Hyperoxemia during the hyperacute phase of aneurysmal subarachnoid hemorrhage is associated with delayed cerebral ischemia and poor outcome: a retrospective observational study

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OBJECTIVE

The harmful effects of hyperoxemia have been reported in critically ill patients with various disorders, including those with brain injuries. However, the effect of hyperoxemia on aneurysmal subarachnoid hemorrhage (aSAH) patients is unclear. In this study the authors aimed to determine whether hyperoxemia during the hyperacute or acute phase in patients with aSAH is associated with delayed cerebral ischemia (DCI) and poor neurological outcome.

METHODS

In this single-center retrospective study, data from patients with aSAH treated between January 2011 and June 2017 were reviewed. The patients were classified into groups according to whether they experienced DCI (DCI group and non-DCI group) and whether they had a poor outcome at discharge (poor outcome group and favorable outcome group). The background characteristics and time-weighted average (TWA) PaO2 during the first 24 hours after arrival at the treatment facility (TWA24h-PaO2) and between the first 24 hours after arrival and day 6 (TWA6d-PaO2), the hyperacute and acute phases, respectively, were compared between the groups. Factors related to DCI and poor outcome were evaluated with logistic regression analyses.

RESULTS

Of 197 patients with aSAH, 42 patients experienced DCI and 82 patients had a poor outcome at discharge. TWA24h-PaO2 was significantly higher in the DCI group than in the non-DCI group (186 [141–213] vs 161 [138–192] mm Hg, p = 0.029) and in the poor outcome group than in the favorable outcome group (176 [154–205] vs 156 [136–188] mm Hg, p = 0.004). TWA6d-PaO2 did not differ significantly between the groups. Logistic regression analyses revealed that higher TWA24h-PaO2 was an independent risk factor for DCI (OR 1.09, 95% CI 1.01–1.17, p = 0.037) and poor outcome (OR 1.17, 95% CI 1.06–1.29, p = 0.002).

CONCLUSIONS

Hyperoxemia during the first 24 hours was associated with DCI and a poor outcome in patients with aSAH. Excessive oxygen therapy might have an adverse effect in the hyperacute phase of aSAH.

ABBREVIATIONS ABG = arterial blood gas; APACHE II = Acute Physiology and Chronic Health Evaluation II; aSAH = aneurysmal subarachnoid hemorrhage; DCI = delayed cerebral ischemia; EBI = early brain injury; FIO2 = fraction of inspired oxygen; GCS = Glasgow Coma Scale; GOS = Glasgow Outcome Scale; ICH = intracerebral hematoma; IVH = intraventricular hemorrhage; PaO2 = partial pressure of arterial oxygen; TWA = time-weighted average; TWA6d = TWA from 24 hours after arrival at the treatment facility to postbleeding day 6; TWA24h = TWA during the first 24 hours after arrival at the treatment facility.
Article Information

Contributor Notes

Correspondence Shinya Fukuda: Advanced Medical Emergency and Critical Care Center, Yamaguchi University Hospital, Yamaguchi, Japan. sfukuda-ygc@umin.ac.jp.INCLUDE WHEN CITING Published online November 15, 2019; DOI: 10.3171/2019.9.JNS19781.Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
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References
  • 1

    Cahill JZhang JH: Subarachnoid hemorrhage: is it time for a new direction? Stroke 40 (3 Suppl):S86S872009

  • 2

    de Graaff AEDongelmans DABinnekade JMde Jonge E: Clinicians’ response to hyperoxia in ventilated patients in a Dutch ICU depends on the level of FiO2. Intensive Care Med 37:46512011

    • Search Google Scholar
    • Export Citation
  • 3

    de Oliveira Manoel ALGoffi AMarotta TRSchweizer TAAbrahamson SMacdonald RL: The critical care management of poor-grade subarachnoid haemorrhage. Crit Care 20:212016

    • Search Google Scholar
    • Export Citation
  • 4

    Dupont SRabinstein AA: CT evaluation of lateral ventricular dilatation after subarachnoid hemorrhage: baseline bicaudate index values [correction of balues]. Neurol Res 35:1031062013

    • Search Google Scholar
    • Export Citation
  • 5

    Eisenhut M: Vasospasm in cerebral inflammation. Int J Inflamm 2014:5097072014

  • 6

    Fisher CMKistler JPDavis JM: Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:191980

    • Search Google Scholar
    • Export Citation
  • 7

    Friedrich BMüller FFeiler SSchöller KPlesnila N: Experimental subarachnoid hemorrhage causes early and long-lasting microarterial constriction and microthrombosis: an in-vivo microscopy study. J Cereb Blood Flow Metab 32:4474552012

    • Search Google Scholar
    • Export Citation
  • 8

    Granger DNKvietys PR: Reperfusion injury and reactive oxygen species: the evolution of a concept. Redox Biol 6:5245512015

  • 9

    Haorah JRamirez SHSchall KSmith DPandya RPersidsky Y: Oxidative stress activates protein tyrosine kinase and matrix metalloproteinases leading to blood-brain barrier dysfunction. J Neurochem 101:5665762007

    • Search Google Scholar
    • Export Citation
  • 10

    Jennett BBond M: Assessment of outcome after severe brain damage. Lancet 1:4804841975

  • 11

    Jeon SBChoi HABadjatia NSchmidt JMLantigua HClaassen J: Hyperoxia may be related to delayed cerebral ischemia and poor outcome after subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry 85:130113072014

