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Article ; Online: Coinfection with influenza A virus enhances SARS-CoV-2 infectivity.

Bai, Lei / Zhao, Yongliang / Dong, Jiazhen / Liang, Simeng / Guo, Ming / Liu, Xinjin / Wang, Xin / Huang, Zhixiang / Sun, Xiaoyi / Zhang, Zhen / Dong, Lianghui / Liu, Qianyun / Zheng, Yucheng / Niu, Danping / Xiang, Min / Song, Kun / Ye, Jiajie / Zheng, Wenchao / Tang, Zhidong /

Tang, Mingliang / Zhou, Yu / Shen, Chao / Dai, Ming / Zhou, Li / Chen, Yu / Yan, Huan / Lan, Ke / Xu, Ke

Cell research

2021 Volume 31, Issue 4, Page(s) 395–403

Abstract: ... with influenza A virus (IAV) and either pseudotyped or live SARS-CoV-2 virus, we found that IAV preinfection ... Moreover, such enhancement of SARS-CoV-2 infectivity was not observed with several other respiratory ... significantly promoted the infectivity of SARS-CoV-2 in a broad range of cell types. Remarkably, in vivo ...

Abstract	The upcoming flu season in the Northern Hemisphere merging with the current COVID-19 pandemic raises a potentially severe threat to public health. Through experimental coinfection with influenza A virus (IAV) and either pseudotyped or live SARS-CoV-2 virus, we found that IAV preinfection significantly promoted the infectivity of SARS-CoV-2 in a broad range of cell types. Remarkably, in vivo, increased SARS-CoV-2 viral load and more severe lung damage were observed in mice coinfected with IAV. Moreover, such enhancement of SARS-CoV-2 infectivity was not observed with several other respiratory viruses, likely due to a unique feature of IAV to elevate ACE2 expression. This study illustrates that IAV has a unique ability to aggravate SARS-CoV-2 infection, and thus, prevention of IAV infection is of great significance during the COVID-19 pandemic.
MeSH term(s)	Angiotensin-Converting Enzyme 2/deficiency ; Angiotensin-Converting Enzyme 2/genetics ; Angiotensin-Converting Enzyme 2/metabolism ; Animals ; COVID-19/pathology ; COVID-19/virology ; Cathepsin L/genetics ; Cathepsin L/metabolism ; Cell Line ; Coinfection/pathology ; Coinfection/virology ; Humans ; Influenza A virus/isolation & purification ; Influenza A virus/physiology ; Lung/pathology ; Mice ; Mice, Transgenic ; Orthomyxoviridae Infections/pathology ; Orthomyxoviridae Infections/virology ; SARS-CoV-2/isolation & purification ; SARS-CoV-2/physiology ; Serine Endopeptidases/genetics ; Serine Endopeptidases/metabolism ; Severity of Illness Index ; Viral Load ; Virus Internalization
Chemical Substances	Ace2 protein, mouse (EC 3.4.17.23) ; Angiotensin-Converting Enzyme 2 (EC 3.4.17.23) ; Serine Endopeptidases (EC 3.4.21.-) ; TMPRSS2 protein, mouse (EC 3.4.21.-) ; Cathepsin L (EC 3.4.22.15)
Language	English
Publishing date	2021-02-18
Publishing country	England
Document type	Journal Article
ZDB-ID	1319303-x
ISSN	1748-7838 ; 1001-0602
ISSN (online)	1748-7838
ISSN	1001-0602
DOI	10.1038/s41422-021-00473-1
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Co-infection of influenza A virus enhances SARS-CoV-2 infectivity

Tang, Mingliang / Zhou, Yu / Shen, Chao / Dai, Ming / Zhou, Li / Chen, Yu / Yan, Huan / Lan, Ke / Xu, Ke

bioRxiv

Abstract: ... with either pseudotyped or SARS-CoV-2 live virus, we found that IAV pre-infection significantly promoted the infectivity ... of the co-infection of influenza A virus (IAV) and SARS-CoV-2. Through experimental co-infection of IAV ... of SARS-CoV-2 in a broad range of cell types. Intriguingly, such enhancement of SARS-CoV-2 infectivity was ...

