Clinical and Immunological Factors That Distinguish COVID-19 From Pandemic Influenza A(H1N1)

José Alberto Choreño-Parra; Luis Armando Jiménez-Álvarez; Alfredo Cruz-Lagunas; Tatiana Sofía Rodríguez-Reyna; Gustavo Ramírez-Martínez; Montserrat Sandoval-Vega; Diana Lizzeth Hernández-García; Eduardo M. Choreño-Parra; Yalbi I. Balderas-Martínez; Mariana Esther Martinez-Sánchez; Eduardo Márquez-García; Edda Sciutto; José Moreno-Rodríguez; José Omar Barreto-Rodríguez; Hazel Vázquez-Rojas; Gustavo Iván Centeno-Sáenz; Néstor Alvarado-Peña; Citlaltepetl Salinas-Lara; Carlos Sánchez-Garibay; David Galeana-Cadena; Gabriela Hernández; Criselda Mendoza-Milla; Andrea Domínguez; Julio Granados; Lula Mena-Hernández; Luis Ángel Pérez-Buenfil; Guillermo Domínguez-Cheritt; Carlos Cabello-Gutiérrez; Cesar Luna-Rivero; Jorge Salas-Hernández; Patricio Santillán-Doherty; Justino Regalado; Angélica Hernández-Martínez; Lorena Orozco; Federico Ávila-Moreno; Ethel A. García-Latorre; Carmen M. Hernández-Cárdenas; Shabaana A. Khader; Albert Zlotnik; Joaquín Zúñiga

doi:10.3389/fimmu.2021.593595

Clinical and Immunological Factors That Distinguish COVID-19 From Pandemic Influenza A(H1N1)

José Alberto Choreño-Parra, Luis Armando Jiménez-Álvarez, Alfredo Cruz-Lagunas, Tatiana Sofía Rodríguez-Reyna, Gustavo Ramírez-Martínez, Montserrat Sandoval-Vega, Diana Lizzeth Hernández-García, Eduardo M. Choreño-Parra, Yalbi I. Balderas-Martínez, Mariana Esther Martinez-Sánchez, Eduardo Márquez-García, Edda Sciutto, José Moreno-Rodríguez, José Omar Barreto-Rodríguez, Hazel Vázquez-Rojas, Gustavo Iván Centeno-Sáenz, Néstor Alvarado-Peña, Citlaltepetl Salinas-Lara, Carlos Sánchez-Garibay, David Galeana-CadenaGabriela Hernández, Criselda Mendoza-Milla, Andrea Domínguez, Julio Granados, Lula Mena-Hernández, Luis Ángel Pérez-Buenfil, Guillermo Domínguez-Cheritt, Carlos Cabello-Gutiérrez, Cesar Luna-Rivero, Jorge Salas-Hernández, Patricio Santillán-Doherty, Justino Regalado, Angélica Hernández-Martínez, Lorena Orozco, Federico Ávila-Moreno, Ethel A. García-Latorre, Carmen M. Hernández-Cárdenas, Shabaana A. Khader, Albert Zlotnik, Joaquín Zúñiga

Research output: Contribution to journal › Article › peer-review

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Abstract

The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of coronavirus disease 2019 (COVID-19), is a global health threat with the potential to cause severe disease manifestations in the lungs. Although COVID-19 has been extensively characterized clinically, the factors distinguishing SARS-CoV-2 from other respiratory viruses are unknown. Here, we compared the clinical, histopathological, and immunological characteristics of patients with COVID-19 and pandemic influenza A(H1N1). We observed a higher frequency of respiratory symptoms, increased tissue injury markers, and a histological pattern of alveolar pneumonia in pandemic influenza A(H1N1) patients. Conversely, dry cough, gastrointestinal symptoms and interstitial lung pathology were observed in COVID-19 cases. Pandemic influenza A(H1N1) was characterized by higher levels of IL-1RA, TNF-α, CCL3, G-CSF, APRIL, sTNF-R1, sTNF-R2, sCD30, and sCD163. Meanwhile, COVID-19 displayed an immune profile distinguished by increased Th1 (IL-12, IFN-γ) and Th2 (IL-4, IL-5, IL-10, IL-13) cytokine levels, along with IL-1β, IL-6, CCL11, VEGF, TWEAK, TSLP, MMP-1, and MMP-3. Our data suggest that SARS-CoV-2 induces a dysbalanced polyfunctional inflammatory response that is different from the immune response against pandemic influenza A(H1N1). Furthermore, we demonstrated the diagnostic potential of some clinical and immune factors to differentiate both diseases. These findings might be relevant for the ongoing and future influenza seasons in the Northern Hemisphere, which are historically unique due to their convergence with the COVID-19 pandemic.

