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Published in: BMC Neurology 1/2016

Open Access 01-12-2016 | Research article

A randomized trial of the effects of the noble gases helium and argon on neuroprotection in a rodent cardiac arrest model

Authors: Patrick Zuercher, Dirk Springe, Denis Grandgirard, Stephen L. Leib, Marius Grossholz, Stephan Jakob, Jukka Takala, Matthias Haenggi

Published in: BMC Neurology | Issue 1/2016

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Abstract

Background

The noble gas xenon is considered as a neuroprotective agent, but availability of the gas is limited. Studies on neuroprotection with the abundant noble gases helium and argon demonstrated mixed results, and data regarding neuroprotection after cardiac arrest are scant. We tested the hypothesis that administration of 50 % helium or 50 % argon for 24 h after resuscitation from cardiac arrest improves clinical and histological outcome in our 8 min rat cardiac arrest model.

Methods

Forty animals had cardiac arrest induced with intravenous potassium/esmolol and were randomized to post-resuscitation ventilation with either helium/oxygen, argon/oxygen or air/oxygen for 24 h. Eight additional animals without cardiac arrest served as reference, these animals were not randomized and not included into the statistical analysis. Primary outcome was assessment of neuronal damage in histology of the region I of hippocampus proper (CA1) from those animals surviving until day 5. Secondary outcome was evaluation of neurobehavior by daily testing of a Neurodeficit Score (NDS), the Tape Removal Test (TRT), a simple vertical pole test (VPT) and the Open Field Test (OFT). Because of the non-parametric distribution of the data, the histological assessments were compared with the Kruskal–Wallis test. Treatment effect in repeated measured assessments was estimated with a linear regression with clustered robust standard errors (SE), where normality is less important.

Results

Twenty-nine out of 40 rats survived until day 5 with significant initial deficits in neurobehavioral, but rapid improvement within all groups randomized to cardiac arrest. There were no statistical significant differences between groups neither in the histological nor in neurobehavioral assessment.

