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Individualized Thresholds of Hypoxemia and Hyperoxemia and their Effect on Outcome in Acute Brain Injured Patients: A Secondary Analysis of the ENIO Study

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Abstract

Background

In acute brain injury (ABI), the effects of hypoxemia as a potential cause of secondary brain damage and poor outcome are well documented, whereas the impact of hyperoxemia is unclear. The primary aim of this study was to assess the episodes of hypoxemia and hyperoxemia in patients with ABI during the intensive care unit (ICU) stay and to determine their association with in-hospital mortality. The secondary aim was to identify the optimal thresholds of arterial partial pressure of oxygen (PaO2) predicting in-hospital mortality.

Methods

We conducted a secondary analysis of a prospective multicenter observational cohort study. Adult patients with ABI (traumatic brain injury, subarachnoid aneurysmal hemorrhage, intracranial hemorrhage, ischemic stroke) with available data on PaO2 during the ICU stay were included. Hypoxemia was defined as PaO2 < 80 mm Hg, normoxemia was defined as PaO2 between 80 and 120 mm Hg, mild/moderate hyperoxemia was defined as PaO2 between 121 and 299 mm Hg, and severe hyperoxemia was defined as PaO2 levels ≥ 300 mm Hg.

Results

A total of 1,407 patients were included in this study. The mean age was 52 (±18) years, and 929 (66%) were male. Over the ICU stay, the fractions of patients in the study cohort who had at least one episode of hypoxemia, mild/moderate hyperoxemia, and severe hyperoxemia were 31.3%, 53.0%, and 1.7%, respectively. PaO2 values below 92 mm Hg and above 156 mm Hg were associated with an increased probability of in-hospital mortality. Differences were observed among subgroups of patients with ABI, with consistent effects only seen in patients without traumatic brain injury.

Conclusions

In patients with ABI, hypoxemia and mild/moderate hyperoxemia were relatively frequent. Hypoxemia and hyperoxemia during ICU stay may influence in-hospital mortality. However, the small number of oxygen values collected represents a major limitation of the study.

