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Acta Neurochirurgica

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01-07-2009 | Clinical Article

Temporal patterns of interstitial pyruvate and amino acids after subarachnoid haemorrhage are related to the level of consciousness—a clinical microdialysis study

Authors: Maria Zetterling, Lars Hillered, Carolina Samuelsson, Torbjörn Karlsson, Per Enblad, Elisabeth Ronne-Engström

Published in: Acta Neurochirurgica | Issue 7/2009

Abstract

Background

Temporal patterns of brain interstitial amino acids after subarachnoid haemorrhage (SAH) were studied in relation to energy metabolite levels and to the severity of the initial global ischaemia as reflected by the level of consciousness at admission.

Method

Intracerebral microdialysis was used to measure brain interstitial amino acids and the energy metabolites glucose, lactate, and pyruvate during five days in 19 patients. Patients who were conscious (n = 11) were compared to those who were unconscious on admission (n = 8).

Findings

Eight non-transmitter amino acids (alanine, aspargine, glutamine, isoleucine, leucine, phenylalanine, serine and tyrosine), as well as glycine and pyruvate showed a pattern of increasing concentrations starting at 60–70 h after the onset of SAH. The conscious patients showed more pronounced elevations of non-transmitter amino acids, glycine, taurine and pyruvate compared to the unconscious patient group. Pyruvate levels were initially critically low for all patients, then normalised in the conscious patients but remained low in the unconscious group.

Conclusions

There was an increase of the cerebral interstitial levels of non-transmitter amino acids and glycine which correlated temporally to pyruvate levels, more pronounced in patients conscious on admission. Pyruvate levels in these patients normalised, but remained reduced in the unconscious patients. The increase of the non-transmitter amino acids and glycine could reflect an increased amino acid turnover in an attempt at repairing the injured brain, which could have been hampered by the lower pyruvate levels. Interstitial pyruvate may be a useful marker of the energy metabolic situation in the acutely injured brain.

Bartnik BL, Lee SM, Hovda DA, Sutton RL (2007) The fate of glucose during the period of decreased metabolism after fluid percussion injury: a 13C NMR study. J Neurotrauma 24:1079–1092. doi:10.1089/neu.2006.0210 PubMedCrossRef

Benveniste H (1989) Brain microdialysis. J Neurochem 52:1667–1679. doi:10.1111/j.1471-4159.1989.tb07243.x PubMedCrossRef

Benveniste H, Drejer J, Schousboe A, Diemer NH (1987) Regional cerebral glucose phosphorylation and blood flow after insertion of a microdialysis fibre through the dorsal hippocampus in the rat. J Neurochem 49:729–734. doi:10.1111/j.1471-4159.1987.tb00954.x PubMedCrossRef

Bielicki L, Krieglstein J (1976) Inhibition of glucose phosphorylation in rat brain by thiopental. Naunyn Schmiedebergs Arch Pharmacol 293:25–29. doi:10.1007/BF00498867 PubMedCrossRef

Bosche B, Dohmen C, Graf R, Neveling M, Staub F, Kracht L, Sobesky J, Lehnhardt FG, Heiss WD (2003) Extracellular concentrations of non-transmitter amino acids in peri-infarct tissue of patients predict malignant middle cerebral artery infarction. Stroke 34:2908–2913. doi:10.1161/01.STR.0000100158.51986.EB PubMedCrossRef

Cesarini KG, Enblad P, Ronne-Engstrom E, Marklund N, Salci K, Nilsson P, Hardemark HG, Hillered L, Persson L (2002) Early cerebral hyperglycinecolysis after subarachnoid haemorrhage correlates with favourable outcome. Acta Neurochir (Wien) 144:1121–1131. doi:10.1007/s00701-002-1011-9 CrossRef

Cesarini KG, Hardemark HG, Persson L (1999) Improved survival after aneurysmal subarachnoid haemorrhage: review of case management during a 12-year period. J Neurosurg 90:664–672PubMedCrossRef

Dahlbacka S, Makela J, Kaakinen T, Alaoja H, Heikkinen J, Laurila P, Kiviluoma K, Salomaki T, Tuominen H, Ohtonen P, Lepola P, Biancari F, Juvonen T (2006) Propofol is associated with impaired brain metabolism during hypothermic circulatory arrest: an experimental microdialysis study. Heart Surg Forum 9:E710–E718. doi:10.1532/HSF98.20061022 discussion E718PubMedCrossRef

Dusick JR, Glenn TC, Lee WN, Vespa PM, Kelly DF, Lee SM, Hovda DA, Martin NA (2007) Increased pentose phosphate pathway flux after clinical traumatic brain injury: a [1, 2–13C2]glucose labelling study in humans. J Cereb Blood Flow Metab 27:1593–1602. doi:10.1038/sj.jcbfm.9600458 PubMedCrossRef

10.

