Biomarkers in Traumatic Brain Injuries: Narrative Review

Vishram Pandey; Dhaval Shukla; Shubham Nirmal; Bhagavatula Indira Devi; Rita Christopher

doi:10.1055/s-0042-1759853

Indian Journal of Neurotrauma, Inhaltsverzeichnis

CC BY 4.0 · Indian Journal of Neurotrauma 2023; 20(01): 004-010
DOI: 10.1055/s-0042-1759853

Review Article

Biomarkers in Traumatic Brain Injuries: Narrative Review

Vishram Pandey

¹Department of Neurosurgery, National Institute of Mental Health and Neurosciences, Bangalore, Karnataka, India

,

Dhaval Shukla

¹Department of Neurosurgery, National Institute of Mental Health and Neurosciences, Bangalore, Karnataka, India

,

Shubham Nirmal

¹Department of Neurosurgery, National Institute of Mental Health and Neurosciences, Bangalore, Karnataka, India

,

Bhagavatula Indira Devi

¹Department of Neurosurgery, National Institute of Mental Health and Neurosciences, Bangalore, Karnataka, India

,

Rita Christopher

¹Department of Neurosurgery, National Institute of Mental Health and Neurosciences, Bangalore, Karnataka, India

› Institutsangaben

Abstract

Traumatic brain injury (TBI) is a multistep interaction of brain antigens, cytokine-mediated humeral, and cellular immune reactions. Because of the limitations of clinical and radiological evaluation in TBI, there has been a considerable advancement toward the need for developing biomarkers that can predict the severity of TBI. Blood-based brain biomarkers hold the potential to predict the absence of intracranial injury and thus decrease unnecessary brain computed tomographic scanning. Various biomarkers have been studied that detects neuronal, axonal, and blood–brain barrier integrity. Biomarkers are still under investigation and hold promise in the future evaluation of TBI patients. They can be used for grading as well as a prognostication of head injury.

