Severe immunosuppression and not a cytokine storm characterizes COVID-19 infections

COVID-19-associated morbidity and mortality have been attributed to a pathologic host response. Two divergent hypotheses have been proposed: hyperinflammatory cytokine storm; and failure of host protective immunity that results in unrestrained viral dissemination and organ injury. A key explanation...

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Published in:JCI insight Vol. 5; no. 17
Main Authors: Remy, Kenneth E., Mazer, Monty, Striker, David A., Ellebedy, Ali H., Walton, Andrew H., Unsinger, Jacqueline, Blood, Teresa M., Mudd, Philip A., Yi, Daehan J., Mannion, Daniel A., Osborne, Dale F., Martin, R. Scott, Anand, Nitin J., Bosanquet, James P., Blood, Jane, Drewry, Anne M., Caldwell, Charles C., Turnbull, Isaiah R., Brakenridge, Scott C., Moldwawer, Lyle L., Hotchkiss, Richard S.
Format: Journal Article
Language:English
Published: United States American Society for Clinical Investigation 03.09.2020
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ISSN:2379-3708, 2379-3708
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Abstract COVID-19-associated morbidity and mortality have been attributed to a pathologic host response. Two divergent hypotheses have been proposed: hyperinflammatory cytokine storm; and failure of host protective immunity that results in unrestrained viral dissemination and organ injury. A key explanation for the inability to address this controversy has been the lack of diagnostic tools to evaluate immune function in COVID-19 infections. ELISpot, a highly sensitive, functional immunoassay, was employed in 27 patients with COVID-19, 51 patients with sepsis, 18 critically ill nonseptic (CINS) patients, and 27 healthy control volunteers to evaluate adaptive and innate immune status by quantitating T cell IFN-ɣ and monocyte TFN-α production. Circulating T cell subsets were profoundly reduced in COVID-19 patients. Additionally, stimulated blood mononuclear cells produced less than 40%-50% of the IFN-ɣ and TNF-α observed in septic and CINS patients, consistent with markedly impaired immune effector cell function. Approximately 25% of COVID-19 patients had increased IL-6 levels that were not associated with elevations in other canonical proinflammatory cytokines. Collectively, these findings support the hypothesis that COVID-19 suppresses host functional adaptive and innate immunity. Importantly, IL-7 administered ex vivo restored T cell IFN-ɣ production in COVID-19 patients. Thus, ELISpot may functionally characterize host immunity in COVID-19 and inform prospective therapies.
AbstractList COVID-19–associated morbidity and mortality have been attributed to a pathologic host response. Two divergent hypotheses have been proposed: hyperinflammatory cytokine storm; and failure of host protective immunity that results in unrestrained viral dissemination and organ injury. A key explanation for the inability to address this controversy has been the lack of diagnostic tools to evaluate immune function in COVID-19 infections. ELISpot, a highly sensitive, functional immunoassay, was employed in 27 patients with COVID-19, 51 patients with sepsis, 18 critically ill nonseptic (CINS) patients, and 27 healthy control volunteers to evaluate adaptive and innate immune status by quantitating T cell IFN-ɣ and monocyte TFN-α production. Circulating T cell subsets were profoundly reduced in COVID-19 patients. Additionally, stimulated blood mononuclear cells produced less than 40%–50% of the IFN-ɣ and TNF-α observed in septic and CINS patients, consistent with markedly impaired immune effector cell function. Approximately 25% of COVID-19 patients had increased IL-6 levels that were not associated with elevations in other canonical proinflammatory cytokines. Collectively, these findings support the hypothesis that COVID-19 suppresses host functional adaptive and innate immunity. Importantly, IL-7 administered ex vivo restored T cell IFN-ɣ production in COVID-19 patients. Thus, ELISpot may functionally characterize host immunity in COVID-19 and inform prospective therapies. ELISpot, a highly sensitive, functional immunoassay, suggests that COVID-19 is immunosuppressive and lacks substantial cytokine storm.
COVID-19–associated morbidity and mortality have been attributed to a pathologic host response. Two divergent hypotheses have been proposed: hyperinflammatory cytokine storm; and failure of host protective immunity that results in unrestrained viral dissemination and organ injury. A key explanation for the inability to address this controversy has been the lack of diagnostic tools to evaluate immune function in COVID-19 infections. ELISpot, a highly sensitive, functional immunoassay, was employed in 27 patients with COVID-19, 51 patients with sepsis, 18 critically ill nonseptic (CINS) patients, and 27 healthy control volunteers to evaluate adaptive and innate immune status by quantitating T cell IFN-ɣ and monocyte TFN-α production. Circulating T cell subsets were profoundly reduced in COVID-19 patients. Additionally, stimulated blood mononuclear cells produced less than 40%–50% of the IFN-ɣ and TNF-α observed in septic and CINS patients, consistent with markedly impaired immune effector cell function. Approximately 25% of COVID-19 patients had increased IL-6 levels that were not associated with elevations in other canonical proinflammatory cytokines. Collectively, these findings support the hypothesis that COVID-19 suppresses host functional adaptive and innate immunity. Importantly, IL-7 administered ex vivo restored T cell IFN-ɣ production in COVID-19 patients. Thus, ELISpot may functionally characterize host immunity in COVID-19 and inform prospective therapies.
