Key characteristics impacting survival of COVID-19 extracorporeal membrane oxygenation

doi:10.1186/s13054-022-04053-6

. 2022 Jun 28;26(1):190.

doi: 10.1186/s13054-022-04053-6.

Key characteristics impacting survival of COVID-19 extracorporeal membrane oxygenation

Johannes Herrmann¹, Christopher Lotz¹, Christian Karagiannidis², Steffen Weber-Carstens³, Stefan Kluge⁴, Christian Putensen⁵, Andreas Wehrfritz⁶, Karsten Schmidt⁷, Richard K Ellerkmann⁸, Daniel Oswald⁹, Gösta Lotz¹⁰, Viviane Zotzmann^{11

12}, Onnen Moerer¹³, Christian Kühn¹⁴, Matthias Kochanek¹⁵, Ralf Muellenbach¹⁶, Matthias Gaertner¹⁷, Falk Fichtner¹⁸, Florian Brettner¹⁹, Michael Findeisen²⁰, Markus Heim²¹, Tobias Lahmer²², Felix Rosenow²³, Nils Haake²⁴, Philipp M Lepper²⁵, Peter Rosenberger²⁶, Stephan Braune²⁷, Mirjam Kohls²⁸, Peter Heuschmann^{28

29}, Patrick Meybohm³⁰; German ECMO COVID Study Group

Collaborators, Affiliations

Collaborators

German ECMO COVID Study Group:
Martha E Hübsch, Quirin Notz, Daniel Röder, Peter Kranke, Michaela L Merten, Dominik Jarczak, Kevin Roedl, Jens-Christian Schewe, Stefan F Ehrentraut, Stefan Kreyer, Ixchel Castellanos, Thorsten Brenner, Frank Herbstreit, Florian Espeter, Jan Wiefhoff, Björn Ellger, Florian J Raimann, Michael Sonntagbauer, Tobias Wengenmayer, Dawid Staudacher, Ruslan Natanov, Caroline Rolfes, Christian Reyher, Iuliu-Emilian Torje, Patricia Glaser, Vanessa Rembold, Rainer Haseneder, Jan Sackarnd, Johannes Lepper, Andre Becker, Guy Danziger, Carlos Metz, Valbona Mirakaj, Stefanie Calov, Anna Grau, Kirsten Haas, Katrin Ungethüm, Karl Bihlmaier