Keywords

traumatic brain injury - biomarkers - UCHL-1 - GFAP - inflammatory markers

Volltext

Referenzen

References
1 Agrawal A, Savardekar A, Singh M. et al. Pattern of reporting and practices for the management of traumatic brain injury: an overview of published literature from India. Neurol India 2018; 66 (04) 976-1002
2 Borg K, Bonomo J, Jauch EC, Kupchak P, Stanton EB, Sawadsky B. Serum levels of biochemical markers of traumatic brain injury. ISRN Emerg Med 2012; 2012: 1-7
3 Padilla-Zambrano H, Pal R, Ghosh A. et al. Biomarkers in acute brain trauma: a narrative review. J Acute Dis 2019; 8 (01) 1-6
4 Chen AY, Colantonio A. Defining neurotrauma in administrative data using the International Classification of Diseases Tenth Revision. Emerg Themes Epidemiol 2011; 8 (01) 4
5 Faul Mxl Wm. Coronado V. Traumatic Brain Injury in The United States: Emergency Department Visits, Hospitalizations and Deaths, 2002–2006. Atlanta Georgia: Centers for Disease Control and Prevention, National Center for Injury Prevention And Control; 2010
6 Algattas H, Huang JH. Traumatic brain injury pathophysiology and treatments: early, intermediate, and late phases post-injury. Int J Mol Sci 2013; 15 (01) 309-341
7 Roozenbeek B, Maas AI, Menon DK. Changing patterns in the epidemiology of traumatic brain injury. Nat Rev Neurol 2013; 9 (04) 231-236
8 Maas AI, Stocchetti N, Bullock R. Moderate and severe traumatic brain injury in adults. Lancet Neurol 2008; 7 (08) 728-741
9 Gururaj G. Sk, Chandramouli Ab, Subbakrishna Dk, Kraus, Jf. Traumatic Brain Injury. National Institute Of Mental Health And Neuro Sciences. 2005a.;Publication No. 61.
10 Pruthi N, Ashok M, Kumar VS, Jhavar K, Sampath S, Devi BI. Magnitude of pedestrian head injuries & fatalities in Bangalore, south India: a retrospective study from an apex neurotrauma center. Indian J Med Res 2012; 136 (06) 1039-1043
11 Road Accidents In India, 2011. Government Of India, Ministry Of Road Transport And Highways, Transport Research Wing, New Delhi. Accessed on December 12, 2022 at: https://morth.nic.in/sites/default/files/Road_Accidents_in_India_2011.pdf
12 Ray SK, Dixon CE, Banik NL. Molecular mechanisms in the pathogenesis of traumatic brain injury. Histol Histopathol 2002; 17 (04) 1137-1152
13 Agrawal A. Brain Injury - Pathogenesis, Monitoring, Recovery and Management [Internet]. London: IntechOpen; 2012. [cited 2022 Dec 07]. 536 p. Available from: https://www.intechopen.com/books/563
14 Smith DH, Meaney DF, Shull WH. Diffuse axonal injury in head trauma. J Head Trauma Rehabil 2003; 18 (04) 307-316
15 Xu J, Rasmussen IA, Lagopoulos J, Håberg A. Diffuse axonal injury in severe traumatic brain injury visualized using high-resolution diffusion tensor imaging. J Neurotrauma 2007; 24 (05) 753-765
16 Wang KK, Yang Z, Zhu T. et al. An update on diagnostic and prognostic biomarkers for traumatic brain injury. Expert Rev Mol Diagn 2018; 18 (02) 165-180
17 Iliff JJ, Lee H, Yu M. et al. Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest 2013; 123 (03) 1299-1309
18 Fan L, Young PR, Barone FC, Feuerstein GZ, Smith DH, McIntosh TK. Experimental brain injury induces expression of interleukin-1 beta mRNA in the rat brain. Brain Res Mol Brain Res 1995; 30 (01) 125-130
19 Benveniste EN. Cytokine actions in the central nervous system. Cytokine Growth Factor Rev 1998; 9 (3-4): 259-275
20 Yatsiv I, Morganti-Kossmann MC, Perez D. et al. Elevated intracranial IL-18 in humans and mice after traumatic brain injury and evidence of neuroprotective effects of IL-18-binding protein after experimental closed head injury. J Cereb Blood Flow Metab 2002; 22 (08) 971-978
21 Brough D, Tyrrell PJ, Allan SM. Regulation of interleukin-1 in acute brain injury. Trends Pharmacol Sci 2011; 32 (10) 617-622
22 Rothwell NJ. Annual review prize lecture cytokines - killers in the brain?. J Physiol 1999; 514 (Pt 1): 3-17
