Skip to main content
Top
Published in: Neurocritical Care 3/2014

01-12-2014 | Original Article

Effect of Prolonged Therapeutic Hypothermia on Intracranial Pressure, Organ Function, and Hospital Outcomes Among Patients with Aneurysmal Subarachnoid Hemorrhage

Authors: Lioudmila V. Karnatovskaia, Augustine S. Lee, Emir Festic, Christopher L. Kramer, William D. Freeman

Published in: Neurocritical Care | Issue 3/2014

Login to get access

Abstract

Background

Global cerebral edema (GCE) with subsequent refractory intracranial hypertension complicates some cases of aneurysmal subarachnoid hemorrhage (aSAH), and typically is associated with poorer outcome. Treatment options for refractory intracranial pressure (ICP) cases are limited to decompressive hemicraniectomy (DHC) and targeted temperature management (TTM) with induced hypothermia (32–34 °C). No outcomes comparison between patients treated with either or both forms of refractory ICP therapy exists, and data on the effect of prolonged hypothermia on ICP and organ function among patients with aSAH are limited.

Methods

This is a retrospective study of aSAH patients who underwent DHC and/or prolonged hypothermia (greater than 48 h) for refractory ICP (i.e., ICP >20 mmHg after osmotherapy) in the intensive care unit of a single, tertiary-care academic center.

Results

Nineteen individuals with aSAH underwent TTM with or without DHC; sixteen patients underwent DHC alone. The patients in TTM group were younger (median age 44 years) than the DHC without TTM population (median age 60 years). TTM was started on median day 2 with a median duration of 7 days. There were no significant group differences in survival to discharge (59 % vs. 69 %) or in the mean modified Rankin score on follow-up (3.6 vs. 3.7), despite the TTM group having longer hospital length of stay (24 vs. 19 days, p = 0.03), longer duration of mechanical ventilation (20 vs. 9 days, p = 0.04), a higher cumulative fluid balance (12.8 vs. 5.1 L, p = 0.01), and higher APACHEII scores. The median maximal ICP decreased from 23.5 to 21 mmHg within 24 h of hypothermia initiation. There were no significant differences in other markers of end-organ function (respiratory, hematologic, renal, liver, and cardiac), infection rate, or adverse events between groups.