Abstract	The upcoming flu season in the northern hemisphere merging with the current COVID-19 pandemic may raise a potentially severe threat to public health. However, little is known about the consequences of the co-infection of influenza A virus (IAV) and SARS-CoV-2. Through experimental co-infection of IAV with either pseudotyped or SARS-CoV-2 live virus, we found that IAV pre-infection significantly promoted the infectivity of SARS-CoV-2 in a broad range of cell types. Intriguingly, such enhancement of SARS-CoV-2 infectivity was only seen under co-infection with IAV but not with several other viruses including Sendai virus, human rhinovirus, human parainfluenza virus, human respiratory syncytial virus, or human enterovirus 71. IAV infection rather than interferon signaling induced elevated expression of ACE2 essential for such enhancement of SARS-CoV-2 infectivity. Remarkably, we further confirmed that the pre-infection of IAV indeed resulted in an increased SARS-CoV-2 viral load and more severe lung damage in hACE2-transgenic mice. This study illustrates that the co-infection of IAV aggravates SARS-CoV-2 infection and disease severity, which in turn suggests that preventing the convergence of flu season and COVID-19 pandemic would be of great significance.
Keywords	covid19
Language	English
Publishing date	2020-10-14
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2020.10.14.335893
Database	COVID19

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Article ; Online: Co-infection of influenza A virus enhances SARS-CoV-2 infectivity

Tang, Mingliang / Zhou, Yu / Shen, Chao / Dai, Ming / Zhou, Li / Chen, Yu / Yan, Huan / Lan, Ke / Xu, Ke

bioRxiv

Abstract: ... with either pseudotyped or SARS-CoV-2 live virus, we found that IAV pre-infection significantly promoted the infectivity ... 2 infectivity was not seen with several other viruses probably due to a unique IAV segment ... lung damage were observed in mice co-infected with IAV in vivo. Moreover, such enhancement of SARS-CoV ...

Abstract	The upcoming flu season in the northern hemisphere merging with the current COVID-19 pandemic raises a potentially severe threat to public health. Through experimental co-infection of IAV with either pseudotyped or SARS-CoV-2 live virus, we found that IAV pre-infection significantly promoted the infectivity of SARS-CoV-2 in a broad range of cell types. Remarkably, increased SARS-CoV-2 viral load and more severe lung damage were observed in mice co-infected with IAV in vivo. Moreover, such enhancement of SARS-CoV-2 infectivity was not seen with several other viruses probably due to a unique IAV segment as an inducer to elevate ACE2 expression. This study illustrates that IAV has a special nature to aggravate SARS-CoV-2 infection, and prevention of IAV is of great significance during the COVID-19 pandemic.
Keywords	covid19
Publisher	BioRxiv; WHO
Document type	Article ; Online
DOI	10.1101/2020.10.14.335893
Database	COVID19

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Article: Counterintuitive effect of antiviral therapy on influenza A-SARS-CoV-2 coinfection due to viral interference.

Cheemarla, Nagarjuna R / Mihaylova, Valia T / Watkins, Timothy A / Foxman, Ellen F

bioRxiv : the preprint server for biology

2023

Abstract: ... influenza A virus (IAV) -SARS-CoV-2 coinfection using differentiated cultures of the human airway epithelium ... The resurgence of influenza and continued circulation of SARS-CoV-2 raise the question of how ... Coexposure to IAV enhanced the tissue antiviral response during SARS-CoV-2 infection and suppressed SARS-CoV ...

