Effect of perfluorocarbons on brain oxygenation and ischemic damage in an acute subdural hematoma model in rats

Restricted access

Object. This study was conducted to determine whether perfluorocarbons (PFCs) improve brain oxygenation and reduce ischemic brain damage in an acute subdural hematoma (SDH) model in rats.

Methods. Forty adult male Sprague—Dawley rats were allocated to four groups: 1) controls, acute SDH treated with saline and 30% O2; 2) 30-PFC group, acute SDH treated with PFC infusion in 30% O2; 3) 100-O2 group, acute SDH treated with 100% O2; and 4) 100-PFC group, acute SDH treated with PFC plus 100% O2. Ten minutes after the induction of acute SDH, a single dose of PFC was infused and 30% or 100% O2 was administered simultaneously. Four hours later, half of the rats were killed by perfusion for histological study to assess the extent of ischemic brain damage. The other half were used to measure brain tissue oxygen tension (PO2). The volume of ischemic brain damage was 162.4 ± 7.6 mm3 in controls, 165.3 ± 11.3 mm3 in the 30-PFC group, 153.4 ± 17.3 mm3 in the 100-O2 group, and 95.9 ± 12.8 mm3 in the 100-PFC group (41% reduction compared with controls, p = 0.002). Baseline brain tissue PO2 values were approximately 20 mm Hg, and after induction of acute SDH, PO2 rapidly decreased and remained at 1 to 2 mm Hg. Treatment with either PFC or 100% O2 improved brain tissue PO2, with final values of 5.14 and 7.02 mm Hg, respectively. Infusion of PFC with 100% O2 improved brain tissue PO2 the most, with a final value of 15.16 mm Hg.

Conclusions. Data from the current study demonstrated that PFC infusion along with 100% O2 can significantly improve brain oxygenation and reduce ischemic brain damage in acute SDH.

Article Information

Address reprint requests to: M. Ross Bullock, M.D., Ph.D., Department of Neurosurgery, Virginia Commonwealth University Health System, P.O. Box 980631, Richmond, Virginia 23290–0631. email: robulloc@hsc.vcu.edu.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Bar graph showing a comparison of the volume of ischemic brain damage among four treatment groups (five animals per group). Treatment with both PFC emulsion and 100% O2 significantly reduced the amount of ischemic damage when compared with that in control animals (41% reduction; p = 0.002). Values are expressed as the means ± SEM.

  • View in gallery

    Graph depicting areas of ischemic damage at the eight predetermined stereotactic planes expressed as a percentage of the total hemispheric area. Significant reduction in the area of ischemic damage was observed in the group treated with PFC emulsion combined with 100% O2, mainly in the frontal region of the forebrain.

  • View in gallery

    Graph illustrating the results of brain tissue PO2. Baseline brain tissue PO2 values in all four groups were approximately 20 mm Hg. After the induction of SDH, these values rapidly decreased to 1 to 2 mm Hg and remained less than 2 mm Hg. In the treated groups, however, as PFC infusion and/or 100% O2 administration was performed 10 minutes after hematoma induction, the decreased PO2 values increased to the final values of 5.14 mm Hg for the PFC plus 30% O2 group, 7.02 mm Hg for the 100% O2 group, and 15.16 mm Hg for the PFC plus 100% O2 group. The differences in the PO2 values among the four groups were statistically significant (ANOVA, p < 0.05). When compared with the control group, the marked increases in the PFC plus 100% O2 group were statistically significant at all measured time points (t-test, *p < 0.05). #p < 0.05 (t-test) compared with controls. Tx = treatment.

References

  • 1.

    Adams JHGraham DIGennarelli TA: Head injury in man and experimental animals: neuropathology. Acta Neurochir Suppl 32:15301983Adams JH Graham DI Gennarelli TA: Head injury in man and experimental animals: neuropathology. Acta Neurochir Suppl 32:15–30 1983

  • 2.

