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Factors Associated with the Development of Anemia After Subarachnoid Hemorrhage

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Anemia is common after subarachnoid hemorrhage (SAH) and may exacerbate the reduction in oxygen delivery that underlies delayed cerebral ischemia. Fall in hemoglobin may relate to blood loss as well as inflammatory suppression of erythropoiesis. Identifying factors associated with anemia may facilitate targeted interventions, such as the use of erythropoiesis-stimulating agents, which could minimize the burden of anemia and reduce red blood cell (RBC) transfusion requirements.


We analyzed a cohort of patients with spontaneous SAH admitted over a 3-year period who survived at least 4 days. All patients had daily hematocrit values drawn while in the ICU. Multivariate regression was performed to determine baseline and early post-admission variables associated with development of anemia (defined as hematocrit < 30%).


Anemia developed in 47% of 243 patients with SAH after a mean of 3.5 days (median 2 days). Admission variables independently associated with anemia were female gender (OR 3.7, 95% CI 1.8–7.6), baseline hematocrit < 36% (OR 3.9, 1.5–10.1 compared to 36–45%), history of hypertension (OR 2.1, 1.05–4.2), and poor clinical grade (OR 5.9, 2.3–15.0). Surgical aneurysm treatment (OR 13.5, 6.0–30.3) and greater admission SIRS score (OR 5.7, 1.7–19.2 if 3–4 criteria for systemic inflammatory response syndrome were met on day of admission compared to none) were also associated with fall in hematocrit.


It may be possible to predict those most likely to develop anemia using simple baseline clinical variables. Anemia was strongly related to surgery, likely through greater blood loss, and greater systemic inflammatory response on admission, possibly explained by cytokine-mediated inhibition of RBC production.

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  1. Kassell NF, Torner JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL. The International Cooperative Study on the Timing of Aneurysm Surgery. Part 1: overall management results. J Neurosurg. 1990;73(1):18–36.

    Article  CAS  PubMed  Google Scholar 

  2. Powers WJ, Grubb RL Jr, Baker RP, Mintun MA, Raichle ME. Regional cerebral blood flow and metabolism in reversible ischemia due to vasospasm. Determination by positron emission tomography. J Neurosurg. 1985;62(4):539–46.

    Article  CAS  PubMed  Google Scholar 

  3. Giller CA, Wills MJ, Giller AM, Samson D. Distribution of hematocrit values after aneurysmal subarachnoid hemorrhage. J Neuroimaging. 1998;8(3):169–70.

    CAS  PubMed  Google Scholar 

  4. Kramer AH, Gurka MJ, Nathan B, Dumont AS, Kassell NF, Bleck TP. Complications associated with anemia and blood transfusion in patients with aneurysmal subarachnoid hemorrhage. Crit Care Med. 2008;36(7):2070–5.

    Article  PubMed  Google Scholar 

  5. Naidech AM, Drescher J, Ault ML, Shaibani A, Batjer HH, Alberts MJ. Higher hemoglobin is associated with less cerebral infarction, poor outcome, and death after subarachnoid hemorrhage. Neurosurgery. 2006;59(4):775–9.

    Article  PubMed  Google Scholar 

  6. Naidech AM, Jovanovic B, Wartenberg KE, et al. Higher hemoglobin is associated with improved outcome after subarachnoid hemorrhage. Crit Care Med. 2007;35(10):2383–9.

    Article  CAS  PubMed  Google Scholar 

  7. 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 2008; doi: 10.1007/s12028-008-9171-y.

  8. Teasdale GM, Drake CG, Hunt W, et al. A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neurosurg Psychiatry. 1988;51(11):1457.

    Article  CAS  PubMed  Google Scholar 

  9. Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980;6(1):1–9.

    Article  CAS  PubMed  Google Scholar 

  10. Bone RC, Balk RA, Cerra FB et al. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 1992; 101(6):1644–55.

  11. Wartenberg KE, Schmidt JM, Claassen J, et al. Impact of medical complications on outcome after subarachnoid hemorrhage. Crit Care Med. 2006;34(3):617–23.

    PubMed  Google Scholar 

  12. Dhar R, Diringer MN. The burden of the systemic inflammatory response predicts vasospasm and outcome after subarachnoid hemorrhage. Neurocrit Care. 2008;8(3):404–12.

    Article  PubMed  Google Scholar 

  13. Corwin HL, Krantz SB. Anemia of the critically ill: “acute” anemia of chronic disease. Crit Care Med. 2000;28(8):3098–9.

