Monitoring of brain interstitial total tau and beta amyloid proteins by microdialysis in patients with traumatic brain injury: Clinical article

Journal of Neurosurgery

Volumn 110, Issue 6, 2009, Pages 1227-1237

  Marklund, Niklas ^a   Blennow, Kaj ^b   Zetterberg, Henrik ^b   Ronne Engström, Elisabeth ^a   Enblad, Per ^a   Hillered, Lars ^a  

^a UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^b SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Amyloid beta; Diffuse axonal injury; Microdialysis; Tau protein; Traumatic brain injury

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; GLUCOSE; GLUTAMIC ACID; GLYCEROL; LACTIC ACID; PYRUVIC ACID; TAU PROTEIN;

ADOLESCENT; ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIALYSIS CATHETER; DIFFUSE AXONAL INJURY; ENERGY METABOLISM; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GLASGOW COMA SCALE; HUMAN; INJURY SEVERITY; MALE; MICRODIALYSIS; PRIORITY JOURNAL; TRAUMATIC BRAIN INJURY;

ADOLESCENT; ADULT; AGED; AMYLOID BETA-PROTEIN; BIOLOGICAL MARKERS; COHORT STUDIES; DIFFUSE AXONAL INJURY; FEMALE; HUMANS; MALE; MICRODIALYSIS; MIDDLE AGED; PEPTIDE FRAGMENTS; PILOT PROJECTS; PREDICTIVE VALUE OF TESTS; RISK FACTORS; TAU PROTEINS; YOUNG ADULT;

EID: 67650810148     PISSN: 00223085     EISSN: 19330693     Source Type: Journal    
DOI: 10.3171/2008.9.JNS08584     Document Type: Article

References (74)

