Skip to main content

S100B as a Marker for Brain Damage and Blood–Brain Barrier Disruption Following Exercise

An Erratum to this article was published on 20 March 2014

Abstract

Background

S100B level in the blood has been used as a marker for brain damage and blood–brain barrier (BBB) disruption. Elevations of S100B levels after exercise have been observed, suggesting that the BBB may be compromised during exercise. However, an increase in S100B levels may be confounded by other variables.

Objectives

The primary objective of this review was to compile findings on the relationship between S100B and exercise in order to determine if this protein is a valid marker for BBB disruptions during exercise. The secondary objective was to consolidate known factors causing S100B increases that may give rise to inaccurate interpretations of S100B levels.

Data Sources and Study Selection

PubMed, Web of Science and ScienceDirect were searched for relevant studies up to January 2013, in which S100B measurements were taken after a bout of exercise. Animal studies were excluded. Variables of interest such as the type of activity, exercise intensities, duration, detection methods, presence and extent of head trauma were examined and compiled.

Results

This review included 23 studies; 15 (65 %) reported S100B increases after exercise, and among these, ten reported S100B increases regardless of intervention, while five reported increases in only some trials but not others. Eight (35 %) studies reported no increases in S100B levels across all trials. Most baseline S100B levels fall below 0.16 μg/L, with an increase in S100B levels of less than 0.07 μg/L following exercise. Factors that are likely to affect S100B levels include exercise intensity, and duration, presence and extent of head trauma. Several other probable factors influencing S100B elevations are muscle breakdown, level of training and oxidative stress, but current findings are still weak and inconclusive.

Conclusions

Elevated S100B levels have been recorded following exercise and are mostly attributed to either an increase in BBB permeability or trauma to the head. However, even in the absence of head trauma, it appears that the BBB may be compromised following exercise, with the severity dependent on exercise intensity.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. 1.

    Gonçalves CA, Leite MC, Nardin P. Biological and methodological features of the measurement of S100B, a putative marker of brain injury. Clin Biochem. 2008;41:755–63.

    PubMed  Google Scholar 

  2. 2.

    Donato R, Sorci G, Riuzzi F, et al. S100B’s double life: intracellular regulator and extracellular signal. Biochim Biophys Acta. 2009;1793:1008–22.

    CAS  PubMed  Google Scholar 

  3. 3.

    Michetti F, Corvino V, Geloso MC, et al. The S100B protein in biological fluids: more than a lifelong biomarker of brain distress. J Neurochem. 2012;120:644–59.

    CAS  PubMed  Google Scholar 

  4. 4.

    Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol. 2001;33:637–68.

    CAS  PubMed  Google Scholar 

  5. 5.

    Cicero TJ, Cowan WM, Moore BW, et al. The cellular localization of the two brain specific proteins, S-100 and 14-3-2. Brain Res. 1970;18:25.

    CAS  PubMed  Google Scholar 

  6. 6.

    Gonçalves CA, Leite MC, Guerra MC. Adipocytes as an important source of serum S100B and possible roles of this protein in adipose tissue. Cardiovasc Psychiatry Neurol. 2010;2010:1–7.

    Google Scholar 

  7. 7.

    Cocchia D. Immunochemical and immunocytochemical localization of S-100 antigen in normal human skin. Nature. 1981;294:85–7.

    CAS  PubMed  Google Scholar 

  8. 8.

    Tubaro C, Arcuri C, Giambanco I, et al. S100B protein in myoblasts modulates myogenic differentiation via NF-κB-dependent inhibition of MyoD expression. J Cell Physiol. 2010;223:270–82.

    CAS  PubMed  Google Scholar 

  9. 9.

    Pham N, Fazio V, Cucullo L, et al. Extracranial sources of S100B do not affect serum levels. PLoS One. 2010;10(5):e12691.

    Google Scholar 

  10. 10.

    Kleindienst A, Hesse F, Bullock MR, et al. The neurotrophic protein S100B: value as a marker of brain damage and possible therapeutic implications. Prog Brain Res. 2007;161:317–25.

    CAS  PubMed  Google Scholar 

  11. 11.