    Agardh CDZhang HSmith MLSiesjo BK: Free radical production and ischemic brain damage: influence of postischemic oxygen tension. Int J Dev Neurosci 9:1271381991Agardh CD Zhang H Smith ML Siesjo BK: Free radical production and ischemic brain damage: influence of postischemic oxygen tension. Int J Dev Neurosci 9:127–138 1991

  • 3.

    Biro GP: Perfluorocarbon-based red blood cell substitutes. Transfus Med Rev 7:84951993Biro GP: Perfluorocarbon-based red blood cell substitutes. Transfus Med Rev 7:84–95 1993

  • 4.

    Bruzzone PDionigi RBellinzona GImberti RStocchetti N: Effects of cerebral perfusion pressure on brain tissue PO2 in patients with severe head injury. Acta Neurochir Suppl (Wien) 71:1111131998Bruzzone P Dionigi R Bellinzona G Imberti R Stocchetti N: Effects of cerebral perfusion pressure on brain tissue PO2 in patients with severe head injury. Acta Neurochir Suppl (Wien) 71:111–113 1998

  • 5.

    Bullock MR: Hyperoxia: good or bad? J Neurosurg 98:9439442003Bullock MR: Hyperoxia: good or bad? J Neurosurg 98:943–944 2003

  • 6.

    Bullock RButcher SMcCulloch J: Changes in extracellular glutamate concentration after acute subdural haematoma in the rat—evidence for an “excitotoxic” mechanism? Acta Neurochir Suppl (Wien) 51:2742761990Bullock R Butcher S McCulloch J: Changes in extracellular glutamate concentration after acute subdural haematoma in the rat—evidence for an “excitotoxic” mechanism? Acta Neurochir Suppl (Wien) 51:274–276 1990

  • 7.

    Bullock RButcher SPChen MHKendall LMcCulloch J: Correlation of the extracellular glutamate concentration with extent of blood flow reduction after subdural hematoma in the rat. J Neurosurg 74:7948021991Bullock R Butcher SP Chen MH Kendall L McCulloch J: Correlation of the extracellular glutamate concentration with extent of blood flow reduction after subdural hematoma in the rat. J Neurosurg 74:794–802 1991

  • 8.

    Burger RVince GHMeixensberger JBendszus MRoosen K: Interrelations of laser doppler flowmetry and brain tissue oxygen pressure during ischemia and reperfusion induced by an experimental mass lesion. J Neurotrauma 16:114911641999Burger R Vince GH Meixensberger J Bendszus M Roosen K: Interrelations of laser doppler flowmetry and brain tissue oxygen pressure during ischemia and reperfusion induced by an experimental mass lesion. J Neurotrauma 16:1149–1164 1999

  • 9.

    Chance BOshimo NSugamo TMayersky A: Basic principles of tissue oxygen determination from mitochondrial signals in Bicher HIBruley DF (eds): Oxygen Transport to Tissue. New York: Plenum1973 pp 277292Chance B Oshimo N Sugamo T Mayersky A: Basic principles of tissue oxygen determination from mitochondrial signals in Bicher HI Bruley DF (eds): Oxygen Transport to Tissue. New York: Plenum 1973 pp 277–292

  • 10.

    Charbel FTHoffman WEMisra MHannigan KAusman JI: Cerebral interstitial tissue oxygen tension, pH, HCO3, CO2. Surg Neurol 48:4144171997Charbel FT Hoffman WE Misra M Hannigan K Ausman JI: Cerebral interstitial tissue oxygen tension pH HCO3 CO2. Surg Neurol 48:414–417 1997

  • 11.

    Di XBullock R: Effect of the novel high-affinity glysine-site N-methyl-D-aspartate antagonist ACEA-1021 on 125I-MK-801 binding after subdural hematoma in the rat: an in vivo autoradiographic study. J Neurosurg 85:6556611996Di X Bullock R: Effect of the novel high-affinity glysine-site N-methyl-D-aspartate antagonist ACEA-1021 on 125I-MK-801 binding after subdural hematoma in the rat: an in vivo autoradiographic study. J Neurosurg 85:655–661 1996

  • 12.

