need to build a better mousetrap?
Morales, D. M., Marklund, N., Lebold, D., Thompson, H. J., Pitkanen, A., Maxwell, W. L., Longhi, L., Laurer, H., Maegele, M., Neugebauer, E., et al. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.030 · Cited by 339 · see citing works
Sexual dimorphism in the inflammatory response to traumatic brain injury
Villapol, S., Loane, D. J., & Burns, M. P. (2017) · Glia · doi:10.1002/glia.23171 · Cited by 310 · see citing works
Progesterone exerts neuroprotective effects after brain injury
Stein, D. G. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.06.012 · Cited by 294 · see citing works
Sex Differences in Concussion Symptoms of High School Athletes
Frommer, L. J., Gurka, K. K., Cross, K. M., Ingersoll, C. D., Comstock, R. D., & SALIBA, S. A. (2011) · Journal of Athletic Training · doi:10.4085/1062-6050-46.1.76 · Cited by 288 · see citing works
Marklund, N., & Hillered, L. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.01163.x · Cited by 254 · see citing works
Li, Y., Li, Y., Li, X., Zhang, S., Zhao, J., Zhu, X., & Tian, G. (2017) · PLoS ONE · doi:10.1371/journal.pone.0169650 · Cited by 243 · see citing works
Longitudinal cognitive changes in traumatic brain injury
Himanen, L., Portin, R. I., Isoniemi, H., Helenius, H. Y. M., Kurki, T. J. I., & Tenovuo, O. S. (2006) · Neurology · doi:10.1212/01.wnl.0000194264.60150.d3 · Cited by 210 · see citing works
Estrogens as neuroprotectants: Estrogenic actions in the context of cognitive aging and brain injury
Engler-Chiurazzi, E. B., Brown, C. M., Povroznik, J. M., & Simpkins, J. W. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.12.008 · Cited by 205 · see citing works
The Effect of Gender on Patients With Moderate to Severe Head Injuries
Berry, C., Ley, E. J., Tillou, A., Cryer, G., Margulies, D. R., & Salim, A. (2009) · Journal of Trauma: Injury, Infection & Critical Care · doi:10.1097/ta.0b013e3181ba3354 · Cited by 197 · see citing works
DeWitt, D. S., & Prough, D. S. (2003) · Journal of Neurotrauma · doi:10.1089/089771503322385755 · Cited by 195 · see citing works
Sex-related responses after traumatic brain injury: Considerations for preclinical modeling
Späni, C. B., Braun, D. J., & Van Eldik, L. J. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.03.006 · Cited by 195 · see citing works
Doran, S. J., Ritzel, R., Glaser, E. P., Henry, R., Faden, A., & Loane, D. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6019 · Cited by 154 · see citing works
Macrophagic and microglial responses after focal traumatic brain injury in the female rat
Turtzo, L., Lescher, J., Janes, L., Dean, D. D., Budde, M. D., & Frank, J. A. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-82 · Cited by 167 · see citing works
Tucker, L. B., Fu, A. H., & McCabe, J. T. (2015) · Journal of Neurotrauma · doi:10.1089/neu.2015.3977 · Cited by 162 · see citing works
Robertson, C. L., Puskar, A., Hoffman, G. E., Murphy, A. Z., Saraswati, M., & Fiskum, G. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2005.09.014 · Cited by 152 · see citing works
Sex hormones modulate brain damage in multiple sclerosis: MRI evidence
Tomassini, V. (2005) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2003.033324 · Cited by 156 · see citing works
Wagner, A. K., Willard, L. A., Kline, A. E., Wenger, M. K., Bolinger, B. D., Ren, D., Zafonte, R. D., & Dixon, C. E. (2004) · Brain Research · doi:10.1016/j.brainres.2003.11.027 · Cited by 141 · see citing works
THE EVIDENCE FOR HYPOTHERMIA AS A NEUROPROTECTANT IN TRAUMATIC BRAIN INJURY
Dietrich, W. D., & Bramlett, H. (2010) · Neurotherapeutics · doi:10.1016/j.nurt.2009.10.015 · Cited by 142 · see citing works
Self-citationNeuroprotection by ovarian hormones in animal models of neurological disease
Hoffman, G., Merchenthaler, I., & Zup, S. (2006) · Endocrine · doi:10.1385/endo:29:2:217 · Cited by 149 · see citing works
Critical appraisal of neuroprotection trials in head injury: What have we learned?
