Distinct systemic immune networks define severe vs. mild COVID-19 in hematologic and solid cancer patients
IntroductionThe COVID-19 pandemic, caused by the coronavirus SARS-CoV-2, has impacted health across all sectors of society. A cytokine-release syndrome, combined with an inefficient response of innate immune cells to directly combat the virus, characterizes the severe form of COVID-19. While immune...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-01-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1052104/full |
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| author | Flávio Pignataro-Oshiro Amanda B. Figueiredo Nayane A. L. Galdino Katia L. P. Morais Walderez O. Dutra Bianca Grassi de Miranda Silva Diego Feriani Flávia de Azevedo Abrantes Ivan Leonardo Avelino França e Silva Jayr Schmidt Filho Juliana Valéria de Souza Framil Marcelle Goldner Cesca Rachel Simões Pimenta Riechelmann Marjorie V. Batista Kenneth J. Gollob Kenneth J. Gollob |
| author_facet | Flávio Pignataro-Oshiro Amanda B. Figueiredo Nayane A. L. Galdino Katia L. P. Morais Walderez O. Dutra Bianca Grassi de Miranda Silva Diego Feriani Flávia de Azevedo Abrantes Ivan Leonardo Avelino França e Silva Jayr Schmidt Filho Juliana Valéria de Souza Framil Marcelle Goldner Cesca Rachel Simões Pimenta Riechelmann Marjorie V. Batista Kenneth J. Gollob Kenneth J. Gollob |
| author_sort | Flávio Pignataro-Oshiro |
| collection | DOAJ |
| description | IntroductionThe COVID-19 pandemic, caused by the coronavirus SARS-CoV-2, has impacted health across all sectors of society. A cytokine-release syndrome, combined with an inefficient response of innate immune cells to directly combat the virus, characterizes the severe form of COVID-19. While immune factors involved in the development of severe COVID-19 in the general population are becoming clearer, identification of the immune mechanisms behind severe disease in oncologic patients remains uncertain.MethodsHere we evaluated the systemic immune response through the analysis of soluble blood immune factors and anti-SARS-CoV-2 antibodies within the early days of a positive SARS-CoV-2 diagnostic in oncologic patients.ResultsIndividuals with hematologic malignancies that went on to die from COVID-19 displayed at diagnosis severe leukopenia, low antibody production against SARS-CoV-2 proteins, and elevated production of innate immune cell recruitment and activation factors. These patients also displayed correlation networks in which IL-2, IL-13, TNF-alpha, IFN-gamma, and FGF2 were the focal points. Hematologic cancer patients that showed highly networked and coordinated anti-SARS-CoV-2 antibody production, with central importance of IL-4, IL-5, IL-12A, IL-15, and IL-17A, presented only mild COVID-19. Conversely, solid tumor patients that had elevated levels of inflammatory cytokines IL-6, CXCL8, and lost the coordinate production of anti-virus antibodies developed severe COVID-19 and died. Patients that displayed positive correlation networks between anti-virus antibodies, and a regulatory axis involving IL-10 and inflammatory cytokines recovered from the disease. We also provided evidence that CXCL8 is a strong predictor of death for oncologic patients and could be an indicator of poor prognosis within days of the positive diagnostic of SARS-CoV-2 infection.ConclusionOur findings defined distinct systemic immune profiles associated with COVID-19 clinical outcome of patients with cancer and COVID-19. These systemic immune networks shed light on potential immune mechanisms involved in disease outcome, as well as identify potential clinically useful biomarkers. |
| first_indexed | 2024-04-11T00:05:06Z |
| format | Article |
| id | doaj.art-113cd73c874e4befb698029452efc7ef |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-11T00:05:06Z |
| publishDate | 2023-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-113cd73c874e4befb698029452efc7ef2023-01-09T11:22:47ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-01-011310.3389/fimmu.2022.10521041052104Distinct systemic immune networks define severe vs. mild COVID-19 in hematologic and solid cancer patientsFlávio Pignataro-Oshiro0Amanda B. Figueiredo1Nayane A. L. Galdino2Katia L. P. Morais3Walderez O. Dutra4Bianca Grassi de Miranda Silva5Diego Feriani6Flávia de Azevedo Abrantes7Ivan Leonardo Avelino França e Silva8Jayr Schmidt Filho9Juliana Valéria de Souza Framil10Marcelle Goldner Cesca11Rachel Simões Pimenta Riechelmann12Marjorie V. Batista13Kenneth J. Gollob14Kenneth J. Gollob15International Research Center, Translational Immuno-oncology Group, A.C.Camargo Cancer Center, São Paulo, BrazilInternational Research Center, Translational Immuno-oncology Group, A.C.Camargo Cancer Center, São Paulo, BrazilInternational Research Center, Translational Immuno-oncology Group, A.C.Camargo Cancer Center, São Paulo, BrazilInternational Research Center, Translational Immuno-oncology Group, A.C.Camargo Cancer Center, São Paulo, BrazilDepartment