. 2023 May 1;24(5):356-371.

doi: 10.1097/PCC.0000000000003212. Epub 2023 Mar 30.

Extracorporeal Membrane Oxygenation Characteristics and Outcomes in Children and Adolescents With COVID-19 or Multisystem Inflammatory Syndrome Admitted to U.S. ICUs

Melania M Bembea¹, Laura L Loftis², Ravi R Thiagarajan³, Cameron C Young⁴, Timothy P McCadden⁴, Margaret M Newhams⁴, Suden Kucukak⁴, Elizabeth H Mack⁵, Julie C Fitzgerald⁶, Courtney M Rowan⁷, Aline B Maddux⁸, Amanda R Kolmar⁹, Katherine Irby¹⁰, Sabrina Heidemann¹¹, Stephanie P Schwartz¹², Michele Kong¹³, Hillary Crandall¹⁴, Kevin M Havlin¹⁵, Aalok R Singh¹⁶, Jennifer E Schuster¹⁷, Mark W Hall¹⁸, Kari A Wellnitz¹⁹, Mia Maamari²⁰, Mary G Gaspers²¹, Ryan A Nofziger²², Peter Paul C Lim²³, Ryan W Carroll²⁴, Alvaro Coronado Munoz²⁵, Tamara T Bradford²⁶, Melissa L Cullimore²⁷, Natasha B Halasa²⁸, Gwenn E McLaughlin²⁹, Pia S Pannaraj³⁰, Natalie Z Cvijanovich³¹, Matt S Zinter³², Bria M Coates³³, Steven M Horwitz³⁴, Charlotte V Hobbs³⁵, Heda Dapul³⁶, Ana Lia Graciano³⁷, Andrew D Butler³⁸, Manish M Patel³⁹, Laura D Zambrano³⁹, Angela P Campbell³⁹, Adrienne G Randolph^{4