    Dings JMeixensberger JAmschler JHamelbeck BRoosen K: Brain tissue pO2 in relation to cerebral perfusion pressure, TCD findings and TCD-CO2-reactivity after severe head injury. Acta Neurochir (Wien) 138:4254341996Dings J Meixensberger J Amschler J Hamelbeck B Roosen K: Brain tissue pO2 in relation to cerebral perfusion pressure TCD findings and TCD-CO2-reactivity after severe head injury. Acta Neurochir (Wien) 138:425–434 1996

  • 13.

    Dings JMeixensberger JJager ARoosen K: Clinical experience with 118 brain tissue oxygen partial pressure catheter probes. Neurosurgery 43:108210951998Dings J Meixensberger J Jager A Roosen K: Clinical experience with 118 brain tissue oxygen partial pressure catheter probes. Neurosurgery 43:1082–1095 1998

  • 14.

    Doppenberg EMRice MRAlessandri BQian YDi XBullock R: Reducing hemoglobin oxygen affinity does not increase hydroxyl radicals after acute subdural hematoma in the rat. J Neurotrauma 16:1231331999Doppenberg EM Rice MR Alessandri B Qian Y Di X Bullock R: Reducing hemoglobin oxygen affinity does not increase hydroxyl radicals after acute subdural hematoma in the rat. J Neurotrauma 16:123–133 1999

  • 15.

    Doppenberg EMRZauner ABullock RWard JDFatouros PPYoung HF: Correlations between brain tissue oxygen tension, carbon dioxide tension, pH, and cerebral blood flow—a better way of monitoring the severely injured brain? Surg Neurol 49:6506541998Doppenberg EMR Zauner A Bullock R Ward JD Fatouros PP Young HF: Correlations between brain tissue oxygen tension carbon dioxide tension pH and cerebral blood flow—a better way of monitoring the severely injured brain? Surg Neurol 49:650–654 1998

  • 16.

    Duhaime ACGennarelli LMBoardman C: Neuroprotection by dextromethorphan in acute experimental subdural hematoma in the rat. J Neurotrauma 13:79841996Duhaime AC Gennarelli LM Boardman C: Neuroprotection by dextromethorphan in acute experimental subdural hematoma in the rat. J Neurotrauma 13:79–84 1996

  • 17.

    Duhaime ACGennarelli LMYachnis A: Acute subdural hematoma: is the blood itself toxic? J Neurotrauma 11:6696781994Duhaime AC Gennarelli LM Yachnis A: Acute subdural hematoma: is the blood itself toxic? J Neurotrauma 11:669–678 1994

  • 18.

    Fujisawa HMaxwell WLGraham DITeasdale GMBullock R: Focal microvascular occlusion after acute subdural haematoma in the rat: a mechanism for ischaemic damage and brain swelling? Acta Neurochir Suppl (Wien) 60:1931961994Fujisawa H Maxwell WL Graham DI Teasdale GM Bullock R: Focal microvascular occlusion after acute subdural haematoma in the rat: a mechanism for ischaemic damage and brain swelling? Acta Neurochir Suppl (Wien) 60:193–196 1994

  • 19.

    Gennarelli TASpielman GMLangfitt TWGildenberg PLHarrington TJane JAet al: Influence of the type of intracranial lesion on outcome from severe head injury. J Neurosurg 56:26321982Gennarelli TA Spielman GM Langfitt TW Gildenberg PL Harrington T Jane JA et al: Influence of the type of intracranial lesion on outcome from severe head injury. J Neurosurg 56:26–32 1982

  • 20.

    Geyer RP: Perfluorochemicals as oxygen transport vehicles. Biomater Artif Cells Artif Organs 16:31491988Geyer RP: Perfluorochemicals as oxygen transport vehicles. Biomater Artif Cells Artif Organs 16:31–49 1988

  • 21.