Affiliations

¹ Department of Anaesthesiology, Intensive Care, Emergency and Pain Medicine, University Hospital Wuerzburg, Oberduerrbacherstr. 6, 97080, Würzburg, Germany.
² Department of Pneumology and Critical Care Medicine, Cologne-Merheim Hospital, ARDS and ECMO Center, Kliniken Der Stadt Köln, Witten/Herdecke University Hospital, Cologne, Germany.
³ Department of Anesthesiology and Operative Intensive Care Medicine (CCM, CVK), Charité - Universitätsmedizin Berlin, Berlin, Germany.
⁴ Department of Intensive Care, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁵ Department of Anesthesiology and Intensive Care Medicine, University Hospital Bonn, Bonn, Germany.
⁶ Department of Anaesthesiology, University Hospital Erlangen, Friedrich-Alexander University, Erlangen-Nuernberg (FAU), Erlangen, Germany.
⁷ Department of Anesthesiology and Intensive Care Medicine, University Hospital Essen, University Duisburg-Essen, Essen, Germany.
⁸ Department of Anesthesiology and Intensive Care Medicine, Klinikum Dortmund, Klinikum University Witten/Herdecke, Dortmund, Germany.
⁹ Department of Anesthesiology, Intensive Care Medicine and Pain Therapy, Clinic Centre Westfalen, Dortmund, Germany.
¹⁰ Department of Anaesthesiology, Intensive Care Medicine and Pain Therapy, University Hospital Frankfurt, Goethe University Frankfurt, Frankfurt, Germany.
¹¹ Department of Cardiology and Angiology I (Heart Center Freiburg - Bad Krozingen), Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
¹² Interdisciplinary Medical Intensive Care (IMIT), Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
¹³ Department of Anesthesiology, University Medical Center Göttingen, Robert-Koch-Str. 40, 37085, Göttingen, Germany.
¹⁴ Department of Cardiothoracic, Transplantation and Vascular Surgery, Hannover Medical School, Hannover, Germany.
¹⁵ Department of Internal Medicine, Division I (Hematology/Oncology), University Hospital of Cologne, Cologne, Germany.
¹⁶ Department of Anesthesiology and Critical Care Medicine, ARDS/ECMO-Center, Campus Kassel of the University of Southampton, Kassel, Germany.
¹⁷ Department of Anaesthesia, Perioperative Medicine and Interdisciplinary Intensive Care Medicine, ECLS/ECMO-Center, Asklepios Klinik Langen, Langen, Germany.
¹⁸ Department of Anesthesiology and Intensive Care Medicine, University of Leipzig Medical Center, Leipzig, Germany.
¹⁹ ARDS- und ECMO Zentrum München-Nymphenburg, Barmherzige Brüder Krankenhaus München, München, Germany.
²⁰ Klinik für Pneumologie, Internistische Intensiv- und Beatmungsmedizin, München Klinik Harlaching, Munich, Germany.
²¹ Department of Anaesthesiology and Intensive Care Medicine, Technical University of Munich, School of Medicine, Munich, Germany.
²² School of Medicine, University Hospital Rechts Der Isar, Department of Internal Medicine II, University of Munich, Ismaninger Str. 22, 81675, Munich, Germany.
²³ Department of Cardiology I - Coronary and Peripheral Vascular Disease, Heart Failure, University Hospital Muenster, Muenster, Germany.
²⁴ Department of Intensive Care Medicine, Imland Klinik Rendsburg, Rendsburg, Germany.
²⁵ Department of Internal Medicine V- Pneumology, Allergology and Critical Care Medicine, Saarland University, Homburg, Germany.
²⁶ Department of Anesthesiology and Intensive Care Medicine, University Hospital Tübingen, Eberhard Karls University Tübingen, Tübingen, Germany.
²⁷ Department of Medical Intensive Care and Emergency Medicine, St. Franziskus-Hospital Muenster, Münster, Germany.
²⁸ Institute of Clinical Epidemiology and Biometry, University of Würzburg, Würzburg, Germany.
²⁹ Clinical Trial Center Würzburg, Universitätsklinikum Würzburg, Würzburg, Germany.
³⁰ Department of Anaesthesiology, Intensive Care, Emergency and Pain Medicine, University Hospital Wuerzburg, Oberduerrbacherstr. 6, 97080, Würzburg, Germany. Meybohm_P@ukw.de.

PMID: 35765102
PMCID: PMC9238175
DOI: 10.1186/s13054-022-04053-6

Key characteristics impacting survival of COVID-19 extracorporeal membrane oxygenation

Johannes Herrmann et al. Crit Care. 2022.

. 2022 Jun 28;26(1):190.

doi: 10.1186/s13054-022-04053-6.

Authors

Collaborators

German ECMO COVID Study Group:
Martha E Hübsch, Quirin Notz, Daniel Röder, Peter Kranke, Michaela L Merten, Dominik Jarczak, Kevin Roedl, Jens-Christian Schewe, Stefan F Ehrentraut, Stefan Kreyer, Ixchel Castellanos, Thorsten Brenner, Frank Herbstreit, Florian Espeter, Jan Wiefhoff, Björn Ellger, Florian J Raimann, Michael Sonntagbauer, Tobias Wengenmayer, Dawid Staudacher, Ruslan Natanov, Caroline Rolfes, Christian Reyher, Iuliu-Emilian Torje, Patricia Glaser, Vanessa Rembold, Rainer Haseneder, Jan Sackarnd, Johannes Lepper, Andre Becker, Guy Danziger, Carlos Metz, Valbona Mirakaj, Stefanie Calov, Anna Grau, Kirsten Haas, Katrin Ungethüm, Karl Bihlmaier