    Van Eldik LJ, Wainwright MS. The Janus face of glial-derived S100B: beneficial and detrimental functions in the brain. Restor Neurol Neurosci. 2003;21:97–108.

    PubMed  Google Scholar 

  12. 12.

    Rothermundt M, Peters M, Prehn JH, et al. S100B in brain damage and neurodegeneration. Microsc Res Tech. 2003;60:614–32.

    CAS  PubMed  Google Scholar 

  13. 13.

    Schiavi P, Laccarino C, Servadei F. The value of the calcium binding protein S100 in the management of patients with traumatic brain injury. Acta Biomed. 2012;83:5–20.

    CAS  PubMed  Google Scholar 

  14. 14.

    Dietrich Mde O, Souza DO, Portela LV. Serum S100B protein: what does it mean during exercise? Clin J Sport Med. 2004;14:368.

    PubMed  Google Scholar 

  15. 15.

    Schulte S, Schiffer T, Sperlich B, et al. Response to the Letter to the Editor of Sorci et al. “Causes of elevated serum levels of S100B protein in athletes”. Eur J Appl Physiol. 2013;113:821–2.

    PubMed  Google Scholar 

  16. 16.

    Donato R, Riuzzi F, Sorci G. Causes of elevated serum levels of S100B protein in athletes. Eur J Appl Physiol. 2013;113:819–20.

    PubMed  Google Scholar 

  17. 17.

    Kretsinger RH. Structure and evolution of calcium-modulated proteins. CRC Crit Rev Biochem. 1980;8:119–74.

    CAS  PubMed  Google Scholar 

  18. 18.

    Donato R. Intracellular and extracellular roles of S100 proteins. Microsc Res Tech. 2003;15(60):540–51.

    Google Scholar 

  19. 19.

    Selinfreund RH, Barger SW, Welsh MJ, et al. Antisense inhibition of glial S100 beta production results in alterations in cell morphology, cytoskeletal organization, and cell proliferation. J Cell Biol. 1990;111:2021–8.

    CAS  PubMed  Google Scholar 

  20. 20.

    Scotto C, Deloulme JC, Rousseau D, et al. Calcium and S100B regulation of p53-dependent cell growth arrest and apoptosis. Mol Cell Biol. 1998;18:4272–81.

    CAS  PubMed Central  PubMed  Google Scholar 

  21. 21.

    Sorci G, Riuzzi F, Arcuri C, et al. The many faces of S100B protein: when an extracellular factor inactivates its own receptor and activates another one. Ital J Anat Embryol. 2010;115:147–51.

    PubMed  Google Scholar 

  22. 22.

    Van Eldik LJ, Christiepope B, Bolin LM, et al. Neurotrophic activity of S-100-beta in cultures of dorsal-root ganglia from embryonic chick and fetal-rat. Brain Res. 1991;1(542):280–5.

    Google Scholar 

  23. 23.

    Winningham-Major F, Staecker JL, Barger SW, et al. Neurite extension and neuronal survival activities of recombinant S100 beta proteins that differ in the content and position of cysteine residues. J Cell Biol. 1989;109:3063–71.

    CAS  PubMed  Google Scholar 

  24. 24.

    Iwasaki Y, Shiojima T, Kinoshita M. S100 beta prevents the death of motor neurons in newborn rats after sciatic nerve section. J Neurol Sci. 1997;3(151):7–12.

    Google Scholar 

  25. 25.

    Bhattacharyya A, Oppenheim RW, Prevette D, et al. S100 is present in developing chicken neurons and Schwann cells and promotes motor neuron survival in vivo. J Neurobiol. 1992;23:451–66.

    CAS  PubMed  Google Scholar 

  26. 26.

    Marshak DR, Pesce SA, Stanley LC, et al. Increased S100β neurotrophic activity in Alzheimer’s disease temporal lobe. Neurobiol Aging. 1992;13:1–7.

    CAS  PubMed  Google Scholar 

  27. 27.

    Mrak RE, Sheng JG, Griffin WS. Correlation of astrocytic S100 beta expression with dystrophic neurites in amyloid plaques of Alzheimer’s disease. J Neuropathol Exp Neurol. 1996;55:273–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  28. 28.

