Cited by 913Traumatic Brain Injury and Neurovascular DisturbancesTraumatic Brain Injury ResearchAutomotive and Human Injury Biomechanics

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Clinical Trials in Head Injury

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Narayan, Raj K., Michel, Mary Ellen, Ansell, Beth, Baethmann, Alex, Biegon, Anat, Bracken, Michael B., Bullock, M. Ross, Choi, Sung C., Clifton, Guy L., Contant, Charles F., Coplin, William M., Dietrich, W. Dalton, Ghajar, Jamshid, Grady, Sean M., Grossman, Robert G., Hall, Edward D., Heetderks, William, Hovda, David A., Jallo, Jack, Katz, Russell L., Knoller, Nachshon, Kochanek, Patrick M., Maas, Andrew I., Majde, Jeannine, Marion, Donald W., Marmarou, Anthony, Marshall, Lawrence F., McIntosh, Tracy K., Miller, Emmy, Mohberg, Noel, Muizelaar, J. Paul, Pitts, Lawrence H., Quinn, Peter, Riesenfeld, Gad, Robertson, Claudia S., Strauss, Kenneth I., Teasdale, Graham, Temkin, Nancy, Tuma, Ronald, Wade, Charles, Walker, Michael D., Weinrich, Michael, Whyte, John, Wilberger, Jack, Young, A. Byron, Yurkewicz, Lorraine·2002·Journal of Neurotrauma

DOI 10.1089/089771502753754037PMC PMC1462953

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Abstract

Traumatic brain injury (TBI) remains a major public health problem globally. In the United States the incidence of closed head injuries admitted to hospitals is conservatively estimated to be 200 per 100,000 population, and the incidence of penetrating head injury is estimated to be 12 per 100,000, the highest of any developed country in the world. This yields an approximate number of 500,000 new cases each year, a sizeable proportion of which demonstrate significant long-term disabilities. Unfortunately, there is a paucity of proven therapies for this disease. For a variety of reasons, clinical trials for this condition have been difficult to design and perform. Despite promising pre-clinical data, most of the trials that have been performed in recent years have failed to demonstrate any significant improvement in outcomes. The reasons for these failures have not always been apparent and any insights gained were not always shared. It was therefore feared that we were running the risk of repeating our mistakes. Recognizing the importance of TBI, the National Institute of Neurological Disorders and Stroke (NINDS) sponsored a workshop that brought together experts from clinical, research, and pharmaceutical backgrounds. This workshop proved to be very informative and yielded many insights into previous and future TBI trials. This paper is an attempt to summarize the key points made at the workshop. It is hoped that these lessons will enhance the planning and design of future efforts in this important field of research.

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COG1410, a Novel Apolipoprotein E–Based Peptide, Improves Functional Recovery in a Murine Model of Traumatic Brain Injury
Laskowitz, D. T., McKenna, S., Song, P., Wang, H., Durham, L., Yeung, N., Christensen, D. J., & Vitek, M. P. (2007) · Journal of Neurotrauma · doi:10.1089/neu.2006.0192 · Cited by 99
“There is a growing consensus that the most beneficial treatment would be directed at multiple targets related to the pathological mechanisms associated with TBI without compromising the neuroprotective effects of these inflammatory mediators (Narayan et al., 2002; Schmidt et al., 2005).”
Promising strategies to minimize secondary brain injury after head trauma
Bayır, H., Clark, R., & Kochanek, P. (2003) · Critical Care Medicine · doi:10.1097/00003246-200301001-00016 · Cited by 104
Self-citation
Response to intracranial hypertension treatment as a predictor of death in patients with severe traumatic brain injury.
Farahvar, A., Gerber, L., Chiu, Y.-L., Härtl, R., Froelich, M., Carney, N., & Ghajar, J. (2011) · Journal of Neurosurgery · doi:10.3171/2010.11.jns101116 · Cited by 102
Self-citation
Unique challenges in clinical trials in traumatic brain injury
Menon, D. (2009) · Critical Care Medicine · doi:10.1097/ccm.0b013e3181921225 · Cited by 101
“Given this, it is reassuring that some postinsult interventions produce significant neuroprotection in experimental TBI (6).”