40}; Overcoming COVID-19 Investigators

Affiliations

¹ Department of Anesthesiology and Critical Care Medicine, Johns Hopkins University School of Medicine, Baltimore, MD.
² Division of Critical Care Medicine, Department of Pediatrics, Baylor College of Medicine, Houston, TX.
³ Division of Cardiac Critical Care, Department of Cardiology, Boston Children's Hospital, Harvard Medical School, Boston, MA.
⁴ Department of Anesthesiology, Critical Care, and Pain Medicine, Boston Children's Hospital, Boston, MA.
⁵ Division of Pediatric Critical Care Medicine, Medical University of South Carolina, Charleston, SC.
⁶ Department of Anesthesiology and Critical Care, Children's Hospital of Philadelphia, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA.
⁷ Division of Pediatric Critical Care Medicine, Department of Pediatrics, Indiana University School of Medicine, Riley Hospital for Children, Indianapolis, IN.
⁸ Department of Pediatrics, Section of Critical Care Medicine, University of Colorado School of Medicine and Children's Hospital Colorado, Aurora, CO.
⁹ Department of Pediatrics, Washington University in St. Louis, St. Louis, MO.
¹⁰ Section of Pediatric Critical Care, Department of Pediatrics, Arkansas Children's Hospital, Little Rock, AR.
¹¹ Division of Pediatric Critical Care Medicine, Department of Pediatrics, Central Michigan University, Detroit, MI.
¹² Department of Pediatrics, University of North Carolina at Chapel Hill Children's Hospital, Chapel Hill, NC.
¹³ Division of Pediatric Critical Care Medicine, Department of Pediatrics, University of Alabama at Birmingham, Birmingham, AL.
¹⁴ Division of Pediatric Critical Care, Department of Pediatrics, University of Utah and Primary Children's Hospital, Salt Lake City, UT.
¹⁵ Department of Pediatrics, Division of Pediatric Critical Care Medicine, University of Louisville, and Norton Children's Hospital, Louisville, KY.
¹⁶ Pediatric Critical Care Division, Maria Fareri Children's Hospital at Westchester Medical Center and New York Medical College, Valhalla, NY.
¹⁷ Division of Pediatric Infectious Disease, Department of Pediatrics, Children's Mercy Kansas City, Kansas City, MO.
¹⁸ Division of Critical Care Medicine, Department of Pediatrics, Nationwide Children's Hospital, Columbus, OH.
¹⁹ Division of Pediatric Critical Care, Stead Family Department of Pediatrics, University of Iowa Carver College of Medicine, Iowa City, IA.
²⁰ Department of Pediatrics, Division of Critical Care Medicine, University of Texas Southwestern, Children's Health Medical Center, Dallas, TX.
²¹ Department of Pediatrics and Banner Children's at Diamond Children's Medical Center, University of Arizona, Tucson, AZ.
²² Division of Critical Care Medicine, Department of Pediatrics, Akron Children's Hospital, Akron, OH.
²³ Division of Pediatric Critical Care Medicine, Rainbow Babies and Children's Hospital, Cleveland, OH.
²⁴ Division of Pediatric Critical Care Medicine, MassGeneral Hospital for Children, Harvard Medical School, Boston, MA.
²⁵ Pediatric Critical Care Division, Department of Pediatrics, University of Texas Health Science Center at Houston, Houston, TX.
²⁶ Division of Cardiology, Department of Pediatrics, Louisiana State University Health Sciences Center and Children's Hospital of New Orleans, New Orleans, LA.
²⁷ Division of Pediatric Critical Care, Department of Pediatrics, Children's Hospital and Medical Center, Omaha, NE.
²⁸ Division of Pediatric Infectious Diseases, Department of Pediatrics, Vanderbilt University Medical Center, Nashville, TN.
²⁹ Division of Pediatric Critical Care Medicine, Department of Pediatrics, University of Miami Miller School of Medicine, Miami, FL.
³⁰ Division of Infectious Diseases, Children's Hospital Los Angeles and Departments of Pediatrics and Molecular Microbiology and Immunology, University of Southern California, Los Angeles, CA.
³¹ Division of Critical Care Medicine, UCSF Benioff Children's Hospital Oakland, Oakland, CA.
³² Department of Pediatrics, Divisions of Critical Care Medicine and Allergy, Immunology, and Bone Marrow Transplant, University of California San Francisco, San Francisco, CA.
³³ Division of Critical Care Medicine, Department of Pediatrics, Northwestern University Feinberg School of Medicine, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL.
³⁴ Department of Pediatrics, Division of Pediatric Critical Care Medicine, Rutgers Robert Wood Johnson Medical School, New Brunswick, NJ.
³⁵ Department of Pediatrics, Division of Infectious Diseases, University of Mississippi Medical Center, Jackson, MS.
³⁶ Department of Pediatrics, Division of Infectious Diseases, New York University Grossman School of Medicine and Hassenfeld Children's Hospital, New York, NY.
³⁷ Department of Pediatrics, Division of Critical Care Medicine, University of Maryland School of Medicine, Baltimore, MD.
³⁸ Division of Pediatric Critical Care, St. Christopher's Hospital for Children, Philadelphia, PA.
³⁹ COVID-19 Response, Centers for Disease Control and Prevention, Atlanta, GA.
⁴⁰ Departments of Anesthesia and Pediatrics, Harvard Medical School, Boston, MA.

PMID: 36995097
PMCID: PMC10153593
DOI: 10.1097/PCC.0000000000003212

Extracorporeal Membrane Oxygenation Characteristics and Outcomes in Children and Adolescents With COVID-19 or Multisystem Inflammatory Syndrome Admitted to U.S. ICUs

Melania M Bembea et al. Pediatr Crit Care Med. 2023.

. 2023 May 1;24(5):356-371.

doi: 10.1097/PCC.0000000000003212. Epub 2023 Mar 30.