    Graham DIAdams JHDoyle D: Ischaemic brain damage in fatal non-missile head injuries. J Neurol Sci 39:2132341978Graham DI Adams JH Doyle D: Ischaemic brain damage in fatal non-missile head injuries. J Neurol Sci 39:213–234 1978

  • 22.

    Haitsma IKMaas AI: Advanced monitoring in the intensive care unit: brain tissue oxygen tension. Curr Opin Crit Care 8:1151202002Haitsma IK Maas AI: Advanced monitoring in the intensive care unit: brain tissue oxygen tension. Curr Opin Crit Care 8:115–120 2002

  • 23.

    Hoffman WECharbel FTEdelman G: Brain tissue oxygen, carbon dioxide, and pH in neurosurgical patients at risk for ischemia. Anesth Analg 82:5825861996Hoffman WE Charbel FT Edelman G: Brain tissue oxygen carbon dioxide and pH in neurosurgical patients at risk for ischemia. Anesth Analg 82:582–586 1996

  • 24.

    Kiening KLHartl RUnterberg AWSchneider GHBardt TLanksch WR: Brain tissue pO2-monitoring in comatose patients: implications for therapy. Neurol Res 19:2332401997Kiening KL Hartl R Unterberg AW Schneider GH Bardt T Lanksch WR: Brain tissue pO2-monitoring in comatose patients: implications for therapy. Neurol Res 19:233–240 1997

  • 25.

    Kiening KLSchneider GHBardt TFUnterberg AWLanksch WR: Bifrontal measurements of brain tissue-PO2 in comatose patients. Acta Neurochir Suppl (Wien) 71:1721731998Kiening KL Schneider GH Bardt TF Unterberg AW Lanksch WR: Bifrontal measurements of brain tissue-PO2 in comatose patients. Acta Neurochir Suppl (Wien) 71:172–173 1998

  • 26.

    Kiening KLUnterberg AWBardt TFSchneider GHLanksch WR: Monitoring of cerebral oxygenation in patients with severe head injuries: brain tissue PO2 versus jugular vein oxygen saturation. J Neurosurg 85:7517571996Kiening KL Unterberg AW Bardt TF Schneider GH Lanksch WR: Monitoring of cerebral oxygenation in patients with severe head injuries: brain tissue PO2 versus jugular vein oxygen saturation. J Neurosurg 85:751–757 1996

  • 27.

    König JFRKlippel RA: The Rat Brain: A Stereotactic Atlas of the Forebrain and Lower Parts of the Brainstem. Baltimore: Williams & Wilkins1963König JFR Klippel RA: The Rat Brain: A Stereotactic Atlas of the Forebrain and Lower Parts of the Brainstem. Baltimore: Williams & Wilkins 1963

  • 28.

    Kuroda YBullock R: Failure of cerebral blood flow-metabolism coupling after acute subdural hematoma in the rat. Neurosurgery 31:106210711992Kuroda Y Bullock R: Failure of cerebral blood flow-metabolism coupling after acute subdural hematoma in the rat. Neurosurgery 31:1062–1071 1992

  • 29.

    Kuschinsky WPaulson OB: Capillary circulation in the brain. Cerebrovasc Brain Metab Rev 4:2612861992Kuschinsky W Paulson OB: Capillary circulation in the brain. Cerebrovasc Brain Metab Rev 4:261–286 1992

  • 30.

    Kwon THChao DLMalloy KSun DAlessandri BBullock MR: Tempol, a novel stable nitroxide, reduces brain damage and free radical production, after acute subdural hematoma in the rat. J Neurotrauma 20:3373452003Kwon TH Chao DL Malloy K Sun D Alessandri B Bullock MR: Tempol a novel stable nitroxide reduces brain damage and free radical production after acute subdural hematoma in the rat. J Neurotrauma 20:337–345 2003

  • 31.

    Maxwell WLIrvine AAdams JHGraham DIGennarelli TA: Response of cerebral microvasculature to brain injury. J Pathol 155:3273351988Maxwell WL Irvine A Adams JH Graham DI Gennarelli TA: Response of cerebral microvasculature to brain injury. J Pathol 155:327–335 1988

  • 32.

