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

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Clinical Trials in Head Injury

Open access

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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Osborne-Crowley, K., & McDonald, S. (2017) · Journal of Neuropsychology · doi:10.1111/jnp.12113 · Cited by 43
Rethinking Neuroprotection in Severe Traumatic Brain Injury: Toward Bedside Neuroprotection
Zoerle, T., Carbonara, M., Zanier, E. R., Ortolano, F., Bertani, G., Magnoni, S., & Stocchetti, N. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00354 · Cited by 46
“Subsequent reappraisals concerning the study design and conduction of clinical trials have been published (11, 13, 14).”
Background
Effects of treating traumatic brain injury with collagen scaffolds and human bone marrow stromal cells on sprouting of corticospinal tract axons into the denervated side of the spinal cord
Mahmood, A., Wu, H., Qu, C., Xiong, Y., & Chopp, M. (2012) · Journal of neurosurgery · doi:10.3171/2012.11.jns12753 · Cited by 45
Pyridoxine Administration Improves Behavioral and Anatomical Outcome after Unilateral Contusion Injury in the Rat
Kuypers, N. J., & Hoane, M. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2010.1327 · Cited by 43
“Of the several therapies that have advanced as far as Phase II and III clinical trials, nearly all have failed to consistently improve functional outcome post-TBI (Narayan et al., 2002).”
Dose-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
Novel therapies in development for the treatment of traumatic brain injury
Vink, R., & Nimmo, A. (2002) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.11.10.1375 · Cited by 43
“Interested readers are referred to some excellent analyses of these trials that have been reviewed elsewhere [2-4].”
Background
Survivin, a key component of the Wnt/β-catenin signaling pathway, contributes to traumatic brain injury-induced adult neurogenesis in the mouse dentate gyrus.
Zhang, L., Yan, R., Zhang, Q., Wang, H.-N., Kang, X.-K., Li, J., Yang, S., Zhang, J.-N., Liu, Z.-L., & Yang, X.-Y. (2013) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2013.1456 · Cited by 42
“Traumatic brain injury (TBI) is a major cause of mortality and morbidity globally (1,2), and continues to be an important public health issue worldwide (3,4).”
Administration of COG1410 Reduces Axonal Amyloid Precursor Protein Immunoreactivity and Microglial Activation after Controlled Cortical Impact in Mice
Jiang, Y. Q., & Brody, D. L. (2012) · Journal of Neurotrauma · doi:10.1089/neu.2012.2362 · Cited by 44
“However, to date, all of them have failed to show a therapeutic beneﬁt, and some have produced worse outcomes for acute or chronic treatment of TBI (Margulies and Hicks, 2009; Narayan et al., 2002).”
The treatment of TBI with human marrow stromal cells impregnated into collagen scaffold: Functional outcome and gene expression profile
Qu, C., Mahmood, A., Liu, X., Xiong, Y., Wang, L., Wu, H., Li, B., Zhang, Z. G., Kaplan, D. L., & Chopp, M. (2010) · Brain Research · doi:10.1016/j.brainres.2010.10.088 · Cited by 41
“-PA Author M anuscript N IH -PA Author M anuscript (Narayan et al., 2002).”
Background
Erythropoietin improves brain mitochondrial function in rats after traumatic brain injury
Xiong, Y., Chopp, M., & Lee, C.-P. (2009) · Neurological Research · doi:10.1179/174313208x353703 · Cited by 42
Curiosity and cure: Translational research strategies for neural repair‐mediated rehabilitation
Dobkin, B. H. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20514 · Cited by 40
“Only one or two acute interventions for each disease have shown some benefit, and even those results are controversial (Bracken et al., 1998; Narayan et al., 2002; Albers et al., 2004; Lees et al., 2006).”