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Data Availability

The data sets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

The ENIO Collaborators: Paër-sélim Abback1, Anaïs Codorniu1, Giuseppe Citerio2, Vittoria Ludovica Sala3, Marinella Astuto4, Eleonora Tringali4, Daniela Alampi5, Monica Rocco5, Jessica Giuseppina Maugeri6, Bellissima Agrippino6, Matteo Filippini7, Nicoletta Lazzeri7, Andrea Cortegiani8, Mariachiara Ippolito8, Chiara Robba9, Denise Battaglini9, Patrick Biston10, Mohamed Fathi Al-Gharyani11, Russell Chabanne12, Léo Astier12, Benjamin Soyer13, Samuel Gaugain13, Alice Zimmerli14, Urs Pietsch15, Miodrag Filipovic15, Giovanna Brandi16, Giulio Bicciato16, Ainhoa Serrano17, Berta Monleon17, Peter van Vliet18, Benjamin Marcel Gerretsen18, Iris Xochitl Ortiz-macias19, Jun Oto20, Noriya Enomoto21, Tomomichi Matsuda22, Nobutaka Masui22, Pierre Garçon23, Jonathan Zarka23, Wytze J. Vermeijden24, Alexander Daniel Cornet24, Sergio Reyes Inurrigarro25, Rafael Cirino Lara Domínguez25, Maria Mercedes Bellini26, Maria Milagros Gomez-Haedo26, Laura Lamot27, Jose Orquera28, Matthieu Biais29, Delphine Georges29, Arvind Baronia30, Roberto Carlos Miranda-Ackerman31, Francisco José Barbosa-Camacho31, John Porter32, Miguel Lopez-Morales32, Thomas Geeraerts33, Baptiste Compagnon33, David Pérez-Torres34, Estefanía Prol-Silva34, Hana Basheer Yahya35, Ala Khaled36, Mohamed Ghula36, Andrea Cracchiolo Neville37, Maria Daniela Palma37, Cristian Deana38, Luigi Vetrugno39, Manuel J. Rivera Chavez40, Rocio Mendoza Trujillo40, Vincent Legros41, Benjamin Brochet41, Olivier Huet42, Marie Geslain42, Mathieu van der Jagt43, Job van Steenkiste43, Hazem Ahmed44, Alexander Edward Coombs45, Jessie Welbourne45, Ana Alicia Velarde Pineda46, Víctor Hugo Nubert Castillo46, Mohammed A. Azab47, Ahmed Y. Azzam47, David Michael Paul van Meenen42, Gilberto Adrian Gascav49, Alfredo Arellano49, Forttino Galicia-Espinosa50, José Carlos García-Ramos50, Ghanshyam Yadav51, Amarendra Kumar Jha51, Vincent Robert-Edan52, Pierre-Andre Rodie-Talbere52, Gaurav Jain53, Sagarika Panda53, Sonika Agarwal54, Yashbir Deewan54, Gilberto Adrian Gasca49, Alfredo Arellano49, Syed Tariq Reza55, Md. Mozaffer Hossain55, Christos Papadas56, Vasiliki Chantziara57, Chrysanthi Sklavou57, Yannick Hourmant58, Nicolas Grillot58, Job van Steenkiste59, Mathieu van der Jagt59, Romain Pirracchio60, Abdelraouf Akkari61, Mohamed Abdelaty62, Ahmed Hashim62, Yoann Launey63, Elodie Masseret63, Sigismond Lasocki64, Soizic Gergaud64, Nicolas Mouclier65, Sulekha Saxena66, Avinash Agrawal66, Shakti Bedanta Mishra67, Samir Samal67, Julio Cesar Mijangos19, Mattias Haënggi14, Mohan Gurjar30, Mohan Gurjar30, Marcus J. Schultz68, Callum Kaye69, Daniela Agustin Godoy28, Pablo Alvarez26, Aikaterini Ioakeimidou56, Yoshitoyo Ueno20, Rafael Badenes70, Abdurrahmaan Ali Suei Elbuzidi61, Michaël Piagnerelli10, Muhammed Elhadi71, Syed Tariq Reza72, Mohammed Atef Azab47, Jean Catherine Digitale73, Nicholas Fong60, Ricardo Campos Cerda74, Norma de la Torre Peredo74. Affiliations: 1Department of Anesthesiology and Critical Care, Beaujon Hospital, DMU Parabol, AP-HP. Nord, 100 Boulevard du General Leclerc, Clichy, France. 2Neurointensive Care Unit, Ospedale San Gerardo, Azienda Socio-Sanitaria Territoriale di Monza, 23 Via Aliprandi, Monza, Italy. 3NeuroIntensive Care Unit, Monza, Italy. 4Anesthesia and Intensive Care Unit, A.O.U. Policlinico “G. Rodolico - S. Marco”, Via Santa Sofia 78, Catania, Italy. 5Sapienza Rome University, A.O.U. Sant'Andrea, Via di grottarossa, 1035/1039, Rome, Italy. 6Arnas garibaldi Catania, Piazza s.maria di gesu' 5, Catania, Italy. 7University Division of Anesthesiology and Critical Care Medicine, Piazzale Spedali Civili, 1, Brescia, Italy. 8Policlinico Paolo Giaccone, Università degli Studi di Palermo, Via del vespro 129, Palermo, Italy. 9San Martino Policlinico Hospital - IRCCS for Oncology and Neurosciences, 10 Largo Rosanna Benzi, Genova. Italy. 10CHU Charleroi- Hôpital Civil Marie-Curie, Université libre de Bruxelles, 140 Chaussée de Bruxelles, Charleroi, Belgium. 11Benghazi Medical Center, Eastern Selmain, Benghazi, Libya. 12Perioperative Medicine Department, Clermont-Ferrand University Hospital, Neurocritical Care Unit, 58 rue Montalembert, Clermont-Ferrand, France. 13Department of Anesthesia and Critical Care, AP-HP, Hôpital Lariboisière, DMU Parabol, Paris, France. 14Department of Intensive Care Medicine, Inselspital, Bern University Hospital, University of Bern, Freiburgstrasse, Bern, Switzerland. 15Department of Anaesthesiology and Intensive Care Medicine, Cantonal Hospital St Gallen, Rorschacher Strasse 95, St. Gallen, Switzerland. 16Institute for Intensive Care Medicine, University Hospital of Zurich, Rämistrasse 100, Zurich, Switzerland. 17Hospital Clinico Universitario Valencia, Avenida Blasco Ibañez, 17, Valencia, Spain. 