1. Abrahamson EE, Ikonomovic MD, Ciallella JR, Hope CE, Paljug WR, Isanski BA, et al: Caspase inhibition therapy abolishes brain trauma-induced increases in Abeta peptide: implications for clinical outcome. Exp Neurol 197:437-450, 2006
2. Adams JH, Graham DI, Jennett B: The structural basis of moderate disability after traumatic brain damage. J Neurol Neurosurg Psychiatry 71:521-524, 2001
3. Adle-Biassette H, Duyckaerts C, Wasowicz M, He Y, Fornes P, Foncin JF, et al: Beta AP deposition and head trauma. Neurobiol Aging 17:415-419, 1996
4. Bellander BM, Cantais E, Enblad P, Hutchinson P, Nordström CH, Robertson C, et al: Consensus meeting on microdialysis in neurointensive care. Intensive Care Med 30:2166-2169, 2004 (Pubitemid 40174251)
5. Blennow K, de Leon MJ, Zetterberg H: Alzheimer's disease. Lancet 368:387-403, 2006
6. Blennow K, Wallin A, Agren H, Spenger C, Siegfried J, Vanmechelen E: Tau protein in cerebrospinal fluid: a biochemical marker for axonal degeneration in Alzheimer disease? Mol Chem Neuropathol 26:231-245, 1995 (Pubitemid 26002016)
7. Blumbergs PC, Scott G, Manavis J, Wainwright H, Simpson DA, McLean AJ: Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury. J Neurotrauma 12:565-572, 1995
8. Chen SF, Richards HK, Smielewski P, Johnström P, Salvador R, Pickard JD, et al: Relationship between flow-metabolism uncoupling and evolving axonal injury after experimental traumatic brain injury. J Cereb Blood Flow Metab 24:1025-1036, 2004 (Pubitemid 39223626)
9. Chen XH, Siman R, Iwata A, Meaney DF, Trojanowski JQ, Smith DH: Long-term accumulation of amyloid-beta, betasecretase, presenilin-1, and caspase-3 in damaged axons following brain trauma. Am J Pathol 165:357-371, 2004 (Pubitemid 38971368)
10. Dekosky ST, Abrahamson EE, Ciallella JR, Paljug WR, Wisniewski SR, Clark RS, et al: Association of increased cortical soluble abeta42 levels with diffuse plaques after severe brain injury in humans. Arch Neurol 64:541-544, 2007
11. Elf K, Nilsson P, Enblad P: Outcome after traumatic brain injury improved by an organized secondary insult program and standardized neurointensive care. Crit Care Med 30:2129-2134, 2002
12. Emmerling MR, Morganti-Kossmann MC, Kossmann T, Stahel PF, Watson MD, Evans LM, et al: Traumatic brain injury elevates the Alzheimer's amyloid peptide A beta 42 in human CSF. A possible role for nerve cell injury. Ann N Y Acad Sci 903:118-122, 2000 (Pubitemid 30251547)
13. Esler WP, Wolfe MS: A portrait of Alzheimer secretases-new features and familiar faces. Science 293:1449-1454, 2001
14. Fork M, Bartels C, Ebert AD, Grubich C, Synowitz H, Wallesch CW, et al: Neuropsychological sequelae of diffuse traumatic brain injury. Brain Inj 19:101-108, 2005
15. Franz G, Beer R, Kampfl A, Engelhardt K, Schmutzhard E, Ulmer H, et al: Amyloid beta 1-42 and tau in cerebrospinal fluid after severe traumatic brain injury. Neurology 60:1457-1461, 2003 (Pubitemid 36554806)
16. Gentleman SM, Graham DI, Roberts GW: Molecular pathology of head trauma: altered beta APP metabolism and the aetiology of Alzheimer's disease. Prog Brain Res 96:237-246, 1993
17. Gentleman SM, Greenberg BD, Savage MJ, Noori M, Newman SJ, Roberts GW, et al: A beta 42 is the predominant form of amyloid beta-protein in the brains of short-term survivors of head injury. Neuroreport 8:1519-1522, 1997 (Pubitemid 27242567)
18. Gentleman SM, Roberts GW, Gennarelli TA, Maxwell WL, Adams JH, Kerr S, et al: Axonal injury: a universal consequence of fatal closed head injury? Acta Neuropathol 89: 537-543, 1995
19. Graham DI, Gentleman SM, Lynch A, Roberts GW: Distribution of beta-amyloid protein in the brain following severe head injury. Neuropathol Appl Neurobiol 21:27-34, 1995