Authors

Affiliations

¹ Department of Anesthesiology and Critical Care Medicine, Johns Hopkins University School of Medicine, Baltimore, MD.
² Division of Critical Care Medicine, Department of Pediatrics, Baylor College of Medicine, Houston, TX.
³ Division of Cardiac Critical Care, Department of Cardiology, Boston Children's Hospital, Harvard Medical School, Boston, MA.
⁴ Department of Anesthesiology, Critical Care, and Pain Medicine, Boston Children's Hospital, Boston, MA.
⁵ Division of Pediatric Critical Care Medicine, Medical University of South Carolina, Charleston, SC.
⁶ Department of Anesthesiology and Critical Care, Children's Hospital of Philadelphia, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA.
⁷ Division of Pediatric Critical Care Medicine, Department of Pediatrics, Indiana University School of Medicine, Riley Hospital for Children, Indianapolis, IN.
⁸ Department of Pediatrics, Section of Critical Care Medicine, University of Colorado School of Medicine and Children's Hospital Colorado, Aurora, CO.
⁹ Department of Pediatrics, Washington University in St. Louis, St. Louis, MO.
¹⁰ Section of Pediatric Critical Care, Department of Pediatrics, Arkansas Children's Hospital, Little Rock, AR.
¹¹ Division of Pediatric Critical Care Medicine, Department of Pediatrics, Central Michigan University, Detroit, MI.
¹² Department of Pediatrics, University of North Carolina at Chapel Hill Children's Hospital, Chapel Hill, NC.
¹³ Division of Pediatric Critical Care Medicine, Department of Pediatrics, University of Alabama at Birmingham, Birmingham, AL.
¹⁴ Division of Pediatric Critical Care, Department of Pediatrics, University of Utah and Primary Children's Hospital, Salt Lake City, UT.
¹⁵ Department of Pediatrics, Division of Pediatric Critical Care Medicine, University of Louisville, and Norton Children's Hospital, Louisville, KY.
¹⁶ Pediatric Critical Care Division, Maria Fareri Children's Hospital at Westchester Medical Center and New York Medical College, Valhalla, NY.
¹⁷ Division of Pediatric Infectious Disease, Department of Pediatrics, Children's Mercy Kansas City, Kansas City, MO.
¹⁸ Division of Critical Care Medicine, Department of Pediatrics, Nationwide Children's Hospital, Columbus, OH.
¹⁹ Division of Pediatric Critical Care, Stead Family Department of Pediatrics, University of Iowa Carver College of Medicine, Iowa City, IA.
²⁰ Department of Pediatrics, Division of Critical Care Medicine, University of Texas Southwestern, Children's Health Medical Center, Dallas, TX.
²¹ Department of Pediatrics and Banner Children's at Diamond Children's Medical Center, University of Arizona, Tucson, AZ.
²² Division of Critical Care Medicine, Department of Pediatrics, Akron Children's Hospital, Akron, OH.
²³ Division of Pediatric Critical Care Medicine, Rainbow Babies and Children's Hospital, Cleveland, OH.
²⁴ Division of Pediatric Critical Care Medicine, MassGeneral Hospital for Children, Harvard Medical School, Boston, MA.
²⁵ Pediatric Critical Care Division, Department of Pediatrics, University of Texas Health Science Center at Houston, Houston, TX.
²⁶ Division of Cardiology, Department of Pediatrics, Louisiana State University Health Sciences Center and Children's Hospital of New Orleans, New Orleans, LA.
²⁷ Division of Pediatric Critical Care, Department of Pediatrics, Children's Hospital and Medical Center, Omaha, NE.
²⁸ Division of Pediatric Infectious Diseases, Department of Pediatrics, Vanderbilt University Medical Center, Nashville, TN.
²⁹ Division of Pediatric Critical Care Medicine, Department of Pediatrics, University of Miami Miller School of Medicine, Miami, FL.
³⁰ Division of Infectious Diseases, Children's Hospital Los Angeles and Departments of Pediatrics and Molecular Microbiology and Immunology, University of Southern California, Los Angeles, CA.
³¹ Division of Critical Care Medicine, UCSF Benioff Children's Hospital Oakland, Oakland, CA.
³² Department of Pediatrics, Divisions of Critical Care Medicine and Allergy, Immunology, and Bone Marrow Transplant, University of California San Francisco, San Francisco, CA.
³³ Division of Critical Care Medicine, Department of Pediatrics, Northwestern University Feinberg School of Medicine, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL.
³⁴ Department of Pediatrics, Division of Pediatric Critical Care Medicine, Rutgers Robert Wood Johnson Medical School, New Brunswick, NJ.
³⁵ Department of Pediatrics, Division of Infectious Diseases, University of Mississippi Medical Center, Jackson, MS.
³⁶ Department of Pediatrics, Division of Infectious Diseases, New York University Grossman School of Medicine and Hassenfeld Children's Hospital, New York, NY.
³⁷ Department of Pediatrics, Division of Critical Care Medicine, University of Maryland School of Medicine, Baltimore, MD.
³⁸ Division of Pediatric Critical Care, St. Christopher's Hospital for Children, Philadelphia, PA.
³⁹ COVID-19 Response, Centers for Disease Control and Prevention, Atlanta, GA.
⁴⁰ Departments of Anesthesia and Pediatrics, Harvard Medical School, Boston, MA.