Tolias, C., & Bullock, M. R. (2011) · NeuroRx · doi:10.1602/neurorx.1.1.71 · Cited by 117 · see citing works
Sex, Sex Steroids, and Brain Injury
Herson, P. S., Koerner, I. P., & Hurn, P. D. (2009) · Seminars in Reproductive Medicine · doi:10.1055/s-0029-1216276 · Cited by 136 · see citing works
Adult or Perinatal Brain Injury
Hurn, P. D., Vannucci, S. J., & Hagberg, H. (2004) · Stroke · doi:10.1161/01.str.0000153064.41332.f6 · Cited by 136 · see citing works
Neuroprotection and traumatic brain injury: theoretical option or realistic proposition
Faden, A. I. (2002) · Current Opinion in Neurology · doi:10.1097/01.wco.0000044767.39452.bf · Cited by 135 · see citing works
Traumatic Brain Injury Outcomes in Pre- and Post- Menopausal Females Versus Age-Matched Males
Davis, D. P., Douglas, D. J., Smith, W., Sise, M. J., Vilke, G. M., Holbrook, T. L., Kennedy, F., Eastman, A. B., Velky, T., & Hoyt, D. B. (2006) · Journal of Neurotrauma · doi:10.1089/neu.2006.23.140 · Cited by 132 · see citing works
Singleton, R. H., Yan, H. Q., Fellows-Mayle, W. K., & Dixon, C. E. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2010.1291 · Cited by 130 · see citing works
Regulation of brain microglia by female gonadal steroids
Habib, P., & Beyer, C. (2015) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.02.018 · Cited by 118 · see citing works
Dose-Dependent Effects of Androgens on Outcome after Focal Cerebral Ischemia in Adult Male Mice
Uchida, M., Palmateer, J., Herson, P. S., DeVries, A. C., Cheng, J., & Hurn, P. D. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.60 · Cited by 118 · see citing works
Vagnerova, K., Koerner, I. P., & Hurn, P. D. (2008) · Anesthesia & Analgesia · doi:10.1213/ane.0b013e31817326a5 · Cited by 115 · see citing works
Understanding Traumatic Brain Injury in Females: A State-of-the-Art Summary and Future Directions
Valera, E. M., Joseph, A.-L. C., Snedaker, K., Breiding, M. J., Robertson, C., Colantonio, A., Levin, H. S., Pugh, M. J., Yurgelun-Todd, D. A., Mannix, R., et al. (2020) · Journal of Head Trauma Rehabilitation · doi:10.1097/htr.0000000000000652 · Cited by 113 · see citing works
Progesterone's role in neuroprotection, a review of the evidence
Deutsch, E. R., Espinoza, T. R., Atif, F., Woodall, E., Kaylor, J., & Wright, D. W. (2013) · Brain Research · doi:10.1016/j.brainres.2013.07.014 · Cited by 110 · see citing works
Considerations for Studying Sex as a Biological Variable in Spinal Cord Injury
Stewart, A. N., MacLean, S. M., Stromberg, A. J., Whelan, J. P., Bailey, W. M., Gensel, J. C., & Wilson, M. E. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00802 · Cited by 110 · see citing works
Murphy, S. J., Littleton‐Kearney, M. T., & Hurn, P. D. (2002) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/01.wcb.0000037990.07114.07 · Cited by 104 · see citing works
Seizure‐induced hippocampal damage in the mature and immature brain
Lado, F. A., Laureta, E. C., & Moshé, S. L. (2002) · Epileptic Disorders · doi:10.1684/j.1950-6945.2002.tb00479.x · Cited by 105 · see citing works
Wagner, A. K., Kline, A. E., Sokoloski, J. E., ZAFONTE, R. D., Capulong, E., & Dixon, C. E. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)01103-5 · Cited by 104 · see citing works
Hyperthermia and central nervous system injury
Dietrich, W. D., & Bramlett, H. M. (2007) · Progress in brain research · doi:10.1016/s0079-6123(06)62011-6 · Cited by 102 · see citing works
Self-citationToung, T. J. K., Chen, T., Littleton‐Kearney, M. T., Hurn, P. D., & Murphy, S. J. (2004) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/01.wcb.0000135594.13576.d2 · Cited by 98 · see citing works
Datto, J. P., Bastidas, J. C., Miller, N. L., Shah, A. K., Arheart, K. L., Marcillo, A. E., Dietrich, W. D., & Pearse, D. D. (2015) · Journal of Neurotrauma · doi:10.1089/neu.2014.3702 · Cited by 96 · see citing works
Self-citationSoy phytoestrogens are neuroprotective against stroke-like injury in vitro
Schreihofer, D. A., & Redmond, L. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.10.003 · Cited by 94 · see citing works
Endogenous neuroprotective factors: neurosteroids.