Conclusions

The replacement of air with either helium or argon in a 50:50 air/oxygen mixture for 24 h did not improve histological or clinical outcome in rats subjected to 8 min of cardiac arrest.
Literature
1.
go back to reference Rossetti AO, Oddo M, Logroscino G, Kaplan PW. Prognostication after cardiac arrest and hypothermia: a prospective study. Ann Neurol. 2010;67(3):301–7.PubMed Rossetti AO, Oddo M, Logroscino G, Kaplan PW. Prognostication after cardiac arrest and hypothermia: a prospective study. Ann Neurol. 2010;67(3):301–7.PubMed
2.
go back to reference Madl C, Holzer M. Brain function after resuscitation from cardiac arrest. Curr Opin Crit Care. 2004;10(3):213–7.CrossRefPubMed Madl C, Holzer M. Brain function after resuscitation from cardiac arrest. Curr Opin Crit Care. 2004;10(3):213–7.CrossRefPubMed
3.
go back to reference Sanghavi P, Jena AB, Newhouse JP, Zaslavsky AM. Outcomes After Out-of-Hospital Cardiac Arrest Treated by Basic vs Advanced Life Support. JAMA Intern Med. 2015;175:196–204.CrossRefPubMedPubMedCentral Sanghavi P, Jena AB, Newhouse JP, Zaslavsky AM. Outcomes After Out-of-Hospital Cardiac Arrest Treated by Basic vs Advanced Life Support. JAMA Intern Med. 2015;175:196–204.CrossRefPubMedPubMedCentral
4.
go back to reference Hossmann KA. Cerebral ischemia: models, methods and outcomes. Neuropharmacology. 2008;55(3):257–70.CrossRefPubMed Hossmann KA. Cerebral ischemia: models, methods and outcomes. Neuropharmacology. 2008;55(3):257–70.CrossRefPubMed
5.
go back to reference Weigl M, Tenze G, Steinlechner B, Skhirtladze K, Reining G, Bernardo M, Pedicelli E, Dworschak M. A systematic review of currently available pharmacological neuroprotective agents as a sole intervention before anticipated or induced cardiac arrest. Resuscitation. 2005;65(1):21–39.CrossRefPubMed Weigl M, Tenze G, Steinlechner B, Skhirtladze K, Reining G, Bernardo M, Pedicelli E, Dworschak M. A systematic review of currently available pharmacological neuroprotective agents as a sole intervention before anticipated or induced cardiac arrest. Resuscitation. 2005;65(1):21–39.CrossRefPubMed
6.
go back to reference Huang L, Applegate PM, Gatling JW, Mangus DB, Zhang J, Applegate 2nd RL. A systematic review of neuroprotective strategies after cardiac arrest: from bench to bedside (part II-comprehensive protection). Med Gas Res. 2014;4:10.CrossRefPubMedPubMedCentral Huang L, Applegate PM, Gatling JW, Mangus DB, Zhang J, Applegate 2nd RL. A systematic review of neuroprotective strategies after cardiac arrest: from bench to bedside (part II-comprehensive protection). Med Gas Res. 2014;4:10.CrossRefPubMedPubMedCentral
7.
go back to reference Bernard SA, Gray TW, Buist MD, Jones BM, Silvester W, Gutteridge G, Smith K. Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med. 2002;346(8):557–63.CrossRefPubMed Bernard SA, Gray TW, Buist MD, Jones BM, Silvester W, Gutteridge G, Smith K. Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med. 2002;346(8):557–63.CrossRefPubMed
8.
go back to reference TherapeuticHypothermiaGroup. Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N Engl J Med. 2002;346(8):549–56.CrossRef TherapeuticHypothermiaGroup. Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N Engl J Med. 2002;346(8):549–56.CrossRef
9.
go back to reference Nielsen N, Wetterslev J, Cronberg T, Erlinge D, Gasche Y, Hassager C, Horn J, Hovdenes J, Kjaergaard J, Kuiper M, et al. Targeted temperature management at 33 degrees C versus 36 degrees C after cardiac arrest. N Engl J Med. 2013;369(23):2197–206.CrossRefPubMed Nielsen N, Wetterslev J, Cronberg T, Erlinge D, Gasche Y, Hassager C, Horn J, Hovdenes J, Kjaergaard J, Kuiper M, et al. Targeted temperature management at 33 degrees C versus 36 degrees C after cardiac arrest. N Engl J Med. 2013;369(23):2197–206.CrossRefPubMed
10.