BackgroundInfluential
Magnetic resonance imaging evidence of progression of subacute brain atrophy in moderate to severe traumatic brain injury.
Ng, K., Mikulis, D., Glazer, J., Kabani, N., Till, C., Greenberg, G., Thompson, A., Lazinski, D., Agid, R., Colella, B., et al. (2008) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2008.07.006 · Cited by 101
Inhibition of the alternative complement activation pathway in traumatic brain injury by a monoclonal anti-factor B antibody: a randomized placebo-controlled study in mice
Leinhase, I., Rozanski, M., Harhausen, D., Thurman, J. M., Schmidt, O., Hossini, A., Taha, M. E., Rittirsch, D., Ward, P. A., Holers, V., et al. (2007) · Journal of Neuroinflammation · doi:10.1186/1742-2094-4-13 · Cited by 101
“Research strategies to prevent the neuroinflammatory pathological sequelae of TBI have largely failed in translation to clinical treatment [8-14].”
NAAG peptidase inhibitor increases dialysate NAAG and reduces glutamate, aspartate and GABA levels in the dorsal hippocampus following fluid percussion injury in the rat
Zhong, C.-L., Zhao, X., Van, K. C., Bzdȩga, T., Smyth, A., Zhou, J., Kozikowski, A., Jiang, J.-Y., O'Connor, W., Berman, R. F., et al. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03786.x · Cited by 101
Cathepsin B is a New Drug Target for Traumatic Brain Injury Therapeutics: Evidence for E64d as a Promising Lead Drug Candidate
Hook, G., Jacobsen, J. S., Grabstein, K. H., Kindy, M. S., & HOOK, V. Y. H. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00178 · Cited by 110
“And in AD and Parkinson’s cell culture models, Aβ(1-42) and α-synuclein cause lysosomal leakage of cathepsin B into the cytoplasm (211–213).”
Background
Rate of Neurodegeneration in the Mouse Controlled Cortical Impact Model Is Influenced by Impactor Tip Shape: Implications for Mechanistic and Therapeutic Studies
Pleasant, J. M., Carlson, S. W., Mao, H., Scheff, S. W., Yang, K. H., & Saatman, K. E. (2011) · Journal of Neurotrauma · doi:10.1089/neu.2010.1499 · Cited by 94
Delayed administration of erythropoietin reducing hippocampal cell loss, enhancing angiogenesis and neurogenesis, and improving functional outcome following traumatic brain injury in rats: comparison of treatment with single and triple dose
Xiong, Y., Mahmood, A., Meng, Y., Zhang, Y., Qu, C., Schallert, T. J., & Chopp, M. (2009) · Journal of neurosurgery · doi:10.3171/2009.9.jns09844 · Cited by 111
Exogenous Administration of PACAP Alleviates Traumatic Brain Injury in Rats through a Mechanism Involving the TLR4/MyD88/NF-κB Pathway
Mao, S., Hua, R., Zhao, X., Qin, X., Sun, Z.-Q., Zhang, Y., Wu, Y.-Q., Jia, M., Cao, J., & Zhang, Y.-M. (2012) · Journal of Neurotrauma · doi:10.1089/neu.2011.2244 · Cited by 93
“…et al., 2004), albumins (Myburgh et al., 2007), magnesium sulfate (Temkin et al., 2007), calcium channel antagonists (e.g., nimodipine; Clausen and Bullock, 2001), excitatory amino acid inhibitors, and free radical scavengers (Narayan et al., 2002), have all been inefﬁcient for TBI treatment.”