Wojtal, K., Trojnar, M. K., & Czuczwar, S. J. (2006) · PubMed · Cited by 93 · see citing works
Day, N. L., Floyd, C. L., D'Alessandro, T. L., Hubbard, W. J., & Chaudry, I. H. (2013) · Journal of Neurotrauma · doi:10.1089/neu.2013.2854 · Cited by 90 · see citing works
Severe traumatic brain injury: is there a gender difference in mortality?
Ottochian, M., Salim, A., Berry, C., Chan, L. S., Wilson, M. T., & Margulies, D. R. (2009) · The American Journal of Surgery · doi:10.1016/j.amjsurg.2008.09.008 · Cited by 87 · see citing works
Reactive gliosis in traumatic brain injury: a comprehensive review
Amlerova, Z., Chmelová, M., Anděrová, M., & Vargová, L. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1335849 · Cited by 86 · see citing works
Hall, E. D., Gibson, T. R., & Pavel, K. M. (2005) · Journal of Neurotrauma · doi:10.1089/neu.2005.22.669 · Cited by 85 · see citing works
Jullienne, A., Salehi, A., Affeldt, B. M., Baghchechi, M., Haddad, E., Avitua, A., Walsworth, M., Enjalric, I., Hamer, M., Bhakta, S., et al. (2018) · Journal of Neurotrauma · doi:10.1089/neu.2017.5547 · Cited by 84 · see citing works
Monaco, C. M., Mattiola, V. V., Folweiler, K. A., Tay, J. K., Yelleswarapu, N. K., Curatolo, L. M., Matter, A. M., B, J. P. C. A., & Kline, A. E. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.01.007 · Cited by 83 · see citing works
Dada, T., Rosenzweig, J. M., Shammary, M. A., Firdaus, W. J. J., Al-Rebh, S., Borbiev, T., Tekes, A., Zhang, J., Alqahtani, E., Mori, S., et al. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.01.014 · Cited by 81 · see citing works
17 β -Estradiol Is Protective in Spinal Cord Injury in Post- and Pre-Menopausal Rats
Chaovipoch, P., Jelks, K. A., Gerhold, L. M., West, E. J., Chongthammakun, S., & Floyd, C. L. (2006) · Journal of Neurotrauma · doi:10.1089/neu.2006.23.830 · Cited by 79 · see citing works
Neuroprotective Anti-Apoptosis Effect of Estrogens in Traumatic Brain Injury
Soustiel, J. F., Palzur, E., Nevo, O., Thaler, I., & Vlodavsky, E. (2005) · Journal of Neurotrauma · doi:10.1089/neu.2005.22.345 · Cited by 78 · see citing works
Maghool, F., Khaksari, M., & khachki, A. S. (2012) · Brain Research · doi:10.1016/j.brainres.2012.12.014 · Cited by 77 · see citing works
More than a decade of estrogen neuroprotection
Simpkins, J. W., & Singh, M. (2007) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2007.10.009 · Cited by 75 · see citing works
Gender and Estrogen Manipulation Do Not Affect Traumatic Brain Injury in Mice
Bruce‐Keller, A. J., Dimayuga, F. O., Reed, J. L., Wang, C., Angers, R. C., Wilson, M. E., Smith, V. D., & Scheff, S. W. (2007) · Journal of Neurotrauma · doi:10.1089/neu.2006.0163 · Cited by 75 · see citing works
Newer pharmacological approaches for antioxidant neuroprotection in traumatic brain injury
Hall, E. D., Wang, J. A., Miller, D. M., Cebak, J. E., & Hill, R. L. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.08.005 · Cited by 73 · see citing works
Traumatic brain injury in women across lifespan
Blaya, M. O., Raval, A. P., & Bramlett, H. M. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105613 · Cited by 69 · see citing works
Self-citationThe importance of gender on the beneficial effects of posttraumatic hypothermia
