Systematic review of clinical research on biomarkers for pediatric traumatic brain injury

Journal of Neurotrauma

Volumn 30, Issue 5, 2013, Pages 324-338

  Papa, Linda ^a   Ramia, Michelle M ^a   Kelly, Jared M ^b   Burks, Stephen S ^c   Pawlowicz, Artur ^d   Berger, Rachel P ^e  

^a ORLANDO REGIONAL MEDICAL CENTER   (United States)

^b SALVE REGINA UNIVERSITY   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

^e CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

biochemical markers; biomarkers; children; CT scanning; diagnosis; head injury; intracranial lesions; pediatric; prognosis proteomics; sensitivity; specificity; systematic review; TBI; trauma, human; traumatic brain injury

Indexed keywords

BIOLOGICAL MARKER; INTERLEUKIN 6; INTERLEUKIN 8; MYELIN BASIC PROTEIN; NEURON SPECIFIC ENOLASE; PROTEIN S100B;

CHILDHOOD INJURY; CLINICAL RESEARCH; COMPUTER ASSISTED TOMOGRAPHY; HUMAN; IONIZING RADIATION; PROTEIN BLOOD LEVEL; RADIATION EXPOSURE; REVIEW; SYSTEMATIC REVIEW; TRAUMATIC BRAIN INJURY;

BIOLOGICAL MARKERS; BRAIN INJURIES; CHILD; HUMANS;

EID: 84874721353     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2545     Document Type: Review

References (75)