Ischemic stroke and traumatic brain injury: The role of the kallikrein–kinin system
Albert-Weißenberger, C., Sirén, A., & Kleinschnitz, C. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.11.004 · Cited by 95
Cyclosporin A Preserves Mitochondrial Function after Traumatic Brain Injury in the Immature Rat and Piglet
Kilbaugh, T. J., Bhandare, S., Lorom, D. H., Saraswati, M., Robertson, C., & Margulies, S. S. (2011) · Journal of Neurotrauma · doi:10.1089/neu.2010.1635 · Cited by 95
Self-citation
Effects of erythropoietin on reducing brain damage and improving functional outcome after traumatic brain injury in mice
Xiong, Y., Lu, D., Qu, C., Goussev, A. V., Schallert, T. J., Mahmood, A., & Chopp, M. (2008) · Journal of neurosurgery · doi:10.3171/jns/2008/109/9/0510 · Cited by 98
Thrombocytopenia Predicts Progressive Hemorrhage after Head Trauma
Engström, M., Romner, B., Schalén, W., & Reinstrup, P. (2005) · Journal of Neurotrauma · doi:10.1089/neu.2005.22.291 · Cited by 97
“There have been several efforts to identify neuroprotective agents or other treatments that could improve outcome in this patient population, but they have so far not been successful in clinical studies (Clausen and Bullock, 2001; Narayan et al., 2002).”
T Lymphocyte Trafficking: A Novel Target for Neuroprotection in Traumatic Brain Injury
Clausen, F., Lorant, T., Lewén, A., & Hillered, L. (2007) · Journal of Neurotrauma · doi:10.1089/neu.2006.0258 · Cited by 95
“However, pharmacological treatments to combat specific components of the secondary injury cascade to further ameliorate the devastating consequences of TBI are still missing (Narayan et al., 2002).”
TREATMENT OF TRAUMATIC BRAIN INJURY WITH A COMBINATION THERAPY OF MARROW STROMAL CELLS AND ATORVASTATIN IN RATS
Mahmood, A., Lu, D., Qu, C., Goussev, A. V., & Chopp, M. (2007) · Neurosurgery · doi:10.1227/01.neu.0000255346.25959.99 · Cited by 87
Erythropoietin Protects from Post-Traumatic Edema in the Rat Brain
Verdonck, O., Lahrech, H., Francony, G., Carle, O., Farion, R., van de Looij, Y., Rémy, C., Segebarth, C., & Payen, J. (2007) · Journal of Cerebral Blood Flow and Metabolism · doi:10.1038/sj.jcbfm.9600443 · Cited by 93
“…shown neuroprotective effects in experimental models of TBI, there is no pharmacological agent specifically aimed at blocking the progression of diffuse brain edema in the clinical setting, and therapy applied to patients with diffuse brain edema is still purely symptomatic (Narayan et al, 2002).”
Background
Quantitative imaging of tyrosine hydroxylase and calmodulin in the human brain
Sutoo, D., Akiyama, K., & Yabe, K. (2001) · Journal of Neuroscience Research · doi:10.1002/1097-4547(20010301)63:5 · Cited by 17
Omega-3 Fatty Acids as a Putative Treatment for Traumatic Brain Injury
Hasadsri, L., Wang, B. H., Lee, J. V., Erdman, J. W., Llano, D. A., Barbey, A. K., Wszalek, T., Sharrock, M. F., & Wang, H. (2013) · Journal of Neurotrauma · doi:10.1089/neu.2012.2672 · Cited by 97
“124,125 Likewise, administration of corticosteroids, well known for their anti-inﬂammatory effects, has shown no clear improvement in outcome or reduction in intracranial pressure, 126 and one large study revealed that such compounds may in fact increase the risk of death after TBI.”
Clinical evaluation of the safety and efficacy of lumbar cerebrospinal fluid drainage for the treatment of refractory increased intracranial pressure.