20. Guo Z, Cupples LA, Kurz A, Auerbach SH, Volicer L, Chui H, et al: Head injury and the risk of AD in the MIRAGE study. Neurology 54:1316-1323, 2000 (Pubitemid 30174053)
21. Hesse C, Rosengren L, Vanmechelen E, Vanderstichele H, Jensen C, Davidsson P, et al: Cerebrospinal fluid markers for Alzheimer's disease evaluated after acute ischemic stroke. J Alzheimers Dis 2:199-206, 2000 (Pubitemid 32095607)
22. Hillered L, Persson L, Nilsson P, Ronne-Engstrom E, Enblad P: Continuous monitoring of cerebral metabolism in traumatic brain injury: a focus on cerebral microdialysis. Curr Opin Crit Care 12:112-118, 2006
23. Hillered L, Vespa PM, Hovda DA: Translational neurochemical research in acute human brain injury: the current status and potential future for cerebral microdialysis. J Neurotrauma 22:3-41, 2005
24. Hillman J, Aneman O, Anderson C, Sjögren F, Säberg C, Mellergård P: A microdialysis technique for routine measurement of macromolecules in the injured human brain. Neurosurgery 56:1264-1268, 2005 (Pubitemid 40770444)
25. Hillman J, Aneman O, Persson M, Andersson C, Dabrosin C, Mellergård P: Variations in the response of interleukins in neurosurgical intensive care patients monitored using intracerebral microdialysis. J Neurosurg 106:820-825, 2007 (Pubitemid 46698667)
26. Horsburgh K, Cole GM, Yang F, Savage MJ, Greenberg BD, Gentleman SM, et al: Beta-amyloid (Abeta)42(43), abeta42, abeta40 and apoE immunostaining of plaques in fatal head injury. Neuropathol Appl Neurobiol 26:124-132, 2000 (Pubitemid 30251385)
27. Hulstaert F, Blennow K, Ivanoiu A, Schoonderwaldt HC, Riemenschneider M, De Deyn PP, et al: Improved discrimination of AD patients using beta-amyloid(1-42) and tau levels in CSF. Neurology 52:1555-1562, 1999 (Pubitemid 29220627)
28. Hutchinson PJ: Microdialysis in traumatic brain injury-methodology and pathophysiology. Acta Neurochir Suppl 95: 441-445, 2005
29. Hutchinson PJ, O'Connell MT, Nortje J, Smith P, Al-Rawi PG, Gupta AK, et al: Cerebral microdialysis methodology-evaluation of 20 kDa and 100 kDa catheters. Physiol Meas 26:423-428, 2005 (Pubitemid 40768140)
30. Ida N, Hartmann T, Pantel J, Schröder J, Zerfass R, Förstl H, et al: Analysis of heterogeneous A4 peptides in human cerebrospinal fluid and blood by a newly developed sensitive Western blot assay. J Biol Chem 271:22908-22914, 1996 (Pubitemid 26304742)
31. Ikonomovic MD, Uryu K, Abrahamson EE, Ciallella JR, Trojanowski JQ, Lee VM, et al: Alzheimer's pathology in human temporal cortex surgically excised after severe brain injury. Exp Neurol 190:192-203, 2004 (Pubitemid 39335718)
32. Iwata A, Chen XH, McIntosh TK, Browne KD, Smith DH: Long-term accumulation of amyloid-beta in axons following brain trauma without persistent upregulation of amyloid precursor protein genes. J Neuropathol Exp Neurol 61:1056-1068, 2002 (Pubitemid 35435024)
33. Kay AD, Petzold A, Kerr M, Keir G, Thompson E, Nicoll J: Alterations in cerebrospinal fluid apolipoprotein E and amyloid beta-protein after traumatic brain injury. J Neurotrauma 20:943-952, 2003 (Pubitemid 37288554)
34. Kay AD, Petzold A, Kerr M, Keir G, Thompson E, Nicoll J: Temporal alterations in cerebrospinal fluid amyloid betaprotein and apolipoprotein E after subarachnoid hemorrhage. Stroke 34:e240-e243, 2003 (Pubitemid 36307384)
35. Lazarov O, Lee M, Peterson DA, Sisodia SS: Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J Neurosci 22:9785-9793, 2002 (Pubitemid 35332862)
36. Lewen A, Li GL, Olsson Y, Hillered L: Changes in microtubule-associated protein 2 and amyloid precursor protein immunoreactivity following traumatic brain injury in rat: influence of MK-801 treatment. Brain Res 719:161-171, 1996 (Pubitemid 26173385)
37. Marshall LF, Marshall SB, Klauber MR, Van Berkum Clark M, Eisenberg H, Jane JA, et al: The diagnosis of head injury requires a classification based on computed axial tomography. J Neurotrauma 9 (Suppl 1):S287-S292, 1992