    Peskind ER, Griffin WS, Akama KT, et al. Cerebrospinal fluid S100B is elevated in the earlier stages of Alzheimer’s disease. Neurochem Int. 2001;39:409–13.

    CAS  PubMed  Google Scholar 

  29. 29.

    Griffin WS, Stanley LC, Ling C, et al. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc Natl Acad Sci USA. 1989;86:7611–5.

    CAS  PubMed Central  PubMed  Google Scholar 

  30. 30.

    Esposito G, Imitola J, Lu J, et al. Genomic and functional profiling of human Down syndrome neural progenitors implicates S100B and aquaporin 4 in cell injury. Hum Mol Genet. 2008;1(17):440–57.

    Google Scholar 

  31. 31.

    Griffin WS, Yeralan O, Sheng JG, et al. Overexpression of the neurotrophic cytokine S100 beta in human temporal lobe epilepsy. J Neurochem. 1995;65:228–33.

    CAS  PubMed Central  PubMed  Google Scholar 

  32. 32.

    Zhang XY, Xiu MH, Song C, et al. Increased serum S100B in never-medicated and medicated schizophrenic patients. J Psychiatr Res. 2010;44:1236–40.

    PubMed  Google Scholar 

  33. 33.

    Yuekui L, Barger SW, Liu L, et al. S100b induction of the proinflammatory cytokine interleukin-6 in neurons. J Neurochem. 2011;74:143–50.

    Google Scholar 

  34. 34.

    Mariggió MA, Fulle S, Calissano P, et al. The brain protein S-100ab induces apoptosis in PC12 cells. Neuroscience. 1994;60:29–35.

    PubMed  Google Scholar 

  35. 35.

    Hu J, Ferreira A, Van Eldik LJ. S100β induces neuronal cell death through nitric oxide release from astrocytes. J Neurochem. 1997;69:2294–301.

    CAS  PubMed  Google Scholar 

  36. 36.

    Pinto SS, Gottfried C, Mendez A, et al. Immunocontent and secretion of S100B in astrocyte cultures from different brain regions in relation to morphology. FEBS Lett. 2000;15(486):203–7.

    Google Scholar 

  37. 37.

    Andreazza AC, Cassini C, Rosa AR, et al. Serum S100B and antioxidant enzymes in bipolar patients. J Psychiatr Res. 2007;41:523–9.

    PubMed  Google Scholar 

  38. 38.

    Yardan T, Erenler AK, Baydin A, et al. Usefulness of S100B protein in neurological disorders. J Pak Med Assoc. 2011;61:276–81.

    PubMed  Google Scholar 

  39. 39.

    Leite MC, Galland F, de Souza DF, et al. Gap junction inhibitors modulates S100B secretion in astrocyte cultures and acute hippocampal slices. J Neurosci Res. 2009;87:2439–46.

    CAS  PubMed  Google Scholar 

  40. 40.

    Mello e Souza T, Rohden A, Meinhardt M. S100B infusion into the rat hippocampus facilitates memory for the inhibitory avoidance task but not for the open-field habituation. Physiol Behav. 2000;71:29–33.

    CAS  PubMed  Google Scholar 

  41. 41.

    Kleindienst A, McGinn MJ, Harvey HB, et al. Enhanced hippocampal neurogenesis by intraventricular S100B infusion is associated with improved cognitive recovery after traumatic brain injury. J Neurotrauma. 2005;22:645–55.

    PubMed  Google Scholar 

  42. 42.

    Marchi N, Fazio V, Cucullo L, et al. Serum transthyretin monomer as a possible marker of blood-to-CSF barrier disruption. J Neurosci. 2003;1(23):1949–55.

    Google Scholar 

  43. 43.

    Grant GA, Janigro D. The blood-brain barrier. In: Winn RH, Youman JR, editors. Youmans neurological surgery, vol. 1. Philadelphia: Saunders; 2004. p. 153–74.

    Google Scholar 

  44. 44.

    Wong CH, Rooney SJ, Bonser RS. S-100β release in hypothermic circulatory arrest and coronary artery surgery. Ann Thorac Surg. 1999;67:1911–4.

    CAS  PubMed  Google Scholar 

  45. 45.