Background
Biologic Transplantation and Neurotrophin-Induced Neuroplasticity After Traumatic Brain Injury
Lu, D., Mahmood, A., & Chopp, M. (2003) · Journal of Head Trauma Rehabilitation · doi:10.1097/00001199-200307000-00006 · Cited by 45
Early diagnosis of traumatic intracranial hematomas
Ayaz, H., Izzetoglu, M., Izzetoglu, K., Onaral, B., & Dor, B. B. (2019) · Journal of Biomedical Optics · doi:10.1117/1.jbo.24.5.051411 · Cited by 41
Immediate and delayed hyperbaric oxygen therapy as a neuroprotective treatment for traumatic brain injury in mice
Baratz-Goldstein, R., Toussia-Cohen, S., Elpaz, A., Rubovitch, V., & Pick, C. G. (2017) · Molecular and cellular neurosciences · doi:10.1016/j.mcn.2017.06.004 · Cited by 41
“Thus, the limited medical and technological tools to address this urgent concern have created a strong need to develop new approaches of treating mTBI sufferers (Narayan et al., 2002; Chua et al., 2007).”
Background
c-Jun N-Terminal Kinase Pathway Activation in Human and Experimental Cerebral Contusion
Ortolano, F., Colombo, A., Zanier, E., Sclip, A., Longhi, L., Perego, C., Stocchetti, N., Borsello, T., & Simoni, M. D. (2009) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/nen.0b013e3181b20670 · Cited by 41
“Despite significant research efforts, effective clinical treatment of TBI remains elusive (1).”
Rehabilitation Pharmacology
Phillips, J., Devier, D. J., & Feeney, D. M. (2003) · Journal of Head Trauma Rehabilitation · doi:10.1097/00001199-200307000-00005 · Cited by 42
“38 There are two important differences between these studies: (1) the average age of study subjects in the Sonde trial was 80 years, which was an exclusionary criteria in the Walker-Batson study; and (2) the Sonde study used the d,l isomer of”
BackgroundResult
Multimodality monitoring in severe traumatic brain injury
Mulvey, J., Dorsch, N., Mudaliar, Y., & Lang, E. W. (2004) · Neurocritical Care · doi:10.1385/ncc:1:3:391 · Cited by 41
Complementary Metal–Oxide–Semiconductor Potentiometric Field-Effect Transistor Array Platform Using Sensor Learning for Multi-ion Imaging
Moser, N., Leong, C., Hu, Y., Cicatiello, C., Gowers, S., Boutelle, M., & Georgiou, P. (2020) · Analytical Chemistry · doi:10.1021/acs.analchem.9b05836 · Cited by 40
Pharmacological inhibition of mannose-binding lectin ameliorates neurobehavioral dysfunction following experimental traumatic brain injury
Blasio, D. D., Fumagalli, S., Longhi, L. G., Orsini, F., Palmioli, A., Stravalaci, M., Vegliante, G., Zanier, E. R., Bernardi, A., Gobbi, M., et al. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16647397 · Cited by 43
Treatment of traumatic brain injury in rats with N-acetyl-seryl-aspartyl-lysyl-proline
Zhang, Y., Zhang, Z. G., Chopp, M., Meng, Y., Zhang, L., Mahmood, A., & Xiong, Y. (2016) · Journal of neurosurgery · doi:10.3171/2016.3.jns152699 · Cited by 44
Efficacy of Progesterone following a Moderate Unilateral Cortical Contusion Injury
Gilmer, L. K., Roberts, K. N., & Scheff, S. (2008) · Journal of Neurotrauma · doi:10.1089/neu.2007.0477 · Cited by 40
Immune enhancing nutrition in traumatic brain injury - A preliminary study.
Painter, T. J., Rickerds, J., & Alban, R. (2015) · International Journal of Surgery · doi:10.1016/j.ijsu.2015.07.008 · Cited by 39
Comparative Study of Outcome Measures and Analysis Methods for Traumatic Brain Injury Trials
Alali, A. S., Vavrek, D. A., Barber, J. K., DIKMEN, S. S., Nathens, A. B., & Temkin, N. R. (2014) · Journal of Neurotrauma · doi:10.1089/neu.2014.3495 · Cited by 42
“15,36 19 Among the main theoretical advantages of using a composite measure as the primary outcome instead of GOSE alone are the greater statistical power to detect a treatment effect than any single measure (provided the treatment effect is constant across all component measures), and the…”
Self-citation
Posttraumatic cerebral infarction in patients with moderate or severe head trauma
Marino, R., Gasparotti, R., Pinelli, L., Manzoni, D., Gritti, P., Mardighian, D., & Latronico, N. (2006) · Neurology · doi:10.1212/01.wnl.0000238081.35281.b5 · Cited by 39
A review of laboratory and clinical data supporting the safety and efficacy of cyclosporin A in traumatic brain injury.