Tuettenberg, J., Czabanka, M., Horn, P., Woitzik, J., Barth, M., Thomé, C., Vajkoczy, P., Schmiedek, P., & Muench, E. (2009) · Journal of Neurosurgery · doi:10.3171/2008.10.jns08293 · Cited by 91
Regional ischemia after head injury
Coles, J. (2004) · Current Opinion in Critical Care · doi:10.1097/00075198-200404000-00008 · Cited by 90
Traumatic brain injury and cognition
Cristofori, I., & Levin, H. S. (2015) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63521-1.00037-6 · Cited by 115
Animal models of traumatic brain injury
Johnson, V. E., Meaney, D. F., Cullen, D. K., & Smith, D. H. (2015) · Handbook of clinical neurology · doi:10.1016/b978-0-444-52892-6.00008-8 · Cited by 151
“Despite this huge impact on society, no treatment has been shown to be efficacious though there have been multiple phase III clinical trials (Narayan et al., 2002; Menon, 2009).”
Background
What’s New in Traumatic Brain Injury: Update on Tracking, Monitoring and Treatment
Reis, C., Wang, Y., Akyol, O., Ho, W., Applegate, R. L., Stier, G. R., Martin, R., & Zhang, J. H. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms160611903 · Cited by 96
“approach to target single receptors or specific mechanisms [304,305], and an approach that encompasses both the multiple direct and indirect injury mechanisms must be developed in order to provide effective treatment for TBI [303].”
Background
Functional Assessment of Long-Term Deficits in Rodent models of Traumatic Brain Injury
Gold, E. M., Su, D., López-Velázquez, L., Haus, D. L., Perez, H. D., Lacuesta, G. A., Anderson, A. J., & Cummings, B. J. (2013) · Regenerative Medicine · doi:10.2217/rme.13.41 · Cited by 90
Randomized controlled trials in adult traumatic brain injury
Lü, J., Gary, K. W., Neimeier, J. P., Ward, J., & Lapane, K. L. (2012) · Brain Injury · doi:10.3109/02699052.2012.722257 · Cited by 80
C1-inhibitor attenuates neurobehavioral deficits and reduces contusion volume after controlled cortical impact brain injury in mice*
Longhi, L. G., Perego, C., Ortolano, F., Zanier, E. R., Bianchi, P. A., Stocchetti, N., McIntosh, T. K., & Simoni, M. G. D. (2009) · Critical Care Medicine · doi:10.1097/ccm.0b013e318195998a · Cited by 90
Self-citation
Incensole Acetate: A Novel Neuroprotective Agent Isolated from Boswellia Carterii
Moussaieff, A., Shein, N. A., Tsenter, J., Grigoriadis, S., Simeonidou, C., Alexandrovich, A. G., Trembovler, V., Ben‐Neriah, Y., Schmitz, M. L., Fiebich, B. L., et al. (2008) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2008.28 · Cited by 72
“Most of the clinical trials conducted so far have failed to show any significant improvement in outcome measures (Marmarou et al, 2005; Narayan et al, 2002).”
Background
Delayed transplantation of human marrow stromal cell-seeded scaffolds increases transcallosal neural fiber length, angiogenesis, and hippocampal neuronal survival and improves functional outcome after traumatic brain injury in rats
Xiong, Y., Qu, C., Mahmood, A., Liu, Z., Ning, R., Li, Y., Kaplan, D. L., Schallert, T. J., & Chopp, M. (2009) · Brain Research · doi:10.1016/j.brainres.2009.01.032 · Cited by 75
“To date, there is no effective treatment to promote functional recovery except for routine medical intervention and care (1998; Narayan et al., 2002; Royo et al., 2003).”
Background
Treatment of traumatic brain injury in mice with marrow stromal cells
Qu, C., Mahmood, A., Lu, D., Goussev, A. V., Xiong, Y., & Chopp, M. (2008) · Brain Research · doi:10.1016/j.brainres.2008.02.042 · Cited by 83
“The incidence of patient’s with closed head injuries admitted annually to hospitals is 200 per 100,000 (Narayan et al., 2002).”