1. Faul, M., Xu, L., Wald, M.M., and Coronado, V.G. (2010). Traumatic Brain Injury in the United States. Emergency Department Visits, Hospitalizations and Deaths 2002-2006. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention: Atlanta, GA.
2. Choudhary, J., and Grant, S.G. (2004). Proteomics in postgenomic neuroscience: the end of the beginning. Nat. Neurosci. 7, 440-445.
3. Collins, M.O., Yu, L., Coba, M.P., Husi, H., Campuzano, I., Blackstock, W.P., Choudhary, J.S., and Grant, S.G. (2005). Proteomic analysis of in vivo phosphorylated synaptic proteins. J. Biol. Chem. 280, 5972-5982.
4. Denslow, N., Michel, M.E., Temple, M.D., Hsu, C.Y., Saatman, K., and Hayes, R.L. (2003). Application of proteomics technology to the field of neurotrauma. J. Neurotrauma 20, 401-407.
5. Ottens, A.K., Kobeissy, F.H., Golden, E.C., Zhang, Z., Haskins, W.E., Chen, S.S., Hayes, R.L., Wang, K.K., and Denslow, N.D. (2006) Neuroproteomics in neurotrauma. Mass Spectrom. Rev. 25, 380-408.
6. Ragan, D.K., McKinstry, R., Benzinger, T., Leonard, J.R., and Pineda, J.A. (2013). Alterations in cerebral oxygen metabolism after traumatic brain injury in children. J. Cereb. Blood Flow Metab. 33, 48-52.
7. Coles, J.P., Fryer, T.D., Smielewski, P., Rice, K., Clark, J.C., Pickard, J.D., and Menon, D.K. (2004). Incidence and mechanisms of cerebral ischemia in early clinical head injury. J. Cereb. Blood Flow Metab. 24, 202-211.
8. Unterberg, A.W., Stover, J., Kress, B., and Kiening, K.L. (2004). Edema and brain trauma. Neuroscience 129, 1021-1029.
9. Chamoun, R., Suki, D., Gopinath, S.P., Goodman, J.C., and Robertson, C. (2010). Role of extracellular glutamate measured by cerebral microdialysis in severe traumatic brain injury. J. Neurosurg. 113, 564-570.
10. Werner, C., Engelhard, K. (2007). Pathophysiology of traumatic brain injury. Br. J. Anaesth. 99, 4-9.
11. Cederberg, D., and Siesjo?, P. What has inflammation to do with traumatic brain injury? (2010). Childs Nerv. Syst. 26, 221-226.
12. Wang, K.K., Ottens, A.K., Liu, M.C., Lewis, S.B., Meegan, C., Oli, M.W., Tortella, F.C., and Hayes, R.L. (2005). Proteomic identification of biomarkers of traumatic brain injury. Expert Rev. Proteomics 2, 603-614.
13. Kochanek, P.M., Berger, R.P., Bayr, H., Wagner, A.K., Jenkins, L.W., and Clark, R.S. (2008). Biomarkers of primary and evolving damage in traumatic and ischemic brain injury: diagnosis, prognosis, probing mechanisms, and therapeutic decision making. Curr. Opin. Crit. Care 14, 135-141.
14. Papa, L., Robinson, G., Oli, M., Pineda, J., Demery, J., Brophy, G., Robicsek, S.A., Gabrielli, A., Robertson, C.S., Wang, K.W., and Hayes, R.L. (2008). Use of biomarkers for diagnosis and management of traumatic brain injury patients. Expert Opinion on Medical Diagnostics 2, 937-945.
15. Berger, R.P. The use of serum biomarkers to predict outcome after traumatic brain injury in adults and children. (2006). J. Head Trauma Rehabil. 21, 315-333.
16. Adelson, P.D., Pineda, J., Bell, M.J., Abend, N.S., Berger, R.P., Giza, C.C., Hotz, G., and Wainwright, M.S. (2012). Common data elements for pediatric traumatic brain injury: recommendations from the working group on demographics and clinical assessment. J. Neurotrauma 29, 639-653.
17. Berger, R.P., Beers, S.R., Papa, L., and Bell, M. (2012). Common data elements for pediatric traumatic brain injury: recommendations from the biospecimens and biomarkers workgroup. J. Neurotrauma 29, 672- 677.
18. Duhaime, A.C., Holshouser, B., Hunter, J.V., and Tong, K. (2012). Common data elements for neuroimaging of traumatic brain injury: pediatric considerations. J. Neurotrauma 29, 629-633.