23 Kossmann T, Hans V, Imhof HG, Trentz O, Morganti-Kossmann MC. Interleukin-6 released in human cerebrospinal fluid following traumatic brain injury may trigger nerve growth factor production in astrocytes. Brain Res 1996; 713 (1-2): 143-152
24 Kossmann T, Stahel PF, Lenzlinger PM. et al. Interleukin-8 released into the cerebrospinal fluid after brain injury is associated with blood-brain barrier dysfunction and nerve growth factor production. J Cereb Blood Flow Metab 1997; 17 (03) 280-289
25 Hergenroeder GW, Moore AN, McCoy Jr JP. et al. Serum IL-6: a candidate biomarker for intracranial pressure elevation following isolated traumatic brain injury. J Neuroinflammation 2010; 7: 19
26 Taşçi A, Okay O, Gezici AR, Ergün R, Ergüngör F. Prognostic value of interleukin-1 beta levels after acute brain injury. Neurol Res 2003; 25 (08) 871-874
27 Hayakata T, Shiozaki T, Tasaki O. et al. Changes in CSF S100B and cytokine concentrations in early-phase severe traumatic brain injury. Shock 2004; 22 (02) 102-107
28 Shiozaki T, Hayakata T, Tasaki O. et al. Cerebrospinal fluid concentrations of anti-inflammatory mediators in early-phase severe traumatic brain injury. Shock 2005; 23 (05) 406-410
29 Perry RT, Collins JS, Wiener H, Acton R, Go RC. The role of TNF and its receptors in Alzheimer's disease. Neurobiol Aging 2001; 22 (06) 873-883
30 Breder CD, Tsujimoto M, Terano Y, Scott DW, Saper CB. Distribution and characterization of tumor necrosis factor-alpha-like immunoreactivity in the murine central nervous system. J Comp Neurol 1993; 337 (04) 543-567
31 Riva-Depaty I, Fardeau C, Mariani J, Bouchaud C, Delhaye-Bouchaud N. Contribution of peripheral macrophages and microglia to the cellular reaction after mechanical or neurotoxin-induced lesions of the rat brain. Exp Neurol 1994; 128 (01) 77-87
32 Shohami E, Gallily R, Mechoulam R, Bass R, Ben-Hur T. Cytokine production in the brain following closed head injury: dexanabinol (HU-211) is a novel TNF-alpha inhibitor and an effective neuroprotectant. J Neuroimmunol 1997; 72 (02) 169-177
33 Frugier T, Morganti-Kossmann MC, O'Reilly D, McLean CA. In situ detection of inflammatory mediators in post mortem human brain tissue after traumatic injury. J Neurotrauma 2010; 27 (03) 497-507
34 Stein DM, Lindell A, Murdock KR. et al. Relationship of serum and cerebrospinal fluid biomarkers with intracranial hypertension and cerebral hypoperfusion after severe traumatic brain injury. J Trauma 2011; 70 (05) 1096-1103
35 Aloisi F, De Simone R, Columba-Cabezas S, Levi G. Opposite effects of interferon-gamma and prostaglandin E2 on tumor necrosis factor and interleukin-10 production in microglia: a regulatory loop controlling microglia pro- and anti-inflammatory activities. J Neurosci Res 1999; 56 (06) 571-580
36 Mesples B, Plaisant F, Gressens P. Effects of interleukin-10 on neonatal excitotoxic brain lesions in mice. Brain Res Dev Brain Res 2003; 141 (1-2): 25-32
37 Wu Z, Zhang J, Nakanishi H. Leptomeningeal cells activate microglia and astrocytes to induce IL-10 production by releasing pro-inflammatory cytokines during systemic inflammation. J Neuroimmunol 2005; 167 (1-2): 90-98
38 Knoblach SM, Faden AI. Interleukin-10 improves outcome and alters proinflammatory cytokine expression after experimental traumatic brain injury. Exp Neurol 1998; 153 (01) 143-151
39 Csuka E, Morganti-Kossmann MC, Lenzlinger PM, Joller H, Trentz O, Kossmann T. IL-10 levels in cerebrospinal fluid and serum of patients with severe traumatic brain injury: relationship to IL-6, TNF-alpha, TGF-beta1 and blood-brain barrier function. J Neuroimmunol 1999; 101 (02) 211-221
40 Dziurdzik P, Krawczyk L, Jalowiecki P, Kondera-Anasz Z, Menon L. Serum interleukin-10 in ICU patients with severe acute central nervous system injuries. Inflamm Res 2004; 53 (08) 338-343
41 Jeter CB, Hergenroeder GW, Hylin MJ, Redell JB, Moore AN, Dash PK. Biomarkers for the diagnosis and prognosis of mild traumatic brain injury/concussion. J Neurotrauma 2013; 30 (08) 657-670