Affiliations

¹ Department of Anaesthesiology, Intensive Care, Emergency and Pain Medicine, University Hospital Wuerzburg, Oberduerrbacherstr. 6, 97080, Würzburg, Germany.
² Department of Pneumology and Critical Care Medicine, Cologne-Merheim Hospital, ARDS and ECMO Center, Kliniken Der Stadt Köln, Witten/Herdecke University Hospital, Cologne, Germany.
³ Department of Anesthesiology and Operative Intensive Care Medicine (CCM, CVK), Charité - Universitätsmedizin Berlin, Berlin, Germany.
⁴ Department of Intensive Care, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁵ Department of Anesthesiology and Intensive Care Medicine, University Hospital Bonn, Bonn, Germany.
⁶ Department of Anaesthesiology, University Hospital Erlangen, Friedrich-Alexander University, Erlangen-Nuernberg (FAU), Erlangen, Germany.
⁷ Department of Anesthesiology and Intensive Care Medicine, University Hospital Essen, University Duisburg-Essen, Essen, Germany.
⁸ Department of Anesthesiology and Intensive Care Medicine, Klinikum Dortmund, Klinikum University Witten/Herdecke, Dortmund, Germany.
⁹ Department of Anesthesiology, Intensive Care Medicine and Pain Therapy, Clinic Centre Westfalen, Dortmund, Germany.
¹⁰ Department of Anaesthesiology, Intensive Care Medicine and Pain Therapy, University Hospital Frankfurt, Goethe University Frankfurt, Frankfurt, Germany.
¹¹ Department of Cardiology and Angiology I (Heart Center Freiburg - Bad Krozingen), Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
¹² Interdisciplinary Medical Intensive Care (IMIT), Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
¹³ Department of Anesthesiology, University Medical Center Göttingen, Robert-Koch-Str. 40, 37085, Göttingen, Germany.
¹⁴ Department of Cardiothoracic, Transplantation and Vascular Surgery, Hannover Medical School, Hannover, Germany.
¹⁵ Department of Internal Medicine, Division I (Hematology/Oncology), University Hospital of Cologne, Cologne, Germany.
¹⁶ Department of Anesthesiology and Critical Care Medicine, ARDS/ECMO-Center, Campus Kassel of the University of Southampton, Kassel, Germany.
¹⁷ Department of Anaesthesia, Perioperative Medicine and Interdisciplinary Intensive Care Medicine, ECLS/ECMO-Center, Asklepios Klinik Langen, Langen, Germany.
¹⁸ Department of Anesthesiology and Intensive Care Medicine, University of Leipzig Medical Center, Leipzig, Germany.
¹⁹ ARDS- und ECMO Zentrum München-Nymphenburg, Barmherzige Brüder Krankenhaus München, München, Germany.
²⁰ Klinik für Pneumologie, Internistische Intensiv- und Beatmungsmedizin, München Klinik Harlaching, Munich, Germany.
²¹ Department of Anaesthesiology and Intensive Care Medicine, Technical University of Munich, School of Medicine, Munich, Germany.
²² School of Medicine, University Hospital Rechts Der Isar, Department of Internal Medicine II, University of Munich, Ismaninger Str. 22, 81675, Munich, Germany.
²³ Department of Cardiology I - Coronary and Peripheral Vascular Disease, Heart Failure, University Hospital Muenster, Muenster, Germany.
²⁴ Department of Intensive Care Medicine, Imland Klinik Rendsburg, Rendsburg, Germany.
²⁵ Department of Internal Medicine V- Pneumology, Allergology and Critical Care Medicine, Saarland University, Homburg, Germany.
²⁶ Department of Anesthesiology and Intensive Care Medicine, University Hospital Tübingen, Eberhard Karls University Tübingen, Tübingen, Germany.
²⁷ Department of Medical Intensive Care and Emergency Medicine, St. Franziskus-Hospital Muenster, Münster, Germany.
²⁸ Institute of Clinical Epidemiology and Biometry, University of Würzburg, Würzburg, Germany.
²⁹ Clinical Trial Center Würzburg, Universitätsklinikum Würzburg, Würzburg, Germany.
³⁰ Department of Anaesthesiology, Intensive Care, Emergency and Pain Medicine, University Hospital Wuerzburg, Oberduerrbacherstr. 6, 97080, Würzburg, Germany. Meybohm_P@ukw.de.