    • Search Google Scholar
    • Export Citation
  • 12

    Kaneda KFujita MYamashita SKaneko TKawamura YIzumi T: Prognostic value of biochemical markers of brain damage and oxidative stress in post-surgical aneurysmal subarachnoid hemorrhage patients. Brain Res Bull 81:1731772010

    • Search Google Scholar
    • Export Citation
  • 13

    Kilgannon JHJones AEShapiro NIAngelos MGMilcarek BHunter K: Association between arterial hyperoxia following resuscitation from cardiac arrest and in-hospital mortality. JAMA 303:216521712010

    • Search Google Scholar
    • Export Citation
  • 14

    Lång MRaj RSkrifvars MBKoivisto TLehto HKivisaari R: Early moderate hyperoxemia does not predict outcome after aneurysmal subarachnoid hemorrhage. Neurosurgery 78:5405452016

    • Search Google Scholar
    • Export Citation
  • 15

    Mattos JDCampos MORocha MPMansur DERocha HNMGarcia VP: Human brain blood flow and metabolism during isocapnic hyperoxia: the role of reactive oxygen species. J Physiol 597:7417552019

    • Search Google Scholar
    • Export Citation
  • 16

    McGirt MJLynch JRBlessing RWarner DSFriedman AHLaskowitz DT: Serum von Willebrand factor, matrix metalloproteinase-9, and vascular endothelial growth factor levels predict the onset of cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery 51:112811352002

    • Search Google Scholar
    • Export Citation
  • 17

    Mehta VRussin JSpirtos AHe SAdamczyk PAmar AP: Matrix metalloproteinases in cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Neurol Res Int 2013:9437612013

    • Search Google Scholar
    • Export Citation
  • 18

    Nieuwkamp DJSetz LEAlgra ALinn FHde Rooij NKRinkel GJ: Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol 8:6356422009

    • Search Google Scholar
    • Export Citation
  • 19

    Parke RLEastwood GMMcGuinness SP: Oxygen therapy in non-intubated adult intensive care patients: a point prevalence study. Crit Care Resusc 15:2872932013

    • Search Google Scholar
    • Export Citation
  • 20

    Passier PEVisser-Meily JMRinkel GJLindeman EPost MW: Life satisfaction and return to work after aneurysmal subarachnoid hemorrhage. J Stroke Cerebrovasc Dis 20:3243292011

    • Search Google Scholar
    • Export Citation
  • 21

    Pierini DBryan NS: Nitric oxide availability as a marker of oxidative stress. Methods Mol Biol 1208:63712015

  • 22

    Qu JChen WHu RFeng H: The injury and therapy of reactive oxygen species in intracerebral hemorrhage looking at mitochondria. Oxid Med Cell Longev 2016:25929352016

    • Search Google Scholar
    • Export Citation
  • 23

    Rincon FKang JMaltenfort MVibbert MUrtecho JAthar MK: Association between hyperoxia and mortality after stroke: a multicenter cohort study. Crit Care Med 42:3873962014

    • Search Google Scholar
    • Export Citation
  • 24

    Roffe CNevatte TSim JBishop JIves NFerdinand P: Effect of routine low-dose oxygen supplementation on death and disability in adults with acute stroke: the Stroke Oxygen Study Randomized Clinical Trial. JAMA 318:112511352017

    • Search Google Scholar
    • Export Citation
  • 25

    Rowland MJHadjipavlou GKelly MWestbrook JPattinson KT: Delayed cerebral ischaemia after subarachnoid haemorrhage: looking beyond vasospasm. Br J Anaesth 109:3153292012

    • Search Google Scholar
    • Export Citation
  • 26

    Sabri MLass EMacdonald RL: Early brain injury: a common mechanism in subarachnoid hemorrhage and global cerebral ischemia. Stroke Res Treat 2013:3940362013

    • Search Google Scholar
    • Export Citation
  • 27

    Sanderson THReynolds CAKumar RPrzyklenk KHüttemann M: Molecular mechanisms of ischemia-reperfusion injury in brain: pivotal role of the mitochondrial membrane potential in reactive oxygen species generation. Mol Neurobiol 47:9232013

    • Search Google Scholar
    • Export Citation
  • 28

    Sehba FAPluta RMZhang JH: Metamorphosis of subarachnoid hemorrhage research: from delayed vasospasm to early brain injury. Mol Neurobiol 43:27402011

    • Search Google Scholar
    • Export Citation
  • 29

    Siuta MZuckerman SLMocco J: Nitric oxide in cerebral vasospasm: theories, measurement, and treatment. Neurol Res Int 2013:9724172013

    • Search Google Scholar
    • Export Citation
  • 30

    Sudlow CLWarlow CP: Comparable studies of the incidence of stroke and its pathological types: results from an international collaboration. Stroke 28:4914991997

    • Search Google Scholar
    • Export Citation
  • 31

    Vereczki VMartin ERosenthal REHof PRHoffman GEFiskum G: Normoxic resuscitation after cardiac arrest protects against hippocampal oxidative stress, metabolic dysfunction, and neuronal death. J Cereb Blood Flow Metab 26:8218352006

    • Search Google Scholar
    • Export Citation
  • 32

    Vespa PMBleck TP: Neurogenic pulmonary edema and other mechanisms of impaired oxygenation after aneurysmal subarachnoid hemorrhage. Neurocrit Care 1:1571702004

    • Search Google Scholar
    • Export Citation
  • 33

    Zwemer CFWhitesall SED’Alecy LG: Cardiopulmonary-cerebral resuscitation with 100% oxygen exacerbates neurological dysfunction following nine minutes of normothermic cardiac arrest in dogs. Resuscitation 27:1591701994

    • Search Google Scholar
    • Export Citation
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