Edvinsson K, Krause DN (2002) Cerebral blood flow and metabolism, second edition. Philadelphia, Lippinicott Williams and Wilkins, pp 162–171, 423–451

11.

Enblad P, Persson L (1997) Impact on clinical outcome of secondary brain insults during the neurointensive care of patients with subarachnoid haemorrhage: a pilot study. J Neurol Neurosurg Psychiatry 62:512–516. doi:10.1136/jnnp.62.5.512 PubMedCrossRef

12.

Fawcett JW, Asher RA (1999) The glial scar and central nervous system repair. Brain Res Bull 49:377–391. doi:10.1016/S0361-9230(99)00072-6 PubMedCrossRef

13.

Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid haemorrhage visualised by computerised tomographic scanning. Neurosurgery 6:1–9. doi:10.1097/00006123-198001000-00001 PubMedCrossRef

14.

Goldsmith JD, Kujawa SG, McLaren JD, Bledsoe SC Jr (1995) In vivo release of neuroactive amino acids from the inferior colliculus of the guinea pig using brain microdialysis. Hear Res 83:80–88. doi:10.1016/0378-5955(94)00193-T PubMedCrossRef

15.

Hargreaves KM, Pardridge WM (1988) Neutral amino acid transport at the human blood-brain barrier. J Biol Chem 263:19392–19397PubMed

16.

Hillered L, Hallstrom A, Segersvard S, Persson L, Ungerstedt U (1989) Dynamics of extracellular metabolites in the striatum after middle cerebral artery occlusion in the rat monitored by intracerebral microdialysis. J Cereb Blood Flow Metab 9:607–616PubMed

17.

Hillered L, Persson L, Nilsson P, Ronne-Engstrom E, Enblad P (2006) Continuous monitoring of cerebral metabolism in traumatic brain injury: a focus on cerebral microdialysis. Curr Opin Crit Care 12:112–118. doi:10.1097/01.ccx.0000216576.11439.df PubMedCrossRef

18.

Hillered L, Persson L, Ponten U, Ungerstedt U (1990) Neurometabolic monitoring of the ischaemic human brain using microdialysis. Acta Neurochir (Wien) 102:91–97. doi:10.1007/BF01405420 CrossRef

19.

Hillered L, Vespa PM, Hovda DA (2005) Translational neurochemical research in acute human brain injury: the current status and potential future for cerebral microdialysis. J Neurotrauma 22:3–41. doi:10.1089/neu.2005.22.3 PubMedCrossRef

20.

Hlatky R, Valadka AB, Goodman JC, Contant CF, Robertson CS (2004) Patterns of energy substrates during ischaemia measured in the brain by microdialysis. J Neurotrauma 21:894–906. doi:10.1089/0897715041526195 PubMedCrossRef

21.

Hutchinson PJ, O’Connell MT, Al-Rawi PG, Kett-White CR, Gupta AK, Maskell LB, Pickard JD, Kirkpatrick PJ (2002) Increases in GABA concentrations during cerebral ischaemia: a microdialysis study of extracellular amino acids. J Neurol Neurosurg Psychiatry 72:99–105. doi:10.1136/jnnp.72.1.99 PubMedCrossRef

22.

Hutchinson PJ, O’Connell MT, Al-Rawi PG, Maskell LB, Kett-White R, Gupta AK, Richards HK, Hutchinson DB, Kirkpatrick PJ, Pickard JD (2000) Clinical cerebral microdialysis: a methodological study. J Neurosurg 93:37–43PubMedCrossRef

23.