PMID: 35765102
PMCID: PMC9238175
DOI: 10.1186/s13054-022-04053-6

Abstract

Background: Severe COVID-19 induced acute respiratory distress syndrome (ARDS) often requires extracorporeal membrane oxygenation (ECMO). Recent German health insurance data revealed low ICU survival rates. Patient characteristics and experience of the ECMO center may determine intensive care unit (ICU) survival. The current study aimed to identify factors affecting ICU survival of COVID-19 ECMO patients.

Methods: 673 COVID-19 ARDS ECMO patients treated in 26 centers between January 1st 2020 and March 22nd 2021 were included. Data on clinical characteristics, adjunct therapies, complications, and outcome were documented. Block wise logistic regression analysis was applied to identify variables associated with ICU-survival.

Results: Most patients were between 50 and 70 years of age. PaO₂/FiO₂ ratio prior to ECMO was 72 mmHg (IQR: 58-99). ICU survival was 31.4%. Survival was significantly lower during the 2nd wave of the COVID-19 pandemic. A subgroup of 284 (42%) patients fulfilling modified EOLIA criteria had a higher survival (38%) (p = 0.0014, OR 0.64 (CI 0.41-0.99)). Survival differed between low, intermediate, and high-volume centers with 20%, 30%, and 38%, respectively (p = 0.0024). Treatment in high volume centers resulted in an odds ratio of 0.55 (CI 0.28-1.02) compared to low volume centers. Additional factors associated with survival were younger age, shorter time between intubation and ECMO initiation, BMI > 35 (compared to < 25), absence of renal replacement therapy or major bleeding/thromboembolic events.

Conclusions: Structural and patient-related factors, including age, comorbidities and ECMO case volume, determined the survival of COVID-19 ECMO. These factors combined with a more liberal ECMO indication during the 2nd wave may explain the reasonably overall low survival rate. Careful selection of patients and treatment in high volume ECMO centers was associated with higher odds of ICU survival.

Trial registration: Registered in the German Clinical Trials Register (study ID: DRKS00022964, retrospectively registered, September 7th 2020, https://www.drks.de/drks_web/navigate.do?navigationId=trial.HTML&TRIAL_ID=DRKS00022964 .

Keywords: Acute respiratory distress syndrome (ARDS); COVID-19; Case-volume relationship; Extracorporeal life support; Intensive care.

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Conflict of interest statement