Original language	English
Article number	593595
Journal	Frontiers in immunology
Volume	12
DOIs	https://doi.org/10.3389/fimmu.2021.593595
State	Published - Apr 21 2021

Keywords

COVID-19
Influenza A(H1N1) pdm09
SARS-CoV-2
acute respiratory distress syndrome
pandemic influenza

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10.3389/fimmu.2021.593595

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Choreño-Parra, J. A., Jiménez-Álvarez, L. A., Cruz-Lagunas, A., Rodríguez-Reyna, T. S., Ramírez-Martínez, G., Sandoval-Vega, M., Hernández-García, D. L., Choreño-Parra, E. M., Balderas-Martínez, Y. I., Martinez-Sánchez, M. E., Márquez-García, E., Sciutto, E., Moreno-Rodríguez, J., Barreto-Rodríguez, J. O., Vázquez-Rojas, H., Centeno-Sáenz, G. I., Alvarado-Peña, N., Salinas-Lara, C., Sánchez-Garibay, C., ... Zúñiga, J. (2021). Clinical and Immunological Factors That Distinguish COVID-19 From Pandemic Influenza A(H1N1). Frontiers in immunology, 12, [593595]. https://doi.org/10.3389/fimmu.2021.593595

@article{5f96b165e3cb4f42a6feb26e2426d594,

title = "Clinical and Immunological Factors That Distinguish COVID-19 From Pandemic Influenza A(H1N1)",

abstract = "The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of coronavirus disease 2019 (COVID-19), is a global health threat with the potential to cause severe disease manifestations in the lungs. Although COVID-19 has been extensively characterized clinically, the factors distinguishing SARS-CoV-2 from other respiratory viruses are unknown. Here, we compared the clinical, histopathological, and immunological characteristics of patients with COVID-19 and pandemic influenza A(H1N1). We observed a higher frequency of respiratory symptoms, increased tissue injury markers, and a histological pattern of alveolar pneumonia in pandemic influenza A(H1N1) patients. Conversely, dry cough, gastrointestinal symptoms and interstitial lung pathology were observed in COVID-19 cases. Pandemic influenza A(H1N1) was characterized by higher levels of IL-1RA, TNF-α, CCL3, G-CSF, APRIL, sTNF-R1, sTNF-R2, sCD30, and sCD163. Meanwhile, COVID-19 displayed an immune profile distinguished by increased Th1 (IL-12, IFN-γ) and Th2 (IL-4, IL-5, IL-10, IL-13) cytokine levels, along with IL-1β, IL-6, CCL11, VEGF, TWEAK, TSLP, MMP-1, and MMP-3. Our data suggest that SARS-CoV-2 induces a dysbalanced polyfunctional inflammatory response that is different from the immune response against pandemic influenza A(H1N1). Furthermore, we demonstrated the diagnostic potential of some clinical and immune factors to differentiate both diseases. These findings might be relevant for the ongoing and future influenza seasons in the Northern Hemisphere, which are historically unique due to their convergence with the COVID-19 pandemic.",

keywords = "COVID-19, Influenza A(H1N1) pdm09, SARS-CoV-2, acute respiratory distress syndrome, pandemic influenza",

