Abstract
Introduction: Brain tissue oxygen (PbrO2) monitoring is an emerging technique for detection of secondary brain injury in neurocritical care. Although it has been extensively reported in traumatic brain injury and aneurysmal subarachnoid hemorrhage, its use in nontraumatic intracerebral hemorrhage (ICH) has not been well described. We report complementary preliminary studies in a large animal model and in patients that demonstrate the feasibility of PbrO2 monitoring after ICH.
Methods: To assess early events after ICH, Licox Clark-type oxygen probes were inserted in the bilateral frontal white matter of four anesthetized swine that subsequently underwent right parietal hematoma formation in an experimental model of ICH. Intracranial pressure (ICP) was monitored as well. Seven patients with acute ICH, who were undergoing ICP monitoring as part of standard neurocritical care, had placement of a frontal oxygen probe, with subsequent monitoring for up to 7 days.
Results: In the swine ICH model, a rise in ICP early after hematoma formation was accompanied by a decrease in ipsilateral and contralateral PbrO2. Secondary increases in hematoma volume resulted in further decreases in PbrO2 over the first hour after ICH. In patients undergoing oxygen monitoring, low PbrO2 (<15 mmHg) was common. In these patients, changes in FiO2, mean arterial pressure, and cerebral perfusion pressure (but not ICP) predicted subsequent change in PbrO2.
Conclusion: Brain tissue oxygen monitoring is feasible in ICH patients, as well as in a swine model of ICH. Translational research that emphasizes complementary information derived from human and animal studies may yield additional insights not available from either alone.
Article PDF
Similar content being viewed by others
References
Meixensberger J, Jaeger M, Vath A, Dings J, Kunze E, Roosen K. Brain tissue oxygen guided treatment supplementing ICP/CPP therapy after traumatic brain injury. J Neurol Neurosurg Psychiatry 2003;74:760–764.
Stocchetti N, Chieregato A, De Marchi M, Croci M, Benti R, Grimoldi N. High cerebral perfusion pressure improves low values of local brain tissue O2 tension (PtiO2) in focal lesions. Acta Neurochir Suppl 1998;71:162–165.
Dings J, Meixensberger J, Jager A, Roosen K. Clinical experience with 118 brain tissue oxygen partial pressure catheter probes. Neurosurgery 1998;43:1082–1095.
Valadka AB, Gopinath SP, Contant CF, Uzura M, Robertson CS. Relationship of brain tissue PO2 to outcome after severe head injury. Crit Care Med 1998;26:1576–1581.
Van Santbrink H, Vd Brink WA, Steyerberg EW, Carmona Suazo JA, Avezaat CJ, Maas AI. Brain tissue oxygen response in severe traumatic brain injury. Acta Neurochir (Wien) 2003;145:429–438.
Wintermark M, Chiolero R, van Melle G, Revelly JP, Porchet F, Regli L, et al. Relationship between brain perfusion computed tomography variables and cerebral perfusion pressure in severe head trauma patients. Crit Care Med 2004;32:1579–1587.
Vath A, Kunze E, Roosen K, Meixensberger J. Therapeutic aspects of brain tissue pO2 monitoring after subarachnoid hemorrhage. Acta Neurochir Suppl 2002;81:307–309.
Charbel FT, Du X, Hoffman WE, Ausman JI. Brain tissue PO(2), PCO(2), and pH during cerebral vasospasm. Surg Neurol 2000;54:432–437; discussion 438.
van den Brink WA, van Santbrink H, Steyerberg EW, Avezaat CJ, Suazo JA, Hogesteeger C, et al. Brain oxygen tension in severe head injury. Neurosurgery 2000;46:868–876; discussion 876–878.
Menzel M, Soukup J, Henze D, et al. Brain tissue oxygen monitoring for assessment of autoregulation: preliminary results suggest a new hypothesis. J Neurosurg Anesthesiol 2003;15:33–41.
Rossi S, Longhi L, Balestreri M, Spagnoli D, deLeo A, Stocchetti N. Brain oxygen tension during hyperoxia in a swine model of cerebral ischaemia. Acta Neurochir Suppl 2000;76:243–245.
Hemphill JC III, Knudson MM, Derugin N, Morabito D, Manley GT. Carbon dioxide reactivity and pressure autoregulation of brain tissue oxygen. Neurosurgery 2001;48:377–383; discussion 383–384.
Bullock R, Brock-Utne J, van Dellen J, Blake G. Intracerebral hemorrhage in a primate model: effect on regional cerebral blood flow. Surg Neurol 1988;29:101–107.