Abstract	The resurgence of influenza and continued circulation of SARS-CoV-2 raise the question of how these viruses interact in a co-exposed host. Here we studied virus-virus and host-virus interactions during influenza A virus (IAV) -SARS-CoV-2 coinfection using differentiated cultures of the human airway epithelium. Coexposure to IAV enhanced the tissue antiviral response during SARS-CoV-2 infection and suppressed SARS-CoV-2 replication. Oseltamivir, an antiviral targeting influenza, reduced IAV replication during coinfection but also reduced the antiviral response and paradoxically restored SARS-CoV-2 replication. These results highlight the importance of diagnosing coinfections and compel further study of how coinfections impact the outcome of antiviral therapy.
Language	English
Publishing date	2023-02-08
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.02.07.527372
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Article ; Online: Viral Interference During Influenza A-SARS-CoV-2 Coinfection of the Human Airway Epithelium and Reversal by Oseltamivir.

Cheemarla, Nagarjuna R / Watkins, Timothy A / Mihaylova, Valia T / Foxman, Ellen F

The Journal of infectious diseases

2023 Volume 229, Issue 5, Page(s) 1430–1434

Abstract: ... replication in both sequential and simultaneous infections, whereas SARS-CoV-2 did not enhance host cell ... severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) coinfections using differentiated human airway epithelial cultures ... restored SARS-CoV-2 replication. These results demonstrate how perturbations in one viral infection ...

Abstract	To gain insight into interactions among respiratory viruses, we modeled influenza A virus (IAV)-severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) coinfections using differentiated human airway epithelial cultures. Replicating IAV induced a more robust interferon response than SARS-CoV-2 and suppressed SARS-CoV-2 replication in both sequential and simultaneous infections, whereas SARS-CoV-2 did not enhance host cell defense during influenza infection or suppress IAV replication. Oseltamivir, an antiviral targeting influenza, reduced IAV replication during coinfection but also reduced the host antiviral response and restored SARS-CoV-2 replication. These results demonstrate how perturbations in one viral infection can impact its effect on a coinfecting virus.
MeSH term(s)	Humans ; Oseltamivir/pharmacology ; Oseltamivir/therapeutic use ; SARS-CoV-2/drug effects ; Antiviral Agents/pharmacology ; Antiviral Agents/therapeutic use ; Coinfection/virology ; Coinfection/drug therapy ; Influenza A virus/drug effects ; Virus Replication/drug effects ; COVID-19/virology ; Influenza, Human/virology ; Influenza, Human/drug therapy ; Viral Interference ; Epithelial Cells/virology ; Respiratory Mucosa/virology ; COVID-19 Drug Treatment
Language	English
Publishing date	2023-08-30
Publishing country	United States
Document type	Journal Article
ZDB-ID	3019-3
ISSN	1537-6613 ; 0022-1899
ISSN (online)	1537-6613
ISSN	0022-1899
DOI	10.1093/infdis/jiad402
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Article ; Online: Prevalence and associated outcomes of coinfection between SARS-CoV-2 and influenza: a systematic review and meta-analysis.

Yan, Xiaolong / Li, Ke / Lei, Zhiqun / Luo, Jiayao / Wang, Qi / Wei, Sheng

International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases

2023 Volume 136, Page(s) 29–36

Abstract: ... of coinfection with influenza virus was 2.45% (95% confidence interval [CI]: 1.67-3.58%), with a high proportion ... Objectives: To estimate the prevalence of influenza coinfection in COVID-19 patients and ... of influenza A. Compared with mono-infected patients (COVID-19 only), the odds ratio (OR) for severe outcomes ...