Conclusions

Use of prolonged TTM among aSAH patients with GCE and refractory ICP elevations is associated with a longer duration of mechanical ventilation but is not different in terms of neurological outcomes measured by modified Rankin score or organ function outcomes compared to patients who received DHC alone.
Literature
1.
go back to reference Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke. 2002;33(5):1225–32.PubMedCrossRef Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke. 2002;33(5):1225–32.PubMedCrossRef
2.
go back to reference le Roux AA, Wallace MC. Outcome and cost of aneurysmal subarachnoid hemorrhage. Neurosurg Clin N Am. 2010;21(2):235–46.PubMedCrossRef le Roux AA, Wallace MC. Outcome and cost of aneurysmal subarachnoid hemorrhage. Neurosurg Clin N Am. 2010;21(2):235–46.PubMedCrossRef
3.
go back to reference Zetterling M, Hallberg L, Ronne-Engström E. Early global brain oedema in relation to clinical admission parameters and outcome in patients with aneurysmal subarachnoid haemorrhage. Acta Neurochir (Wien). 2010;152(9):1527–33.CrossRef Zetterling M, Hallberg L, Ronne-Engström E. Early global brain oedema in relation to clinical admission parameters and outcome in patients with aneurysmal subarachnoid haemorrhage. Acta Neurochir (Wien). 2010;152(9):1527–33.CrossRef
4.
go back to reference Kreiter KT, Copeland D, Bernardini GL, et al. Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke. 2002;33(1):200–8.PubMedCrossRef Kreiter KT, Copeland D, Bernardini GL, et al. Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke. 2002;33(1):200–8.PubMedCrossRef
5.
go back to reference Andrews PJ et al; Eurotherm3235Trial collaborators. European society of intensive care medicine study of therapeutic hypothermia (32–35 °C) for intracranial pressure reduction after traumatic brain injury (the Eurotherm3235Trial). Trials. 2011;12:8. Andrews PJ et al; Eurotherm3235Trial collaborators. European society of intensive care medicine study of therapeutic hypothermia (32–35 °C) for intracranial pressure reduction after traumatic brain injury (the Eurotherm3235Trial). Trials. 2011;12:8.
6.
go back to reference Dorfer C, Frick A, Knosp E, Gruber A. Decompressive hemicraniectomy after aneurysmal subarachnoid hemorrhage. World Neurosurg. 2010;74(4–5):465–71.PubMedCrossRef Dorfer C, Frick A, Knosp E, Gruber A. Decompressive hemicraniectomy after aneurysmal subarachnoid hemorrhage. World Neurosurg. 2010;74(4–5):465–71.PubMedCrossRef
7.
go back to reference Zetterling M, Hallberg L, Hillered L, et al. Brain energy metabolism in patients with spontaneous subarachnoid hemorrhage and global cerebral edema. Neurosurgery. 2010;66(6):1102–10.PubMedCrossRef Zetterling M, Hallberg L, Hillered L, et al. Brain energy metabolism in patients with spontaneous subarachnoid hemorrhage and global cerebral edema. Neurosurgery. 2010;66(6):1102–10.PubMedCrossRef
8.
go back to reference Scaravilli V, Tinchero G, Citerio G. Participants in the international multi-disciplinary consensus conference on the critical care management of subarachnoid hemorrhage. Fever management in SAH. Neurocrit Care. 2011;15(2):287–94.PubMedCrossRef Scaravilli V, Tinchero G, Citerio G. Participants in the international multi-disciplinary consensus conference on the critical care management of subarachnoid hemorrhage. Fever management in SAH. Neurocrit Care. 2011;15(2):287–94.PubMedCrossRef
9.
go back to reference Gasser S, Khan N, Yonekawa Y, Imhof HG, Keller E. Long-term hypothermia in patients with severe brain edema after poor-grade subarachnoid hemorrhage: feasibility and intensive care complications. J Neurosurg Anesthesiol. 2003;15(3):240–8.PubMedCrossRef Gasser S, Khan N, Yonekawa Y, Imhof HG, Keller E. Long-term hypothermia in patients with severe brain edema after poor-grade subarachnoid hemorrhage: feasibility and intensive care complications. J Neurosurg Anesthesiol. 2003;15(3):240–8.PubMedCrossRef