PMID: 36995097
PMCID: PMC10153593
DOI: 10.1097/PCC.0000000000003212

Abstract

Objectives: Extracorporeal membrane oxygenation (ECMO) has been used successfully to support adults with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-related cardiac or respiratory failure refractory to conventional therapies. Comprehensive reports of children and adolescents with SARS-CoV-2-related ECMO support for conditions, including multisystem inflammatory syndrome in children (MIS-C) and acute COVID-19, are needed.

Design: Case series of patients from the Overcoming COVID-19 public health surveillance registry.

Setting: Sixty-three hospitals in 32 U.S. states reporting to the registry between March 15, 2020, and December 31, 2021.

Patients: Patients less than 21 years admitted to the ICU meeting Centers for Disease Control criteria for MIS-C or acute COVID-19.

Interventions: None.

Measurements and main results: The final cohort included 2,733 patients with MIS-C ( n = 1,530; 37 [2.4%] requiring ECMO) or acute COVID-19 ( n = 1,203; 71 [5.9%] requiring ECMO). ECMO patients in both groups were older than those without ECMO support (MIS-C median 15.4 vs 9.9 yr; acute COVID-19 median 15.3 vs 13.6 yr). The body mass index percentile was similar in the MIS-C ECMO versus no ECMO groups (89.9 vs 85.8; p = 0.22) but higher in the COVID-19 ECMO versus no ECMO groups (98.3 vs 96.5; p = 0.03). Patients on ECMO with MIS-C versus COVID-19 were supported more often with venoarterial ECMO (92% vs 41%) for primary cardiac indications (87% vs 23%), had ECMO initiated earlier (median 1 vs 5 d from hospitalization), shorter ECMO courses (median 3.9 vs 14 d), shorter hospital length of stay (median 20 vs 52 d), lower in-hospital mortality (27% vs 37%), and less major morbidity at discharge in survivors (new tracheostomy, oxygen or mechanical ventilation need or neurologic deficit; 0% vs 11%, 0% vs 20%, and 8% vs 15%, respectively). Most patients with MIS-C requiring ECMO support (87%) were admitted during the pre-Delta (variant B.1.617.2) period, while most patients with acute COVID-19 requiring ECMO support (70%) were admitted during the Delta variant period.

Conclusions: ECMO support for SARS-CoV-2-related critical illness was uncommon, but type, initiation, and duration of ECMO use in MIS-C and acute COVID-19 were markedly different. Like pre-pandemic pediatric ECMO cohorts, most patients survived to hospital discharge.

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Conflict of interest statement