    Járányi Z, Székely M, Bobek I, et al. Impairment of blood-brain barrier integrity during carotid surgery as assessed by serum S-100B protein concentrations. Clin Chem Lab Med. 2003;41:1320–2.

    PubMed  Google Scholar 

  46. 46.

    Marchi N, Angelov L, Masaryk T, et al. Seizure-promoting effect of blood-brain barrier disruption. Epilepsia. 2007;48:732–42.

    CAS  PubMed  Google Scholar 

  47. 47.

    Kapural M, Krizanac-Bengez Lj, Barnett G, et al. Serum S-100β as a possible marker of blood–brain barrier disruption. Brain Res. 2002;14(940):102–4.

    Google Scholar 

  48. 48.

    Kanner AA, Marchi N, Fazio V, et al. Serum S100beta: a noninvasive marker of blood-brain barrier function and brain lesions. Cancer. 2003;1(97):2806–13.

    Google Scholar 

  49. 49.

    Marchi N, Cavaglia M, Fazio V, et al. Peripheral markers of blood–brain barrier damage. Clin Chim Acta. 2004;342:1–12.

    CAS  PubMed  Google Scholar 

  50. 50.

    Herrmann M, Curio N, Jost S, et al. Release of biochemical markers of damage to neuronal and glial brain tissue is associated with short and long term neuropsychological outcome after traumatic brain injury. J Neurol Neurosurg Psychiatry. 2001;70:95–100.

    CAS  PubMed Central  PubMed  Google Scholar 

  51. 51.

    Vogelbaum MA, Masaryk T, Mazzone P, et al. S100β as a predictor of brain metastases. Cancer. 2005;15(104):817–24.

    Google Scholar 

  52. 52.

    Ghanem G, Loir B, Morandini R, et al. On the release and half-life of S100B protein in the peripheral blood of melanoma patients. Int J Cancer. 2001;94:586–90.

    CAS  PubMed  Google Scholar 

  53. 53.

    Ohrt-Nissen S, Friis-Hansen L, Dahl B, et al. How does extracerebral trauma affect the clinical value of S100B measurements? Emerg Med J. 2011;28:941–4.

    PubMed Central  PubMed  Google Scholar 

  54. 54.

    Ilg EC, Schäfer BW, Heizmann CW. Expression pattern of S100 calcium-binding proteins in human tumors. Int J Cancer. 1996;68:325–32.

    CAS  PubMed  Google Scholar 

  55. 55.

    Brochez L, Naeyaert JM. Serological markers for melanoma. Br J Dermatol. 2000;143:256–68.

    CAS  PubMed  Google Scholar 

  56. 56.

    Johnsson P, Lundqvist C, Lindgren A, et al. Cerebral complications after cardiac surgery assessed by S-100 and NSE levels in blood. J Cardiothorac Vasc Anesth. 1995;9:694–9.

    CAS  PubMed  Google Scholar 

  57. 57.

    Ali MS, Harmer M, Vaughan R. Serum S100 protein as a marker of cerebral damage during cardiac surgery. Br J Anaesth. 2000;85:287–98.

    CAS  PubMed  Google Scholar 

  58. 58.

    Anderson RE, Hansson LO, Nilsson O, et al. High serum S100B levels for trauma patients without head injuries. Neurosurgery. 2001;48:1255–8.

    CAS  PubMed  Google Scholar 

  59. 59.

    Johnsson P, Bäckström M, Bergh C, et al. Increased S100B in blood after cardiac surgery is a powerful predictor of late mortality. Ann Thorac Surg. 2003;75:162–8.

    PubMed  Google Scholar 

  60. 60.

    Fazio V, Bhudia SK, Marchi N, et al. Peripheral detection of S100β during cardiothoracic surgery: what are we really measuring? Ann Thorac Surg. 2004;78:46–52.

    PubMed  Google Scholar 

  61. 61.

    Suzuki F, Kato K, Nakajima T. Hormonal regulation of adipose S-100 protein release. J Neurochem. 2006;43:1336–41.

    Google Scholar 

  62. 62.

    Holtkamp K, Bühren K, Ponath G, et al. Serum levels of S100B are decreased in chronic starvation and normalize with weight gain. J Neural Transm. 2008;115:937–40.

    CAS  PubMed  Google Scholar 

  63. 63.