18Haaglanden Medical Center, Lijnbaan 32, The Hague, Netherlands. 19Hospital Civil de Guadalajara "Fray Antonio Alcalde", Hospital No. 278, Col. El Retiro, Guadalajara, Mexico. 20Tokushima University Hospital, 2-50-1, Kuramoto-cho, Tokushima, Japan. 21Tokushima Prefectural Central Hospital, 1-10-3, Kuramoto-cho, Tokushima, Japan. 22Sapporo Higashi Tokushukai Hospital, 3-1, Kita 33-jo Higashi 14-chome, Higashi-ku, Sapporo, Japan. 23Service de reanimation, 2-4 Cours de la Gondoire, Jossigny, France. 24Department of intensive care, Medisch Spectrum Twente MST, Enschede, the Netherlands, Koningsplein 1, Enschede, The Netherlands, 25UMAE Hospital de Traumatologia y Ortopedia IMSS, Diagonal Defensores de la Republica esquin 6 poniente, Puebla, Mexico. 26Hospital Maciel, ASSE, 25 de Mayo 174, Montevideo, Uruguay. 27Hospital Municipal Leonidas Lucero, Bahia Blanca, Buenos Aires, Argentina.28Sanatorio Pasteur, Chacabuco 675, Catamarca, Argentina. 29Pellegrin SAR Tripode, Pellegrin SAR Tripode, Bordeaux, France. 30Department of Critical Care Medicine, Sanjay Gandhi Postgraduate Institute of Medical Sciences (SGPGIMS), Lucknow. 31Hospital San Javier, Av Pablo Casals 640, Prados Providencia, Guadalajara, Jalisco, Mexico. 32St George's Hospital, Blackshaw Road, London, UK. 33Toulouse University Hospital, Place du Dr Baylac, Toulouse, France. 34Servicio de Medicina Intensiva, Hospital Universitario Río Hortega, Calle Dulzaina, 2, Valladolid, Spain. 35Zliten Medical Centre, Zliten, Libya. 36Abo Selim Trauma Hospital, Tripoli, Libya. 37Terapia Intensiva Con Trauma Center Arnas Ospedale Civico Palermo, Piazza n Leotta 4, Palermo, Italy. 38Academic Hospital of Udine, Piazzale S.Maria della Misericordia, 15, Udine, Chieti, Italy. 39University of Chieti-Pescara, Chieti, Italy. 40Hospital de Alta Especialidad del Bajio, Blvd.Milenio #130 Col. San Carlos la Roncha, León Guanajuato, Mexico. 41Department of Anesthesiology and Critical Care, University Hospital of Reims, Hopital Maison Blanche, 45 Rue Cognacq Jay, Reims, France. 42Department of Anesthesiology and Critical Care, La Cavale Blanche, Boulevard Tanguy Prigent, Brest, France. 43Erasmus MC, Dr Molewaterplein 40, Rotterdam, Netherlands. 44Seoul Clinic, Tripoli, Libya. 45Department of Intensive Care Medicine, University Hospital Plymouth, Derriford Road, Plymouth, Devon, Plymouth, UK. 46Hospital General Regional # 180 IMSS, Carretera a San Sebastian # 1000 Col. Las cumbres 2 Tlajomulco de Zúñiga, Guadalajara, Mexico. 47Cairo University, Giza, Cairo, Egypt. 48Amsterdam UMC, Meibergdreef 9, Amsterdam, Netherlands. 49Hospital Regional de Alta Especialidad de Ixtapaluca, Carretera Federal Mexico -Puebla Km. 34.5, Pueblo de Zoquiapan, Ixtapaluca, Mexico. 50UMAE Hospital de Traumatología y Ortopedia No 21, IMSS Monterrey, Av. J.M. Pino Suárez S/N esq. 15 de Mayo, Monterrey, Mexico. 51Department of Anesthesia, IMS, BHU, Trauma ICU, Varanasi, India. 52Nantes-Laennec, Hopital Laennec CHU Nantes, 1 Bd Jacques Monod, Nantes, France. 53Critical Care Unit, Dept. Of Anaesthesiology and Critical Care, All India Institute of Medical Sciences, Rishikesh, India. 54HIMS, B18/8, HIMS Campus, Dehradun, India. 55Department of Anaesthesia, Analgesia, Palliative & Intensive Care, Dhaka Medical College Hospital, Dhaka, Bangladesh. 56ICU of ASKLEPIEIO G.H.A, V.PAULOU 1, Athens, Greece. 57Saint Savvas Hospital, 151 Alexandras Avenue, Athens, Greece . 58Department of Anesthesiology and Critical Care, Hôtel-Dieu, 1 place Alexis Ricordeau, Nantes, France. 59Erasmus Medical Centre, Doctor Molewaterplein 40, Rotterdam, Netherlands. 60Department of Anesthesia and Perioperative Care, University of California, UCSF, 1001 Potrero Ave, San Francisco, USA. 61Qatar-1, HMC-Doha-Qatar, Doha, Qatar. 62Qatar-2, HMC-Doha-Qatar, Doha, Qatar. 63Department of Anesthesiology and Critical Care, Hopital Pontchaillou, 2 rue Henri le Guilloux, Rennes, France. 64Department of Anesthesiology and Critical Care, 4 rue Larrey, Angers, France. 65Department of Anesthesiology and Critical Care, Hôtel-Dieu, 1 place Alexis Ricordeau , Nantes, France. 66Department of Critical Care Medicine, King George's Medical University, Lucknow, India. 67IMS and SUM Hospital, K8 Kalinga Nagar, Bhubaneswar, India. 68Department of Intensive Care, Amsterdam University Medical Centers, Amsterdam, Netherlands. 69Aberdeen Royal Infirmary, Foresthill, Aberdeen, UK. 70Hospital Clínico Universitario Valencia, Valencia, Spain. 71Faculty of Medicine, University of Tripoli, Furnaj, University road, Tripoli, Lybia. 72Dhaka Medical College Hospital, Dhaka, Bangladesh. 73University of California, UCSF, 550 16th St, San Francisco, USA. 74Critical Care Unit, Hospital General Regional no. 46, Instituto Mexicano del Seguro Social, 2063 Lazaro Cárdenas Av, Guadalajara , Mexico