go back to reference Maze M. Preclinical neuroprotective actions of xenon and possible implications for human therapeutics: a narrative review. Can J Anaesth. 2016;63(2):212–26.CrossRefPubMed Maze M. Preclinical neuroprotective actions of xenon and possible implications for human therapeutics: a narrative review. Can J Anaesth. 2016;63(2):212–26.CrossRefPubMed
11.
go back to reference David HN, Haelewyn B, Rouillon C, Lecoq M, Chazalviel L, Apiou G, Risso JJ, Lemaire M, Abraini JH. Neuroprotective effects of xenon: a therapeutic window of opportunity in rats subjected to transient cerebral ischemia. FASEB J. 2008;22(4):1275–86.CrossRefPubMed David HN, Haelewyn B, Rouillon C, Lecoq M, Chazalviel L, Apiou G, Risso JJ, Lemaire M, Abraini JH. Neuroprotective effects of xenon: a therapeutic window of opportunity in rats subjected to transient cerebral ischemia. FASEB J. 2008;22(4):1275–86.CrossRefPubMed
12.
go back to reference Homi HM, Yokoo N, Ma D, Warner DS, Franks NP, Maze M, Grocott HP. The neuroprotective effect of xenon administration during transient middle cerebral artery occlusion in mice. Anesthesiology. 2003;99(4):876–81.CrossRefPubMed Homi HM, Yokoo N, Ma D, Warner DS, Franks NP, Maze M, Grocott HP. The neuroprotective effect of xenon administration during transient middle cerebral artery occlusion in mice. Anesthesiology. 2003;99(4):876–81.CrossRefPubMed
13.
go back to reference Petzelt C, Blom P, Schmehl W, Muller J, Kox WJ. Xenon prevents cellular damage in differentiated PC-12 cells exposed to hypoxia. BMC Neurosci. 2004;5:55.CrossRefPubMedPubMedCentral Petzelt C, Blom P, Schmehl W, Muller J, Kox WJ. Xenon prevents cellular damage in differentiated PC-12 cells exposed to hypoxia. BMC Neurosci. 2004;5:55.CrossRefPubMedPubMedCentral
14.
go back to reference Harris K, Armstrong SP, Campos-Pires R, Kiru L, Franks NP, Dickinson R. Neuroprotection against traumatic brain injury by xenon, but not argon, is mediated by inhibition at the N-methyl-D-aspartate receptor glycine site. Anesthesiology. 2013;119(5):1137–48.CrossRefPubMed Harris K, Armstrong SP, Campos-Pires R, Kiru L, Franks NP, Dickinson R. Neuroprotection against traumatic brain injury by xenon, but not argon, is mediated by inhibition at the N-methyl-D-aspartate receptor glycine site. Anesthesiology. 2013;119(5):1137–48.CrossRefPubMed
15.
go back to reference Fries M, Brucken A, Cizen A, Westerkamp M, Lower C, Deike-Glindemann J, Schnorrenberger NK, Rex S, Coburn M, Nolte KW, et al. Combining xenon and mild therapeutic hypothermia preserves neurological function after prolonged cardiac arrest in pigs. Crit Care Med. 2012;40(4):1297–303.CrossRefPubMed Fries M, Brucken A, Cizen A, Westerkamp M, Lower C, Deike-Glindemann J, Schnorrenberger NK, Rex S, Coburn M, Nolte KW, et al. Combining xenon and mild therapeutic hypothermia preserves neurological function after prolonged cardiac arrest in pigs. Crit Care Med. 2012;40(4):1297–303.CrossRefPubMed
16.
go back to reference Dickinson R, Franks NP. Bench-to-bedside review: Molecular pharmacology and clinical use of inert gases in anesthesia and neuroprotection. Crit Care. 2010;14(4):229.CrossRefPubMedPubMedCentral Dickinson R, Franks NP. Bench-to-bedside review: Molecular pharmacology and clinical use of inert gases in anesthesia and neuroprotection. Crit Care. 2010;14(4):229.CrossRefPubMedPubMedCentral
17.
go back to reference Coburn M, Maze M, Franks NP. The neuroprotective effects of xenon and helium in an in vitro model of traumatic brain injury. Crit Care Med. 2008;36(2):588–95.CrossRefPubMed Coburn M, Maze M, Franks NP. The neuroprotective effects of xenon and helium in an in vitro model of traumatic brain injury. Crit Care Med. 2008;36(2):588–95.CrossRefPubMed
18.
go back to reference Loetscher PD, Rossaint J, Rossaint R, Weis J, Fries M, Fahlenkamp A, Ryang YM, Grottke O, Coburn M. Argon: neuroprotection in in vitro models of cerebral ischemia and traumatic brain injury. Crit Care. 2009;13(6):R206.CrossRefPubMedPubMedCentral Loetscher PD, Rossaint J, Rossaint R, Weis J, Fries M, Fahlenkamp A, Ryang YM, Grottke O, Coburn M. Argon: neuroprotection in in vitro models of cerebral ischemia and traumatic brain injury. Crit Care. 2009;13(6):R206.CrossRefPubMedPubMedCentral