    Savola O, Pyhtinen J, Leino TK, et al. Effects of head and extracranial injuries on serum protein S100B levels in trauma patients. J Trauma. 2004;56:1229–34.

    CAS  PubMed  Google Scholar 

  64. 64.

    Korfias S, Stranjalis G, Psachoulia C, et al. Slight and short-lasting increase of serum S-100B protein in extra-cranial trauma. Brain Inj. 2006;20:867–72.

    PubMed  Google Scholar 

  65. 65.

    Hasselblatt M, Mooren FC, von Ahsen N, et al. Serum S100beta increases in marathon runners reflect extracranial release rather than glial damage. Neurology. 2004;11(62):1634–6.

    Google Scholar 

  66. 66.

    Riuzzi F, Sorci G, Beccafico S, et al. S100B engages RAGE of bFGF/FGFR1 in myoblasts depending on its own concentration and myoblast density. Implications for muscle regeneration. PLoS One. 2012;7:e28700.

    CAS  PubMed Central  PubMed  Google Scholar 

  67. 67.

    Schulpis KH, Margeli A, Akalestos A, et al. Effects of mode of delivery on maternal-neonatal plasma antioxidant status and on protein S100B serum concentrations. Scand J Clin Lab Invest. 2006;66:733–42.

    CAS  PubMed  Google Scholar 

  68. 68.

    Bjursten H, Ederoth P, Sigurdsson E, et al. S100B profiles and cognitive function at high altitude. High Alt Med Biol. 2010;11:31–8.

    CAS  PubMed  Google Scholar 

  69. 69.

    Gazzolo D, Florio P, Zullino E. S100B protein increases in human blood and urine during stressful activity. Clin Chem Lab Med. 2010;48:1363–5.

    CAS  PubMed  Google Scholar 

  70. 70.

    Davis JM, Bailey SP. Possible mechanisms of central nervous system fatigue during exercise. Med Sci Sports Exerc. 1997;29:45–57.

    CAS  PubMed  Google Scholar 

  71. 71.

    Noakes TD. Fatigue is a brain-derived emotion that regulates the exercise behavior to ensure the protection of whole body homeostasis. Front Physiol. 2012;3(82):1–13.

    Google Scholar 

  72. 72.

    Meeusen R, Watson P, Hasegawa H, et al. Central fatigue: the serotonin hypothesis and beyond. Sports Med. 2006;36:881–909.

    PubMed  Google Scholar 

  73. 73.

    Nybo L. CNS fatigue provoked by prolonged exercise in the heat. Front Biosci (Elite Ed). 2010;2:779–92.

    Google Scholar 

  74. 74.

    Noakes TD, St Clair Gibson A, Lambert EV. From catastrophe to complexity: a novel model of integrative central neural regulation of effort and fatigue during exercise in humans: summary and conclusions. Br J Sports Med. 2005;39:120–4.

    CAS  PubMed Central  PubMed  Google Scholar 

  75. 75.

    Marino FE. The critical limiting temperature and selective brain cooling: neuroprotection during exercise? Int J Hyperth. 2011;27:582–90.

    Google Scholar 

  76. 76.

    Knaepen K, Goekint M, Heyman EM, et al. Neuroplasticity exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects. Sports Med. 2010;1(40):765–801.

    Google Scholar 

  77. 77.

    Bailey DM, Evans KA, McEneny J, et al. Exercise-induced oxidative-nitrosative stress is associated with impaired dynamic cerebral autoregulation and blood-brain barrier leakage. Exp Physiol. 2011;96:1196–207.

    CAS  PubMed  Google Scholar 

  78. 78.

    Cheuvront SN, Chinevere TD, Ely BR, et al. Serum S-100beta response to exercise-heat strain before and after acclimation. Med Sci Sports Exerc. 2008;40:1477–82.

    CAS  PubMed  Google Scholar 

  79. 79.

    Dietrich MO, Tort AB, Schaf DV, et al. Increase in serum S100B protein level after a swimming race. Can J Appl Physiol. 2003;28:710–6.

    CAS  PubMed  Google Scholar 

  80. 80.