38. Medana IM, Esiri MM: Axonal damage: a key predictor of outcome in human CNS diseases. Brain 126:515-530, 2003
39. Naredi S, Eden E, Zall S, Stephensen H, Rydenhag B: A standardized neurosurgical neurointensive therapy directed toward vasogenic edema after severe traumatic brain injury: clinical results. Intensive Care Med 24:446-451, 1998 (Pubitemid 28274156)
40. Nunan J, Small DH: Regulation of APP cleavage by alpha-, beta- and gamma-secretases. FEBS Lett 483:6-10, 2000 (Pubitemid 30738598)
41. Olsson A, Csajbok L, Ost M, Höglund K, Nylén K, Rosengren L, et al: Marked increase of beta-amyloid(1-42) and amyloid precursor protein in ventricular cerebrospinal fluid after severe traumatic brain injury. J Neurol 251:870-876, 2004 (Pubitemid 39005974)
42. Ost M, Nylen K, Csajbok L, Ohrfelt AO, Tullberg M, Wikkelsö C, et al: Initial CSF total tau correlates with 1-year outcome in patients with traumatic brain injury. Neurology 67:1600-1604, 2006 (Pubitemid 44747930)
43. Park JH, Gimbel DA, GrandPre T, Lee JK, Kim JE, Li W, et al: Alzheimer precursor protein interaction with the Nogo-66 receptor reduces amyloid-beta plaque deposition. J Neurosci 26:1386-1395, 2006 (Pubitemid 43237009)
44. Pierce JE, Trojanowski JQ, Graham DI, Smith DH, McIntosh TK: Immunohistochemical characterization of alterations in the distribution of amyloid precursor proteins and beta-amyloid peptide after experimental brain injury in the rat. J Neurosci 16:1083-1090, 1996
45. Plassman BL, Havlik RJ, Steffens DC, Helms MJ, Newman TN, Drosdick D, et al: Documented head injury in early adulthood and risk of Alzheimer's disease and other dementias. Neurology 55:1158-1166, 2000 (Pubitemid 30802995)
46. Povlishock JT, Katz DI: Update of neuropathology and neurological recovery after traumatic brain injury. J Head Trauma Rehabil 20:76-94, 2005 (Pubitemid 40250687)
47. Raby CA, Morganti-Kossmann MC, Kossmann T, Stahel PF, Watson MD, Evans LM, et al: Traumatic brain injury increases beta-amyloid peptide 1-42 in cerebrospinal fluid. J Neurochem 71:2505-2509, 1998 (Pubitemid 28531261)
48. Reinstrup P, Stahl N, Mellergard P, Uski T, Ungerstedt U, Nordström CH: Intracerebral microdialysis in clinical practice: baseline values for chemical markers during wakefulness, anesthesia, and neurosurgery. Neurosurgery 47:701-709, 2000 (Pubitemid 32044717)
49. Roberts GW, Gentleman SM, Lynch A, Graham DI: Beta A4 amyloid protein deposition in brain after head trauma. Lancet 338:1422-1423, 1991
50. Roberts GW, Gentleman SM, Lynch A, Murray L, Landon M, Graham DI: Beta amyloid protein deposition in the brain after severe head injury: implications for the pathogenesis of Alzheimer's disease. J Neurol Neurosurg Psychiatry 57:419-425, 1994 (Pubitemid 24118136)
51. Ronne-Engstrom E, Cesarini KG, Enblad P, Hesselager G, Marklund N, Nilsson P, et al: Intracerebral microdialysis in neurointensive care: the use of urea as an endogenous reference compound. J Neurosurg 94:397-402, 2001 (Pubitemid 32786017)
52. Sarrafzadeh AS, Sakowitz OW, Callsen TA, Lanksch WR, Unterberg AW: Bedside icrodialysis for early detection of cerebral hypoxia in traumatic brain injury. Neurosurg Focus 9(5):E2, 2000
53. Schulz MK, Wang LP, Tange M, Bjerre P: Cerebral microdialysis monitoring: determination of normal and ischemic cerebral metabolisms in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg 93:808-814, 2000 (Pubitemid 32803404)
54. Selkoe DJ, Schenk D: Alzheimer's disease: molecular understanding predicts amyloid-based therapeutics. Annu Rev Pharmacol Toxicol 43:545-584, 2003
55. Selkoe DJ, Wolfe MS: In search of gamma-secretase: presenilin at the cutting edge. Proc Natl Acad Sci U S A 97:5690-5692, 2000