19.
go back to reference Jawad N, Rizvi M, Gu J, Adeyi O, Tao G, Maze M, Ma D. Neuroprotection (and lack of neuroprotection) afforded by a series of noble gases in an in vitro model of neuronal injury. Neurosci Lett. 2009;460(3):232–6.CrossRefPubMed Jawad N, Rizvi M, Gu J, Adeyi O, Tao G, Maze M, Ma D. Neuroprotection (and lack of neuroprotection) afforded by a series of noble gases in an in vitro model of neuronal injury. Neurosci Lett. 2009;460(3):232–6.CrossRefPubMed
20.
go back to reference David HN, Haelewyn B, Degoulet M, Colomb Jr DG, Risso JJ, Abraini JH. Ex vivo and in vivo neuroprotection induced by argon when given after an excitotoxic or ischemic insult. PLoS One. 2012;7(2):e30934.CrossRefPubMedPubMedCentral David HN, Haelewyn B, Degoulet M, Colomb Jr DG, Risso JJ, Abraini JH. Ex vivo and in vivo neuroprotection induced by argon when given after an excitotoxic or ischemic insult. PLoS One. 2012;7(2):e30934.CrossRefPubMedPubMedCentral
21.
go back to reference Zhuang L, Yang T, Zhao H, Fidalgo AR, Vizcaychipi MP, Sanders RD, Yu B, Takata M, Johnson MR, Ma D. The protective profile of argon, helium, and xenon in a model of neonatal asphyxia in rats. Crit Care Med. 2012;40(6):1724–30.CrossRefPubMed Zhuang L, Yang T, Zhao H, Fidalgo AR, Vizcaychipi MP, Sanders RD, Yu B, Takata M, Johnson MR, Ma D. The protective profile of argon, helium, and xenon in a model of neonatal asphyxia in rats. Crit Care Med. 2012;40(6):1724–30.CrossRefPubMed
22.
go back to reference Brevoord D, Beurskens C, Juffermans N, Van den Bergh W, Lagrand W, Preckel B, Horn J. Helium ventilation is safe and feasible in ICU patients admitted after cardiac arrest. Crit Care. 2012;16 Suppl 1:279.CrossRef Brevoord D, Beurskens C, Juffermans N, Van den Bergh W, Lagrand W, Preckel B, Horn J. Helium ventilation is safe and feasible in ICU patients admitted after cardiac arrest. Crit Care. 2012;16 Suppl 1:279.CrossRef
23.
go back to reference Ryang YM, Fahlenkamp AV, Rossaint R, Wesp D, Loetscher PD, Beyer C, Coburn M. Neuroprotective effects of argon in an in vivo model of transient middle cerebral artery occlusion in rats. Crit Care Med. 2011;39(6):1448–53.CrossRefPubMed Ryang YM, Fahlenkamp AV, Rossaint R, Wesp D, Loetscher PD, Beyer C, Coburn M. Neuroprotective effects of argon in an in vivo model of transient middle cerebral artery occlusion in rats. Crit Care Med. 2011;39(6):1448–53.CrossRefPubMed
24.
go back to reference Brucken A, Cizen A, Fera C, Meinhardt A, Weis J, Nolte K, Rossaint R, Pufe T, Marx G, Fries M. Argon reduces neurohistopathological damage and preserves functional recovery after cardiac arrest in rats. Br J Anaesth. 2013;110 Suppl 1:i106–112.CrossRefPubMed Brucken A, Cizen A, Fera C, Meinhardt A, Weis J, Nolte K, Rossaint R, Pufe T, Marx G, Fries M. Argon reduces neurohistopathological damage and preserves functional recovery after cardiac arrest in rats. Br J Anaesth. 2013;110 Suppl 1:i106–112.CrossRefPubMed
25.
go back to reference Brucken A, Kurnaz P, Bleilevens C, Derwall M, Weis J, Nolte K, Rossaint R, Fries M. Dose dependent neuroprotection of the noble gas argon after cardiac arrest in rats is not mediated by KATP-Channel opening. Resuscitation. 2014;85(6):826–32.CrossRefPubMed Brucken A, Kurnaz P, Bleilevens C, Derwall M, Weis J, Nolte K, Rossaint R, Fries M. Dose dependent neuroprotection of the noble gas argon after cardiac arrest in rats is not mediated by KATP-Channel opening. Resuscitation. 2014;85(6):826–32.CrossRefPubMed
26.
go back to reference Brucken A, Kurnaz P, Bleilevens C, Derwall M, Weis J, Nolte K, Rossaint R, Fries M. Delayed Argon Administration Provides Robust Protection Against Cardiac Arrest-Induced Neurological Damage. Neurocrit Care. 2015;22:112–20.CrossRefPubMed Brucken A, Kurnaz P, Bleilevens C, Derwall M, Weis J, Nolte K, Rossaint R, Fries M. Delayed Argon Administration Provides Robust Protection Against Cardiac Arrest-Induced Neurological Damage. Neurocrit Care. 2015;22:112–20.CrossRefPubMed