19. McCauley, S.R., Wilde, E.A., Anderson, V.A., Bedell, G., Beers, S.R., Campbell, T.F., Chapman, S.B., Ewing-Cobbs, L., Gerring, J.P., Gioia, G.A., Levin, H.S., Michaud, L.J., Prasad, M.R., Swaine, B.R., Turkstra, L.S., Wade, S.L., and Yeates, K.O. (2012). Recommendations for the use of common outcome measures in pediatric traumatic brain injury research. J. Neurotrauma 29, 678-705.
20. Miller, A.C., Odenkirchen, J., Duhaime, A.C., and Hicks, R. (2012). Common data elements for research on traumatic brain injury: pediatric considerations. J. Neurotrauma 29, 634-638.
21. Brenner, D.J. (2002). Estimating cancer risks from pediatric CT: going from the qualitative to the quantitative. Pediatr. Radiol. 32, 228-224.
22. Brenner, D.J., Hall, E.J. (2007). Computed tomography - an increasing source of radiation exposure. N. Engl. J. Med. 357, 2277- 2284.
23. Berger, R.P., Hayes, R.L., Richichi, R., Beers, S.R., and Wang, K.K. (2012). Serum concentrations of ubiquitin C-terminal hydrolase-L1 and alphaII-spectrin breakdown product 145 kDa correlate with outcome after pediatric TBI. J. Neurotrauma 29, 162-167.
24. Papa L, Lewis LM, Silvestri S, Falk JL, Giordano P, Brophy GM, Demery JA, Liu MC, Mo J, Akinyi L, Mondello S, Schmid K, Robertson CS, Tortella FC, Hayes RL, and Wang KK. (2012) Serum levels of ubiquitin C-terminal hydrolase distinguish mild traumatic brain injury from trauma controls and are elevated in mild and moderate traumatic brain injury patients with intracranial lesions and neurosurgical intervention. J. Trauma Acute Care Surg. 72, 1335- 1344.
25. Papa, L., Lewis, L.M., Falk, J.L., Zhang, Z., Silvestri, S., Giordano, P., Brophy, G.M., Demery, J.A., Dixit, N.K., Ferguson, I., Liu, M.C., Mo, J., Akinyi, L., Schmid, K., Mondello, S., Robertson, C.S., Tortella, F.C., Hayes, R.L., and Wang, K.K. (2012). Elevated levels of serum glial fibrillary acidic protein breakdown products in mild and moderate traumatic brain injury are associated with intracranial lesions and neurosurgical intervention. Ann. Emerg. Med. 59, 471-483.
26. Parks, S.E., Kegler, S.R., Annest, J.L., and Mercy, J.A. (2012). Characteristics of fatal abusive head trauma among children in the USA: 2003-2007: an application of the CDC operational case definition to national vital statistics data. Inj. Prev. 18, 193-199.
27. Ingebrigtsen, T., Waterloo, K., Jacobsen, E.A., Langbakk, B., and Romner, B. (1999). Traumatic brain damage in minor head injury: relation of serum S-100 protein measurements to magnetic resonance imaging and neurobehavioral outcome. Neurosurgery 45, 468-476.
28. Romner, B., Ingebrigtsen, T., Kongstad, P., Borgesen, S.E. (2000). Traumatic brain damage: serum S-100 protein measurements related to neuroradiological findings. J. Neurotrauma 17, 641-647.
29. Tenedieva, V.D., Potapov, A.A., Gaitur, E.I., Amcheslavski, V.G., Micrikova, L.V., Tenedieva, N.D., and Voronov, V.G. (2000). Thyroid hormones in comatose patients with traumatic brain injury. Acta Neurochir. Suppl. 76, 385-391.
30. Murshid, W.R., and Gader, A.G. (2002). The coagulopathy in acute head injury: comparison of cerebral versus peripheral measurements of haemostatic activation markers. Br. J. Neurosurg. 16, 362- 369.
31. Vos, P.E., Lamers, K.J., Hendriks, J.C., van Haaren, M., Beems, T., Zimmerman, C., van Geel, W., de Reus, H., Biert, J., and Verbeek, M.M. (2004). Glial and neuronal proteins in serum predict outcome after severe traumatic brain injury. Neurology 62, 1303-1310.