Suzuki, T., Bramlett, H. M., & Dietrich, W. D. (2003) · Experimental Neurology · doi:10.1016/s0014-4886(03)00389-3 · Cited by 67 · see citing works
Self-citationChakrabarti, M., Das, A., Samantaray, S., Smith, J. A., Banik, N. L., Haque, A., & Ray, S. K. (2015) · Reviews in the Neurosciences · doi:10.1515/revneuro-2015-0032 · Cited by 65 · see citing works
Wilcox, B. J., Beckwith, J. G., Greenwald, R. M., Raukar, N. P., Chu, J. J., McAllister, T. W., Flashman, L. A., Maerlender, A., Duhaime, A., & Crisco, J. J. (2015) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2015.04.005 · Cited by 64 · see citing works
Sex differences in orbitofrontal connectivity in male and female veterans with TBI
McGlade, E., Rogowska, J., & Yurgelun-Todd, D. (2015) · Brain Imaging and Behavior · doi:10.1007/s11682-015-9379-3 · Cited by 63 · see citing works
Qu, C., Lu, D., Goussev, A. V., Schallert, T. J., Mahmood, A., & Chopp, M. (2005) · Journal of neurosurgery · doi:10.3171/jns.2005.103.4.0695 · Cited by 62 · see citing works
Dietrich, W. D., & Bramlett, H. M. (2017) · Brain Circulation · doi:10.4103/bc.bc_28_17 · Cited by 62 · see citing works
Self-citationHigh-soy diet decreases infarct size after permanent middle cerebral artery occlusion in female rats
Schreihofer, D. A., Do, K. D., & Schreihofer, A. M. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00642.2004 · Cited by 60 · see citing works
The Effects of Early Post-Traumatic Hyperthermia in Female and Ovariectomized Rats
Suzuki, T., Bramlett, H. M., Ruenes, G., & Dietrich, W. D. (2004) · Journal of Neurotrauma · doi:10.1089/0897715041526186 · Cited by 59 · see citing works
Self-citationSex hormones modulate pathogenic processes in experimental traumatic brain injury
Gölz, C., Kirchhoff, F. P., Westerhorstmann, J., Schmidt, M., Hirnet, T., Rune, G. M., Bender, R. A., & Schäfer, M. K. E. (2019) · Journal of Neurochemistry · doi:10.1111/jnc.14678 · Cited by 58 · see citing works
Effect of Gender on Recovery After Spinal Cord Injury
Chan, W.-M., Mohammed, Y. A. A., Lee, I., & Pearse, D. D. (2013) · Translational Stroke Research · doi:10.1007/s12975-012-0249-7 · Cited by 57 · see citing works
Progesterone protects mitochondrial function in a rat model of pediatric traumatic brain injury
Robertson, C. L., & Saraswati, M. (2015) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-014-9585-5 · Cited by 56 · see citing works
Meconi, A., Wortman, R. C., Wright, D. K., Neale, K. J., Clarkson, M., Shultz, S. R., & Christie, B. R. (2018) · PLoS ONE · doi:10.1371/journal.pone.0197187 · Cited by 55 · see citing works
Jones, N. C., Constantin, D., Prior, M. J. W., Morris, P. G., Marsden, C. A., & Murphy, S. P. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03995.x · Cited by 55 · see citing works
Coughlan, T. C., Gibson, C. L., & Murphy, S. P. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03068.x · Cited by 54 · see citing works
Ventilation and phrenic output following high cervical spinal hemisection in male vs. female rats
Doperalski, N. J., Sandhu, M. S., Bavis, R. W., Reier, P. J., & Fuller, D. D. (2008) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2008.06.005 · Cited by 53 · see citing works
The search for neuroprotective strategies in stroke.
