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 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
American Society for Clinical Investigation
03.09.2020
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| Subjects: | |
| ISSN: | 2379-3708, 2379-3708 |
| Online Access: | Get full text |
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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. |
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| 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 givenname: David A. surname: Striker fullname: Striker, David A. – sequence: 4 givenname: Ali H. surname: Ellebedy fullname: Ellebedy, Ali H. – sequence: 5 givenname: Andrew H. orcidid: 0000-0003-2805-6666 surname: Walton fullname: Walton, Andrew H. – sequence: 6 givenname: Jacqueline surname: Unsinger fullname: Unsinger, Jacqueline – sequence: 7 givenname: Teresa M. orcidid: 0000-0001-8623-5684 surname: Blood fullname: Blood, Teresa M. – sequence: 8 givenname: Philip A. orcidid: 0000-0002-3860-5473 surname: Mudd fullname: Mudd, Philip A. – sequence: 9 givenname: Daehan J. surname: Yi fullname: Yi, Daehan J. – sequence: 10 givenname: Daniel A. surname: Mannion fullname: Mannion, Daniel A. – sequence: 11 givenname: Dale F. surname: Osborne fullname: Osborne, Dale F. – sequence: 12 givenname: R. Scott surname: Martin fullname: Martin, R. Scott – sequence: 13 givenname: Nitin J. surname: Anand fullname: Anand, Nitin J. – sequence: 14 givenname: James P. surname: Bosanquet fullname: Bosanquet, James P. – sequence: 15 givenname: Jane orcidid: 0000-0002-5012-5560 surname: Blood fullname: Blood, Jane – sequence: 16 givenname: Anne M. surname: Drewry fullname: Drewry, Anne M. – sequence: 17 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. – sequence: 19 givenname: Scott C. orcidid: 0000-0002-7327-3718 surname: Brakenridge fullname: Brakenridge, Scott C. – sequence: 20 givenname: Lyle L. surname: Moldwawer 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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| References_xml | – ident: B9 doi: 10.1159/000507423 – volume: 23 start-page: 488 issue: 6 year: 2005 ident: B37 article-title: Plasma cytokine measurements augment prognostic scores as indicators of outcome in patients with severe sepsis publication-title: Shock – ident: B11 doi: 10.1016/S0140-6736(20)30183-5 – ident: B45 doi: 10.2217/imt-2016-0020 – ident: B36 doi: 10.1097/CCM.0b013e31819fcc08 – ident: B26 doi: 10.2139/ssrn.3555267 – ident: B13 doi: 10.1001/jama.2020.1585 – volume: 151 start-page: 147 issue: 2 &3 year: 2020 ident: B8 article-title: The 2019 novel coronavirus disease (COVID-19) pandemic: a review of the current evidence publication-title: Indian J Med Res doi: 10.4103/ijmr.IJMR_519_20 – ident: B27 doi: 10.1016/j.jaad.2020.04.097 – volume: 14 year: 2020 ident: B28 article-title: Associations between immune-suppressive and stimulating drugs and novel COVID-19-a systematic review of current evidence publication-title: Ecancermedicalscience doi: 10.3332/ecancer.2020.1022 – ident: B44 doi: 10.1084/jem.169.1.333 – volume: 47 start-page: 17 issue: 1S suppl 1 year: 2017 ident: B35 article-title: Sepsis Through the eyes of proteomics: the progress in the last decade publication-title: Shock doi: 10.1097/SHK.0000000000000698 – ident: B50 doi: 10.7326/M20-2003 – ident: B31 – ident: B51 doi: 10.1111/his.14134 – ident: B52 doi: 10.1084/jem.20200678 – ident: B21 doi: 10.1038/s41423-020-0402-2 – volume: 98 start-page: 1080 issue: 6 pt 1 year: 1996 ident: B46 article-title: Expression of IL-6, IL-8, and RANTES on human bronchial epithelial cells, NCI-H292, induced by influenza virus A publication-title: J Allergy Clin Immunol doi: 10.1016/S0091-6749(96)80195-3 – ident: B23 doi: 10.1136/jclinpath-2020-206522 – volume: 36 start-page: 21 issue: 1 year: 2020 ident: B49 article-title: Gross examination report of a COVID-19 death autopsy publication-title: Fa Yi Xue Za Zhi – ident: B22 doi: 10.1182/blood-2008-10-186601 – ident: B47 doi: 10.1038/nri3152 – ident: B16 doi: 10.1016/j.ijantimicag.2020.105938 – ident: B40 doi: 10.1016/S2213-2600(20)30216-2 – ident: B38 doi: 10.4049/jimmunol.1900637 – ident: B34 doi: 10.1371/journal.pone.0222403 – ident: B18 doi: 10.1016/j.jaad.2020.03.056 – volume: 11 year: 2020 ident: B19 article-title: Reduction and functional exhaustion of t cells in patients with coronavirus disease 2019 (COVID-19) publication-title: Front Immunol doi: 10.3389/fimmu.2020.00827 – ident: B48 doi: 10.1016/S0140-6736(20)30566-3 – ident: B53 doi: 10.1056/NEJMcibr1917242 – volume: 38 start-page: 337 issue: 2 year: 2020 ident: B5 article-title: COVID-19, cytokines and immunosuppression: what can we learn from severe acute respiratory syndrome? publication-title: Clin Exp Rheumatol doi: 10.55563/clinexprheumatol/xcdary – ident: B24 doi: 10.1093/infdis/jiaa150 – ident: B42 doi: 10.1016/j.autrev.2020.102562 – ident: B12 doi: 10.1017/dmp.2020.60 – ident: B43 doi: 10.1016/S1473-3099(20)30376-5 – ident: B30 doi: 10.1136/annrheumdis-2020-217706 – ident: B7 doi: 10.1016/j.ijantimicag.2020.105954 – ident: B20 doi: 10.1038/s41423-020-0401-3 – ident: B4 doi: 10.1093/cid/ciaa248 – ident: B15 doi: 10.1016/S2213-2600(20)30217-4 – ident: B54 doi: 10.1172/jci.insight.98960 – volume: 7 issue: 1 year: 2020 ident: B2 article-title: The origin, transmission and clinical therapies on coronavirus disease 2019 (COVID-19) outbreak - an update on the status publication-title: Mil Med Res – ident: B25 doi: 10.1080/22221751.2020.1747363 – ident: B39 doi: 10.1371/journal.pone.0199497 – ident: B29 doi: 10.1126/sciimmunol.abc5367 – volume: 69 year: 2020 ident: B33 article-title: Comparative study of the differences in shoulder muscle activation according to arm rotation angle publication-title: Hum Mov Sci doi: 10.1016/j.humov.2019.102567 – volume: 140 year: 2020 ident: B6 article-title: Cytokine storms in COVID-19 cases? publication-title: Tidsskr Nor Laegeforen – ident: B1 doi: 10.1093/cid/ciaa449 – ident: B55 doi: 10.1097/SHK.0000000000001083 – ident: B3 doi: 10.1016/j.autrev.2020.102537 – ident: B41 doi: 10.1016/S0140-6736(20)30628-0 – ident: B32 – ident: B17 doi: 10.1001/jama.2020.4940 – ident: B10 doi: 10.1513/AnnalsATS.202003-225OC – ident: B14 doi: 10.1164/rccm.202003-0543OC |
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| Title | Severe immunosuppression and not a cytokine storm characterizes COVID-19 infections |
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