Neurocritical Care

, Volume 13, Issue 1, pp 10–16

Anemia is Associated with Metabolic Distress and Brain Tissue Hypoxia After Subarachnoid Hemorrhage

  • Pedro Kurtz
  • J. Michael Schmidt
  • Jan Claassen
  • Emmanuel Carrera
  • Luis Fernandez
  • Raimund Helbok
  • Mary Presciutti
  • R. Morgan Stuart
  • E. Sander Connolly
  • Neeraj Badjatia
  • Stephan A. Mayer
  • Kiwon Lee
Original Article

Abstract

Background

Anemia is frequently encountered in critically ill patients and adversely affects cerebral oxygen delivery and brain tissue oxygen (PbtO2). The objective of this study is to assess whether there is an association between anemia and metabolic distress or brain tissue hypoxia in patients with subarachnoid hemorrhage.

Methods

Retrospective study was conducted in a neurological intensive care unit in a university hospital. Patients with subarachnoid hemorrhage that underwent multimodality monitoring with intracranial pressure, PbtO2 and microdialysis were analyzed. The relationships between hemoglobin (Hb) concentrations and brain tissue hypoxia (PbtO2 ≤ 15 mmHg) and metabolic distress (lactate/pyruvate ratio ≥40) were analyzed with general linear models of logistic function for dichotomized outcomes utilizing generalized estimating equations.

Results

A total of 359 matched neuromonitoring hours and Hb measurements were analyzed from 34 consecutive patients. The median hemoglobin was 9.7 g/dl (interquartile range 8.8–10.5). After adjusting for significant covariates, reduced hemoglobin concentration was associated with a progressively increased risk of brain tissue hypoxia (adjusted OR 1.7 [1.1–2.4]; P = 0.01 for every unit decrease). Also after adjusting for significant covariates, hemoglobin concentrations below 9 g/dl and between 9.1 and 10 g/dl were associated with an increased risk of metabolic distress as compared to concentrations between 10.1 and 11 g/dl (adjusted OR 3.7 [1.5–9.4]; P = 0.004 for Hb ≤ 9 g/dl and adjusted OR 1.9 [1.1–3.3]; P = 0.03 for Hb 9.1–10 g/dl).

Conclusions

Anemia is associated with a progressively increased risk of cerebral metabolic distress and brain tissue hypoxia after subarachnoid hemorrhage.

Keywords

Brain injury Cerebral microdialysis Anemia Brain tissue oxygen Subarachnoid hemorrhage 