Christian Karagiannidis reports support for the present manuscript by Xenios (advisory board member), Getinge (personal fees); personal fees by Bayer, Xenios, Pfizer, Getinge; President of the German Society of internal Intensive Care Medicine; Lead of the German ICU Registry. Stefan Kluge reports consulting fees by Baxter, Fresenius Medical Care; payment by Baxter, Fresenius Medical Care. Karsten Schmidt reports research grants from Stiftung Universitätsmedizin Essen (Microcirculation/Sepsis/Covid-19), Heidelberger Stiftung Chirurgie (Microcirculation/Sepsis); payment for lectures (Buthylcholinesterase and Inflammation) by Dr. Franz Köhler Chemie GmbH. Onnen Moerer reports research grants from CSL Behring: Unrestricted Grant from CS Behring (research related to extracorporeal membrane oxygenation); Member of the national CEOsys network Germany (Covid ecosystem), which is funded by the Federal Ministry of Education and Research (BMBF). [FKZ 01KX2021]; Participation as speaker in workshops on haemodynamic monitoring at the European Medical School in Oldenburg, Germany; Expert testimonies for legal proceedings related to Critical Care or Anesthesiology cases on malpractice accusation by district courts and conciliation committees. Matthias Kochanek reports payment for lectures for Astellas, MSD, Gilead, Pfizer; stock or stock options by Biontech, Moderna; member of DGIIN, DGIM, DIVI. Tobias Lahmer reports payment for lectures and presentations by Gilead, MSD, Pfizer, ADVITOS GmbH. Peter Heuschmann reports research grants from German Ministry of Research and Education, European Union, Charité – Universitätsmedizin Berlin, Berlin Chamber of Physicians, German Parkinson Society, University Hospital Würzburg, Robert Koch Institute, German Heart Foundation, Federal Joint Committee (G-BA) within the Innovationfond, German Research Foundation, Bavarian State (ministry for science and the arts), German Cancer Aid, Charité – Universitätsmedizin Berlin (within Mondafis; supported by an unrestricted research grant to the Charité from Bayer), University Göttingen (within FIND-AF randomized; supported by an unrestricted research grant to the University Göttingen from Boehringer-Ingelheim), University Hospital Heidelberg (within RASUNOA-prime; supported by an unrestricted research grant to the University Hospital Heidelberg from Bayer, BMS, Boehringer-Ingelheim, Daiichi Sankyo), outside the submitted work. Peter Kranke reports research grants for CEOsys projects in the Network University Medicine (NUM) (institutional grants); chairman of the ESAIC guideline committee. Thorsten Brenner reports research grants from Deutsche Forschungsgemeinschaft (DFG), Dietmar Hopp Stiftung, Innovationsfonds/Gemeinsamer Bundesauschuss (G-BA), Stiftung Universitäts-medizin Essen; payments by CSL Behring GmbH, Schöchl medical education GmbH, Boehringer Ingelheim Pharma GmbH, Biotest AG, Baxter Deutschland GmbH, Astellas Pharma GmbH, B. Braun Melsungen AG, MSD Sharp & Dohme GmbH, Lücke Kongresse GmbH, Akademie für Infektionsmedizin e.V.; 2 patents on biomarkers in sepsis/septic shock with BRAHMS GmbH. Frank Herbstreit reports speaker honoria by Biotest; paid expert witness at several courts; International Anesthesia Research Society: Support for Attendance of Annual Meeting; Senior Editor: Anesthesia & Analgesia. All other authors declare no conflict of interest.

Figures

**Fig. 1**
Flowchart patient recruitment

**Fig. 2**
Volume-outcome relationship of COVID-19 ECMO. Case volume. Case volume vs. survival in low (n = 96, survival 20%), intermediate (n = 329, survival 30%) and high volume (n = 248, survival 38%) ECMO centers. Annual case volumes prior to the pandemic were defined as low (< 20/year), intermediate (20–49/year) and high (> 50/year). Lower lines (ECMO ICU discharged alive) depict the percentage of patents discharged alive from the ECMO providing ICU. ICU discharge destinations were mainly other ICUs (40%), rehabilitation facilities (33%), or general wards (23%) (data not shown)

**Fig. 3**
Risk factors for mortality. Adjusted odds ratios (OR) and 95% confidence intervals (CI) of risk factors for mortality according to the final model of block wise logistic regression (Table 3, Block 1–4). References for each variable are indicated (ref)

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References

1. Karagiannidis C, Brodie D, Strassmann S, Stoelben E, Philipp A, Bein T, et al. Extracorporeal membrane oxygenation: evolving epidemiology and mortality. Intensive Care Med. 2016;42(5):889–896. doi: 10.1007/s00134-016-4273-z. - DOI - PubMed
1. Abrams D, Lorusso R, Vincent JL, Brodie D. ECMO during the COVID-19 pandemic: when is it unjustified? Crit Care (Lond, Engl) 2020;24(1):507. doi: 10.1186/s13054-020-03230-9. - DOI - PMC - PubMed
1. Karagiannidis C, Mostert C, Hentschker C, Voshaar T, Malzahn J, Schillinger G, et al. Case characteristics, resource use, and outcomes of 10 021 patients with COVID-19 admitted to 920 German hospitals: an observational study. Lancet Respir Med. 2020;8(9):853–862. doi: 10.1016/S2213-2600(20)30316-7. - DOI - PMC - PubMed
1. Friedrichson B, Kloka JA, Neef V, Mutlak H, Old O, Zacharowski K, et al. Extracorporeal membrane oxygenation in coronavirus disease 2019: a nationwide cohort analysis of 4279 runs from Germany. Eur J Anaesthesiol. 2022;39(5):445–451. doi: 10.1097/EJA.0000000000001670. - DOI - PubMed
1. Ramanathan K, Antognini D, Combes A, Paden M, Zakhary B, Ogino M, et al. Planning and provision of ECMO services for severe ARDS during the COVID-19 pandemic and other outbreaks of emerging infectious diseases. Lancet Respir Med. 2020;8(5):518–526. doi: 10.1016/S2213-2600(20)30121-1. - DOI - PMC - PubMed