Dr. Bembea’s institution received funding from the National Institute of Neurological Disorders and Stroke (R01NS106292) and Grifols Investigator Sponsored Research Grant. Drs. Bembea, Heidemann, Zinter, and Randolph received support for article research from the National Institutes of Health (NIH). Dr. Thiagarjan’s institution received funding from the U.S. Department of Defense (Peer Reviewed Medical Research Project Clinical Trial Award No. W81XWH2210301 Trial of Indication-based Transfusion of Red blood cells in Extracorporeal Membrane Oxygenation); he received funding from Society of Critical Care Medicine and the Extracorporeal Life Support Organization. Drs. Young’s, McCadden’s, Newhams’s, Kucuak’s, Mack’s, Fitzgerald’s, Rowan’s, Maddux’s, Kolmar’s, Heidemann’s, Schwartz’s, Kong’s, Crandall’s, Singh’s, Schuster’s, Hall’s, Wellnitz’s, Maamari’s, Gaspers’s, Nofziger’s, Cullimore’s, Halasa’s, McLaughlin’s, Pannaraj’s, Cvijanovich’s, Coates’s, Horwitz’s, Hobbs’s, Dapul’s, and Randolph’s institutions received funding from the U.S. Centers for Disease Control and Prevention (CDC). Dr. McCadden disclosed work for hire. Dr. Newhams’ institution received funding from the National Institute of Allergy and Infectious Diseases. Drs. Fitzgerald’s, Kong’s, Cullimore’s, Cvijanovich’s, and Randolph’s institutions received funding from the NIH. Dr. Rowan’s institution received funding from the National Heart, Lung, and Blood Institute (NHLBI) (K23HL150244). Dr. Maddux’s institution received funding from the National Institute of Child Health and Human Development (K23HD096018). Drs. Irby, Crandall, Singh, Wellnitz, Nofziger, Bradford, McLaughlin, Coates, Hobbs, and Zambrano received support for article research from the CDC. Dr. Schuster’s institution received funding from Merck. Dr. Hall received funding from Abbvie, Kiadis, and the American Board of Pediatrics. Dr. Wellnitz’s institution received funding from the University of Pennsylvania (prime sponsor NIH) and the University of Nebraska (prime sponsor Administration for Strategic Preparedness and Response). Dr. Gaspers received funding from Abbott Laboratories. Dr. Munoz’s institution received funding from Boston’s Children’s Hospital; he received funding from the University of Texas Health Science Center at Houston. Dr. Halasa’s institution received funding from Sanofi. Dr. McLaughlin received funding from expert witness fees from two entities. Dr. Pannaraj’s institution received funding from AstraZeneca and Pfizer. Dr. Coates’ institution received funding from the NHLBI and the American Lung Association; she received funding from Sobi. Drs. Hobbs and Randolph received funding from UpToDate. Dr. Hobbs received funding from Dynamed.com; she disclosed that she was a speaker for Biomerieux 2021–2022. Drs. Zambrano and Campbell disclosed government work. Dr. Randolph had full access to all the data in the investigation and takes responsibility for the integrity of the data and the accuracy of the data analysis. The remaining authors have disclosed that they do not have any potential conflicts of interest.

Figures

**Figure 1.**
Eligibility flowchart of hospitalized patients with COVID-19–related illness and extracorporeal membrane oxygenation (ECMO) requirement, March 15, 2020, to December 31, 2021. CDC = Centers for Disease Control and Prevention, MIS-C = multisystem inflammatory syndrome in children.

**Figure 2.**
Admission laboratory markers among multisystem inflammatory syndrome in children (MIS-C) and acute COVID-19 patient with and without extracorporeal membrane oxygenation (ECMO) support. *Denotes significant difference between ECMO and non-ECMO patients (p < 0.05). ALC = absolute lymphocyte count, ANC = absolute neutrophil count, CRP = C-reactive protein.

See this image and copyright information in PMC

Comment in

Tickle Me ECMO…Differences and Outcomes Unearthed for Kids Requiring Extracorporeal Membrane Oxygenation in Severe Acute Respiratory Syndrome Coronavirus 2-Associated Disease.
Kilgallon KB, Remy KE. Kilgallon KB, et al. Pediatr Crit Care Med. 2023 May 1;24(5):419-422. doi: 10.1097/PCC.0000000000003225. Epub 2023 May 4. Pediatr Crit Care Med. 2023. PMID: 37140332 Free PMC article. No abstract available.

References

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1. Feldstein LR, Tenforde MW, Friedman KG, et al. : Characteristics and outcomes of US children and adolescents with Multisystem Inflammatory Syndrome in Children (MIS-C) compared with severe acute COVID-19. JAMA 2021; 325:1074–1087 - PMC - PubMed
1. Castagnoli R, Votto M, Licari A, et al. : Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in children and adolescents: A systematic review. JAMA Pediatr 2020; 174:882–889 - PubMed
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Extracorporeal Membrane Oxygenation Characteristics and Outcomes in Children and Adolescents With COVID-19 or Multisystem Inflammatory Syndrome Admitted to U.S. ICUs

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Extracorporeal Membrane Oxygenation Characteristics and Outcomes in Children and Adolescents With COVID-19 or Multisystem Inflammatory Syndrome Admitted to U.S. ICUs

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