Background
Spatiotemporal pH dynamics following insertion of neural microelectrode arrays
Johnson, M. D., Kao, O. E., & Kipke, D. R. (2006) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2006.09.023 · Cited by 80
The effects of nicotinamide on apoptosis and blood-brain barrier breakdown following traumatic brain injury.
Hoane, M., Kaplan, S., & Ellis, A. L. (2006) · Brain Research · doi:10.1016/j.brainres.2006.10.019 · Cited by 85
Traumatic brain injury enhances neuroinflammation and lesion volume in caveolin deficient mice
Niesman, I., Schilling, J., Shapiro, L. A., Kellerhals, S., Bonds, J. A., Kleschevnikov, A., Cui, W.-H., Voong, A., Krajewski, S., Ali, S., et al. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-39 · Cited by 84
“Despite intensive investigative efforts, there is a paucity of interventions designed to reduce morbidity and mortality associated with TBI [1].”
Background
Nutrition and Traumatic Brain Injury: Improving Acute and Subacute Health Outcomes in Military Personnel
Erdman, J., Oria, M., & Pillsbury, L. (2011) · doi:10.17226/13121 · Cited by 83
Beneficial effects of hydrogen gas in a rat model of traumatic brain injury via reducing oxidative stress.
Ji, X.-T., Liu, W., Xie, K., Liu, W.-P., Qu, Y., Chao, X., Chen, T., Zhou, J., & Fei, Z. (2010) · Brain Research · doi:10.1016/j.brainres.2010.07.038 · Cited by 83
Cerium Oxide Nanoparticles Improve Outcome after In Vitro and In Vivo Mild Traumatic Brain Injury
Bailey, Z. S., Nilson, E., Bates, J., Oyalowo, A., Hockey, K. S., Sajja, V. S., Thorpe, C., Rogers, H., Dunn, B., Frey, A., et al. (2016) · Journal of Neurotrauma · doi:10.1089/neu.2016.4644 · Cited by 82
“Traditional antioxidants have been utilized in attempts to mitigate the pathological effects of TBI, but have met with limited success in clinical trials.(15) A”
Background
Investigational agents for treatment of traumatic brain injury
Xiong, Y., Zhang, Y.-L., Mahmood, A., & Chopp, M. (2015) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.2015.1021919 · Cited by 82
“Over the past 40 years, > 100 RCTs in TBI were conducted [11,23,34-41].”
Background
Toward an International Initiative for Traumatic Brain Injury Research
Tosetti, P., Hicks, R. R., Theriault, E., Phillips, A. G., Koroshetz, W. J., & Draghia‐Akli, R. (2013) · Journal of Neurotrauma · doi:10.1089/neu.2013.2896 · Cited by 80
“Several of these factors may have contributed to the failure of a number of novel neuroprotective interventions to translate into benefit in patients with a head injury.(10,11) Multiple treatments are currently available, but there are still limitations to characterization and prognostication in individual patients.”
Histone deacetylase inhibitors are neuroprotective and preserve NGF-mediated cell survival following traumatic brain injury
Lu, J., Frerich, J. M., Turtzo, L. C., Li, S., Chiang, J. Y., Yang, C., Wang, X., Zhang, C., Wu, C., Sun, Z., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308950110 · Cited by 89
“0001; caspase 3, one-way ANOVA F(2,6) = 252.”
BackgroundMethodInfluential
Adjustment for Strong Predictors of Outcome in Traumatic Brain Injury Trials: 25% Reduction in Sample Size Requirements in the IMPACT Study
Hernandez, A. V., Steyerberg, E., Butcher, I., Mushkudiani, N., Taylor, G., Murray, G. D., Marmarou, A., Choi, S. C., Lu, J., Habbema, J. F., et al. (2006) · Journal of Neurotrauma · doi:10.1089/neu.2006.23.1295 · Cited by 82
“…sizes, insensitive outcome measures, over-opti-mistic expectations, ineffective therapies, inappropriate selection of patients, and heterogeneity of the patient population (Narayan et al., 2002; Doppenberg et al., 2004; Maas et al., 1999; Dickinson et al., 2000; Choi et al., 2002; Wilson, 2001).”