    Article  CAS  PubMed  Google Scholar 

  14. Rodriguez RM, Corwin HL, Gettinger A, Corwin MJ, Gubler D, Pearl RG. Nutritional deficiencies and blunted erythropoietin response as causes of the anemia of critical illness. J Crit Care. 2001;16(1):36–41.

    Article  CAS  PubMed  Google Scholar 

  15. Fink MP. Pathophysiology of intensive care unit-acquired anemia. Crit Care. 2004;8(Suppl 2):S9–10.

    Article  PubMed  Google Scholar 

  16. Gruber A, Rossler K, Graninger W, Donner A, Illievich MU, Czech T. Ventricular cerebrospinal fluid and serum concentrations of sTNFR-I, IL-1ra, and IL-6 after aneurysmal subarachnoid hemorrhage. J Neurosurg Anesthesiol. 2000;12(4):297–306.

    Article  CAS  PubMed  Google Scholar 

  17. Naredi S, Lambert G, Friberg P, et al. Sympathetic activation and inflammatory response in patients with subarachnoid haemorrhage. Intensive Care Med. 2006;32(12):1955–61.

    Article  CAS  PubMed  Google Scholar 

  18. Yoshimoto Y, Tanaka Y, Hoya K. Acute systemic inflammatory response syndrome in subarachnoid hemorrhage. Stroke. 2001;32(9):1989–93.

    Article  CAS  PubMed  Google Scholar 

  19. Morikawa S, Takabe W, Mataki C, et al. The effect of statins on mRNA levels of genes related to inflammation, coagulation, and vascular constriction in HUVEC. Human umbilical vein endothelial cells. J Atheroscler Thromb. 2002;9(4):178–83.

    CAS  PubMed  Google Scholar 

  20. Chello M, Patti G, Candura D, et al. Effects of atorvastatin on systemic inflammatory response after coronary bypass surgery. Crit Care Med. 2006;34(3):660–7.

    Article  CAS  PubMed  Google Scholar 

  21. McGirt MJ, Pradilla G, Legnani FG, et al. Systemic administration of simvastatin after the onset of experimental subarachnoid hemorrhage attenuates cerebral vasospasm. Neurosurgery. 2006;58(5):945–51.

    Article  PubMed  Google Scholar 

  22. Corwin HL, Gettinger A, Rodriguez RM, et al. Efficacy of recombinant human erythropoietin in the critically ill patient: a randomized, double-blind, placebo-controlled trial. Crit Care Med. 1999;27(11):2346–50.

    Article  CAS  PubMed  Google Scholar 

  23. Corwin HL, Gettinger A, Pearl RG, et al. Efficacy of recombinant human erythropoietin in critically ill patients: a randomized controlled trial. JAMA. 2002;288(22):2827–35.

    Article  CAS  PubMed  Google Scholar 

  24. Marik PE, Corwin HL. Efficacy of red blood cell transfusion in the critically ill: a systematic review of the literature. Crit Care Med. 2008;36(9):2667–74.

    Article  PubMed  Google Scholar 

  25. Smith MJ, Le Roux PD, Elliott JP, Winn HR. Blood transfusion and increased risk for vasospasm and poor outcome after subarachnoid hemorrhage. J Neurosurg. 2004;101(1):1–7.

    Article  PubMed  Google Scholar 

  26. van der Kooij MA, Groenendaal F, Kavelaars A, Heijnen CJ, van Bel F. Neuroprotective properties and mechanisms of erythropoietin in in vitro and in vivo experimental models for hypoxia/ischemia. Brain Res Rev. 2008;59(1):22–33.

    Article  PubMed  Google Scholar 

  27. Grasso G, Buemi M, Alafaci C, et al. Beneficial effects of systemic administration of recombinant human erythropoietin in rabbits subjected to subarachnoid hemorrhage. Proc Natl Acad Sci USA. 2002;99(8):5627–31.

    Article  CAS  PubMed  Google Scholar 

  28. Tseng MY, Hutchinson PJ, Richards HK, et al. Acute systemic erythropoietin therapy to reduce delayed ischemic deficits following aneurysmal subarachnoid hemorrhage: a Phase II randomized, double-blind, placebo-controlled trial. J Neurosurg. 2009;111:171–80.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Rajat Dhar.

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Sampson, T.R., Dhar, R. & Diringer, M.N. Factors Associated with the Development of Anemia After Subarachnoid Hemorrhage. Neurocrit Care 12, 4–9 (2010).

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