Lack of utility of arteriojugular venous differences of lactate as a reliable indicator of increased brain anaerobic metabolism in traumatic brain injury

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Object

Ischemic lesions are highly prevalent in patients with traumatic brain injuries (TBIs) and are the single most important cause of secondary brain damage. The prevention and early treatment of these lesions is the primary aim in the modern treatment of these patients. One of the most widely used monitoring techniques at the bedside is quantification of brain extracellular level of lactate by using arteriojugular venous differences of lactate (AVDL). The purpose of this study was to determine the sensitivity, specificity, and predictive value of AVDL as an indicator of increases in brain lactate production in patients with TBIs.

Methods

Arteriojugular venous differences of lactate were calculated every 6 hours using samples obtained though a catheter placed in the jugular bulb in 45 patients with diffuse head injuries (57.8%) or evacuated brain lesions (42.2%). Cerebral lactate concentration obtained with a 20-kD microdialysis catheter implanted in undamaged tissue was used as the de facto gold standard.

Six hundred seventy-three AVDL determinations and cerebral microdialysis samples were obtained simultaneously; 543 microdialysis samples (81%) showed lactate values greater than 2 mmol/L, but only 21 AVDL determinations (3.1%) showed an increase in brain lactate. No correlation was found between AVDL and cerebral lactate concentration (ρ = 0.014, p = 0.719). Arteriojugular venous differences of lactate had a sensitivity and specificity of 3.3 and 97.7%, respectively, with a false-negative rate of 96.7% and a false-positive rate of 2.3%.

Conclusions

Arteriojugular venous differences of lactate do not reliably reflect increased cerebral lactate production and consequently are not reliable in ruling out brain ischemia in patients with TBIs. The clinical use of this monitoring method in neurocritical care should be reconsidered.

Abbreviations used in this paper: AVDL = arteriojugular venous differences of lactate; AVDO2 = AVD of O2; BBB = blood–brain barrier; CBF = cerebral blood flow; CI = confidence interval; CT = computed tomography; GCS = Glasgow Coma Scale; ICP = intracranial pressure; ICU = intensive care unit; LOI = lactate-O2 index; SaO2 = arterial O2 saturation; SjO2 = jugular O2 saturation; TBI = traumatic brain injury.

Article Information

Address reprint requests to: Juan Sahuquillo, M.D., Ph.D., Department of Neurosurgery, Vall d'Hebron University Hospital, Paseo Vall d'Hebron 119-129, 08035 Barcelona, Spain. email: sahuquillo@neurotrauma.net.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Computed tomography scans obtained in a patient with an evacuated left frontal contusion. An intraparenchymatous ICP sensor was inserted into the left hemisphere; brain tissue PO2 and microdialysis catheters were inserted in the right hemisphere. The arrows show the location of the microdialysis catheter, into which a small quantity of air was injected before removal.

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    Box-and-whisker plot showing the distribution of normal values of AVDL (values obtained from Gibbs et al.).

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    Scatterplot demonstrating a nonsignificant correlation between AVDL values and brain lactate values obtained by cerebral microdialysis.

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    Scatterplot showing a nonsignficant correlation between LOI values and brain lactate values obtained by cerebral microdialysis.

References

1

Ames A III: CNS energy metabolism as related to function. Brain Res Rev 34:42682000

2

Anonymous: The Brain Trauma Foundation. The American Association of Neurological Surgeons The Joint Section on Neurotrauma Critical Care Management and prognosis of severe traumatic brain injury Part 1: guidelines for the management of severe traumatic brain injury. J Neurotrauma 17:4576272000

3

Artru FDailler FBurel EBodonian CGrousson SConvert J: Assessment of jugular blood oxygen and lactate indices for detection of cerebral ischemia and prognosis. J Neurosurg Anesthesiol 16:2262312004

4

Bakker EPvan Dam K: The movement of monocarboxylic acids across phospholipid membranes: evidence for an exchange diffusion between pyruvate and other monocarboxylate ions. Biochim Biophys Acta 339:2852891974

5

Chen TQian YZDi XRice AZhu JPBullock R: Lactate/glucose dynamics after rat fluid percussion brain injury. J Neurotrauma 17:1351422000

6

Chen TQian YZDi XZhu JPBullock R: Evidence for lactate uptake after rat fluid percussion brain injury. Acta Neurochir Suppl76:3593642000

7

Crockard HATaylor AR: Serial CSF lactate-pyruvate values as a guide to prognosis in head injury coma. Eur Neurol 8:1511571972

8

Cruz JZager ELSchnee CLGennarelli TAHoffstad OJ: Failure of jugular lactate determinations to disclose cerebral ischemia in posttraumatic cerebral infarction: case report. J Trauma 35:8058071993

9

Fellows LKBoutelle MGFillenz M: Physiological stimulation increases nonoxidative glucose metabolism in the brain of the freely moving rat. J Neurochem 60:125812631993