References

  1. 1.
    Corwin HL, Gettinger A, Pearl RG, et al. The CRIT Study: anemia and blood transfusion in the critically ill-current clinical practice in the United States. Crit Care Med. 2004;32:39–52.CrossRefPubMedGoogle Scholar
  2. 2.
    Vincent JL, Baron JF, Reinhart K, et al. Anemia and blood transfusion in critically ill patients. JAMA. 2002;288:1499–507.CrossRefPubMedGoogle Scholar
  3. 3.
    Kramer AH, Zygun DA, Bleck TP, Dumont AS, Kassell NF, Nathan B. Relationship between hemoglobin concentrations and outcomes across subgroups of patients with aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2009;10:157–65.CrossRefPubMedGoogle Scholar
  4. 4.
    Springer MV, Schmidt JM, Wartenberg KE, Frontera JA, Badjatia N, Mayer SA. Predictors of global cognitive impairment 1 year after subarachnoid hemorrhage. Neurosurgery. 2009;65:1043–50. (discussion 50–1).CrossRefPubMedGoogle Scholar
  5. 5.
    Naidech AM, Jovanovic B, Wartenberg KE, et al. Higher hemoglobin is associated with improved outcome after subarachnoid hemorrhage. Crit Care Med. 2007;35:2383–9.CrossRefPubMedGoogle Scholar
  6. 6.
    Wartenberg KE, Schmidt JM, Claassen J, et al. Impact of medical complications on outcome after subarachnoid hemorrhage. Crit Care Med. 2006;34:617–23. (quiz 24).CrossRefPubMedGoogle Scholar
  7. 7.
    Hebert PC, Wells G, Blajchman MA, et al. A multicenter, randomized, controlled clinical trial of transfusion requirements in critical care. Transfusion Requirements in Critical Care Investigators, Canadian Critical Care Trials Group. N Engl J Med. 1999;340:409–17.CrossRefPubMedGoogle Scholar
  8. 8.
    Hare GM. Anemia and the brain. Curr Opin Anaesthesiol. 2004;17:363–9.CrossRefPubMedGoogle Scholar
  9. 9.
    Leal-Noval SR, Rincon-Ferrari MD, Marin-Niebla A, et al. Transfusion of erythrocyte concentrates produces a variable increment on cerebral oxygenation in patients with severe traumatic brain injury: a preliminary study. Intensive Care Med. 2006;32:1733–40.CrossRefPubMedGoogle Scholar
  10. 10.
    Leal-Noval SR, Munoz-Gomez M, Arellano-Orden V, et al. Impact of age of transfused blood on cerebral oxygenation in male patients with severe traumatic brain injury. Crit Care Med. 2008;36:1290–6.CrossRefPubMedGoogle Scholar
  11. 11.
    Smith MJ, Stiefel MF, Magge S, et al. Packed red blood cell transfusion increases local cerebral oxygenation. Crit Care Med. 2005;33:1104–8.CrossRefPubMedGoogle Scholar
  12. 12.
    van den Brink WA, van Santbrink H, Steyerberg EW, et al. Brain oxygen tension in severe head injury. Neurosurgery. 2000;46:868–76. (discussion 76–8).CrossRefPubMedGoogle Scholar
  13. 13.
    Meixensberger J, Renner C, Simanowski R, Schmidtke A, Dings J, Roosen K. Influence of cerebral oxygenation following severe head injury on neuropsychological testing. Neurol Res. 2004;26:414–7.CrossRefPubMedGoogle Scholar
  14. 14.
    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;26:1576–81.CrossRefPubMedGoogle Scholar
  15. 15.
    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;145:429–38. (discussion 38).Google Scholar
  16. 16.
    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;74:760–4.CrossRefPubMedGoogle Scholar
  17. 17.
    Hemphill JC III, Morabito D, Farrant M, Manley GT. Brain tissue oxygen monitoring in intracerebral hemorrhage. Neurocrit Care. 2005;3:260–70.CrossRefPubMedGoogle Scholar
  18. 18.
    Johnston AJ, Steiner LA, Coles JP, et al. Effect of cerebral perfusion pressure augmentation on regional oxygenation and metabolism after head injury. Crit Care Med. 2005;33:189–95. (discussion 255–7).CrossRefPubMedGoogle Scholar
  19. 19.
    Carvi y Nievas M, Toktamis S, Hollerhage HG, Haas E. Hyperacute measurement of brain-tissue oxygen, carbon dioxide, pH, and intracranial pressure before, during, and after cerebral angiography in patients with aneurysmatic subarachnoid hemorrhage in poor condition. Surg Neurol. 2005;64:362–7. (discussion 7).CrossRefPubMedGoogle Scholar
  20. 20.