27.
go back to reference Ristagno G, Fumagalli F, Russo I, Tantillo S, Zani DD, Locatelli V, De Maglie M, Novelli D, Staszewsky L, Vago T, et al. Postresuscitation treatment with argon improves early neurological recovery in a porcine model of cardiac arrest. Shock. 2014;41(1):72–8.CrossRefPubMed Ristagno G, Fumagalli F, Russo I, Tantillo S, Zani DD, Locatelli V, De Maglie M, Novelli D, Staszewsky L, Vago T, et al. Postresuscitation treatment with argon improves early neurological recovery in a porcine model of cardiac arrest. Shock. 2014;41(1):72–8.CrossRefPubMed
28.
go back to reference Bendel S, Springe D, Pereira A, Grandgirard D, Leib SL, Putzu A, Schlickeiser J, Jakob SM, Takala J, Haenggi M. Do different anesthesia regimes affect hippocampal apoptosis and neurologic deficits in a rodent cardiac arrest model? BMC Anesthesiol. 2015;15:2.CrossRefPubMedPubMedCentral Bendel S, Springe D, Pereira A, Grandgirard D, Leib SL, Putzu A, Schlickeiser J, Jakob SM, Takala J, Haenggi M. Do different anesthesia regimes affect hippocampal apoptosis and neurologic deficits in a rodent cardiac arrest model? BMC Anesthesiol. 2015;15:2.CrossRefPubMedPubMedCentral
29.
go back to reference Schmued LC, Hopkins KJ. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res. 2000;874(2):123–30.CrossRefPubMed Schmued LC, Hopkins KJ. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res. 2000;874(2):123–30.CrossRefPubMed
30.
go back to reference Frick T, Springe D, Grandgirard D, Leib SL, Haenggi M: An improved simple rat model for global cerebral ischaemia by induced cardiac arrest. Neurol Res. 2015:1743132815Y0000000090. [Epub ahead of print]. Frick T, Springe D, Grandgirard D, Leib SL, Haenggi M: An improved simple rat model for global cerebral ischaemia by induced cardiac arrest. Neurol Res. 2015:1743132815Y0000000090. [Epub ahead of print].
31.
go back to reference Adamczyk S, Robin E, Simerabet M, Kipnis E, Tavernier B, Vallet B, Bordet R, Lebuffe G. Sevoflurane pre- and post-conditioning protect the brain via the mitochondrial K ATP channel. Br J Anaesth. 2010;104(2):191–200.CrossRefPubMed Adamczyk S, Robin E, Simerabet M, Kipnis E, Tavernier B, Vallet B, Bordet R, Lebuffe G. Sevoflurane pre- and post-conditioning protect the brain via the mitochondrial K ATP channel. Br J Anaesth. 2010;104(2):191–200.CrossRefPubMed
32.
go back to reference Zhang LM, Zhao XC, Sun WB, Li R, Jiang XJ. Sevoflurane post-conditioning protects primary rat cortical neurons against oxygen-glucose deprivation/resuscitation via down-regulation in mitochondrial apoptosis axis of Bid, Bim, Puma-Bax and Bak mediated by Erk1/2. J Neurol Sci. 2015;357(1–2):80–7.CrossRefPubMed Zhang LM, Zhao XC, Sun WB, Li R, Jiang XJ. Sevoflurane post-conditioning protects primary rat cortical neurons against oxygen-glucose deprivation/resuscitation via down-regulation in mitochondrial apoptosis axis of Bid, Bim, Puma-Bax and Bak mediated by Erk1/2. J Neurol Sci. 2015;357(1–2):80–7.CrossRefPubMed
33.
go back to reference Katz L, Ebmeyer U, Safar P, Radovsky A, Neumar R. Outcome model of asphyxial cardiac arrest in rats. J Cereb Blood Flow Metab. 1995;15(6):1032–9.CrossRefPubMed Katz L, Ebmeyer U, Safar P, Radovsky A, Neumar R. Outcome model of asphyxial cardiac arrest in rats. J Cereb Blood Flow Metab. 1995;15(6):1032–9.CrossRefPubMed
34.
go back to reference Manwani B, Liu F, Xu Y, Persky R, Li J, McCullough LD. Functional recovery in aging mice after experimental stroke. Brain Behav Immun. 2011;25(8):1689–700.CrossRefPubMedPubMedCentral Manwani B, Liu F, Xu Y, Persky R, Li J, McCullough LD. Functional recovery in aging mice after experimental stroke. Brain Behav Immun. 2011;25(8):1689–700.CrossRefPubMedPubMedCentral
35.