COVID-19-associated morbidity and mortality have been attributed to a pathologic host response. Two divergent hypotheses have been proposed: hyperinflammatory cytokine storm; and failure of host protective immunity that results in unrestrained viral dissemination and organ injury. A key explanation for the inability to address this controversy has been the lack of diagnostic tools to evaluate immune function in COVID-19 infections. ELISpot, a highly sensitive, functional immunoassay, was employed in 27 patients with COVID-19, 51 patients with sepsis, 18 critically ill nonseptic (CINS) patients, and 27 healthy control volunteers to evaluate adaptive and innate immune status by quantitating T cell IFN-ɣ and monocyte TFN-α production. Circulating T cell subsets were profoundly reduced in COVID-19 patients. Additionally, stimulated blood mononuclear cells produced less than 40%-50% of the IFN-ɣ and TNF-α observed in septic and CINS patients, consistent with markedly impaired immune effector cell function. Approximately 25% of COVID-19 patients had increased IL-6 levels that were not associated with elevations in other canonical proinflammatory cytokines. Collectively, these findings support the hypothesis that COVID-19 suppresses host functional adaptive and innate immunity. Importantly, IL-7 administered ex vivo restored T cell IFN-ɣ production in COVID-19 patients. Thus, ELISpot may functionally characterize host immunity in COVID-19 and inform prospective therapies.COVID-19-associated morbidity and mortality have been attributed to a pathologic host response. Two divergent hypotheses have been proposed: hyperinflammatory cytokine storm; and failure of host protective immunity that results in unrestrained viral dissemination and organ injury. A key explanation for the inability to address this controversy has been the lack of diagnostic tools to evaluate immune function in COVID-19 infections. ELISpot, a highly sensitive, functional immunoassay, was employed in 27 patients with COVID-19, 51 patients with sepsis, 18 critically ill nonseptic (CINS) patients, and 27 healthy control volunteers to evaluate adaptive and innate immune status by quantitating T cell IFN-ɣ and monocyte TFN-α production. Circulating T cell subsets were profoundly reduced in COVID-19 patients. Additionally, stimulated blood mononuclear cells produced less than 40%-50% of the IFN-ɣ and TNF-α observed in septic and CINS patients, consistent with markedly impaired immune effector cell function. Approximately 25% of COVID-19 patients had increased IL-6 levels that were not associated with elevations in other canonical proinflammatory cytokines. Collectively, these findings support the hypothesis that COVID-19 suppresses host functional adaptive and innate immunity. Importantly, IL-7 administered ex vivo restored T cell IFN-ɣ production in COVID-19 patients. Thus, ELISpot may functionally characterize host immunity in COVID-19 and inform prospective therapies.
Author Mannion, Daniel A.
Walton, Andrew H.
Ellebedy, Ali H.
Martin, R. Scott
Unsinger, Jacqueline
Drewry, Anne M.
Caldwell, Charles C.
Brakenridge, Scott C.
Turnbull, Isaiah R.
Moldwawer, Lyle L.
Yi, Daehan J.
Mazer, Monty
Blood, Teresa M.
Mudd, Philip A.
Anand, Nitin J.
Blood, Jane
Striker, David A.
Remy, Kenneth E.
Bosanquet, James P.
Osborne, Dale F.
Hotchkiss, Richard S.
AuthorAffiliation 7 Saint Louis University School of Medicine, St. Louis, Missouri, USA
8 Department of Surgery, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA
5 Department of Pathology and Immunology, and
4 Department of Critical Care, Missouri Baptist Medical Center, St. Louis, USA
10 Department of Surgery, Sepsis and Critical Illness Research Center, University of Florida College of Medicine, Gainesville, Florida, USA
1 Department of Pediatrics
3 Department of Anesthesiology, Washington University School of Medicine in St. Louis, St. Louis, Missouri, USA
2 Department of Internal Medicine, and
6 Department of Emergency Medicine, Washington University School of Medicine in St. Louis, St. Louis, Missouri, USA
9 Department of Surgery, Washington University School of Medicine in St. Louis, St. Louis, Missouri, USA
AuthorAffiliation_xml – name: 1 Department of Pediatrics
– name: 2 Department of Internal Medicine, and
– name: 7 Saint Louis University School of Medicine, St. Louis, Missouri, USA
– name: 5 Department of Pathology and Immunology, and
– name: 10 Department of Surgery, Sepsis and Critical Illness Research Center, University of Florida College of Medicine, Gainesville, Florida, USA
– name: 3 Department of Anesthesiology, Washington University School of Medicine in St. Louis, St. Louis, Missouri, USA
– name: 9 Department of Surgery, Washington University School of Medicine in St. Louis, St. Louis, Missouri, USA
– name: 6 Department of Emergency Medicine, Washington University School of Medicine in St. Louis, St. Louis, Missouri, USA
– name: 4 Department of Critical Care, Missouri Baptist Medical Center, St. Louis, USA
– name: 8 Department of Surgery, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA
Author_xml – sequence: 1
  givenname: Kenneth E.
  orcidid: 0000-0001-5222-9884
  surname: Remy
  fullname: Remy, Kenneth E.