Mendelow AD. Mechanisms of ischemic brain damage with intracerebral hemorrhage. Stroke 1993;24:1115–1117; discussion 1118–1119.
Qureshi AI, Wilson DA, Hanley DF, Traystman RJ. No evidence for an ischemic penumbra in massive experimental intracerebral hemorrhage. Neurology 1999;52:266–272.
Zazulia AR, Diringer MN, Videen TO, Adams RE, Yundt K, Aiyagari V, et al. Hypoperfusion without ischemia surrounding acute intracerebral hemorrhage. J Cereb Blood Flow Metab 2001;21:804–810.
Kidwell CS, Saver JL, Mattiello J, Warach S, Liebeskind DS, Starkman S, et al. Diffusion-perfusion MR evaluation of perihematomal injury in hyperacute intracerebral hemorrhage. Neurology 2001;57:1611–1617.
Kobayashi M, Takayama H, Suga S, Mihara B. Longitudinal changes of metabolites in frontal lobes after hemorrhagic stroke of basal ganglia: a proton magnetic resonance spectroscopy study. Stroke 2001;32:2237–2245.
Lee KR, Colon GP, Betz AL, Keep RF, Kim S, Hoff JT. Edema from intracerebral hemorrhage: the role of thrombin. J Neurosurg 1996;84:91–96.
Kitaoka T, Hua Y, Xi G, Nagao S, Hoff JT, Keep RF. Effect of delayed argatroban treatment on intracerebral hemorrhage-induced edema in the rat. Acta Neurochir Suppl 2003;86:457–461.
Mayer SA. Ultra-early hemostatic therapy for intracerebral hemorrhage. Stroke 2003;34:224–229.
Mayer SA, Brun NC, Begtrup K, et al. Recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med 2005;352:777–785.
Qureshi AI, Wilson DA, Traystman RJ. Treatment of elevated intracranial pressure in experimental intracerebral hemorrhage: comparison between mannitol and hypertonic saline. Neurosurgery 1999;44:1055–1063; discussion 1063–1064.
Broderick JP, Adams HP Jr, Barsan W, Feinberg W, Feldmann E, Grotta J, et al. Guidelines for the management of spontaneous intracerebral hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 1999;30:905–915.
Struchen MA, Hannay HJ, Contant CF, Robertson CS. The relation between acute physiological variables and outcome on the Glasgow Outcome Scale and Disability Rating Scale following severe traumatic brain injury. J Neurotrauma 2001;18:115–125.
Barton CW, Hemphill JC, Morabito D, Manley GT. A novel method of evaluating the impact of secondary brain insults on functional outcomes in traumatic brain injured patients. Acad Emerg Med 2005;12:1–6.
Dings 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 1996;138:425–434.
Sarrafzadeh AS, Sakowitz OW, Callsen TA, Lanksch WR, Unterberg AW. Detection of secondary insults by brain tissue pO2 and bedside microdialysis in severe head injury. Acta Neurochir Suppl 2002;81:319–321.
Sarrafzadeh AS, Kiening KL, Bardt TF, Schneider GH, Unterberg AW, Lanksch WR. Cerebral oxygenation in contusioned vs. nonlesioned brain tissue: monitoring of PtiO2 with Licox and Paratrend. Acta Neurochir Suppl 1998;71:186–189.
Kiening KL, Hartl R, Unterberg AW, Schneider GH, Bardt T, Lanksch WR. Brain tissue pO2-monitoring in compatose patients: implications for therapy. Neurol Res 1997;19:233–240.
Kiening 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 1996;85:751–757.
Steiner T, Pilz J, Schellinger P, Wirtz R, Friederichs V, Aschoff A, et al. Multimodal online monitoring in middle cerebral artery territory stroke. Stroke 2001;32:2500–2506.
Kett-White R, Hutchinson PJ, Czosnyka M, Boniface S, Pickard JD, Kirkpatrick PJ. Multi-modal monitoring of acute brain injury. Adv Tech Stand Neurosurg 2002;27:87–134.
De Georgia MA. Multimodal monitoring in neurocritical care. Cleve Clin J Med 2004;71(Suppl 1):S16-S17.
Sarrafzadeh AS, Sakowitz OW, Kiening KL, Benndorf G, Lanksch WR, Unterberg AW. Bedside microdialysis: a tool to monitor cerebral metabolism in subarachnoid hemorrhage patients? Crit Care Med 2002;30:1062–1070.
Hemphill JC III, Bonovich DC, Besmertis L, Manley GT, Johnston SC. The ICH score: a simple, reliable grading scale for intracerebral hemorrhage. Stroke 2001;32:891–897.