10.
go back to reference Seule MA, Muroi C, Mink S, Yonekawa Y, Keller E. Therapeutic hypothermia in patients with aneurysmal subarachnoid hemorrhage, refractory intracranial hypertension, or cerebral vasospasm. Neurosurgery. 2009;64(1):86–92.PubMedCrossRef Seule MA, Muroi C, Mink S, Yonekawa Y, Keller E. Therapeutic hypothermia in patients with aneurysmal subarachnoid hemorrhage, refractory intracranial hypertension, or cerebral vasospasm. Neurosurgery. 2009;64(1):86–92.PubMedCrossRef
11.
go back to reference Kollmar R, Staykov D, Dörfler A, Schellinger PD, Schwab S, Bardutzky J. Hypothermia reduces perihemorrhagic edema after intracerebral hemorrhage. Stroke. 2010;41(8):1684–9.PubMedCrossRef Kollmar R, Staykov D, Dörfler A, Schellinger PD, Schwab S, Bardutzky J. Hypothermia reduces perihemorrhagic edema after intracerebral hemorrhage. Stroke. 2010;41(8):1684–9.PubMedCrossRef
12.
go back to reference Staykov D, Wagner I, Volbers B, Doerfler A, Schwab S, Kollmar R. Mild prolonged hypothermia for large intracerebral hemorrhage. Neurocrit Care. 2013;18(2):178–83.PubMedCrossRef Staykov D, Wagner I, Volbers B, Doerfler A, Schwab S, Kollmar R. Mild prolonged hypothermia for large intracerebral hemorrhage. Neurocrit Care. 2013;18(2):178–83.PubMedCrossRef
13.
go back to reference Nunnally ME, Jaeschke R, Bellingan GJ, et al. Targeted temperature management in critical care: a report and recommendations from five professional societies. Crit Care Med. 2011;39(5):1113–25.PubMedCrossRef Nunnally ME, Jaeschke R, Bellingan GJ, et al. Targeted temperature management in critical care: a report and recommendations from five professional societies. Crit Care Med. 2011;39(5):1113–25.PubMedCrossRef
14.
go back to reference Polderman KH, Herold I. Therapeutic hypothermia and controlled normothermia in the intensive care unit: practical considerations, side effects, and cooling methods. Crit Care Med. 2009;37(3):1101–20.PubMedCrossRef Polderman KH, Herold I. Therapeutic hypothermia and controlled normothermia in the intensive care unit: practical considerations, side effects, and cooling methods. Crit Care Med. 2009;37(3):1101–20.PubMedCrossRef
15.
go back to reference Connolly ES Jr, Rabinstein AA, Carhuapoma JR, et al; American Heart Association Stroke Council; Council on Cardiovascular Radiology and Intervention; Council on Cardiovascular Nursing; Council on Cardiovascular Surgery and Anesthesia; Council on Clinical Cardiology. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke. 2012;43(6):1711–37. Connolly ES Jr, Rabinstein AA, Carhuapoma JR, et al; American Heart Association Stroke Council; Council on Cardiovascular Radiology and Intervention; Council on Cardiovascular Nursing; Council on Cardiovascular Surgery and Anesthesia; Council on Clinical Cardiology. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke. 2012;43(6):1711–37.
16.
go back to reference Pillai S, Praharaj SS, Rao GS, Kolluri VR. Cerebral perfusion pressure management of severe diffuse head injury: effect on brain compliance and intracranial pressure. Neurol India. 2004;52(1):67–71.PubMed Pillai S, Praharaj SS, Rao GS, Kolluri VR. Cerebral perfusion pressure management of severe diffuse head injury: effect on brain compliance and intracranial pressure. Neurol India. 2004;52(1):67–71.PubMed
17.