32. Bayir, A., Kalkan, E., Kocak, S., Ak, A., Cander, B., and Bodur, S. (2006). Fibrinolytic markers and neurologic outcome in traumatic brain injury. Neurol. India 54, 363-365.
33. Bazarian, J.J., Zemlan, F.P., Mookerjee, S., and Stigbrand, T. (2006). Serum S-100B and cleaved-tau are poor predictors of long-term outcome after mild traumatic brain injury. Brain Inj. 20, 759-765.
34. Nylen, K., Ost, M., Csajbok, L.Z., Nilsson, I., Hall, C., Blennow, K., Nellgard, B., and Rosengren, L. (2008). Serum levels of S100B, S100A1B and S100BB are all related to outcome after severe traumatic brain injury. Acta Neurochir. (Wien) 150, 221-227.
35. Morochovic, R., Racz, O., Kitka, M., Pingorova, S., Cibur, P., Tomkova, D., and Lenartova, R. (2009). Serum S100B protein in early management of patients after mild traumatic brain injury. Eur. J. Neurol. 16, 1112-1117.
36. Stahel, P.F., Kossmann, T., Joller, H., Trentz, O., and Morganti- Kossmann, M.C. (1998). Increased interleukin-12 levels in human cerebrospinal fluid following severe head trauma. Neurosci. Lett. 249, 123-126.
37. Kossmann, T., Hans, V., Imhof, H.G., Trentz, O., and Morganti- Kossmann, M.C. (1996). Interleukin-6 released in human cerebrospinal fluid following traumatic brain injury may trigger nerve growth factor production in astrocytes. Brain Res. 713, 143-52.
38. Hayakata, T., Shiozaki, T., Tasaki, O., Ikegawa, H., Inoue, Y., Toshiyuki, F., Hosotubo, H., Kieko, F., Yamashita, T., Tanaka, H., Shimazu, T., and Sugimoto, H. (2004). Changes in CSF S100B and cytokine concentrations in early-phase severe traumatic brain injury. Shock 22, 102-107.
39. Uzan, M., Erman, H., Tanriverdi, T., Sanus, G.Z., Kafadar, A., and Uzun, H. (2006). Evaluation of apoptosis in cerebrospinal fluid of patients with severe head injury. Acta Neurochir. (Wien) 148, 1157- 1164.
40. Whalen, M.J., Carlos, T.M., Kochanek, P.M., Wisniewski, S.R., Bell, M.J., Carcillo, J.A., Clark, R.S., DeKosky, S.T., and Adelson, P.D. (1998). Soluble adhesion molecules in CSF are increased in children with severe head injury. J. Neurotrauma 15, 777-787.
41. Whalen, M.J., Carlos, T.M., Kochanek, P.M., Wisniewski, S.R., Bell, M.J., Clark, R.S., DeKosky, S.T., Marion, D.W., and Adelson, P.D. (2000). Interleukin-8 is increased in cerebrospinal fluid of children with severe head injury. Crit. Care Med. 28, 929-934.
42. Shore, P.M., Thomas, N.J., Clark, R.S., Adelson, P.D., Wisniewski, S.R., Janesko, K.L., Bayir, H., Jackson, E.K., and Kochanek, P.M. (2004). Continuous versus intermittent cerebrospinal fluid drainage after severe traumatic brain injury in children: effect on biochemical markers. J. Neurotrauma 21, 1113-1122.
43. Satchell, M.A., Lai, Y., Kochanek, P.M., Wisniewski, S.R., Fink, E.L., Siedberg, N.A., Berger, R.P., DeKosky, S.T., Adelson, P.D., and Clark, R.S. (2005). Cytochrome c, a biomarker of apoptosis, is increased in cerebrospinal fluid from infants with inflicted brain injury from child abuse. J. Cereb. Blood Flow Metab. 25, 919-927.
44. Cousar, J.L., Lai, Y., Marco, C.D., Bayir, H., Adelson, P.D., Janesko- Feldman, K.L., Kochanek, P.M., and Clark, R.S. (2006). Heme oxygenase 1 in cerebrospinal fluid from infants and children after severe traumatic brain injury. Dev. Neurosci. 28, 342-327.
45. Lai, Y., Stange, C., Wisniewski, S.R., Adelson, P.D., Janesko- Feldman, K.L., Brown, D.S., Kochanek, P.M., and Clark, R.S. (2006). Mitochondrial heat shock protein 60 is increased in cerebrospinal fluid following pediatric traumatic brain injury. Dev. Neurosci. 28, 336- 341.