    Menzel MDoppenberg EMZauner ASoukup JReinert MMBullock R: Increased inspired oxygen concentration as a factor in improved brain tissue oxygenation and tissue lactate levels after severe human head injury. J Neurosurg 91:1101999Menzel M Doppenberg EM Zauner A Soukup J Reinert MM Bullock R: Increased inspired oxygen concentration as a factor in improved brain tissue oxygenation and tissue lactate levels after severe human head injury. J Neurosurg 91:1–10 1999

  • 33.

    Miller JDBullock RGraham DIChen MHTeasdale GM: Ischemic brain damage in a model of acute subdural hematoma. Neurosurgery 27:4334391990Miller JD Bullock R Graham DI Chen MH Teasdale GM: Ischemic brain damage in a model of acute subdural hematoma. Neurosurgery 27:433–439 1990

  • 34.

    Nair PKHellums JDOlson JS: Prediction of oxygen transport rates in blood flowing in large capillaries. Microvasc Res 38:2692851989Nair PK Hellums JD Olson JS: Prediction of oxygen transport rates in blood flowing in large capillaries. Microvasc Res 38:269–285 1989

  • 35.

    Nakajima SMeyer JSAmano TShaw TOkabe TMortel KF: Cerebral vasomotor responsiveness during 100% oxygen inhalation in cerebral ischemia. Arch Neurol 40:2712761983Nakajima S Meyer JS Amano T Shaw T Okabe T Mortel KF: Cerebral vasomotor responsiveness during 100% oxygen inhalation in cerebral ischemia. Arch Neurol 40:271–276 1983

  • 36.

    Osborne KAShigeno TBalarsky AMFord IMcCulloch JTeadale GMet al: Quantitative assessment of early brain damage in a rat model of focal cerebral ischaemia. J Neurol Neurosurg Psychiatry 50:4024101987Osborne KA Shigeno T Balarsky AM Ford I McCulloch J Teadale GM et al: Quantitative assessment of early brain damage in a rat model of focal cerebral ischaemia. J Neurol Neurosurg Psychiatry 50:402–410 1987

  • 37.

    Padnick LBLinsenmeier RAGoldstick TK: Perfluorocarbon emulsion improves oxygenation of the cat primary visual cortex. J Appl Physiol 86:149715041999Padnick LB Linsenmeier RA Goldstick TK: Perfluorocarbon emulsion improves oxygenation of the cat primary visual cortex. J Appl Physiol 86:1497–1504 1999

  • 38.

    Patel TRSchielke GPHoff JTKeep RFLorris Betz A: Comparison of cerebral blood flow and injury following intracerebral and subdural hematoma in the rat. Brain Res 829:1251331999Patel TR Schielke GP Hoff JT Keep RF Lorris Betz A: Comparison of cerebral blood flow and injury following intracerebral and subdural hematoma in the rat. Brain Res 829:125–133 1999

  • 39.

    Rockswold GLFord SEAnderson DCBergman TASherman RE: Results of a prospective randomized trial for treatment of severely brain-injured patients with hyperbaric oxygen. J Neurosurg 76:9299341992Rockswold GL Ford SE Anderson DC Bergman TA Sherman RE: Results of a prospective randomized trial for treatment of severely brain-injured patients with hyperbaric oxygen. J Neurosurg 76:929–934 1992

  • 40.

    Sakas DEStranjalis GWhittaker KWhitwell HL: Perfluorochemical oxygen carriers: potential uses in neurosciences. Cerebrovasc Brain Metab Rev 8:2092291996Sakas DE Stranjalis G Whittaker K Whitwell HL: Perfluorochemical oxygen carriers: potential uses in neurosciences. Cerebrovasc Brain Metab Rev 8:209–229 1996

  • 41.