Danton, G. H., & Dietrich, W. D. (2004) · PubMed Central · Cited by 53 · see citing works
Self-citationScaled Cortical Impact in Immature Swine: Effect of Age and Gender on Lesion Volume
Missios, S., Harris, B. T., Simoni, M. K., Dodge, C. P., Costine, B. A., Quebada, P. B., Clerkin, P. Q., Adams, L. B., Duhaime, A.-C., & Lee, Y.-L. (2009) · Journal of Neurotrauma · doi:10.1089/neu.2009.0956 · Cited by 50 · see citing works
Khaksari, M., Soltani, Z., & Shahrokhi, N. (2017) · Translational Stroke Research · doi:10.1007/s12975-017-0588-5 · Cited by 50 · see citing works
Clevenger, A. C., Kim, H., Salcedo, E. E., Yonchek, J. C., Rodgers, K. M., Orfila, J. E., Dietz, R. M., Quillinan, N., Traystman, R. J., & Herson, P. S. (2018) · Journal of Molecular Neuroscience · doi:10.1007/s12031-018-1038-x · Cited by 50 · see citing works
The Role of Estradiol in Traumatic Brain Injury: Mechanism and Treatment Potential
Kövesdi, E., Szabó‐Meleg, E., & Ábrahám, I. M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010011 · Cited by 50 · see citing works
Sex-Dependent Macromolecule and Nanoparticle Delivery in Experimental Brain Injury
Bharadwaj, V. N., Copeland, C., Mathew, E., Newbern, J. M., Anderson, T. R., Lifshitz, J., Kodibagkar, V. D., & Stabenfeldt, S. E. (2020) · Tissue Engineering Part A · doi:10.1089/ten.tea.2020.0040 · Cited by 50 · see citing works
Mondello, S., Cantrell, A., Italiano, D., Fodale, V., Mondello, P., & Ang, D. N. (2014) · BioMed Research International · doi:10.1155/2014/473419 · Cited by 44 · see citing works
Sex Differences in Cerebral Blood Flow Associated with a History of Concussion
Hamer, J., Churchill, N. W., Hutchison, M. G., Graham, S. J., & Schweizer, T. A. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2019.6800 · Cited by 43 · see citing works
Thompson, 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 · see citing works
Littleton‐Kearney, M. T., Klaus, J. A., & Hurn, P. D. (2005) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600052 · Cited by 43 · see citing works
The sex-specific interaction of the microbiome in neurodegenerative diseases
Cox, L. M., Abou‐El‐Hassan, H., Maghzi, A. H., Vincentini, J., & Weiner, H. L. (2019) · Brain Research · doi:10.1016/j.brainres.2019.146385 · Cited by 42 · see citing works
Reglődi, D., Lubics, A., Kiss, P., Lengvári, I., Gaszner, B., Tóth, G. K., Hegyi, O., & Tamás, A. (2006) · Neuropeptides · doi:10.1016/j.npep.2006.06.001 · Cited by 39 · see citing works
The evolution of traumatic brain injury in a rat focal contusion model
Turtzo, L. C., Budde, M. D., Gold, E. M., Lewis, B. K., Janes, L. E., Yarnell, A. M., Grunberg, N. E., Watson, W., & Frank, J. A. (2012) · NMR in Biomedicine · doi:10.1002/nbm.2886 · Cited by 36 · see citing works
Nudi, E., Jacqmain, J., Dubbs, K., Geeck, K., Salois, G., Searles, M. A., & Smith, J. S. (2014) · Journal of Neurotrauma · doi:10.1089/neu.2014.3618 · Cited by 34 · see citing works
Cui, Q., Wang, L.-Y., Wei, Z.-H., & Qu, W.-S. (2014) · Neurochemical Research · doi:10.1007/s11064-014-1306-2 · Cited by 30 · see citing works
Hönikl, L. S., Lämmer, F., Gempt, J., Meyer, B., Schlegel, J., & Delbridge, C. (2020) · Journal of Neuro-Oncology · doi:10.1007/s11060-020-03467-y · Cited by 34 · see citing works