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[1] Karagiannidis C, Brodie D, Strassmann S, Stoelben E, Philipp A, Bein T, et al. Extracorporeal membrane oxygenation: evolving epidemiology and mortality. Intensive Care Med. 2016;42(5):889–896. doi: 10.1007/s00134-016-4273-z. - DOI - PubMed

[2] Karagiannidis C, Brodie D, Strassmann S, Stoelben E, Philipp A, Bein T, et al. Extracorporeal membrane oxygenation: evolving epidemiology and mortality. Intensive Care Med. 2016;42(5):889–896. doi: 10.1007/s00134-016-4273-z. - DOI - PubMed

[3] Abrams D, Lorusso R, Vincent JL, Brodie D. ECMO during the COVID-19 pandemic: when is it unjustified? Crit Care (Lond, Engl) 2020;24(1):507. doi: 10.1186/s13054-020-03230-9. - DOI - PMC - PubMed

[4] Abrams D, Lorusso R, Vincent JL, Brodie D. ECMO during the COVID-19 pandemic: when is it unjustified? Crit Care (Lond, Engl) 2020;24(1):507. doi: 10.1186/s13054-020-03230-9. - DOI - PMC - PubMed

[5] Karagiannidis C, Mostert C, Hentschker C, Voshaar T, Malzahn J, Schillinger G, et al. Case characteristics, resource use, and outcomes of 10 021 patients with COVID-19 admitted to 920 German hospitals: an observational study. Lancet Respir Med. 2020;8(9):853–862. doi: 10.1016/S2213-2600(20)30316-7. - DOI - PMC - PubMed

[6] Karagiannidis C, Mostert C, Hentschker C, Voshaar T, Malzahn J, Schillinger G, et al. Case characteristics, resource use, and outcomes of 10 021 patients with COVID-19 admitted to 920 German hospitals: an observational study. Lancet Respir Med. 2020;8(9):853–862. doi: 10.1016/S2213-2600(20)30316-7. - DOI - PMC - PubMed

[7] Friedrichson B, Kloka JA, Neef V, Mutlak H, Old O, Zacharowski K, et al. Extracorporeal membrane oxygenation in coronavirus disease 2019: a nationwide cohort analysis of 4279 runs from Germany. Eur J Anaesthesiol. 2022;39(5):445–451. doi: 10.1097/EJA.0000000000001670. - DOI - PubMed

[8] Friedrichson B, Kloka JA, Neef V, Mutlak H, Old O, Zacharowski K, et al. Extracorporeal membrane oxygenation in coronavirus disease 2019: a nationwide cohort analysis of 4279 runs from Germany. Eur J Anaesthesiol. 2022;39(5):445–451. doi: 10.1097/EJA.0000000000001670. - DOI - PubMed

[9] Ramanathan K, Antognini D, Combes A, Paden M, Zakhary B, Ogino M, et al. Planning and provision of ECMO services for severe ARDS during the COVID-19 pandemic and other outbreaks of emerging infectious diseases. Lancet Respir Med. 2020;8(5):518–526. doi: 10.1016/S2213-2600(20)30121-1. - DOI - PMC - PubMed

[10] Ramanathan K, Antognini D, Combes A, Paden M, Zakhary B, Ogino M, et al. Planning and provision of ECMO services for severe ARDS during the COVID-19 pandemic and other outbreaks of emerging infectious diseases. Lancet Respir Med. 2020;8(5):518–526. doi: 10.1016/S2213-2600(20)30121-1. - DOI - PMC - PubMed

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Key characteristics impacting survival of COVID-19 extracorporeal membrane oxygenation

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Key characteristics impacting survival of COVID-19 extracorporeal membrane oxygenation

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