go back to reference Mourand I, Escuret E, Héroum C, et al. Feasibility of hypothermia beyond 3 weeks in severe ischemic stroke: an open pilot study using γ-hydroxybutyrate. J Neurol Sci. 2012;316(1–2):104–7.PubMedCrossRef Mourand I, Escuret E, Héroum C, et al. Feasibility of hypothermia beyond 3 weeks in severe ischemic stroke: an open pilot study using γ-hydroxybutyrate. J Neurol Sci. 2012;316(1–2):104–7.PubMedCrossRef
18.
go back to reference ARDS Definition Task Force, Ranieri VM, Rubenfeld GD, Thompson BT, et al. Acute respiratory distress syndrome: the Berlin Definition. JAMA. 2012;307(23):2526–33.PubMed ARDS Definition Task Force, Ranieri VM, Rubenfeld GD, Thompson BT, et al. Acute respiratory distress syndrome: the Berlin Definition. JAMA. 2012;307(23):2526–33.PubMed
19.
go back to reference Heuer GG, Smith MJ, Elliott JP, Winn HR, LeRoux PD. Relationship between intracranial pressure and other clinical variables in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg. 2004;101(3):408–16.PubMedCrossRef Heuer GG, Smith MJ, Elliott JP, Winn HR, LeRoux PD. Relationship between intracranial pressure and other clinical variables in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg. 2004;101(3):408–16.PubMedCrossRef
20.
go back to reference Smith ER, Carter BS, Ogilvy CS. Proposed use of prophylactic decompressive craniectomy in poor-grade aneurysmal subarachnoid hemorrhage patients presenting with associated large sylvian hematomas. Neurosurgery. 2002;51(1):117–24.PubMedCrossRef Smith ER, Carter BS, Ogilvy CS. Proposed use of prophylactic decompressive craniectomy in poor-grade aneurysmal subarachnoid hemorrhage patients presenting with associated large sylvian hematomas. Neurosurgery. 2002;51(1):117–24.PubMedCrossRef
21.
go back to reference Schirmer CM, Hoit DA, Malek AM. Decompressive hemicraniectomy for the treatment of intractable intracranial hypertension after aneurysmal subarachnoid hemorrhage. Stroke. 2007;38(3):987–92.PubMedCrossRef Schirmer CM, Hoit DA, Malek AM. Decompressive hemicraniectomy for the treatment of intractable intracranial hypertension after aneurysmal subarachnoid hemorrhage. Stroke. 2007;38(3):987–92.PubMedCrossRef
22.
go back to reference Ziai WC, Port JD, Cowan JA, Garonzik IM, Bhardwaj A, Rigamonti D. Decompressive craniectomy for intractable cerebral edema: experience of a single center. J Neurosurg Anesthesiol. 2003;15(1):25–32.PubMedCrossRef Ziai WC, Port JD, Cowan JA, Garonzik IM, Bhardwaj A, Rigamonti D. Decompressive craniectomy for intractable cerebral edema: experience of a single center. J Neurosurg Anesthesiol. 2003;15(1):25–32.PubMedCrossRef
23.
go back to reference D’Ambrosio AL, Sughrue ME, Yorgason JG, et al. Decompressive hemicraniectomy for poor-grade aneurysmal subarachnoid hemorrhage patients with associated intracerebral hemorrhage: clinical outcome and quality of life assessment. Neurosurgery. 2005;56(1):12–20.PubMed D’Ambrosio AL, Sughrue ME, Yorgason JG, et al. Decompressive hemicraniectomy for poor-grade aneurysmal subarachnoid hemorrhage patients with associated intracerebral hemorrhage: clinical outcome and quality of life assessment. Neurosurgery. 2005;56(1):12–20.PubMed
24.
go back to reference Murakami M, Tsukahara T, Ishikura H, et al. Successful use of prolonged mild hypothermia in a patient with severe head injury and diffuse brain swelling. Case report. Neurol Med Chir (Tokyo). 2007;47(3):116–20.CrossRef Murakami M, Tsukahara T, Ishikura H, et al. Successful use of prolonged mild hypothermia in a patient with severe head injury and diffuse brain swelling. Case report. Neurol Med Chir (Tokyo). 2007;47(3):116–20.CrossRef
25.