    Schulz MK, Wang LP, Tange M, Bjerre P. Cerebral microdialysis monitoring: determination of normal and ischemic cerebral metabolisms in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg. 2000;93:808–14.CrossRefPubMedGoogle Scholar
  21. 21.
    Vespa P, Bergsneider M, Hattori N, 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;25:763–74.CrossRefPubMedGoogle Scholar
  22. 22.
    Samuelsson C, Hillered L, Zetterling M, et al. Cerebral glutamine and glutamate levels in relation to compromised energy metabolism: a microdialysis study in subarachnoid hemorrhage patients. J Cereb Blood Flow Metab. 2007;27:1309–17.CrossRefPubMedGoogle Scholar
  23. 23.
    Oddo M, Milby A, Chen I, et al. Hemoglobin concentration and cerebral metabolism in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2009;40:1275–81.CrossRefPubMedGoogle Scholar
  24. 24.
    Hillered L, Vespa PM, Hovda DA. Translational neurochemical research in acute human brain injury: the current status and potential future for cerebral microdialysis. J Neurotrauma. 2005;22:3–41.CrossRefPubMedGoogle Scholar
  25. 25.
    Bellander BM, Cantais E, Enblad P, et al. Consensus meeting on microdialysis in neurointensive care. Intensive Care Med. 2004;30:2166–9.CrossRefPubMedGoogle Scholar
  26. 26.
    Bratton SL, Chestnut RM, Ghajar J. et al. Guidelines for the management of severe traumatic brain injury. XV. Steroids. J Neurotrauma. 2007;24(Suppl 1):S91–5.PubMedGoogle Scholar
  27. 27.
    Bederson JB, Connolly ES Jr, Batjer HH, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke. 2009;40:994–1025.CrossRefPubMedGoogle Scholar
  28. 28.
    Broderick J, Connolly S, Feldmann E, et al. Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group. Circulation. 2007;116:e391–413.CrossRefPubMedGoogle Scholar
  29. 29.
    Badjatia N, Strongilis E, Gordon E, et al. Metabolic impact of shivering during therapeutic temperature modulation: the Bedside Shivering Assessment Scale. Stroke. 2008;39:3242–7.CrossRefPubMedGoogle Scholar
  30. 30.
    Pan W. Model selection in estimating equations. Biometrics. 2001;57:529–34.CrossRefPubMedGoogle Scholar
  31. 31.
    Pan W. Akaike’s information criterion in generalized estimating equations. Biometrics. 2001;57:120–5.CrossRefPubMedGoogle Scholar
  32. 32.
    Robertson C. Desaturation episodes after severe head injury: influence on outcome. Acta Neurochir Suppl (Wien). 1993;59:98–101.Google Scholar
  33. 33.
    Cruz J. The first decade of continuous monitoring of jugular bulb oxyhemoglobin saturation: management strategies and clinical outcome. Crit Care Med. 1998;26:344–51.CrossRefPubMedGoogle Scholar
  34. 34.
    Robertson CS, Gopinath SP, Goodman JC, Contant CF, Valadka AB, Narayan RK. SjvO2 monitoring in head-injured patients. J Neurotrauma. 1995;12:891–6.CrossRefPubMedGoogle Scholar
  35. 35.
    Hare GM, Mazer CD, Hutchison JS, et al. Severe hemodilutional anemia increases cerebral tissue injury following acute neurotrauma. J Appl Physiol. 2007;103:1021–9.CrossRefPubMedGoogle Scholar
  36. 36.
    Rosenthal G, Morabito D, Cohen M, et al. Use of hemoglobin-based oxygen-carrying solution-201 to improve resuscitation parameters and prevent secondary brain injury in a swine model of traumatic brain injury and hemorrhage: laboratory investigation. J Neurosurg. 2008;108:575–87.CrossRefPubMedGoogle Scholar
  37. 37.
    Stern S, Rice J, Philbin N, et al. Resuscitation with the hemoglobin-based oxygen carrier, HBOC-201, in a swine model of severe uncontrolled hemorrhage and traumatic brain injury. Shock. 2009;31:64–79.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Pedro Kurtz
    • 1
    • 2
  • J. Michael Schmidt
    • 1
  • Jan Claassen
    • 1
  • Emmanuel Carrera
    • 1
  • Luis Fernandez
    • 1
  • Raimund Helbok
    • 1
  • Mary Presciutti
    • 1
  • R. Morgan Stuart
    • 1
  • E. Sander Connolly
    • 1
  • Neeraj Badjatia
    • 1
  • Stephan A. Mayer
    • 1
  • Kiwon Lee
    • 1
  1. 1.Division of Critical Care Neurology, Department of NeurologyColumbia UniversityNew YorkUSA
  2. 2.Intensive Care Unit, Casa de Saúde São JoséRio de JaneiroBrazil

Personalised recommendations