author = "Chore{\~n}o-Parra, {Jos{\'e} Alberto} and Jim{\'e}nez-{\'A}lvarez, {Luis Armando} and Alfredo Cruz-Lagunas and Rodr{\'i}guez-Reyna, {Tatiana Sof{\'i}a} and Gustavo Ram{\'i}rez-Mart{\'i}nez and Montserrat Sandoval-Vega and Hern{\'a}ndez-Garc{\'i}a, {Diana Lizzeth} and Chore{\~n}o-Parra, {Eduardo M.} and Balderas-Mart{\'i}nez, {Yalbi I.} and Martinez-S{\'a}nchez, {Mariana Esther} and Eduardo M{\'a}rquez-Garc{\'i}a and Edda Sciutto and Jos{\'e} Moreno-Rodr{\'i}guez and Barreto-Rodr{\'i}guez, {Jos{\'e} Omar} and Hazel V{\'a}zquez-Rojas and Centeno-S{\'a}enz, {Gustavo Iv{\'a}n} and N{\'e}stor Alvarado-Pe{\~n}a and Citlaltepetl Salinas-Lara and Carlos S{\'a}nchez-Garibay and David Galeana-Cadena and Gabriela Hern{\'a}ndez and Criselda Mendoza-Milla and Andrea Dom{\'i}nguez and Julio Granados and Lula Mena-Hern{\'a}ndez and P{\'e}rez-Buenfil, {Luis {\'A}ngel} and Guillermo Dom{\'i}nguez-Cheritt and Carlos Cabello-Guti{\'e}rrez and Cesar Luna-Rivero and Jorge Salas-Hern{\'a}ndez and Patricio Santill{\'a}n-Doherty and Justino Regalado and Ang{\'e}lica Hern{\'a}ndez-Mart{\'i}nez and Lorena Orozco and Federico {\'A}vila-Moreno and Garc{\'i}a-Latorre, {Ethel A.} and Hern{\'a}ndez-C{\'a}rdenas, {Carmen M.} and Khader, {Shabaana A.} and Albert Zlotnik and Joaqu{\'i}n Z{\'u}{\~n}iga",

note = "Funding Information: JC-P was supported by the National Council of Science and Technology of Mexico (CONACyT) to achieve his PhD degree (CONACyT-CVU 737347). The current study received funding from institutional research grants of INER, from the UNAM-INER interinstitutional collaboration agreement (UNAM: 43355-3065-17-XI-15, to FA-M), from the Direcci{\'o}n General de Personal Acad{\'e}mico de la Universidad Nacional Aut{\'o}noma de M{\'e}xico (UNAM, grant #IV201020 to ES), and from CONACyT under the research contracts: CONACYT-Support for scientific research, technological development and innovation in health during COVID-19 contingency (CONACyT-COVID-19), with the project numbers 313517 and 00311999 to TR-R; SECTEI/050/2020, Secretar{\'ı}a de Ciencia, Tecnologı{\'a} e Innovaci{\'o}n de la Ciudad de M{\'e}xico (SECTEI CDMX); FORDECYT/10SE/2020/05/14-06 and FORDECYT/10SE/2020/05/14-07 from the Fondo Institucional de Fomento Regional para el Desarrollo Cientıf{\'i} co y Tecnol{\'o}gico y de Innovaci{\'o}n (FORDECYT) to JZ. Publisher Copyright: {\textcopyright} Copyright {\textcopyright} 2021 Chore{\~n}o-Parra, Jim{\'e}nez-{\'A}lvarez, Cruz-Lagunas, Rodr{\'i}guez-Reyna, Ram{\'i}rez-Mart{\'i}nez, Sandoval-Vega, Hern{\'a}ndez-Garc{\'i}a, Chore{\~n}o-Parra, Balderas-Mart{\'i}nez, Martinez-S{\'a}nchez, M{\'a}rquez-Garc{\'i}a, Sciutto, Moreno-Rodr{\'i}guez, Barreto-Rodr{\'i}guez, V{\'a}zquez-Rojas, Centeno-S{\'a}enz, Alvarado-Pe{\~n}a, Salinas-Lara, S{\'a}nchez-Garibay, Galeana-Cadena, Hern{\'a}ndez, Mendoza-Milla, Dom{\'i}nguez, Granados, Mena-Hern{\'a}ndez, P{\'e}rez-Buenfil, Dom{\'i}nguez-Cheritt, Cabello-Guti{\'e}rrez, Luna-Rivero, Salas-Hern{\'a}ndez, Santill{\'a}n-Doherty, Regalado, Hern{\'a}ndez-Mart{\'i}nez, Orozco, {\'A}vila-Moreno, Garc{\'i}a-Latorre, Hern{\'a}ndez-C{\'a}rdenas, Khader, Zlotnik and Z{\'u}{\~n}iga.",