46. Shore, P.M., Berger, R.P., Varma, S., Janesko, K.L., Wisniewski, S.R., Clark, R.S., Adelson, P.D., Thomas, N.J., Lai, Y.C., Bayir, H., and Kochanek, P.M. (2007). Cerebrospinal fluid biomarkers versus glasgow coma scale and glasgow outcome scale in pediatric traumatic brain injury: the role of young age and inflicted injury. J. Neurotrauma 24, 75-86.
47. Chiaretti, A., Antonelli, A., Mastrangelo, A., Pezzotti, P., Tortorolo, L., Tosi, F., and Genovese, O. (2008). Interleukin-6 and nerve growth factor upregulation correlates with improved outcome in children with severe traumatic brain injury. J. Neurotrauma 25, 225-234.
48. Chiaretti, A., Antonelli, A., Riccardi, R., Genovese, O., Pezzotti, P., Di Rocco, C., Tortorolo, L., and Piedimonte, G. (2008). Nerve growth factor expression correlates with severity and outcome of traumatic brain injury in children. Eur. J. Paediatr. Neurol. 12, 195-204.
49. Chiaretti, A., Barone, G., Riccardi, R., Antonelli, A., Pezzotti, P., Genovese, O., Tortorolo, L., and Conti, G. (2009). NGF, DCX, and NSE upregulation correlates with severity and outcome of head trauma in children. Neurology 72, 609-616.
50. Takahashi, H., Sato, H., and Tsuji, Y. (1989). Biochemical markers in the acute stage of head injury - aldosterone and CK-BB. Neurol. Med. Chir. (Tokyo) 29, 192-195.
51. Ben Abraham, R., Lahat, E., Sheinman, G., Feldman, Z., Barzilai, A., Harel, R., Barzilay, Z., and Paret, G. (2000). Metabolic and clinical markers of prognosis in the era of CT imaging in children with acute epidural hematomas. Pediatr. Neurosurg. 33, 70-75.
52. Fridriksson, T., Kini, N., Walsh-Kelly, C., and Hennes, H. (2000). Serum neuron-specific enolase as a predictor of intracranial lesions in children with head trauma: a pilot study. Acad. Emerg. Med. 7, 816- 820.
53. Berger, R.P., Pierce, M.C., Wisniewski, S.R., Adelson, P.D., and Kochanek, P.M. (2002). Serum S100B concentrations are increased after closed head injury in children: a preliminary study. J. Neurotrauma 19, 1405-1409.
54. Akhtar, J.I., Spear, R.M., Senac, M.O., Peterson, B.M., and Diaz, S.M. (2003). Detection of traumatic brain injury with magnetic resonance imaging and S-100B protein in children, despite normal computed tomography of the brain. Pediatr. Crit. Care Med. 4, 322-326.
55. Spinella, P.C., Dominguez, T., Drott, H.R., Huh, J., McCormick, L., Rajendra, A., Argon, J., McIntosh, T., and Helfaer, M. (2003). S- 100beta protein-serum levels in healthy children and its association with outcome in pediatric traumatic brain injury. Crit. Care. Med. 31, 939-945.
56. Bandyopadhyay, S., Hennes, H., Gorelick, M.H., Wells, R.G., and Walsh-Kelly, C.M. (2005). Serum neuron-specific enolase as a predictor of short-term outcome in children with closed traumatic brain injury. Acad. Emerg. Med. 12, 732-738.
57. Berger, R.P., Adelson, P.D., Pierce, M.C., Dulani, T., Cassidy, L.D., and Kochanek, P.M. (2005). Serum neuron-specific enolase, S100B, and myelin basic protein concentrations after inflicted and noninflicted traumatic brain injury in children. J. Neurosurg. 103, Suppl. 1, 61-68.
58. Berger, R.P., Adelson, P.D., Richichi, R., and Kochanek, P.M. (2006). Serum biomarkers after traumatic and hypoxemic brain injuries: insight into the biochemical response of the pediatric brain to inflicted brain injury. Dev. Neurosci. 28, 327-335.
59. Berger, R.P., Dulani, T., Adelson, P.D., Leventhal, J.M., Richichi, R., and Kochanek, P.M. (2006). Identification of inflicted traumatic brain injury in well-appearing infants using serum and cerebrospinal marker: a possible screening tool. Pediatrics 117, 325-332.
