Extracellular brain pH with or without hypoxia is a marker of profound metabolic derangement and increased mortality after traumatic brain injury

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 3, 2013, Pages 422-427

  Timofeev, Ivan ^a   Nortje, Jurgens ^b   Al Rawi, Pippa G ^a   Hutchinson, Peter J A ^a   Gupta, Arun K ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

brain ischemia; brain trauma; energy metabolism; microdialysis; neurocritial care; pH

Indexed keywords

GLUCOSE; GLYCEROL; LACTIC ACID; PYRUVIC ACID;

ACIDOSIS; ADULT; ARTICLE; BRAIN HYPOXIA; BRAIN METABOLISM; CEREBRAL ACIDOSIS; CLINICAL EVALUATION; CONTROLLED STUDY; CORRELATIONAL STUDY; EXTRACELLULAR SPACE; FEMALE; GLUCOSE BRAIN LEVEL; HUMAN; INTRACRANIAL PRESSURE; MAJOR CLINICAL STUDY; MALE; METABOLIC DISORDER; MICRODIALYSIS; MORTALITY; PATIENT MONITORING; PH; PRIORITY JOURNAL; PROSPECTIVE STUDY; TISSUE OXYGENATION; TRAUMATIC BRAIN INJURY;

ADULT; BIOLOGICAL MARKERS; BRAIN; BRAIN INJURIES; DISEASE-FREE SURVIVAL; FEMALE; GLUCOSE; HUMANS; HYDROGEN-ION CONCENTRATION; HYPOXIA, BRAIN; LACTIC ACID; MALE; MIDDLE AGED; PYRUVIC ACID; SURVIVAL RATE;

EID: 84874664553     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2012.186     Document Type: Article

References (41)