42 Richter-Landsberg C, Heinrich M. S-100 immunoreactivity in rat brain glial cultures is associated with both astrocytes and oligodendrocytes. J Neurosci Res 1995; 42 (05) 657-665
43 Diaz-Romero J, Quintin A, Schoenholzer E. et al. S100A1 and S100B expression patterns identify differentiation status of human articular chondrocytes. J Cell Physiol 2014; 229 (08) 1106-1117
44 Van Eldik LJ, Griffin WS. S100 beta expression in Alzheimer's disease: relation to neuropathology in brain regions. Biochim Biophys Acta 1994; 1223 (03) 398-403
45 Puvenna V, Brennan C, Shaw G. et al. Significance of ubiquitin carboxy-terminal hydrolase L1 elevations in athletes after sub-concussive head hits. PLoS One 2014; 9 (05) e96296
46 Blyth BJ, Farhavar A, Gee C. et al. Validation of serum markers for blood-brain barrier disruption in traumatic brain injury. J Neurotrauma 2009; 26 (09) 1497-1507
47 Winter C, Bell C, Whyte T, Cardinal J, Macfarlane D, Rose S. Blood-brain barrier dysfunction following traumatic brain injury: correlation of K(trans) (DCE-MRI) and SUVR (99mTc-DTPA SPECT) but not serum S100B. Neurol Res 2015; 37 (07) 599-606
48 Kövesdi E, Lückl J, Bukovics P. et al. Update on protein biomarkers in traumatic brain injury with emphasis on clinical use in adults and pediatrics. Acta Neurochir (Wien) 2010; 152 (01) 1-17
49 Dorminy M, Hoogeveen A, Tierney RT, Higgins M, McDevitt JK, Kretzschmar J. Effect of soccer heading ball speed on S100B, sideline concussion assessments and head impact kinematics. Brain Inj 2015; 29 (10) 1158-1164
50 Ohrt-Nissen S, Friis-Hansen L, Dahl B, Stensballe J, Romner B, Rasmussen LS. How does extracerebral trauma affect the clinical value of S100B measurements?. Emerg Med J 2011; 28 (11) 941-944
51 Pham N, Fazio V, Cucullo L. et al. Extracranial sources of S100B do not affect serum levels. PLoS One 2010; 5 (09) e12691
52 Townend W, Dibble C, Abid K, Vail A, Sherwood R, Lecky F. Rapid elimination of protein S-100B from serum after minor head trauma. J Neurotrauma 2006; 23 (02) 149-155
53 Yang Z, Wang KK. Glial fibrillary acidic protein: from intermediate filament assembly and gliosis to neurobiomarker. Trends Neurosci 2015; 38 (06) 364-374
54 Eng LF, Ghirnikar RS, Lee YL. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res 2000; 25 (9-10): 1439-1451
55 Gao K, Wang CR, Jiang F. et al. Traumatic scratch injury in astrocytes triggers calcium influx to activate the JNK/c-Jun/AP-1 pathway and switch on GFAP expression. Glia 2013; 61 (12) 2063-2077
56 Di Pietro V, Amorini AM, Lazzarino G. et al. S100B and glial fibrillary acidic protein as indexes to monitor damage severity in an in vitro model of traumatic brain injury. Neurochem Res 2015; 40 (05) 991-999
57 Foerch C, Niessner M, Back T. et al; BE FAST Study Group. Diagnostic accuracy of plasma glial fibrillary acidic protein for differentiating intracerebral hemorrhage and cerebral ischemia in patients with symptoms of acute stroke. Clin Chem 2012; 58 (01) 237-245
58 Pelinka LE, Kroepfl A, Schmidhammer R. et al. Glial fibrillary acidic protein in serum after traumatic brain injury and multiple trauma. J Trauma 2004; 57 (05) 1006-1012
59 Mondello S, Papa L, Buki A. et al. Neuronal and glial markers are differently associated with computed tomography findings and outcome in patients with severe traumatic brain injury: a case control study. Crit Care 2011; 15 (03) R156
60 Metting Z, Wilczak N, Rodiger LA, Schaaf JM, van der Naalt J. GFAP and S100B in the acute phase of mild traumatic brain injury. Neurology 2012; 78 (18) 1428-1433
61 McAleese SM, Dunbar B, Fothergill JE, Hinks LJ, Day IN. Complete amino acid sequence of the neurone-specific gamma isozyme of enolase (NSE) from human brain and comparison with the non-neuronal alpha form (NNE). Eur J Biochem 1988; 178 (02) 413-417