60. Berger, R.P., Kochanek, P.M. (2006). Urinary S100B concentrations are increased after brain injury in children: A preliminary study. Pediatr. Crit. Care. Med. 7, 557-561.
61. Briassoulis, G., Mavrikiou, M., Margeli, A., Lazaropoulou, C., Natsi, L., Papassotiriou, I., and Hatzis, T. (2006). Circulating levels of KL-6 in acute respiratory distress syndrome sepsis or traumatic brain injury in critically ill children. Pediatr. Pulmonol. 41, 790-795.
62. Beers, S.R., Berger, R.P., and Adelson, P.D. (2007). Neurocognitive outcome and serum biomarkers in inflicted versus non-inflicted traumatic brain injury in young children. J. Neurotrauma 24, 97-105.
63. Berger, R.P., Beers, S.R., Richichi, R., Wiesman, D., and Adelson, P.D. (2007). Serum biomarker concentrations and outcome after pediatric traumatic brain injury. J. Neurotrauma 24, 1793-1801.
64. Briassoulis, G., Papassotiriou, I., Mavrikiou, M., Lazaropoulou, C., and Margeli, A. (2007). Longitudinal course and clinical significance of TGF-beta1, sL- and sE-Selectins and sICAM-1 levels during severe acute stress in children. Clin Biochem. 40, 299-304.
65. Haqqani, A.S., Hutchison, J.S., Ward, R., Stanimirovic, D.B. (2007). Biomarkers and diagnosis; protein biomarkers in serum of pediatric patients with severe traumatic brain injury identified by ICAT-LCMS/ MS. J. Neurotrauma 24, 54-74.
66. Piazza, O., Storti, M.P., Cotena, S., Stoppa, F., Perrotta, D., Esposito, G., Pirozzi, N., and Tufano, R. (2007). S100B is not a reliable prognostic index in paediatric TBI. Pediatr. Neurosurg. 43, 258-264.
67. Bechtel, K., Frasure, S., Marshall, C., Dziura, J., and Simpson, C. (2009). Relationship of serum S100B levels and intracranial injury in children with closed head trauma. Pediatrics 124, e697-e704.
68. Berger, R.P., Ta'asan, S., Rand, A., Lokshin, A., and Kochanek, P. (2009). Multiplex assessment of serum biomarker concentrations in well-appearing children with inflicted traumatic brain injury. Pediatr. Res. 65, 97-102.
69. Castellani, C., Bim bashi, P., Ruttenstock, E., Sacherer, P., Stojakovic, T., and Weinberg, A.M. (2009). Neuroprotein s-100B - a useful parameter in paediatric patients with mild traumatic brain injury? Acta Paediatr. 98, 1607-1612.
70. Geyer, C., Ulrich, A., Gra?fe, G., Stach, B., Till, H. (2009). Diagnostic value of S100B and neuron-specific enolase in mild pediatric traumatic brain injury. J. Neurosurg. Pediatr. 4, 339-344.
71. Berger, R.P., Bazaco, M.C., Wagner, A.K., Kochanek, P.M., and Fabio, A. (2010). Trajectory analysis of serum biomarker concentrations facilitates outcome prediction after pediatric traumatic and hypoxemic brain injury. Dev. Neurosci. 32, 396-405.
72. Chang, T.P., and Nager, AL. (2010). Pediatric traumatic brain injury: the utility of beta- natriuretic peptide. J. Trauma 68, 1401-1405.
73. Lo, T.Y., Jones, P.A., and Minns, R.A. (2010). Combining coma score and serum biomarker levels to predict unfavorable outcome following childhood brain trauma. J. Neurotrauma 27, 2139-2145.
74. Swanson, C.A., Burns, J.C., and Peterson, B.M. (2010). Low plasma D-dimer concentration predicts the absence of traumatic brain injury in children. J. Trauma 68, 1072-1077.
75. Fraser, D.D., Close, T.E., Rose, K.L., Ward, R., Mehl, M., Farrell, C., Lacroix. J., Creery. D., Kesselman, M., Stanimirovic, D., and Hutchison, J.S. (2011). Severe traumatic brain injury in children elevates glial fibrillary acidic protein in cerebrospinal fluid and serum. Pediatr. Crit. Care. Med. 12, 319-324.