go back to reference Ng HK, Hanel R, Freeman W. Prolonged mild-to-moderate hypothermia for refractory intracranial hypertension. J Vasc Interv Neurol. 2009;2(1):142–6.PubMedCentralPubMed Ng HK, Hanel R, Freeman W. Prolonged mild-to-moderate hypothermia for refractory intracranial hypertension. J Vasc Interv Neurol. 2009;2(1):142–6.PubMedCentralPubMed
26.
go back to reference Polderman KH, Tjong Tjin Joe R, Peerdeman SM, Vandertop WP, Girbes AR. Effects of therapeutic hypothermia on intracranial pressure and outcome in patients with severe head injury. Intensive Care Med. 2002;28(11):1563–73.PubMedCrossRef Polderman KH, Tjong Tjin Joe R, Peerdeman SM, Vandertop WP, Girbes AR. Effects of therapeutic hypothermia on intracranial pressure and outcome in patients with severe head injury. Intensive Care Med. 2002;28(11):1563–73.PubMedCrossRef
27.
go back to reference Nagao S, Irie K, Kawai N, et al. Protective effect of mild hypothermia on symptomatic vasospasm: a preliminary report. Acta Neurochir Suppl. 2000;76:547–50.PubMed Nagao S, Irie K, Kawai N, et al. Protective effect of mild hypothermia on symptomatic vasospasm: a preliminary report. Acta Neurochir Suppl. 2000;76:547–50.PubMed
28.
go back to reference Anei R, Sakai H, Iihara K, Nagata I. Effectiveness of brain hypothermia treatment in patients with severe subarachnoid hemorrhage: comparisons at a single facility. Neurol Med Chir (Tokyo). 2010;50(10):879–83.PubMedCrossRef Anei R, Sakai H, Iihara K, Nagata I. Effectiveness of brain hypothermia treatment in patients with severe subarachnoid hemorrhage: comparisons at a single facility. Neurol Med Chir (Tokyo). 2010;50(10):879–83.PubMedCrossRef
29.
go back to reference Clifton GL, Valadka A, Zygun D, et al. Very early hypothermia induction in patients with severe brain injury (the National Acute Brain Injury Study: Hypothermia II): a randomised trial. Lancet Neurol. 2011;10:131–9.PubMedCentralPubMedCrossRef Clifton GL, Valadka A, Zygun D, et al. Very early hypothermia induction in patients with severe brain injury (the National Acute Brain Injury Study: Hypothermia II): a randomised trial. Lancet Neurol. 2011;10:131–9.PubMedCentralPubMedCrossRef
30.
go back to reference Polderman KH. Mechanisms of action, physiological effects, and complications of hypothermia. Crit Care Med. 2009;37(7 Suppl):S186–202.PubMedCrossRef Polderman KH. Mechanisms of action, physiological effects, and complications of hypothermia. Crit Care Med. 2009;37(7 Suppl):S186–202.PubMedCrossRef
31.
go back to reference Burger CD, Resar RK. “Ventilator bundle” approach to prevention of ventilator-associated pneumonia. Mayo Clin Proc. 2006;81(6):849–50.PubMedCrossRef Burger CD, Resar RK. “Ventilator bundle” approach to prevention of ventilator-associated pneumonia. Mayo Clin Proc. 2006;81(6):849–50.PubMedCrossRef
32.
go back to reference Kamps M, Bisschops LA, van der Hoeven JG, Hoedemaekers CW. Hypothermia does not increase the risk of infection: a case control study. Crit Care. 2011;15(1):R48.PubMedCentralPubMedCrossRef Kamps M, Bisschops LA, van der Hoeven JG, Hoedemaekers CW. Hypothermia does not increase the risk of infection: a case control study. Crit Care. 2011;15(1):R48.PubMedCentralPubMedCrossRef
33.
go back to reference Ramsey, D, Hurst, R, Soto Soto, J, Freeman, M, Divertie, G, Freeman, WD. The “NAP-VAP” Study: CT chest is strongly predictive of neurologic aspiration pneumonia when compared to chest X ray on admission.In: 9th Annual Neurocritical Care Society Meeting, 2011. Poster #233. Ramsey, D, Hurst, R, Soto Soto, J, Freeman, M, Divertie, G, Freeman, WD. The “NAP-VAP” Study: CT chest is strongly predictive of neurologic aspiration pneumonia when compared to chest X ray on admission.In: 9th Annual Neurocritical Care Society Meeting, 2011. Poster #233.
34.