year = "2021",

month = apr,

day = "21",

doi = "10.3389/fimmu.2021.593595",

language = "English",

volume = "12",

journal = "Frontiers in Immunology",

issn = "1664-3224",

}

Choreño-Parra, JA, Jiménez-Álvarez, LA, Cruz-Lagunas, A, Rodríguez-Reyna, TS, Ramírez-Martínez, G, Sandoval-Vega, M, Hernández-García, DL, Choreño-Parra, EM, Balderas-Martínez, YI, Martinez-Sánchez, ME, Márquez-García, E, Sciutto, E, Moreno-Rodríguez, J, Barreto-Rodríguez, JO, Vázquez-Rojas, H, Centeno-Sáenz, GI, Alvarado-Peña, N, Salinas-Lara, C, Sánchez-Garibay, C, Galeana-Cadena, D, Hernández, G, Mendoza-Milla, C, Domínguez, A, Granados, J, Mena-Hernández, L, Pérez-Buenfil, LÁ, Domínguez-Cheritt, G, Cabello-Gutiérrez, C, Luna-Rivero, C, Salas-Hernández, J, Santillán-Doherty, P, Regalado, J, Hernández-Martínez, A, Orozco, L, Ávila-Moreno, F, García-Latorre, EA, Hernández-Cárdenas, CM, Khader, SA, Zlotnik, A & Zúñiga, J 2021, 'Clinical and Immunological Factors That Distinguish COVID-19 From Pandemic Influenza A(H1N1)', Frontiers in immunology, vol. 12, 593595. https://doi.org/10.3389/fimmu.2021.593595

TY - JOUR

T1 - Clinical and Immunological Factors That Distinguish COVID-19 From Pandemic Influenza A(H1N1)

AU - Choreño-Parra, José Alberto

AU - Jiménez-Álvarez, Luis Armando

AU - Cruz-Lagunas, Alfredo

AU - Rodríguez-Reyna, Tatiana Sofía

AU - Ramírez-Martínez, Gustavo

AU - Sandoval-Vega, Montserrat

AU - Hernández-García, Diana Lizzeth

AU - Choreño-Parra, Eduardo M.

AU - Balderas-Martínez, Yalbi I.

AU - Martinez-Sánchez, Mariana Esther

AU - Márquez-García, Eduardo

AU - Sciutto, Edda

AU - Moreno-Rodríguez, José

AU - Barreto-Rodríguez, José Omar

AU - Vázquez-Rojas, Hazel

AU - Centeno-Sáenz, Gustavo Iván

AU - Alvarado-Peña, Néstor

AU - Salinas-Lara, Citlaltepetl

AU - Sánchez-Garibay, Carlos

AU - Galeana-Cadena, David

AU - Hernández, Gabriela

AU - Mendoza-Milla, Criselda

AU - Domínguez, Andrea

AU - Granados, Julio

AU - Mena-Hernández, Lula

AU - Pérez-Buenfil, Luis Ángel

AU - Domínguez-Cheritt, Guillermo

AU - Cabello-Gutiérrez, Carlos

AU - Luna-Rivero, Cesar

AU - Salas-Hernández, Jorge

AU - Santillán-Doherty, Patricio

AU - Regalado, Justino

AU - Hernández-Martínez, Angélica

AU - Orozco, Lorena

AU - Ávila-Moreno, Federico

AU - García-Latorre, Ethel A.

AU - Hernández-Cárdenas, Carmen M.

AU - Khader, Shabaana A.

AU - Zlotnik, Albert

AU - Zúñiga, Joaquín

N1 - Funding Information: JC-P was supported by the National Council of Science and Technology of Mexico (CONACyT) to achieve his PhD degree (CONACyT-CVU 737347). The current study received funding from institutional research grants of INER, from the UNAM-INER interinstitutional collaboration agreement (UNAM: 43355-3065-17-XI-15, to FA-M), from the Dirección General de Personal Académico de la Universidad Nacional Autónoma de México (UNAM, grant #IV201020 to ES), and from CONACyT under the research contracts: CONACYT-Support for scientific research, technological development and innovation in health during COVID-19 contingency (CONACyT-COVID-19), with the project numbers 313517 and 00311999 to TR-R; SECTEI/050/2020, Secretarı́a de Ciencia, Tecnologıá e Innovación de la Ciudad de México (SECTEI CDMX); FORDECYT/10SE/2020/05/14-06 and FORDECYT/10SE/2020/05/14-07 from the Fondo Institucional de Fomento Regional para el Desarrollo Cientıfí co y Tecnológico y de Innovación (FORDECYT) to JZ. Publisher Copyright: © Copyright © 2021 Choreño-Parra, Jiménez-Álvarez, Cruz-Lagunas, Rodríguez-Reyna, Ramírez-Martínez, Sandoval-Vega, Hernández-García, Choreño-Parra, Balderas-Martínez, Martinez-Sánchez, Márquez-García, Sciutto, Moreno-Rodríguez, Barreto-Rodríguez, Vázquez-Rojas, Centeno-Sáenz, Alvarado-Peña, Salinas-Lara, Sánchez-Garibay, Galeana-Cadena, Hernández, Mendoza-Milla, Domínguez, Granados, Mena-Hernández, Pérez-Buenfil, Domínguez-Cheritt, Cabello-Gutiérrez, Luna-Rivero, Salas-Hernández, Santillán-Doherty, Regalado, Hernández-Martínez, Orozco, Ávila-Moreno, García-Latorre, Hernández-Cárdenas, Khader, Zlotnik and Zúñiga.