    Sakas DEWhittaker KWCrowell RMZervas NT: Perfluorocarbons: recent developments and implications for neurosurgery. J Neurosurg 85:2482541996Sakas DE Whittaker KW Crowell RM Zervas NT: Perfluorocarbons: recent developments and implications for neurosurgery. J Neurosurg 85:248–254 1996

  • 42.

    Scheufler KMRohrborn HJZentner J: Does tissue oxygen-tension reliably reflect cerebral oxygen delivery and consumption? Anesth Analg 95:104210482002Scheufler KM Rohrborn HJ Zentner J: Does tissue oxygen-tension reliably reflect cerebral oxygen delivery and consumption? Anesth Analg 95:1042–1048 2002

  • 43.

    Sciamanna MALee CP: Ischemia/reperfusion-induced injury of forebrain mitochondria and protection by ascorbate. Arch Biochem Biophys 305:2152241993Sciamanna MA Lee CP: Ischemia/reperfusion-induced injury of forebrain mitochondria and protection by ascorbate. Arch Biochem Biophys 305:215–224 1993

  • 44.

    Seelig JMBecker DPMiller JDGreenberg RPWard JDChoi SC: Traumatic acute subdural hematoma: major mortality reduction in comatose patients treated within four hours. N Engl J Med 304:151115181981Seelig JM Becker DP Miller JD Greenberg RP Ward JD Choi SC: Traumatic acute subdural hematoma: major mortality reduction in comatose patients treated within four hours. N Engl J Med 304:1511–1518 1981

  • 45.

    Siesjo BKSiesjo P: Mechanisms of secondary brain injury. Eur J Anaesthesiol 13:2472681996Siesjo BK Siesjo P: Mechanisms of secondary brain injury. Eur J Anaesthesiol 13:247–268 1996

  • 46.

    Singhal ABDijkhuizen RMRosen BRLo EH: Normobaric hyperoxia reduces MRI diffusion abnormalities and infarct size in experimental stroke. Neurology 58:9459522002Singhal AB Dijkhuizen RM Rosen BR Lo EH: Normobaric hyperoxia reduces MRI diffusion abnormalities and infarct size in experimental stroke. Neurology 58:945–952 2002

  • 47.

    Singhal ABWang XSumii TMori TLo EH: Effects of normobaric hyperoxia in a rat model of focal cerebral ischemia-reperfusion. J Cereb Blood Flow Metab 22:8618682002Singhal AB Wang X Sumii T Mori T Lo EH: Effects of normobaric hyperoxia in a rat model of focal cerebral ischemia-reperfusion. J Cereb Blood Flow Metab 22:861–868 2002

  • 48.

    Stowell CPLevin JSpiess BDWinslow RM: Progress in the development of RBC substitutes. Transfusion 41:2872992001Stowell CP Levin J Spiess BD Winslow RM: Progress in the development of RBC substitutes. Transfusion 41:287–299 2001

  • 49.

    Sunami KTakeda YHashimoto MHirakawa M: Hyperbaric oxygen reduces infarct volume in rats by increasing oxygen supply to the ischemic periphery. Crit Care Med 28:283128362000Sunami K Takeda Y Hashimoto M Hirakawa M: Hyperbaric oxygen reduces infarct volume in rats by increasing oxygen supply to the ischemic periphery. Crit Care Med 28:2831–2836 2000

  • 50.

    Tajima ANakata HLin SZAcuff VFenstermacher J: Differences and similarities in albumin and red blood cell flows through cerebral microvessels. Am J Physiol 262:H1515H15241992Tajima A Nakata H Lin SZ Acuff V Fenstermacher J: Differences and similarities in albumin and red blood cell flows through cerebral microvessels. Am J Physiol 262:H1515–H1524 1992

  • 51.

    Theilen HSchrock HKuschinsky W: Gross persistence of capillary plasma perfusion after middle cerebral artery occlusion in the rat brain. J Cereb Blood Flow Metab 14:105510611994Theilen H Schrock H Kuschinsky W: Gross persistence of capillary plasma perfusion after middle cerebral artery occlusion in the rat brain. J Cereb Blood Flow Metab 14:1055–1061 1994

  • 52.