Funding

The authors have not received any financial support for the research, authorship, and/or publication of this article.

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Author notes

  1. Chiara Robba, Denise Battaglini, Rafael Badenes and Paolo Pelosi have equally contributed.

Authors and Affiliations

  1. IRCCS Ospedale Policlinico San Martino, Genova, Italy

    Chiara Robba, Denise Battaglini & Paolo Pelosi

  2. Department of Surgical Science and Integrated Diagnostic, University of Genova, Genova, Italy

    Chiara Robba & Paolo Pelosi

  3. Department of Anesthesia and Critical Care, CHU Nantes, Nantes Université, Hôtel Dieu, Nantes, France

    Raphael Cinotti & Karim Asehnoune

  4. UMR 1246 SPHERE Methods in Patients-Centered Outcomes and Health Research, University of Nantes, University of Tours, INSERM, Nantes, France

    Raphael Cinotti

  5. Department of Anesthesiology and Critical Care Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Robert Stevens

  6. Department of Intensive Care, Hôpital Universitaire de Bruxelles, Brussels, Belgium

    Fabio Silvio Taccone

  7. Anesthesiology and Surgical-Trauma Intensive Care, University Clinic Hospital, Valencia, Spain

    Rafael Badenes

  8. Department of Surgery, University of Valencia, Valencia, Spain

    Rafael Badenes

  9. INCLIVA Research Medical Institute, Valencia, Spain

    Rafael Badenes

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  1. Chiara Robba
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The ENIO Collaborators