of Morphology, Federal University of Minas Gerais, Belo Horizonte, BrazilInfectious Diseases Department, A.C.Camargo Cancer Center, Sao Paulo, BrazilInfectious Diseases Department, A.C.Camargo Cancer Center, Sao Paulo, BrazilInfectious Diseases Department, A.C.Camargo Cancer Center, Sao Paulo, BrazilInfectious Diseases Department, A.C.Camargo Cancer Center, Sao Paulo, BrazilHematology Department, A.C.Camargo Cancer Center, Sao Paulo, BrazilInfectious Diseases Department, A.C.Camargo Cancer Center, Sao Paulo, BrazilClinical Oncology Department, A.C.Camargo Cancer Center, Sao Paulo, BrazilClinical Oncology Department, A.C.Camargo Cancer Center, Sao Paulo, BrazilInfectious Diseases Department, A.C.Camargo Cancer Center, Sao Paulo, BrazilInternational Research Center, Translational Immuno-oncology Group, A.C.Camargo Cancer Center, São Paulo, BrazilHospital Israelita Albert Einstein, Israelite Institute for Education and Research, Translational Immuno-oncology Laboratory, São Paulo, BrazilIntroductionThe COVID-19 pandemic, caused by the coronavirus SARS-CoV-2, has impacted health across all sectors of society. A cytokine-release syndrome, combined with an inefficient response of innate immune cells to directly combat the virus, characterizes the severe form of COVID-19. While immune factors involved in the development of severe COVID-19 in the general population are becoming clearer, identification of the immune mechanisms behind severe disease in oncologic patients remains uncertain.MethodsHere we evaluated the systemic immune response through the analysis of soluble blood immune factors and anti-SARS-CoV-2 antibodies within the early days of a positive SARS-CoV-2 diagnostic in oncologic patients.ResultsIndividuals with hematologic malignancies that went on to die from COVID-19 displayed at diagnosis severe leukopenia, low antibody production against SARS-CoV-2 proteins, and elevated production of innate immune cell recruitment and activation factors. These patients also displayed correlation networks in which IL-2, IL-13, TNF-alpha, IFN-gamma, and FGF2 were the focal points. Hematologic cancer patients that showed highly networked and coordinated anti-SARS-CoV-2 antibody production, with central importance of IL-4, IL-5, IL-12A, IL-15, and IL-17A, presented only mild COVID-19. Conversely, solid tumor patients that had elevated levels of inflammatory cytokines IL-6, CXCL8, and lost the coordinate production of anti-virus antibodies developed severe COVID-19 and died. Patients that displayed positive correlation networks between anti-virus antibodies, and a regulatory axis involving IL-10 and inflammatory cytokines recovered from the disease. We also provided evidence that CXCL8 is a strong predictor of death for oncologic patients and could be an indicator of poor prognosis within days of the positive diagnostic of SARS-CoV-2 infection.ConclusionOur findings defined distinct systemic immune profiles associated with COVID-19 clinical outcome of patients with cancer and COVID-19. These systemic immune networks shed light on potential immune mechanisms involved in disease outcome, as well as identify potential clinically useful biomarkers.https://www.frontiersin.org/articles/10.3389/fimmu.2022.1052104/fullSARS-CoV-2COVID-19cancersystemic immune profiledisease severity predictioncytokine-release syndrome |
| spellingShingle | Flávio Pignataro-Oshiro Amanda B. Figueiredo Nayane A. L. Galdino Katia L. P. Morais Walderez O. Dutra Bianca Grassi de Miranda Silva Diego Feriani Flávia de Azevedo Abrantes Ivan Leonardo Avelino França e Silva Jayr Schmidt Filho Juliana Valéria de Souza Framil Marcelle Goldner Cesca Rachel Simões Pimenta Riechelmann Marjorie V. Batista Kenneth J. Gollob Kenneth J. Gollob Distinct systemic immune networks define severe vs. mild COVID-19 in hematologic and solid cancer patients Frontiers in Immunology SARS-CoV-2 COVID-19 cancer systemic immune profile disease severity prediction cytokine-release syndrome |
| title | Distinct systemic immune networks define severe vs. mild COVID-19 in hematologic and solid cancer patients |
| title_full | Distinct systemic immune networks define severe vs. mild COVID-19 in hematologic and solid cancer patients |
| title_fullStr | Distinct systemic immune networks define severe vs. mild COVID-19 in hematologic and solid cancer patients |
| title_full_unstemmed | Distinct systemic immune networks define severe vs. mild COVID-19 in hematologic and solid cancer patients |
| title_short | Distinct systemic immune networks define severe vs. mild COVID-19 in hematologic and solid cancer patients |
| title_sort | distinct systemic immune networks define severe vs mild covid 19 in hematologic and solid cancer patients |
| topic | SARS-CoV-2 COVID-19 cancer systemic immune profile disease severity prediction cytokine-release syndrome |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1052104/full |
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