    Graham MR, Myers T, Evans P, et al. Direct hits to the head during amateur boxing is associated with a rise in serum biomarkers for brain injury. Int J Immunopathol Pharmacol. 2011;24:119–25.

    CAS  PubMed  Google Scholar 

  81. 81.

    Michetti F, Bruschettini M, Frigiola A, et al. Saliva S100B in professional sportsmen: high levels at resting conditions and increased after vigorous physical activity. Clin Biochem. 2011;44:245–7.

    CAS  PubMed  Google Scholar 

  82. 82.

    Mussack T, Dvorak J, Graf-Baumann T, et al. Serum S-100B protein levels in young amateur soccer players after controlled heading and normal exercise. Eur J Med Res. 2003;22(8):457–64.

    Google Scholar 

  83. 83.

    Neselius S, Brisby H, Theodorsson A, et al. CSF-biomarkers in Olympic boxing: diagnosis and effects of repetitive head trauma. PLoS One. 2012;7:e33606.

    CAS  PubMed Central  PubMed  Google Scholar 

  84. 84.

    Otto M, Holthusen S, Bahn E, et al. Boxing and running lead to a rise in serum levels of S-100B protein. Int J Sports Med. 2000;21:551–5.

    CAS  PubMed  Google Scholar 

  85. 85.

    Saenz AJ, Lee-Lewandrowski E, Wood MJ, et al. Measurement of a plasma stroke biomarker panel and cardiac troponin T in marathon runners before and after the 2005 Boston marathon. Am J Clin Pathol. 2006;126:185–9.

    CAS  PubMed  Google Scholar 

  86. 86.

    Schulpis KH, Moukas M, Parthimos T, et al. The effect of alpha-Tocopherol supplementation on training-induced elevation of S100B protein in sera of basketball players. Clin Biochem. 2007;40:900–6.

    CAS  PubMed  Google Scholar 

  87. 87.

    Schulte S, Schiffer T, Sperlich B, et al. Serum concentrations of S100B are not affected by cycling to exhaustion with or without vibration. J Hum Kinet. 2011;30:59–63.

    PubMed Central  PubMed  Google Scholar 

  88. 88.

    Stålnacke BM, Sojka P. Repeatedly heading a soccer ball does not increase serum levels of S-100B, a biochemical marker of brain tissue damage: an experimental study. Biomark Insights. 2008;29(3):87–91.

    Google Scholar 

  89. 89.

    Stålnacke BM, Tegner Y, Sojka P. Playing ice hockey and basketball increases serum levels of S-100B in elite players: a pilot study. Clin J Sport Med. 2003;13:292–302.

    PubMed  Google Scholar 

  90. 90.

    Stålnacke BM, Tegner Y, Sojka P. Playing soccer increases serum concentrations of the biochemical markers of brain damage S-100B and neuron-specific enolase in elite players: a pilot study. Brain Inj. 2004;18:899–909.

    PubMed  Google Scholar 

  91. 91.

    Stålnacke BM, Ohlsson A, Tegner Y, et al. Serum concentrations of two biochemical markers of brain tissue damage S-100B and neurone specific enolase are increased in elite female soccer players after a competitive game. Br J Sports Med. 2006;40:313–6.

    PubMed Central  PubMed  Google Scholar 

  92. 92.

    Stavrinou LC, Kalamatianos T, Stavrinou P, et al. Serum levels of S-100B after recreational scuba diving. Int J Sports Med. 2011;32:912–5.

    CAS  PubMed  Google Scholar 

  93. 93.

    Straume-Naesheim TM, Andersen TE, Jochum M, et al. Minor head trauma in soccer and serum levels of S100B. Neurosurgery. 2008;62:1297–305.

    PubMed  Google Scholar 

  94. 94.

    Tyler CJ, Wild P, Sunderland C. Practical neck cooling and time-trial running performance in a hot environment. Eur J Appl Physiol. 2010;110:1063–74.

    PubMed  Google Scholar 

  95. 95.

    Watson P, Shirreffs SM, Maughan RJ. Blood-brain barrier integrity may be threatened by exercise in a warm environment. Am J Physiol Regul Integr Comp Physiol. 2005;288:R1689–94.

    CAS  PubMed  Google Scholar 

  96. 96.