Self-citation

Authors: Narayan, R. K., Michel, M. E., Ansell, B., Baethmann, A., Biegon, A., Bracken, M. B., Bullock, M. R., Choi, S. C., Clifton, G. L., Contant, C. F., Coplin, W. M., Dietrich, W. D., Ghajar, J., Grady, S. M., Grossman, R. G., Hall, E. D., Heetderks, W., Hovda, D. A., Jallo, J., Katz, R. L., Knoller, N., Kochanek, P. M., Maas, A. I., Majde, J., Marion, D. W., Marmarou, A., Marshall, L. F., McIntosh, T. K., Miller, E., Mohberg, N., Muizelaar, J. P., Pitts, L. H., Quinn, P., Riesenfeld, G., Robertson, C. S., Strauss, K. I., Teasdale, G., Temkin, N., Tuma, R., Wade, C., Walker, M. D., Weinrich, M., Whyte, J., Wilberger, J., Young, A. B., & Yurkewicz, L.
Affiliations: Temple University Hospital (US)
National Institute of Neurological Disorders and Stroke (US)
National Institutes of Health (US)
Ludwig-Maximilians-Universität München (DE)
Lawrence Berkeley National Laboratory (US)
Yale University (US)
Virginia Commonwealth University (US)
The University of Texas Health Science Center at Houston (US)
Baylor College of Medicine (US)
Wayne State University (US)
University of Miami (US)
Brain Trauma Foundation (US)
Hospital of the University of Pennsylvania (US)
Pfizer (United States) (US)
University of California, Los Angeles (US)
Temple University (US)
United States Food and Drug Administration (US)
Sheba Medical Center (IL)
University of Pittsburgh (US)
Academisch Ziekenhuis Rotterdam (NL)
Office of Naval Research (US)
University of California San Diego (US)
University of California Davis Medical Center (US)
University of California, San Francisco (US)
Southern General Hospital (GB)
University of Washington (US)
Allegheny General Hospital (US)
Albert B. Chandler Hospital (US)
ORCID: Narayan, Raj K.
Biegon, Anat
Choi, Sung C.
Dietrich, W. Dalton
Grady, Sean M.
Grossman, Robert G.
Heetderks, William
Jallo, Jack
Kochanek, Patrick M.
Maas, Andrew I.
Marion, Donald W.
McIntosh, Tracy K.
Robertson, Claudia S.
Temkin, Nancy
Wade, Charles
Walker, Michael D.
Weinrich, Michael
Whyte, John
Venue: Journal of Neurotrauma
Publisher: SAGE Publications
Published: 2002-05
Volume: 19
Issue: 5
Pages: 503-557
ISSN: 0897-7151 (ISSN-L)
1557-9042
DOI: 10.1089/089771502753754037
PMC: PMC1462953
OpenAlex: W2045663952
Cited by: 913
References: 0
Citations by year: 2026: 11 · 2025: 16 · 2024: 20 · 2023: 14 · 2022: 15 · 2021: 20 · 2020: 35 · 2019: 43 · 2018: 43 · 2017: 40 · 2016: 42 · 2015: 55 · 2014: 49 · 2013: 56 · 2012: 61
FWCI: 20.60
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.liebertpub.com/nv/resources-tools/text-and-data-mining-policy/121/ (tdm)
Locations: Journal of Neurotrauma (publishedVersion)
PubMed (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
PubMed Central (acceptedVersion)
Deep Blue (University of Michigan) (submittedVersion, public-domain)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
Funders: National Institutes of Health (7r01ns038654-04)
National Institute of Neurological Disorders and Stroke (R01-NS038654)
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, clinical trial design, closed head injury, penetrating head injury, translational research, treatment failure, long-term disability
MeSH terms: Brain Injuries, Clinical Trials as Topic, Humans

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