  • Paër-sélim Abback
  • , Anaïs Codorniu
  • , Giuseppe Citerio
  • , Vittoria Ludovica Sala
  • , Marinella Astuto
  • , Eleonora Tringali
  • , Daniela Alampi
  • , Monica Rocco
  • , Jessica Giuseppina Maugeri
  • , Bellissima Agrippino
  • , Matteo Filippini
  • , Nicoletta Lazzeri
  • , Andrea Cortegiani
  • , Mariachiara Ippolito
  • , Chiara Robba
  • , Denise Battaglini
  • , Patrick Biston
  • , Mohamed Fathi Al-Gharyani
  • , Russell Chabanne
  • , Léo Astier
  • , Benjamin Soyer
  • , Samuel Gaugain
  • , Alice Zimmerli
  • , Urs Pietsch
  • , Miodrag Filipovic
  • , Giovanna Brandi
  • , Giulio Bicciato
  • , Ainhoa Serrano
  • , Berta Monleon
  • , Peter van Vliet
  • , Benjamin Marcel Gerretsen
  • , Iris Xochitl Ortiz-macias
  • , Jun Oto
  • , Noriya Enomoto
  • , Tomomichi Matsuda
  • , Nobutaka Masui
  • , Pierre Garçon
  • , Jonathan Zarka
  • , Wytze J. Vermeijden
  • , Alexander Daniel Cornet
  • , Sergio Reyes Inurrigarro
  • , Rafael Cirino Lara Domínguez
  • , Maria Mercedes Bellini
  • , Maria Milagros Gomez-Haedo
  • , Laura Lamot
  • , Jose Orquera
  • , Matthieu Biais
  • , Delphine Georges
  • , Arvind Baronia
  • , Roberto Carlos Miranda-Ackerman
  • , Francisco José Barbosa-Camacho
  • , John Porter
  • , Miguel Lopez-Morales
  • , Thomas Geeraerts
  • , Baptiste Compagnon
  • , David Pérez-Torres
  • , Estefanía Prol-Silva
  • , Hana Basheer Yahya
  • , Ala Khaled
  • , Mohamed Ghula
  • , Andrea Cracchiolo Neville
  • , Maria Daniela Palma
  • , Cristian Deana
  • , Luigi Vetrugno
  • , Manuel J. Rivera Chavez
  • , Rocio Mendoza Trujillo
  • , Vincent Legros
  • , Benjamin Brochet
  • , Olivier Huet
  • , Marie Geslain
  • , Mathieu van der Jagt
  • , Job van Steenkiste
  • , Hazem Ahmed
  • , Alexander Edward Coombs
  • , Jessie Welbourne
  • , Ana Alicia Velarde Pineda
  • , Víctor Hugo Nubert Castillo
  • , Mohammed A. Azab
  • , Ahmed Y. Azzam
  • , David Michael Paul van Meenen
  • , Gilberto Adrian Gasca
  • , Alfredo Arellano
  • , Forttino Galicia-Espinosa
  • , José Carlos García-Ramos
  • , Ghanshyam Yadav
  • , Amarendra Kumar Jha
  • , Vincent Robert-Edan
  • , Pierre-Andre Rodie-Talbere
  • , Gaurav Jain
  • , Sagarika Panda
  • , Sonika Agarwal
  • , Yashbir Deewan
  • , Gilberto Adrian Gasca
  • , Alfredo Arellano
  • , Syed Tariq Reza
  • , Md. Mozaffer Hossain
  • , Christos Papadas
  • , Vasiliki Chantziara
  • , Chrysanthi Sklavou
  • , Yannick Hourmant
  • , Nicolas Grillot
  • , Job van Steenkiste
  • , Mathieu van der Jagt
  • , Romain Pirracchio
  • , Abdelraouf Akkari
  • , Mohamed Abdelaty
  • , Ahmed Hashim
  • , Yoann Launey
  • , Elodie Masseret
  • , Sigismond Lasocki
  • , Soizic Gergaud
  • , Nicolas Mouclier
  • , Sulekha Saxena
  • , Avinash Agrawal
  • , Shakti Bedanta Mishra
  • , Samir Samal
  • , Julio Cesar Mijangos
  • , Mattias Haënggi
  • , Mohan Gurjar
  • , Mohan Gurjar
  • , Marcus J. Schultz
  • , Callum Kaye
  • , Daniela Agustin Godoy
  • , Pablo Alvarez
  • , Aikaterini Ioakeimidou
  • , Yoshitoyo Ueno
  • , Rafael Badenes
  • , Abdurrahmaan Ali Suei Elbuzidi
  • , Michaël Piagnerelli
  • , Muhammed Elhadi
  • , Syed Tariq Reza
  • , Mohammed Atef Azab
  • , Jean Catherine Digitale
  • , Nicholas Fong
  • , Ricardo Campos Cerda
  •  & Norma de la Torre Peredo

Contributions

CR and PP: conception of the work, design. CR, DB, RB, and PP: data interpretation, drafting the manuscript, critical revision of the manuscript, final approval. RB and PP: supervision of the work. All authors: critical revision of the manuscript, final approval.

Corresponding author

Correspondence to Denise Battaglini.

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Conflict of Interest

The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethical Approval/Informed Consent

Approval to conduct this subanalysis was not necessary. Approval to enroll patients in the ENIO main study was obtained from the institutional review board of the promoter center (Groupe Nantais d’Éthique dans le Domaine de la Santé, IRB No. 7/11/2017) and of each participating center. Informed consent was generally waived in accordance with the observational nature of the ENIO study but if necessary was collected in accordance with the local regulations of each involved institutional review board. Informed consent was obtained from the patient or from the patient’s next of kin in case the patient was unable to give the consent at the time of enrollment.

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The ENIO Collaborators: Authors and affiliations are present in Acknowledgment section.

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Robba, C., Battaglini, D., Cinotti, R. et al. Individualized Thresholds of Hypoxemia and Hyperoxemia and their Effect on Outcome in Acute Brain Injured Patients: A Secondary Analysis of the ENIO Study. Neurocrit Care 40, 515–528 (2024). https://doi.org/10.1007/s12028-023-01761-x

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