    Valadka ABGopinath SPContant CFUzura MRobertson CS: Relationship of brain tissue PO2 to outcome after severe head injury. Crit Care Med 26:157615811998Valadka AB Gopinath SP Contant CF Uzura M Robertson CS: Relationship of brain tissue PO2 to outcome after severe head injury. Crit Care Med 26:1576–1581 1998

  • 53.

    van den Brink WA: Experimental Closed Head Injury marginally impairs brain oxygenation, systemic parameters are of influence on brain oxygen values in van den Brink WA (ed): Head Injury from Man to Model. Delft, The Netherlands: Eburon2001 pp 145161van den Brink WA: Experimental Closed Head Injury marginally impairs brain oxygenation systemic parameters are of influence on brain oxygen values in van den Brink WA (ed): Head Injury from Man to Model. Delft The Netherlands: Eburon 2001 pp 145–161

  • 54.

    van den Brink WAvan Santbrink HAvezaat CJHogesteeger CJansen WKloos LMet al: Monitoring brain oxygen tension in severe head injury: the Rotterdam experience. Acta Neurochir Suppl (Wien) 71:1901941998van den Brink WA van Santbrink H Avezaat CJ Hogesteeger C Jansen W Kloos LM et al: Monitoring brain oxygen tension in severe head injury: the Rotterdam experience. Acta Neurochir Suppl (Wien) 71:190–194 1998

  • 55.

    van den Brink WAvan Santbrink HSteyerberg EWAvezaat CJSuazo JAHogesteeger Cet al: Brain oxygen tension in severe head injury. Neurosurgery 46:8688782000van den Brink WA van Santbrink H Steyerberg EW Avezaat CJ Suazo JA Hogesteeger C et al: Brain oxygen tension in severe head injury. Neurosurgery 46:868–878 2000

  • 56.

    van Santbrink HMaas AIAvezaat CJ: Continuous monitoring of partial pressure of brain tissue oxygen in patients with severe head injury. Neurosurgery 38:21311996van Santbrink H Maas AI Avezaat CJ: Continuous monitoring of partial pressure of brain tissue oxygen in patients with severe head injury. Neurosurgery 38:21–31 1996

  • 57.

    Vaz RSarmento ABorges NCruz CAzevedo I: Ultrastructural study of brain microvessels in patients with traumatic cerebral contusions. Acta Neurochir (Wien) 139:2152201997Vaz R Sarmento A Borges N Cruz C Azevedo I: Ultrastructural study of brain microvessels in patients with traumatic cerebral contusions. Acta Neurochir (Wien) 139:215–220 1997

  • 58.

    Watson NABeards SCAltaf NKassner AJackson A: The effect of hyperoxia on cerebral blood flow: a study in healthy volunteers using magnetic resonance phase-contrast angiography. Eur J Anaesthesiol 17:1521592000Watson NA Beards SC Altaf N Kassner A Jackson A: The effect of hyperoxia on cerebral blood flow: a study in healthy volunteers using magnetic resonance phase-contrast angiography. Eur J Anaesthesiol 17:152–159 2000

  • 59.

    Wilberger JE JrHarris MDiamond DL: Acute subdural hematoma: morbidity and mortality related to timing of operative intervention. J Trauma 30:7337361990Wilberger JE Jr Harris M Diamond DL: Acute subdural hematoma: morbidity and mortality related to timing of operative intervention. J Trauma 30:733–736 1990

  • 60.

    Zauner ADaugherty WPBullock MRWarner DS: Brain oxygenation and energy metabolism: part I—biological function and pathophysiology. Neurosurgery 51:2893022002Zauner A Daugherty WP Bullock MR Warner DS: Brain oxygenation and energy metabolism: part I—biological function and pathophysiology. Neurosurgery 51:289–302 2002

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 135 135 9
Full Text Views 175 175 2
PDF Downloads 108 108 0
EPUB Downloads 0 0 0

PubMed

Google Scholar