– sequence: 2
  givenname: Monty
  orcidid: 0000-0002-4159-8585
  surname: Mazer
  fullname: Mazer, Monty
– sequence: 3
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  fullname: Striker, David A.
– sequence: 4
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  surname: Ellebedy
  fullname: Ellebedy, Ali H.
– sequence: 5
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  surname: Walton
  fullname: Walton, Andrew H.
– sequence: 6
  givenname: Jacqueline
  surname: Unsinger
  fullname: Unsinger, Jacqueline
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  orcidid: 0000-0001-8623-5684
  surname: Blood
  fullname: Blood, Teresa M.
– sequence: 8
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  orcidid: 0000-0002-3860-5473
  surname: Mudd
  fullname: Mudd, Philip A.
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  givenname: Daehan J.
  surname: Yi
  fullname: Yi, Daehan J.
– sequence: 10
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  fullname: Mannion, Daniel A.
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  surname: Osborne
  fullname: Osborne, Dale F.
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  surname: Martin
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  surname: Anand
  fullname: Anand, Nitin J.
– sequence: 14
  givenname: James P.
  surname: Bosanquet
  fullname: Bosanquet, James P.
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  surname: Blood
  fullname: Blood, Jane
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  surname: Drewry
  fullname: Drewry, Anne M.
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  givenname: Charles C.
  orcidid: 0000-0003-1692-4550
  surname: Caldwell
  fullname: Caldwell, Charles C.
– sequence: 18
  givenname: Isaiah R.
  orcidid: 0000-0002-1437-8480
  surname: Turnbull
  fullname: Turnbull, Isaiah R.
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  givenname: Scott C.
  orcidid: 0000-0002-7327-3718
  surname: Brakenridge
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  fullname: Moldwawer, Lyle L.
– sequence: 21
  givenname: Richard S.
  surname: Hotchkiss
  fullname: Hotchkiss, Richard S.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32687484$$D View this record in MEDLINE/PubMed
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10.1017/dmp.2020.60
10.1016/S1473-3099(20)30376-5
10.1136/annrheumdis-2020-217706
10.1016/j.ijantimicag.2020.105954
10.1038/s41423-020-0401-3
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10.1016/S2213-2600(20)30217-4
10.1172/jci.insight.98960
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10.1371/journal.pone.0199497
10.1126/sciimmunol.abc5367
10.1016/j.humov.2019.102567
10.1093/cid/ciaa449
10.1097/SHK.0000000000001083
10.1016/j.autrev.2020.102537
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10.1001/jama.2020.4940
10.1513/AnnalsATS.202003-225OC
10.1164/rccm.202003-0543OC
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Keywords COVID-19
Adaptive immunity
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Snippet COVID-19-associated morbidity and mortality have been attributed to a pathologic host response. Two divergent hypotheses have been proposed: hyperinflammatory...
COVID-19–associated morbidity and mortality have been attributed to a pathologic host response. Two divergent hypotheses have been proposed: hyperinflammatory...
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SubjectTerms Adaptive Immunity - immunology
Adolescent
Adult
Aged
Aged, 80 and over
Antibodies
Betacoronavirus
Case-Control Studies
Coronavirus Infections - immunology
Coronaviruses
COVID-19
Critical Illness
Cytokine Release Syndrome - immunology
Cytokine storm
Enzyme-linked immunosorbent assay
Enzyme-Linked Immunospot Assay
Female
Healthy Volunteers
Humans
Immune response
Immune status
Immune Tolerance - immunology
Immunity, Innate - immunology
Immunoassay
Immunosuppression
Infections
Innate immunity
Interferon-gamma - immunology
Interferon-gamma - metabolism
Interleukin-6 - immunology
Leukocytes (mononuclear)
Lymphocytes
Lymphocytes T
Male
Middle Aged
Monocytes
Monocytes - immunology
Monocytes - metabolism
Morbidity
Mortality
Pandemics
Patients
Plasma
Pneumonia, Viral - immunology
SARS-CoV-2
Sepsis
Sepsis - immunology
T-Lymphocyte Subsets - immunology
T-Lymphocyte Subsets - metabolism
T-Lymphocytes - immunology
T-Lymphocytes - metabolism
Tumor Necrosis Factor-alpha - immunology
Tumor Necrosis Factor-alpha - metabolism
Tumor necrosis factor-α
Young Adult
Title Severe immunosuppression and not a cytokine storm characterizes COVID-19 infections
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