1. Nortje J, Coles JP, Timofeev I, Fryer TD, Aigbirhio FI, Smielewski P et al. Effect of hyperoxia on regional oxygenation and metabolism after severe traumatic brain injury: preliminary findings. Crit Care Med 2008; 36(1): 273-81.
2. Verweij BH, Muizelaar JP, Vinas FC, Peterson PL, Xiong Y, Lee CP. Impaired cerebral mitochondrial function after traumatic brain injury in humans. J Neurosurg 2000; 93(5): 815-20.
3. Vespa P, Bergsneider M, Hattori N, Wu HM, Huang SC, Martin NA et al. Metabolic crisis without brain ischemia is common after traumatic brain injury: a combined microdialysis and positron emission tomography study. J Cereb Blood Flow Metab 2005; 25(6): 763-74.
4. Yermolaieva O, Leonard AS, Schnizler MK, Abboud FM, Welsh MJ. Extracellular acidosis increases neuronal cell calcium by activating acid-sensing ion channel 1a. Proc Natl Acad Sci USA 2004; 101(17): 6752-7.
5. Siesjo BK. Pathophysiology and treatment of focal cerebral ischemia. Part I: Pathophysiology. J Neurosurg 1992; 77(2): 169-84.
6. Ying W, Han SK, Miller JW, Swanson RA. Acidosis potentiates oxidative neuronal death by multiple mechanisms. J Neurochem 1999; 73(4): 1549-56.
7. McDonald JW, Bhattacharyya T, Sensi SL, Lobner D, Ying HS, Canzoniero LM et al. Extracellular acidity potentiates AMPA receptor-mediated cortical neuronal death. J Neurosci 1998; 18(16): 6290-9.
8. Velisek L. Extracellular acidosis and high levels of carbon dioxide suppress synaptic transmission and prevent the induction of long-term potentiation in the CA1 region of rat hippocampal slices. Hippocampus 1998; 8(1): 24-32.
9. Swanson RA, Farrell K, Simon RP. Acidosis causes failure of astrocyte glutamate uptake during hypoxia. J Cereb Blood Flow Metab 1995; 15(3): 417-24.
10. Swanson RA, Benington JH. Astrocyte glucose metabolism under normal and pathological conditions in vitro. Dev Neurosci 1996; 18(5-6): 515-21.
11. Nagy Z, Szabo M, Huttner I. Blood-brain barrier impairment by low pH buffer perfusion via the internal carotid artery in rat. Acta Neuropathol (Berl) 1985; 68(2): 160-3.
12. Kristian T, Bernardi P, Siesjo BK. Acidosis promotes the permeability transition in energized mitochondria: implications for reperfusion injury. J Neurotrauma 2001; 18(10): 1059-1074.
13. Mellergard P, Ouyang YB, Siesjo BK. The regulation of intracellular pH is strongly dependent on extracellular pH in cultured rat astrocytes and neurons. Acta Neurochir Suppl (Wien) 1994; 60: 34-7.
14. Hoffman WE, Charbel FT, Edelman G, Ausman JI. Brain tissue acid-base changes during ischemia. Neurosurg Focus 1997; 2(5): E2 , discussion 1 p following E2.
15. Huang Y, McNamara JO. Ischemic stroke: 'acidotoxicity' is a perpetrator. Cell 2004; 118(6): 665-6.
16. Shiogai T, Nara I, Saruta K, Hara M, Saito I. Continuous monitoring of cerebrospinal fluid acid-base balance and oxygen metabolism in patients with severe head injury: pathophysiology and treatments for cerebral acidosis and ischemia. Acta Neurochir Suppl 1999; 75: 49-55.
17. McIntosh TK, Faden AI, Bendall MR, Vink R. Traumatic brain injury in the rat: alterations in brain lactate and pH as characterized by 1H and 31P nuclear magnetic resonance. J Neurochem 1987; 49(5): 1530-40.
18. Clausen T, Khaldi A, Zauner A, Reinert M, Doppenberg E, Menzel M et al. Cerebral acid-base homeostasis after severe traumatic brain injury. J Neurosurg 2005; 103(4): 597-607.
19. Zauner A, Clausen T, Alves OL, Rice A, Levasseur J, Young HF et al. Cerebral metabolism after fluid-percussion injury and hypoxia in a feline model. J Neurosurg 2002; 97(3): 643-9.
20. Brooke NS, Ouwerkerk R, Adams CB, Radda GK, Ledingham JG, Rajagopalan B. Phosphorus-31 magnetic resonance spectra reveal prolonged intracellular acidosis in the brain following subarachnoid hemorrhage. Proc Natl Acad Sci USA 1994; 91(5): 1903-7.
21. Yokota H, Yamamoto Y, Naoe Y, Fuse A, Sato H, Unemoto K et al. Measurements of cortical cellular pH by intracranial tonometer in severe head injury. Crit Care Med 2000; 28(9): 3275-80.
22. Gupta AK, Zygun DA, Johnston AJ, Steiner LA, Al-Rawi PG, Chatfield D et al. Extracellular brain pH and outcome following severe traumatic brain injury. J Neurotrauma 2004; 21(6): 678-84.
23. Brain Trauma Foundation. Guidelines for the management of severe traumatic brain injury, 3rd edition. J Neurotrauma 2007; 24(Suppl 1): S1-106.
24. Maas AI, Dearden M, Teasdale GM, Braakman R, Cohadon F, Iannotti F et al. EBICguidelines for management of severe head injury in adults. European Brain Injury Consortium. Acta Neurochir (Wien) 1997; 139(4): 286-94.
25. Menon DK. Cerebral protection in severe brain injury: physiological determinants of outcome and their optimisation. Br Med Bull 1999; 55(1): 226-58.
26. Smielewski P, Lavinio A, Timofeev I, Radolovich D, Perkes I, Pickard JD et al. ICM\+, a flexible platform for investigations of cerebrospinal dynamics in clinical practice. Acta Neurochir Suppl 2009; 102: 145-151.
27. Menon DK, Coles JP, Gupta AK, Fryer TD, Smielewski P, Chatfield DA et al. Diffusion limited oxygen delivery following head injury. Crit Care Med 2004; 32(6): 1384-90.
28. Hoffman TL, LaManna JC, Pundik S, Selman WR, Whittingham TS, Ratcheson RA et al. Early reversal of acidosis and metabolic recovery following ischemia. J Neurosurg 1994; 81(4): 567-73.
29. Zygun DA, Steiner LA, Johnston AJ, Hutchinson PJ, Al-Rawi PG, Chatfield D et al. Hyperglycemia and brain tissue pH after traumatic brain injury. Neurosurgery 2004; 55(4): 877-81, discussion 882.
30. Holbein M, Bechir M, Ludwig S, Sommerfeld J, Cottini SR, Keel M et al. Differential influence of arterial blood glucose on cerebral metabolism following severe traumatic brain injury. Crit Care 2009; 13(1): 6.
31. Li PA, Siesjo BK. Role of hyperglycaemia-related acidosis in ischaemic brain damage. Acta Physiol Scand 1997; 161(4): 567-80.
32. Yoshida K, Marmarou A. Effects of tromethamine and hyperventilation on brain injury in the cat. J Neurosurg 1991; 74(1): 87-96.
33. Yoshida K, Corwin F, Marmarou A. Effect of THAM on brain oedema in experimental brain injury. Acta Neurochir Suppl (Wien) 1990; 51: 317-9.
34. Wolf AL, Levi L, Marmarou A, Ward JD, Muizelaar PJ, Choi S et al. Effect of THAM upon outcome in severe head injury: a randomized prospective clinical trial. J Neurosurg 1993; 78(1): 54-9.
35. Marmarou A, Holdaway R, Ward JD, Yoshida K, Choi SC, Muizelaar JP et al. Traumatic brain tissue acidosis: experimental and clinical studies. Acta Neurochir Suppl (Wien) 1993; 57: 160-4.
36. Rosner MJ, Becker DP. Experimental brain injury: successful therapy with the weak base, tromethamine. With an overview of CNS acidosis. J Neurosurg 1984; 60(5): 961-71.
37. Hoelper BM, Alessandri B, Heimann A, Behr R, Kempski O. Brain oxygen monitoring: in-vitro accuracy, long-term drift and response-time of Licox-and Neurotrend sensors. Acta Neurochir (Wien) 2005; 147(7): 767-74.
38. Jaeger M, Soehle M, Meixensberger J. Brain tissue oxygen (PtiO2): a clinical comparison of two monitoring devices. Acta Neurochir Suppl 2005; 95: 79-81.
39. Grant SA, Bettencourt K, Krulevitch P, Hamilton J, Glass R. In vitro and in vivo measurements of fiber optic and electrochemical sensors to monitor brain tissue pH. Sensors and Actuators B: Chemical 2001; 72(2): 174-179.
40. Wu S, Cheng W, Qiu Y, Li Z, Shuang S, Dong C. Fiber optic pH sensor based on mode-filtered light detection. Sensors Actuators B: Chem 2010; 144(1): 255-259.
41. Korostynska O, Arshak K, Gill E, Arshak A. Review paper: materials and techniques for in vivo pH monitoring. IEEE Sensors J 2008; 8(1): 20.