Amer, D. A. M., Kretzschmar, G., Müller, N., Stanke, N., Lindemann, D., & Vollmer, G. (2010) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2010.04.018 · Cited by 34 · see citing works
Gender-related differences in intracranial hypertension and outcome after traumatic brain injury
Czosnyka, M., Radolovich, D. K., Balestreri, M., Lavinio, A., Hutchinson, P. J., Timofeev, I. S., Smielewski, P. S., & Pickard, J. D. (2008) · Acta neurochirurgica. Supplementum · doi:10.1007/978-3-211-85578-2_5 · Cited by 34 · see citing works
Taylor, A. N., Tio, D. L., Paydar, A., & Sutton, R. L. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2017.5238 · Cited by 33 · see citing works
Scott, M. C., Prabhakara, K. S., Walters, A. J., Olson, S. D., & Cox, C. S. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.753570 · Cited by 32 · see citing works
Sex shapes experimental ischemic brain injury
Cheng, J. G., & Hurn, P. D. (2009) · Steroids · doi:10.1016/j.steroids.2009.10.014 · Cited by 33 · see citing works
Unmasking the Adverse Impacts of Sex Bias on Science and Research Animal Welfare
Nunamaker, E. A., & Turner, P. V. (2023) · Animals · doi:10.3390/ani13172792 · Cited by 32 · see citing works
Neuroprotective Effects of Testosterone on Regenerating Spinal Cord Motoneurons in Rats
Tehranipour, M., & Moghimi, A. (2010) · Journal of Motor Behavior · doi:10.1080/00222891003697921 · Cited by 32 · see citing works
Jones, K., Prah, P., Starkey, N. J., Theadom, A., Barker-Collo, S. L., Ameratunga, S. N., Feigin, V. L., & for the BIONIC Study Group (2019) · Brain Injury · doi:10.1080/02699052.2019.1606445 · Cited by 31 · see citing works
Baker, K. A., & Hagg, T. (2005) · Journal of Neurotrauma · doi:10.1089/neu.2005.22.415 · Cited by 31 · see citing works
O'Hara, R. M., Luzon, A., Hubbard, J. T., & Zeitzer, J. M. (2009) · The Journal of Rehabilitation Research and Development · doi:10.1682/jrrd.2008.10.0140 · Cited by 31 · see citing works
- Authors
- Bramlett, H. M., & Dietrich, W. D.
- Affiliations
- University of Miami (US)
- Venue
- Journal of Neurotrauma
- Publisher
- SAGE Publications
- Published
- 2001-09
- Volume
- 18
- Issue
- 9
- Pages
- 891-900
- ISSN
- 0897-7151 (ISSN-L)
- 1557-9042
- OpenAlex
- W1970991292
- Cited by
- 213
- References
- 59
- Citations by year
- 2026: 7 · 2025: 5 · 2024: 10 · 2023: 7 · 2022: 8 · 2021: 8 · 2020: 13 · 2019: 9 · 2018: 7 · 2017: 14 · 2016: 9 · 2015: 11 · 2014: 9 · 2013: 5 · 2012: 5
- FWCI
- 4.24
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurotrauma (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eli Lilly and Company
- National Institute of Neurological Disorders and Stroke (NS-30291, P50NS030291)
- Topics
- Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Automotive and Human Injury Biomechanics
- Keywords
- traumatic brain injury, fluid percussion injury, sex differences, ovariectomy, endogenous hormones, neuroprotection, estrous cycle, proestrus, cortical contusion, female rats, hormone therapy
- MeSH terms
- Animals, Brain Injuries, Cell Count, Estrogens, Female, Hippocampus, Male, Ovariectomy, Proestrus, Progesterone, Sex Factors, Rats, Sprague-Dawley, Recovery of Function, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review