56. Servadei F, Murray GD, Penny K, Teasdale GM, Dearden M, Iannotti F, et al: The value of the "worst" computed tomographic scan in clinical studies of moderate and severe head injury. European Brain Injury Consortium. Neurosurgery 46:70-75, 2000 (Pubitemid 30030267)
57. Sherriff FE, Bridges LR, Gentleman SM, Sivaloganathan S, Wilson S: Markers of axonal injury in post mortem human brain. Acta Neuropathol 88:433-439, 1994 (Pubitemid 24331029)
58. Siman R, Card JP, Nelson RB, Davis LG: Expression of betaamyloid precursor protein in reactive astrocytes following neuronal damage. Neuron 3:275-285, 1989
59. Smith DH, Chen XH, Iwata A, Graham DI: Amyloid beta accumulation in axons after traumatic brain injury in humans. J Neurosurg 98:1072-1077, 2003 (Pubitemid 36460899)
60. Smith DH, Chen XH, Nonaka M, Trojanowski JQ, Lee VM, Saatman KE, et al: Accumulation of amyloid beta and tau and the formation of neurofilament inclusions following diffuse brain injury in the pig. J Neuropathol Exp Neurol 58:982-992, 1999 (Pubitemid 29441926)
61. Stalhammar D, Starmark JE, Holmgren E, Eriksson N, Nordström CH, Fedders O, et al: Assessment of responsiveness in acute cerebral disorders. A multicentre study on the reaction level scale (RLS 85). Acta Neurochir (Wien) 90:73-80, 1988 (Pubitemid 18065674)
62. Stone JR, Okonkwo DO, Singleton RH, Mutlu LK, Helm GA, Povlishock JT: Caspase-3-ediated cleavage of amyloid precursor protein and formation of amyloid Beta peptide in traumatic axonal injury. J Neurotrauma 19:601-614, 2002
63. Teasdale G, Jennett B: Assessment of coma and impaired consciousness. A practical scale. Lancet 2:81-84, 1974
64. Tomaiuolo F, Carlesimo GA, Di Paola M, Petrides M, Fera F, Bonanni R, et al: Gross morphology and morphometric sequelae in the hippocampus, fornix, and corpus callosum of patients with severe non-missile traumatic brain injury without macroscopically detectable lesions: a T1 weighted MRI study. J Neurol Neurosurg Psychiatry 75:1314-1322, 2004 (Pubitemid 39141341)
65. Uryu K, Chen XH, Martinez D, Browne KD, Johnson VE, Graham DI, et al: Multiple proteins implicated in neurodegenerative diseases accumulate in axons after brain trauma in humans. Exp Neurol 208:185-192, 2007 (Pubitemid 350101496)
66. Vandermeeren M, Mercken M, Vanmechelen E, Six J, van de Voorde A, Martin JJ, et al: Detection of tau proteins in normal and Alzheimer's disease cerebrospinal fluid with a sensitive sandwich enzyme-linked immunosorbent assay. J Neurochem 61:1828-1834, 1993
67. Vanderstichele H, Van KE, Hesse C, Davidsson P, Buyse MA, Andreasen N, et al: Standardization of measurement of betaamyloid(1-42) in cerebrospinal fluid and plasma. Amyloid 7:245-258, 2000
68. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, et al: Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286:735-741, 1999 (Pubitemid 129515714)
69. Vespa PM: The implications of cerebral ischemia and metabolic dysfunction for treatment strategies in neurointensive care. Curr Opin Crit Care 12:119-123, 2006
70. Wang H, Duan G, Zhang J, Zhou D: Clinical studies on diffuse axonal injury in patients with severe closed head injury. Chin Med J (Engl) 111:59-62, 1998 (Pubitemid 128515230)
71. Whittle IR, Glasby M, Lammie A, Bell H, Ungerstedt U: Neuropathological findings after intracerebral implantation of microdialysis catheters. Neuroreport 9:2821-2825, 1998 (Pubitemid 28435170)
72. Wilhelmsen KC: The tangled biology of tau. Proc Natl Acad Sci U S A 96:7120-7121, 1999
73. Zetterberg H, Hietala MA, Jonsson M, Andreasen N, Styrud E, Karlsson I, et al: Neurochemical aftermath of amateur boxing. Arch Neurol 63:1277-1280, 2006
74. Marklund N, Blennow K, Zetterberg H, Nilsson P, Lewen A, Ronne-Engström E, et al: Monitoring of interstital axonal injury markers following human traumatic brain injury. J Neurotrauma 23:754, 2006