go back to reference Young AB, Ott LG, Beard D, Dempsey RJ, Tibbs PA, McClain CJ. The acute-phase response of the brain-injured patient. J Neurosurg. 1988;69(3):375–80.PubMedCrossRef Young AB, Ott LG, Beard D, Dempsey RJ, Tibbs PA, McClain CJ. The acute-phase response of the brain-injured patient. J Neurosurg. 1988;69(3):375–80.PubMedCrossRef
35.
go back to reference Rodling-Wahlström M, Olivecrona M, Koskinen LO, Naredi S, Hultin M. Subarachnoid haemorrhage induces an inflammatory response followed by a delayed persisting increase in asymmetric dimethylarginine. Scand J Clin Lab Invest. 2012;72(6):484–9.PubMedCrossRef Rodling-Wahlström M, Olivecrona M, Koskinen LO, Naredi S, Hultin M. Subarachnoid haemorrhage induces an inflammatory response followed by a delayed persisting increase in asymmetric dimethylarginine. Scand J Clin Lab Invest. 2012;72(6):484–9.PubMedCrossRef
36.
go back to reference Hoesch RE, Lin E, Young M, et al. Acute lung injury in critical neurological illness. Crit Care Med. 2012;40(2):587–93.PubMedCrossRef Hoesch RE, Lin E, Young M, et al. Acute lung injury in critical neurological illness. Crit Care Med. 2012;40(2):587–93.PubMedCrossRef
37.
go back to reference Bratton SL, Davis RL. Acute lung injury in isolated traumatic brain injury. Neurosurgery. 1997;40(4):707–12.PubMedCrossRef Bratton SL, Davis RL. Acute lung injury in isolated traumatic brain injury. Neurosurgery. 1997;40(4):707–12.PubMedCrossRef
38.
go back to reference Salim A, Martin M, Brown C, et al. The presence of the adult respiratory distress syndrome does not worsen mortality or discharge disability in blunt trauma patients with severe traumatic brain injury. Injury. 2008;39(1):30–5.PubMedCrossRef Salim A, Martin M, Brown C, et al. The presence of the adult respiratory distress syndrome does not worsen mortality or discharge disability in blunt trauma patients with severe traumatic brain injury. Injury. 2008;39(1):30–5.PubMedCrossRef
39.
go back to reference Petridis AK, Doukas A, Kienke S, et al. The effect of lung-protective permissive hypercapnia in intracerebral pressure in patients with subarachnoid haemorrhage and ARDS. A retrospective study. Acta Neurochir (Wien). 2010;152(12):2143–5.CrossRef Petridis AK, Doukas A, Kienke S, et al. The effect of lung-protective permissive hypercapnia in intracerebral pressure in patients with subarachnoid haemorrhage and ARDS. A retrospective study. Acta Neurochir (Wien). 2010;152(12):2143–5.CrossRef
40.
go back to reference Duan M, Berra L, Kumar A, et al. Use of hypothermia to allow low-tidal-volume ventilation in a patient with ARDS. Respir Care. 2011;56(12):1956–8.PubMedCrossRef Duan M, Berra L, Kumar A, et al. Use of hypothermia to allow low-tidal-volume ventilation in a patient with ARDS. Respir Care. 2011;56(12):1956–8.PubMedCrossRef
41.
go back to reference Villar J, Slutsky AS. Effects of induced hypothermia in patients with septic adult respiratory distress syndrome. Resuscitation. 1993;26(2):183–92.PubMedCrossRef Villar J, Slutsky AS. Effects of induced hypothermia in patients with septic adult respiratory distress syndrome. Resuscitation. 1993;26(2):183–92.PubMedCrossRef
Metadata
Title
Effect of Prolonged Therapeutic Hypothermia on Intracranial Pressure, Organ Function, and Hospital Outcomes Among Patients with Aneurysmal Subarachnoid Hemorrhage
Authors
Lioudmila V. Karnatovskaia
Augustine S. Lee
Emir Festic
Christopher L. Kramer
William D. Freeman
Publication date
01-12-2014
Publisher
Springer US
Published in
Neurocritical Care / Issue 3/2014
Print ISSN: 1541-6933
Electronic ISSN: 1556-0961
DOI
https://doi.org/10.1007/s12028-014-9989-4

Other articles of this Issue 3/2014

Neurocritical Care 3/2014 Go to the issue