Lulic, D., Burns, J., Bae, E., van Loveren, H. V., & Borlongan, C. (2011) · Neurosurgery · doi:10.1227/neu.0b013e31820c6cdc · Cited by 38
Early attenuation of lesional interleukin‐16 up‐regulation by dexamethasone and FTY720 in experimental traumatic brain injury
Zhang, Z., Fauser, U., & Schluesener, H. J. (2007) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2007.00893.x · Cited by 38
Mesenchymal stem cell-derived extracellular vesicles as a cell-free therapy for traumatic brain injury via neuroprotection and neurorestoration
Xiong, Y., Mahmood, A., & Chopp, M. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.374143 · Cited by 43
“…to demonstrate therapeutic efficacy in TBI clinical trials and TBI often needs long-term care, with immense socioeconomic and emotional burdens (Narayan et al., 2002; Loane and Faden, 2010; Briones, 2015; Tortella, 2016; Maas et al., 2017; Alves et al., 2019; Ng and Lee, 2019; Shultz et al.,…”
Background
Sensory Sensitivity in TBI: Implications for Chronic Disability
Callahan, M. L., & Lim, M. M. (2018) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-018-0867-x · Cited by 43
Decreased mortality in traumatic brain injury following regionalization across hospital systems
Kelly, M. L., Banerjee, A., Nowak, M., Steinmetz, M., & Claridge, J. A. (2015) · Journal of Trauma and Acute Care Surgery · doi:10.1097/ta.0000000000000590 · Cited by 37
Magnesium Gluconate Offers No More Protection than Magnesium Sulphate Following Diffuse Traumatic Brain Injury in Rats
Turner, R., Dasilva, K., O'Connor, C., van den Heuvel, C., & Vink, R. (2004) · Journal of the American College of Nutrition · doi:10.1080/07315724.2004.10719399 · Cited by 37
“This is consistent with the observation that antioxidants and free radical scavengers have not been successful in clinical trials of TBI [16].”
Result
Variation in chronic nicotinamide treatment after traumatic brain injury can alter components of functional recovery independent of histological damage
Hoane, M., Pierce, J. L., Kaufman, N. A., & Beare, J. E. (2008) · Oxidative Medicine and Cellular Longevity · doi:10.4161/oxim.1.1.6694 · Cited by 37
Comprehensive evaluation of mitochondrial redox profile, calcium dynamics, membrane integrity and apoptosis markers in a preclinical model of severe penetrating traumatic brain injury
Pandya, J. D., Musyaju, S., Modi, H. R., Cao, Y. J., Flerlage, W. J., Huynh, L., Kociuba, B., Visavadiya, N. P., Kobeissy, F. H., Wang, K., et al. (2023) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2023.02.001 · Cited by 42
High-Performance Bioinstrumentation for Real-Time Neuroelectrochemical Traumatic Brain Injury Monitoring
Papadimitriou, K. I., Wang, C., Rogers, M. L., Gowers, S. A. N., Leong, C. L., Boutelle, M. G., & Drakakis, E. M. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00212 · Cited by 33
Exploring the physiological correlates of chronic mild traumatic brain injury symptoms
Astafiev, S. V., Zinn, K., Shulman, G. L., & Corbetta, M. (2016) · NeuroImage Clinical · doi:10.1016/j.nicl.2016.01.004 · Cited by 43
Risk of unfavorable long-term outcome in older adults with traumatic intracranial hemorrhage and anticoagulant or antiplatelet use
Nishijima, D. K., Shahlaie, K., Sarkar, K., Rudisill, N., & Holmes, J. F. (2013) · The American Journal of Emergency Medicine · doi:10.1016/j.ajem.2013.04.035 · Cited by 40
“The GOS-E is the most commonly used measure of global functional performance after TBI and has been recommended as the criterion standard outcome measure for TBI studies [10,11].”