Jennett B, Bond M (1975) Assessment of outcome after severe brain damage. Lancet 1:480–484. doi:10.1016/S0140-6736(75)92830-5 PubMedCrossRef

24.

Johnstone AJ, Lohlun JC, Miller JD, McIntosh CA, Gregori A, Brown R, Jones PA, Anderson SI, Tocher JL (1993) A comparison of the Glasgow Coma Scale and the Swedish Reaction Level Scale. Brain Inj 7:501–506. doi:10.3109/02699059309008177 PubMedCrossRef

25.

Lehmann A (1990) Derangements in cerebral osmohomeostasis: a common denominator for stimulation of taurine and phosphoethanolamine release. Prog Clin Biol Res 351:337–347PubMed

26.

Lehmann A, Carlstrom C, Nagelhus EA, Ottersen OP (1991) Elevation of taurine in hippocampal extracellular fluid and cerebrospinal fluid of acutely hypo-osmotic rats: contribution by influx from blood? J Neurochem 56:690–697. doi:10.1111/j.1471-4159.1991.tb08204.x PubMedCrossRef

27.

Meyerson BA, Linderoth B, Karlsson H, Ungerstedt U (1990) Microdialysis in the human brain: extracellular measurements in the thalamus of Parkinsonian patients. Life Sci 46:301–308. doi:10.1016/0024-3205(90)90037-R PubMedCrossRef

28.

Nagelhus EA, Amiry-Moghaddam M, Lehmann A, Ottersen OP (1994) Taurine as an organic osmolyte in the intact brain: immunocytochemical and biochemical studies. Adv Exp Med Biol 359:325–334PubMed

29.

O'Kane RL, Hawkins RA (2003) Na + -dependent transport of large neutral amino acids occurs at the abluminal membrane of the blood-brain barrier. Am J Physiol Endocrinol Metab 285:E1167–E1173PubMed

30.

O'Kane RL, Vina JR, Simpson I, Hawkins RA (2004) Na + -dependent neutral amino acid transporters A, ASC, and N of the blood-brain barrier: mechanisms for neutral amino acid removal. Am J Physiol Endocrinol Metab 287:E622–E629. doi:10.1152/ajpendo.00187.2004 PubMedCrossRef

31.

Ori C, Cavallini L, Freo U, Ruggero S, Ermani M, Pizzolato G, Dam M (1997) The effects of propofol on cerebral high energy metabolites, lactate, and glucose in normoxic and severely hypoxic rats. Life Sci 60:1349–1357. doi:10.1016/S0024-3205(97)00080-5 PubMedCrossRef

32.

Raivich G, Bohatschek M, Kloss CU, Werner A, Jones LL, Kreutzberg GW (1999) Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res Brain Res Rev 30:77–105. doi:10.1016/S0165-0173(99)00007-7 PubMedCrossRef

33.

Ronne Engstrom E, Hillered L, Enblad P, Karlsson T (2005) Cerebral interstitial levels of glutamate and glutamine after intravenous administration of nutritional amino acids in neurointensive care patients. Neurosci Lett 384:7–10. doi:10.1016/j.neulet.2005.04.030 PubMedCrossRef

34.

Ronne-Engstrom E, Cesarini KG, Enblad P, Hesselager G, Marklund N, Nilsson P, Salci K, Persson L, Hillered L (2001) Intracerebral microdialysis in neurointensive care: the use of urea as an endogenous reference compound. J Neurosurg 94:397–402PubMedCrossRef

35.

Ronne-Engstrom E, Hillered L, Flink R, Spannare B, Ungerstedt U, Carlson H (1992) Intracerebral microdialysis of extracellular amino acids in the human epileptic focus. J Cereb Blood Flow Metab 12:873–876PubMed

36.

Runnerstam M, von Essen C, Nystrom B, Rosengren L, Hamberger A (1997) Extracellular glial fibrillary acidic protein and amino acids in brain regions of patients with subarachnoid haemorrhage—correlation with level of consciousness and site of bleeding. Neurol Res 19:361–368PubMed

37.

Ryttlefors M, Howells T, Nilsson P, Ronne-Engstrom E, Enblad P (2007) Secondary insults in subarachnoid haemorrhage: occurrence and impact on outcome and clinical deterioration. Neurosurgery 61:704–714. doi:10.1227/01.NEU.0000298898.38979.E3 discussion 714–705PubMedCrossRef

38.