PY - 2021/4/21

Y1 - 2021/4/21

N2 - The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of coronavirus disease 2019 (COVID-19), is a global health threat with the potential to cause severe disease manifestations in the lungs. Although COVID-19 has been extensively characterized clinically, the factors distinguishing SARS-CoV-2 from other respiratory viruses are unknown. Here, we compared the clinical, histopathological, and immunological characteristics of patients with COVID-19 and pandemic influenza A(H1N1). We observed a higher frequency of respiratory symptoms, increased tissue injury markers, and a histological pattern of alveolar pneumonia in pandemic influenza A(H1N1) patients. Conversely, dry cough, gastrointestinal symptoms and interstitial lung pathology were observed in COVID-19 cases. Pandemic influenza A(H1N1) was characterized by higher levels of IL-1RA, TNF-α, CCL3, G-CSF, APRIL, sTNF-R1, sTNF-R2, sCD30, and sCD163. Meanwhile, COVID-19 displayed an immune profile distinguished by increased Th1 (IL-12, IFN-γ) and Th2 (IL-4, IL-5, IL-10, IL-13) cytokine levels, along with IL-1β, IL-6, CCL11, VEGF, TWEAK, TSLP, MMP-1, and MMP-3. Our data suggest that SARS-CoV-2 induces a dysbalanced polyfunctional inflammatory response that is different from the immune response against pandemic influenza A(H1N1). Furthermore, we demonstrated the diagnostic potential of some clinical and immune factors to differentiate both diseases. These findings might be relevant for the ongoing and future influenza seasons in the Northern Hemisphere, which are historically unique due to their convergence with the COVID-19 pandemic.

AB - The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of coronavirus disease 2019 (COVID-19), is a global health threat with the potential to cause severe disease manifestations in the lungs. Although COVID-19 has been extensively characterized clinically, the factors distinguishing SARS-CoV-2 from other respiratory viruses are unknown. Here, we compared the clinical, histopathological, and immunological characteristics of patients with COVID-19 and pandemic influenza A(H1N1). We observed a higher frequency of respiratory symptoms, increased tissue injury markers, and a histological pattern of alveolar pneumonia in pandemic influenza A(H1N1) patients. Conversely, dry cough, gastrointestinal symptoms and interstitial lung pathology were observed in COVID-19 cases. Pandemic influenza A(H1N1) was characterized by higher levels of IL-1RA, TNF-α, CCL3, G-CSF, APRIL, sTNF-R1, sTNF-R2, sCD30, and sCD163. Meanwhile, COVID-19 displayed an immune profile distinguished by increased Th1 (IL-12, IFN-γ) and Th2 (IL-4, IL-5, IL-10, IL-13) cytokine levels, along with IL-1β, IL-6, CCL11, VEGF, TWEAK, TSLP, MMP-1, and MMP-3. Our data suggest that SARS-CoV-2 induces a dysbalanced polyfunctional inflammatory response that is different from the immune response against pandemic influenza A(H1N1). Furthermore, we demonstrated the diagnostic potential of some clinical and immune factors to differentiate both diseases. These findings might be relevant for the ongoing and future influenza seasons in the Northern Hemisphere, which are historically unique due to their convergence with the COVID-19 pandemic.

KW - COVID-19

KW - Influenza A(H1N1) pdm09

KW - SARS-CoV-2

KW - acute respiratory distress syndrome

KW - pandemic influenza

UR - http://www.scopus.com/inward/record.url?scp=85105932887&partnerID=8YFLogxK

U2 - 10.3389/fimmu.2021.593595

DO - 10.3389/fimmu.2021.593595

M3 - Article

C2 - 33995342

AN - SCOPUS:85105932887

VL - 12

JO - Frontiers in Immunology

JF - Frontiers in Immunology

SN - 1664-3224

M1 - 593595

ER -

Clinical and Immunological Factors That Distinguish COVID-19 From Pandemic Influenza A(H1N1)

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