10

Gibbs ELLennox WGNims LFGibbs FA: Arterial and cerebral venous blood arterial-venous differences in man. J Biol Chem 144:3253321942

11

Graham DIFord DIAdams JHDoyle DTeasdale GMLawrence AE: Ischaemic brain damage is still common in fatal non-missile head injury. J Neurol Neurosurg Psychiatry 52:3463501989

12

Hillered LPersson LMicrodialysis for neurochemical monitoring in the human brain injury. Tsubokawa TMarmarou ARobertson CTeasdale G: Neurochemical Monitoring in the Intensive Care Unit. Microdialysis Jugular Venous Oximetry and Near-Infrared Spectroscopy TokyoSpringer-Verlag1995. 5963

13

Hillered LPersson LPonten UUngerstedt U: Neurometabolic monitoring of the ischaemic human brain using microdialysis. Acta Neurochir (Wien) 102:91971990

14

Hutchinson PJO'Connell MTAl-Rawi PGMaskell LBKett-White RGupta AK: Clinical cerebral microdialysis: a methodological study. J Neurosurg 93:37432000

15

Hutchinson PJO'Connell MTMaskell LBPickard JD: Monitoring by subcutaneous microdialysis in neurosurgical intensive care. Acta Neurochir Suppl75:57591999

16

Ide KSchmalbruch IKQuistorff BHorn ASecher NH: Lactate, glucose and O2 uptake in human brain during recovery from maximal exercise. J Physiol 522:1591642000

17

Johnston AJGupta AK: Advanced monitoring in the neurology intensive care unit: microdialysis. Curr Opin Crit Care 8:1211272002

18

Kett-White RHutchinson PJCzosnyka MBoniface SPickard JDKirkpatrick PJ: Multi-modal monitoring of acute brain injury. Adv Tech Stand Neurosurg 27:871342002

19

Langemann HAlessandri BMendelowitsch AFeuerstein TLandolt HGratzl O: Extracellular levels of glucose and lactate measured by quantitative microdialysis in the human brain. Neurol Res 23:5315362001

20

Larrabee MG: Lactate metabolism and its effects on glucose metabolism in an excised neural tissue. J Neurochem 64:173417411995

21

Lutz PLNilsson GE: The Brain Without Oxygen Austin, TexasLandes Bioscience1997. 1207

22

Magistretti PJPellerin L: Astrocytes couple synaptic activity to glucose utilization in the brain. News Physiol Sci 14:1771821999

23

Magistretti PJPellerin L: The cellular bases of functional brain imaging: evidence for astrocyte-neuron metabolic coupling. The Neuroscientist 3:3613651997

24

Marshall LFMarshall SBKlauber MRVan Berkum Clark MEisenberg HMJane JA: A new classification of head injury based on computerized tomography. J Neurosurg 75:SupplS14S201991

25

Miller JD: Head injury and brain ischaemia—implications for therapy. Br J Anaesth 57:1201301985

26

Munar FFerrer AMde Nadal MPoca MAPedraza SSahuquillo J: Cerebral hemodynamic effects of 7.2% hypertonic saline in patients with head injury and raised intracranial pressure. J Neurotrauma 17:41512000

27

Murr RStummer WSchurer LPolasek J: Cerebral lactate production in relation to intracranial pressure, cranial computed tomography findings, and outcome in patients with severe head injury. Acta Neurochir (Wien) 138:9289371996

28

Nemoto EMHoff JTSeveringhaus JW: Lactate uptake and metabolism by brain during hyperlactatemia and hypoglycemia. Stroke 5:48531974

29

Oldendorf WH: Brain uptake of metabolites and drugs following carotid arterial injections. Trans Am Neurol Assoc 96:46501971

30

Oldendorf WH: Carrier-mediated blood-brain barrier transport of short-chain monocarboxylic organic acids. Am J Physiol 224:145014531973

31

Pardridge WMConnor JDCrawford IL: Permeability changes in the blood-brain barrier: causes and consequences. CRC Crit Rev Toxicol 3:1591991975

32

Pardridge WMOldendorf WH: Transport of metabolic substrates through the blood-brain barrier. J Neurochem 28:5121977

33

Pellerin L: Lactate as a pivotal element in neuron-glia metabolic cooperation. Neurochem Int 43:3313382003

34

Pellerin LPellegri GBittar PGCharnay YBouras CMartin JL: Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev Neurosci 20:2912991998

35

Poca MASahuquillo JVilalta ADe los Rios JRobles AExposito L: Percutaneous implantation of cerebral microdialysis catheters by twist-drill craniostomy in neurocritical patients: description of the technique and results of a feasibility study in 97 patients. J Neurotrauma 23:151015172006

36

Poole RCHalestrap AP: Transport of lactate and other monocarboxylates across mammalian plasma membranes. Am J Physiol 264:C761C7821993