go back to reference Bouet V, Freret T, Toutain J, Divoux D, Boulouard M, Schumann-Bard P. Sensorimotor and cognitive deficits after transient middle cerebral artery occlusion in the mouse. Exp Neurol. 2007;203(2):555–67.CrossRefPubMed Bouet V, Freret T, Toutain J, Divoux D, Boulouard M, Schumann-Bard P. Sensorimotor and cognitive deficits after transient middle cerebral artery occlusion in the mouse. Exp Neurol. 2007;203(2):555–67.CrossRefPubMed
36.
go back to reference Albertsmeier M, Teschendorf P, Popp E, Galmbacher R, Vogel P, Bottiger BW. Evaluation of a tape removal test to assess neurological deficit after cardiac arrest in rats. Resuscitation. 2007;74(3):552–8.CrossRefPubMed Albertsmeier M, Teschendorf P, Popp E, Galmbacher R, Vogel P, Bottiger BW. Evaluation of a tape removal test to assess neurological deficit after cardiac arrest in rats. Resuscitation. 2007;74(3):552–8.CrossRefPubMed
37.
38.
go back to reference Schmidt-Kastner R, Freund TF. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience. 1991;40(3):599–636.CrossRefPubMed Schmidt-Kastner R, Freund TF. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience. 1991;40(3):599–636.CrossRefPubMed
39.
go back to reference Schmidt-Kastner R, Hossmann KA. Distribution of ischemic neuronal damage in the dorsal hippocampus of rat. Acta Neuropathol. 1988;76(4):411–21.CrossRefPubMed Schmidt-Kastner R, Hossmann KA. Distribution of ischemic neuronal damage in the dorsal hippocampus of rat. Acta Neuropathol. 1988;76(4):411–21.CrossRefPubMed
40.
go back to reference Abd-Allah SA, Rogers MS, Terry M, Gross M, Perkin RM. Helium-oxygen therapy for pediatric acute severe asthma requiring mechanical ventilation. Pediatr Crit Care Med. 2003;4(3):353–7.CrossRefPubMed Abd-Allah SA, Rogers MS, Terry M, Gross M, Perkin RM. Helium-oxygen therapy for pediatric acute severe asthma requiring mechanical ventilation. Pediatr Crit Care Med. 2003;4(3):353–7.CrossRefPubMed
41.
go back to reference Pan Y, Zhang H, Acharya AB, Cruz-Flores S, Panneton WM. The effect of heliox treatment in a rat model of focal transient cerebral ischemia. Neurosci Lett. 2011;497(2):144–7.CrossRefPubMed Pan Y, Zhang H, Acharya AB, Cruz-Flores S, Panneton WM. The effect of heliox treatment in a rat model of focal transient cerebral ischemia. Neurosci Lett. 2011;497(2):144–7.CrossRefPubMed
42.
go back to reference David HN, Haelewyn B, Chazalviel L, Lecocq M, Degoulet M, Risso JJ, Abraini JH. Post-ischemic helium provides neuroprotection in rats subjected to middle cerebral artery occlusion-induced ischemia by producing hypothermia. J Cereb Blood Flow Metab. 2009;29(6):1159–65.CrossRefPubMed David HN, Haelewyn B, Chazalviel L, Lecocq M, Degoulet M, Risso JJ, Abraini JH. Post-ischemic helium provides neuroprotection in rats subjected to middle cerebral artery occlusion-induced ischemia by producing hypothermia. J Cereb Blood Flow Metab. 2009;29(6):1159–65.CrossRefPubMed
43.
go back to reference Bevins RA, Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study ‘recognition memory’. Nat Protoc. 2006;1(3):1306–11.CrossRefPubMed Bevins RA, Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study ‘recognition memory’. Nat Protoc. 2006;1(3):1306–11.CrossRefPubMed
44.
go back to reference Kiryk A, Pluta R, Figiel I, Mikosz M, Ulamek M, Niewiadomska G, Jablonski M, Kaczmarek L. Transient brain ischemia due to cardiac arrest causes irreversible long-lasting cognitive injury. Behav Brain Res. 2011;219(1):1–7.CrossRefPubMed Kiryk A, Pluta R, Figiel I, Mikosz M, Ulamek M, Niewiadomska G, Jablonski M, Kaczmarek L. Transient brain ischemia due to cardiac arrest causes irreversible long-lasting cognitive injury. Behav Brain Res. 2011;219(1):1–7.CrossRefPubMed
Metadata
Title
A randomized trial of the effects of the noble gases helium and argon on neuroprotection in a rodent cardiac arrest model
Authors
Patrick Zuercher
Dirk Springe
Denis Grandgirard
Stephen L. Leib
Marius Grossholz
Stephan Jakob
Jukka Takala
Matthias Haenggi
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2016
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-016-0565-8

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