Tuhrim S, Horowitz DR, Sacher M, Godbold JH. Volume of ventricular blood is an important determinant of outcome in supratentorial intracerebral hemorrhage. Crit Care Med 1999;27:617–621.
Tuhrim S, Horowitz DR, Sacher M, Godbold JH. Validation and comparison of models predicting survival following intracerebral hemorrhage. Crit Care Med 1995;23:950–954.
Broderick JP, Brott TG, Duldner JE, Tomsick T, Huster G. Volume of intracerebral hemorrhage. A powerful and easy-to-use predictor of 30-day mortality. Stroke 1993;24:987–993.
Lisk DR, Pasteur W, Rhoades H, Putnam RD, Grotta JC. Early presentation of hemispheric intracerebral hemorrhage: prediction of outcome and guidelines for treatment allocation. Neurology 1994;44:133–139.
Juvela S. Risk factors for impaired outcome after spontaneous intracerebral hemorrhage. Arch Neurol 1995;52:1193–1200.
Qureshi AI, Suri MF, Ostrow PT, Kim SH, Ali Z, Shatla AA, et al. Apoptosis as a form of cell death in intracerebral hemorrhage. Neurosurgery 2003;52:1041–1047; discussion 1047–1048.
Tang J, Liu J, Zhou C, et al. Mmp-9 deficiency enhances collagenase-induced intracerebral hemorrhage and brain injury in mutant mice. J Cereb Blood Flow Metab 2004;24:1133–1145.
Xi G, Wagner KR, Keep RF, Hua Y, de Courten-Myers GM, Broderick JP, et al. Role of blood clot formation on early edema development after experimental intracerebral hemorrhage. Stroke 1998;29:2580–2586.
Xi G, Hua Y, Keep RF, Younger JG, Hoff JT. Brain edema after intracerebral hemorrhage: the effects of systemic complement depletion. Acta Neurochir Suppl 2002;81:253–256.
Burbridge B, Matte G, Remedios A. Complex intracranial arterial anatomy in swine is unsuitable for cerebral infarction projects. Can Assoc Radiol J 2004;55:326–329.
Brott T, Broderick J, Kothari R, et al. Early hemorrhage growth in patients with intracerebral hemorrhage. Stroke 1997;28: 1–5.
Kazui S, Naritomi H, Yamamoto H, Sawada T, Yamaguchi T. Enlargement of spontaneous intracerebral hemorrhage. Incidence and time course. Stroke 1996;27:1783–1787.
van den Brink WA, Haitsma IK, Avezaat CJ, Houtsmuller AB, Kros JM, Maas AI. Brain parenchyma/pO2 catheter interface: a histopathological study in the rat. J Neurotrauma 1998;15:813–824.
Valadka AB, Gopinath SP, Contant CF, Uzura M, Robertson CS. Relationship of brain tissue PO2 to outcome after severe head injury. Crit Care Med 1998;26:1576–1581.
Hirano T, Read SJ, Abbott DF, Sachinidis JI, Tochon-Danguy HJ, Egan GF, et al. No evidence of hypoxic tissue on 18F-fluoromisonidazole PET after intracerebral hemorrhage. Neurology 1999;53:2179–2182.
Mayer SA, Lignelli A, Fink ME, Kessler DB, Thomas CE, Swarup R, et al. Perilesional blood flow and edema formation in acute intracerebral hemorrhage: a SPECT study. Stroke 1998;29:1791–1798.
Hemphill JC, Smith WS, Sonne DC, Morabito D, Manley GT. Relationship between brain tissue oxygen tension and CT perfusion: feasibility and initial results. AJNR Am J Neuroradiol 2005;26:1095–1100.
Doppenberg EM, 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 1998;49:650–654.
Jaeger M, Soehle M, Schuhmann MU, Winkler D, Meixensberger J. Correlation of continuously monitored regional cerebral blood flow and brain tissue oxygen. Acta Neurochir (Wien) 2005;147:51–56.
Valadka AB, Hlatky R, Furuya Y, Robertson CS. Brain tissue pO2: correlation with cerebral blood flow. Acta Neurochir Suppl 2002;81:299–301.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hemphill, J.C., Morabito, D., Farrant, M. et al. Brain tissue oxygen monitoring in intracerebral hemorrhage. Neurocrit Care 3, 260–270 (2005). https://doi.org/10.1385/NCC:3:3:260
Issue Date:
DOI: https://doi.org/10.1385/NCC:3:3:260