Method
A Comparison of the Effects of Nicotinamide and Progesterone on Functional Recovery of Cognitive Behavior following Cortical Contusion Injury in the Rat
Peterson, T. C., Anderson, G., Kantor, E., & Hoane, M. (2012) · Journal of Neurotrauma · doi:10.1089/neu.2012.2471 · Cited by 36
“tablish the dosage regimen, dose-response curves, and optimal dosing windows; and to work toward direct comparison studies and potential combination therapies.(3) One point of special emphasis has been the direct comparison of compounds that have shown pre-”
Background
Effect of Therapeutic Mild Hypothermia on the Genomics of the Hippocampus After Moderate Traumatic Brain Injury in Rats
Feng, J., Zhang, K., Jiang, J., Gao, G., Fu, X., & Liang, Y.-M. (2010) · Neurosurgery · doi:10.1227/01.neu.0000378023.81727.6e · Cited by 33
Mitochondria-Targeted Antioxidant Therapeutics for Traumatic Brain Injury
Modi, H. R., Musyaju, S., Ratcliffe, M., Shear, D. A., Scultetus, A. H., & Pandya, J. D. (2024) · Antioxidants · doi:10.3390/antiox13030303 · Cited by 44
Efficacy of progesterone for moderate to severe traumatic brain injury: a meta-analysis of randomized clinical trials
Lin, C., He, H., Li, Z., Liu, Y., Chao, H., Ji, J., & Liu, N. (2015) · Scientific Reports · doi:10.1038/srep13442 · Cited by 35
Isoflurane preconditioning protects astrocytes from oxygen and glucose deprivation independent of innate cell sex
Fuller, G., Bouamra, O., Woodford, M., Jenks, T., Patel, H., Coats, T., Oakley, P., Mendelow, A., Pigott, T., Hutchinson, P., et al. (2011) · Journal of Neurosurgical Anesthesiology · doi:10.1097/ana.0b013e3182161816 · Cited by 35
“SBP <90mm Hg (%, 95% CI) 7 (6-8) 10 (9-12) P<0.”
Continuous measurement of intracranial pressure in awake rats after experimental closed head injury.
Rooker, S., Jorens, P., Reempts, J. V. V., Borgers, M., & Verlooy, J. (2003) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(03)00233-4 · Cited by 35
Neuroimmunophilin Ligand V-10,367 is Neuroprotective after 24-Hour Delayed Administration in a Mouse Model of Diffuse Traumatic Brain Injury
Kupina, N., Detloff, M., Dutta, S., & Hall, E. (2002) · Journal of Cerebral Blood Flow and Metabolism · doi:10.1097/01.wbc.0000037994.34930.bc · Cited by 35
“However, a careful historical analysis of the pursuit of marketable neuroprotective agents has revealed that, in the case of most compounds destined for clinical trials, the preclinical data obtained prior to trial design have been grossly inadequate (Narayan and Michel, 2002).”
BackgroundInfluentialSelf-citation
Neurochemical Characterization of Traumatic Brain Injury in Humans
Regner, A., Alves, L. B., Chemale, I. M., Costa, M. S., Friedman, G., Achaval, M., Leal, L., & Emanuelli, T. (2001) · Journal of Neurotrauma · doi:10.1089/089771501316919148 · Cited by 31
“Despite constituting a major health care problem, no effective pharmacological interventions currently exist and, at present, most effort has been focused on supportive measures (Brocker et al., 1991; Reinert and Bullock, 1999).”
Drugs with anti-inflammatory effects to improve outcome of traumatic brain injury: a meta-analysis
Begemann, M., Leon, M., van der Horn, H. J., van der Naalt, J., & Sommer, I. (2020) · Scientific Reports · doi:10.1038/s41598-020-73227-5 · Cited by 34
Traumatic brain injury (TBI) outcomes in an LMIC tertiary care centre and performance of trauma scores
Samanamalee, S., Sigera, P. C., Silva, A. D. D., Thilakasiri, K., Rashan, A., Wadanambi, S., Jayasinghe, K. S., Dondorp, A., & Haniffa, R. (2018) · BMC Anesthesiology · doi:10.1186/s12871-017-0463-7 · Cited by 34
“Severe TBI was defined as a Glasgow Coma Scale (GCS) of <9 and moderate TBI was by a GCS of 9–12 at hospital admission [15, 16].”
Method

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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