    Watson P, Black KE, Clark SC, et al. Exercise in the heat: effect of fluid ingestion on blood brain barrier permeability. Med Sci Sports Exerc. 2006;38:2118–24.

    PubMed  Google Scholar 

  97. 97.

    Zetterberg H, Jonsson M, Rasulzada A, et al. No neurochemical evidence for brain injury caused by heading in soccer. Br J Sports Med. 2007;41:574–7.

    PubMed Central  PubMed  Google Scholar 

  98. 98.

    Zetterberg H, Tanriverdi F, Unluhizarci K, et al. Sustained release of neuron-specific enolase to serum in amateur boxers. Brain Inj. 2009;23:723–6.

    PubMed  Google Scholar 

  99. 99.

    Andersson JP, Linér MH, Jönsson H. Increased serum levels of the brain damage marker S100B after apnea in trained breath-hold divers: a study including respiratory and cardiovascular observations. J Appl Physiol (1985). 2009;107:809–15.

    Google Scholar 

  100. 100.

    Wright HE, Selkirk GA, Rhind SG, et al. Peripheral markers of central fatigue in trained and untrained during uncompensable heat stress. Eur J Appl Physiol. 2012;112:1047–57.

    PubMed  Google Scholar 

  101. 101.

    Portela LV, Tort AB, Schaf DV, et al. The serum S100B concentration is age dependent. Clin Chem. 2002;48:950–2.

    CAS  PubMed  Google Scholar 

  102. 102.

    Gazzolo D, Lituania M, Bruschettini M, et al. S100B protein levels in saliva: correlation with gestational age in normal term and preterm newborns. Clin Biochem. 2005;38:229–33.

    CAS  PubMed  Google Scholar 

  103. 103.

    Gazzolo D, Abella R, Frigiola A, et al. Neuromarkers and unconventional biological fluids. J Matern Fetal Neonatal Med. 2010;23(Suppl 3):66–9.

    CAS  PubMed  Google Scholar 

  104. 104.

    Persson L, Hårdemark HG, Gustafsson J, et al. S-100 protein and neuron-specific enolase in cerebrospinal fluid and serum: markers of cell damage in human central nervous system. Stroke. 1987;18:911–8.

    CAS  PubMed  Google Scholar 

  105. 105.

    Woertgen C, Rothoerl RD, Brawanski A. Neuron-specific enolase serum levels after controlled cortical impact injury in the rat. J Neurotrauma. 2001;18:569–73.

    CAS  PubMed  Google Scholar 

  106. 106.

    Clarkson PM, Tremblay I. Exercise-induced muscle damage, repair, and adaptation in humans. J Appl Physiol (1985). 1988;65:1–6.

    CAS  Google Scholar 

  107. 107.

    Newham DJ, Jones DA, Edwards RH. Large delayed plasma creatine kinase changes after stepping exercise. Muscle Nerve. 1983;6:380–5.

    CAS  PubMed  Google Scholar 

  108. 108.

    Pace A, Savarese A, Picardo M, et al. Neuroprotective effect of vitamin E supplementation in patients treated with cisplatin chemotherapy. J Clin Oncol. 2003;1(21):927–31.

    Google Scholar 

  109. 109.

    Khanna S, Roy S, Slivka A, et al. Neuroprotective properties of the natural vitamin E alpha-tocotrienol. Stroke. 2005;36:2258–64.

    PubMed Central  PubMed  Google Scholar 

  110. 110.

    Bialowas-McGoey LA, Lesicka A, Whitaker-Azmitia PM. Vitamin E increases S100B-mediated microglial activation in an S100B-overexpressing mouse model of pathological aging. Glia. 2008;56:1780–90.

    PubMed  Google Scholar 

Download references

Acknowledgments

No conflicts of interest and no funding are involved in the writing of this manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jason K. W. Lee.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Koh, S.X.T., Lee, J.K.W. S100B as a Marker for Brain Damage and Blood–Brain Barrier Disruption Following Exercise. Sports Med 44, 369–385 (2014). https://doi.org/10.1007/s40279-013-0119-9

Download citation

Keywords

  • Creatine Kinase
  • Head Trauma
  • Head Impact
  • S100B Level
  • Serum S100B