37

Prasad MRRamaiah CMcIntosh TKDempsey RJHipkens SYurek D: Regional levels of lactate and norepinephrine after experimental brain injury. J Neurochem 63:108610941994

38

Price NTJackson VNHalestrap AP: Cloning and sequencing of four new mammalian monocarboxylate transporter (MCT) homologues confirms the existence of a transporter family with an ancient past. Biochem J 329:3213281998

39

Reinstrup PStahl NMellergard PUski TUngerstedt UNordstrom CH: Intracerebral microdialysis in clinical practice: baseline values for chemical markers during wakefulness, anesthesia, and neurosurgery. Neurosurgery 47:7017102000

40

Robertson CSAnaerobic metabolism within the brain: its relationship to brain failure in head-injuried patients. Bihari DHoladay JW: Update in Intensive Care and Emergency Medicine 9. Brain Failure BerlinSpringer-Verlag1989. 85102

41

Robertson CSGopinath SPUzura MValadka ABGoodman JC: Metabolic changes in the brain during transient ischemia measured with microdialysis. Neurol Res 20:1 SupplS91S941998

42

Robertson CSGrossman RGGoodman JCNarayan RK: The predictive value of cerebral anaerobic metabolism with cerebral infarction after head injury. J Neurosurg 67:3613681987

43

Robertson CSNarayan RKGokaslan ZLPahwa RGrossman RGCaram P Jr: Cerebral arteriovenous oxygen difference as an estimate of cerebral blood flow in comatose patients. J Neurosurg 70:2222301989

44

Sahuquillo JBiestro AMena MPAmoros SLung MPoca MA: [First tier measures in the treatment of intracranial hypertension in the patient with severe craniocerebral trauma. Proposal and justification of a protocol.]. Neurocirugia 13:781002002. (Spanish)

45

Sahuquillo JPoca MAArribas MGarnacho ARubio E: Interhemispheric supratentorial intracranial pressure gradients in head-injured patients: are they clinically important?. J Neurosurg 90:16261999

46

Sahuquillo JPoca MAGarnacho ARobles ACoello FGodet C: Early ischaemia after severe head injury. Preliminary results in patients with diffuse brain injuries. Acta Neurochir (Wien) 122:2042141993

47

Sappey-Marinier DCalabrese GFein GHugg JWBiggins CWeiner MW: Effect of photic stimulation on human visual cortex lactate and phosphates using 1H and 31P magnetic resonance spectroscopy. J Cereb Blood Flow Metab 12:5845921992

48

Sarrafzadeh ASSakowitz OWLanksch WRUnterberg AW: Time course of various interstitial metabolites following subarachnoid hemorrhage studied by on-line microdialysis. Acta Neurochir Suppl77:1451472001

49

Schurr AWest CARigor BM: Lactate-supported synaptic function in the rat hippocampal slice preparation. Science 240:132613281988

50

Sood SCGulati SCKumar MKak VK: Cerebral metabolism following brain injury. II. Lactic acid changes. Acta Neurochir (Wien) 53:47511980

51

Tofteng FLarsen FS: Monitoring extracellular concentrations of lactate, glutamate, and glycerol by in vivo microdialysis in the brain during liver transplantation in acute liver failure. Liver Transpl 8:3023052002

52

Ungerstedt U: Microdialysis—principles and applications for studies in animals and man. J Intern Med 230:3653731991

53

Ungerstedt UBellander BMNordstrom C: Microdialysis in Neuromonitoring: Principles Procedures and Interpretations 2000. (http://www.microdialysis.se/pdffiler/mdbook.pdf) [Accessed 10 January 2007]

54

Valadka ABFuruya YHlatky RRobertson CS: Global and regional techniques for monitoring cerebral oxidative metabolism after severe traumatic brain injury. Neurosurg Focus 9:E32000

55

Vespa PBergsneider MHattori TWu HMHuang SCMartin NA: Metabolic crisis without brain ischemia is common after traumatic brain injury: a combined microdialysis and positron emission tomography study. J Cereb Blood Flow Metab 25:7637742005

56

Vespa PMMcArthur DO'Phelan KGlenn TEtchepare MKelly D: Persistently low extracellular glucose correlates with poor outcome 6 months after human traumatic brain injury despite a lack of increased lactate: a microdialysis study. J Cereb Blood Flow Metab 23:8658772003

57

Weibel ER: The Pathway for Oxygen. Structure and Function in the Mammalian Respiratory System Cambridge, MAHarvard University Press1984

58

Yang MSDeWitt DSBecker DPHayes RL: Regional brain metabolite levels following mild experimental head injury in the cat. J Neurosurg 63:6176211985

59

Zauner ADoppenberg EMWoodward JJChoi SCYoung HFBullock R: Continuous monitoring of cerebral substrate delivery and clearance: initial experience in 24 patients with severe acute brain injuries. Neurosurgery 41:108210931997

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