Samuelsson C, Hillered L, Zetterling M, Enblad P, Hesselager G, Ryttlefors M, Kumlien E, Lewen A, Marklund N, Nilsson P, Salci K, Ronne-Engstrom E (2007) Cerebral glutamine and glutamate levels in relation to compromised energy metabolism: a microdialysis study in subarachnoid haemorrhage patients. J Cereb Blood Flow Metab

39.

Sarrafzadeh A, Haux D, Sakowitz O, Benndorf G, Herzog H, Kuechler I, Unterberg A (2003) Acute focal neurological deficits in aneurysmal subarachnoid haemorrhage: relation of clinical course, CT findings, and metabolite abnormalities monitored with bedside microdialysis. Stroke 34:1382–1388. doi:10.1161/01.STR.0000074036.97859.02 PubMedCrossRef

40.

Sarrafzadeh AS, Sakowitz OW, Kiening KL, Benndorf G, Lanksch WR, Unterberg AW (2002) Bedside microdialysis: a tool to monitor cerebral metabolism in subarachnoid haemorrhage patients? Crit Care Med 30:1062–1070. doi:10.1097/00003246-200205000-00018 PubMedCrossRef

41.

Schulz MK, Wang LP, Tange M, Bjerre P (2000) Cerebral microdialysis monitoring: determination of normal and ischaemic cerebral metabolisms in patients with aneurysmal subarachnoid haemorrhage. J Neurosurg 93:808–814PubMedCrossRef

42.

Skjoth-Rasmussen J, Schulz M, Kristensen SR, Bjerre P (2004) Delayed neurological deficits detected by an ischaemic pattern in the extracellular cerebral metabolites in patients with aneurysmal subarachnoid haemorrhage. J Neurosurg 100:8–15PubMedCrossRef

43.

Starmark JE, Stalhammar D, Holmgren E (1988) The Reaction Level Scale (RLS85). Manual and guidelines. Acta Neurochir (Wien) 91:12–20. doi:10.1007/BF01400521 CrossRef

44.

Staub F, Graf R, Gabel P, Kochling M, Klug N, Heiss WD (2000) Multiple interstitial substances measured by microdialysis in patients with subarachnoid haemorrhage. Neurosurgery 47:1106–1115. doi:10.1097/00006123-200011000-00016 discussion 1115–1106PubMedCrossRef

45.

Vespa P, Bergsneider M, Hattori N, Wu HM, Huang SC, Martin NA, Glenn TC, McArthur DL, Hovda DA (2005) Metabolic crisis without brain ischaemia is common after traumatic brain injury: a combined microdialysis and positron emission tomography study. J Cereb Blood Flow Metab 25:763–774. doi:10.1038/sj.jcbfm.9600073 PubMedCrossRef

46.

Vespa PM, O'Phelan K, McArthur D, Miller C, Eliseo M, Hirt D, Glenn T, Hovda DA (2007) Pericontusional brain tissue exhibits persistent elevation of lactate/pyruvate ratio independent of cerebral perfusion pressure. Crit Care Med 35:1153–1160. doi:10.1097/01.CCM.0000259466.66310.4F PubMedCrossRef

47.

von Holst H, Hagenfeldt L (1985) Increased levels of amino acids in human lumbar and central cerebrospinal fluid after subarachnoid haemorrhage. Acta Neurochir (Wien) 78:46–56. doi:10.1007/BF01809241 CrossRef

Title: Temporal patterns of interstitial pyruvate and amino acids after subarachnoid haemorrhage are related to the level of consciousness—a clinical microdialysis study
Authors: Maria Zetterling
Lars Hillered
Carolina Samuelsson
Torbjörn Karlsson
Per Enblad
Elisabeth Ronne-Engström
Publication date: 01-07-2009
Publisher: Springer Vienna
Published in: Acta Neurochirurgica / Issue 7/2009
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-009-0384-4

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Temporal patterns of interstitial pyruvate and amino acids after subarachnoid haemorrhage are related to the level of consciousness—a clinical microdialysis study

Abstract

Background

Method

Findings

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Method

Findings

Conclusions

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