62 Ogata M, Tsuganezawa O. Neuron-specific enolase as an effective immunohistochemical marker for injured axons after fatal brain injury. Int J Legal Med 1999; 113 (01) 19-25
63 Schoerkhuber W, Kittler H, Sterz F. et al. Time course of serum neuron-specific enolase. A predictor of neurological outcome in patients resuscitated from cardiac arrest. Stroke 1999; 30 (08) 1598-1603
64 Cheng F, Yuan Q, Yang J, Wang W, Liu H. The prognostic value of serum neuron-specific enolase in traumatic brain injury: systematic review and meta-analysis. PLoS One 2014; 9 (09) e106680
65 Skogseid IM, Nordby HK, Urdal P, Paus E, Lilleaas F. Increased serum creatine kinase BB and neuron specific enolase following head injury indicates brain damage. Acta Neurochir (Wien) 1992; 115 (3-4): 106-111
66 Vos PE, Lamers KJ, Hendriks JC. et al. Glial and neuronal proteins in serum predict outcome after severe traumatic brain injury. Neurology 2004; 62 (08) 1303-1310
67 Guzel A, Er U, Tatli M. et al. Serum neuron-specific enolase as a predictor of short-term outcome and its correlation with Glasgow Coma Scale in traumatic brain injury. Neurosurg Rev 2008; 31 (04) 439-444 , discussion 444–445
68 Zetterberg H, Tanriverdi F, Unluhizarci K, Selcuklu A, Kelestimur F, Blennow K. Sustained release of neuron-specific enolase to serum in amateur boxers. Brain Inj 2009; 23 (09) 723-726
69 Berger RP, Adelson PD, Pierce MC, Dulani T, Cassidy LD, Kochanek PM. Serum neuron-specific enolase, S100B, and myelin basic protein concentrations after inflicted and noninflicted traumatic brain injury in children. J Neurosurg 2005; 103 (1, Suppl): 61-68
70 Yamazaki Y, Yada K, Morii S, Kitahara T, Ohwada T. Diagnostic significance of serum neuron-specific enolase and myelin basic protein assay in patients with acute head injury. Surg Neurol 1995; 43 (03) 267-270 , discussion 270–271
71 Ng HK, Mahaliyana RD, Poon WS. The pathological spectrum of diffuse axonal injury in blunt head trauma: assessment with axon and myelin strains. Clin Neurol Neurosurg 1994; 96 (01) 24-31
72 Singh GP, Nigam R, Tomar GS. et al. Early and rapid detection of UCHL1 in the serum of brain-trauma patients: a novel gold nanoparticle-based method for diagnosing the severity of brain injury. Analyst (Lond) 2018; 143 (14) 3366-3373
73 Mondello S, Linnet A, Buki A. et al. Clinical utility of serum levels of ubiquitin C-terminal hydrolase as a biomarker for severe traumatic brain injury. Neurosurgery 2012; 70 (03) 666-675
74 Rodríguez A, Cervera E, Villalba P. Neuronal and Glial Biomarkers Research for Traumatic Brain Injury. In: Zhou Y.. editor. Traumatic Brain Injury - Neurobiology, Diagnosis and Treatment [Internet]. London: IntechOpen; 2019. [cited 2022 Dec 07]. Available from: https://www.intechopen.com/chapters/66463
75 Bazarian JJ, Biberthaler P, Welch RD. et al. Serum GFAP and UCH-L1 for prediction of absence of intracranial injuries on head CT (ALERT-TBI): a multicentre observational study. Lancet Neurol 2018; 17 (09) 782-789
76 Food Administration D. et al. FDA authorizes marketing of first blood test to aid in the evaluation of concussion in adults. FDA News Release. 2018. p 2–4. https://www.fda.gov/news-events/press-announcements/fda-authorizes-marketing-first-blood-test-aid-evaluation-concussion-adults. Accessed December 31, 2021
77 Schencker L. A rapid blood test for mild concussions? New Abbott test gains FDA clearance. Chicago Tribune. 2021 https://www.chicagotribune.com/business/ct-biz-abbott-blood-test-concussions-fda-approval-20210111-5qddey336fdnjeuiwopcioykty-story.html Accessed December 31, 2021
78 Forouzan A, Motamed H, Delirrooyfard A, Zallaghi S. Serum cleaved tau protein and clinical outcome in patients with minor head trauma. Open Access Emerg Med 2020; 12: 7-12
79 Hier DB, Obafemi-Ajayi T, Thimgan MS. et al. Blood biomarkers for mild traumatic brain injury: a selective review of unresolved issues. Biomark Res 2021; 9 (01) 70