Abstract	Objectives: To estimate the prevalence of influenza coinfection in COVID-19 patients and investigate its association with severe clinical outcomes. Methods: We systematically searched the Web of Science, PubMed, Scopus, Embase, The Cochrane Library, and CNKI for studies published between January 01, 2020, and May 31, 2023. Meta-analysis was performed to estimate the pooled prevalence of coinfection and the impact on clinical outcomes. Systematic review registered in PROSPERO (CRD42023423113). Results: A total of 95 studies involving 62,107 COVID-19 patients were included. The pooled prevalence of coinfection with influenza virus was 2.45% (95% confidence interval [CI]: 1.67-3.58%), with a high proportion of influenza A. Compared with mono-infected patients (COVID-19 only), the odds ratio (OR) for severe outcomes (including intensive care unit admission [OR = 2.20, 95% CI: 1.68-2.87, P < 0.001], mechanical ventilation support [OR = 2.73, 95% CI: 1.46-5.10, P = 0.002], and mortality [OR = 2.92, 95% CI: 1.16-7.30, P = 0.022]) was significantly higher among patients coinfected influenza A. Conclusion: Although the prevalence of coinfection is low, coinfected patients are at higher risk of severe outcomes. Enhanced identification of both viruses, as well as individualized treatment protocols for coinfection, are recommended to reduce the occurrence of serious disease outcomes in the future.
MeSH term(s)	Humans ; SARS-CoV-2 ; COVID-19/epidemiology ; COVID-19/therapy ; Influenza, Human/complications ; Influenza, Human/epidemiology ; Influenza, Human/therapy ; Coinfection/epidemiology ; Prevalence
Language	English
Publishing date	2023-08-28
Publishing country	Canada
Document type	Meta-Analysis ; Systematic Review ; Journal Article
ZDB-ID	1331197-9
ISSN	1878-3511 ; 1201-9712
ISSN (online)	1878-3511
ISSN	1201-9712
DOI	10.1016/j.ijid.2023.08.021
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Article ; Online: Counterintuitive effect of antiviral therapy on influenza A-SARS-CoV-2 coinfection due to viral interference

Cheemarla, Nagarjuna R. / Mihaylova, Valia T. / Watkins, Timothy A. / Foxman, Ellen F.

bioRxiv

Abstract	The resurgence of influenza and continued circulation of SARS-CoV-2 raise the question of how these viruses interact in a co-exposed host. Here we studied virus-virus and host-virus interactions during influenza A virus (IAV) -SARS-CoV-2 coinfection using differentiated cultures of the human airway epithelium. Coexposure to IAV enhanced the tissue antiviral response during SARS-CoV-2 infection and suppressed SARS-CoV-2 replication. Oseltamivir, an antiviral targeting influenza, reduced IAV replication during coinfection but also reduced the antiviral response and paradoxically restored SARS-CoV-2 replication. These results highlight the importance of diagnosing coinfections and compel further study of how coinfections impact the outcome of antiviral therapy.
Keywords	covid19
Language	English
Publishing date	2023-02-08
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2023.02.07.527372
Database	COVID19

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Article ; Online: Increased lethality in influenza and SARS-CoV-2 coinfection is prevented by influenza immunity but not SARS-CoV-2 immunity.

Achdout, Hagit / Vitner, Einat B / Politi, Boaz / Melamed, Sharon / Yahalom-Ronen, Yfat / Tamir, Hadas / Erez, Noam / Avraham, Roy / Weiss, Shay / Cherry, Lilach / Bar-Haim, Erez / Makdasi, Efi / Gur, David / Aftalion, Moshe / Chitlaru, Theodor / Vagima, Yaron / Paran, Nir / Israely, Tomer

Nature communications

2021 Volume 12, Issue 1, Page(s) 5819

Abstract: ... outcome of influenza A virus (IAV) and SARS-CoV-2 coinfection in K18-hACE2 mice. Our data indicate enhance ... of influenza/SARS-CoV-2 coinfection, which may result in severe disease. In this study, we examine the disease ... In contrast to nonfatal influenza and lower mortality rates due to SARS-CoV-2 alone, this coinfection results ...

Abstract	Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the cause of the ongoing coronavirus disease 2019 (COVID-19) pandemic. The continued spread of SARS-CoV-2 increases the probability of influenza/SARS-CoV-2 coinfection, which may result in severe disease. In this study, we examine the disease outcome of influenza A virus (IAV) and SARS-CoV-2 coinfection in K18-hACE2 mice. Our data indicate enhance susceptibility of IAV-infected mice to developing severe disease upon coinfection with SARS-CoV-2 two days later. In contrast to nonfatal influenza and lower mortality rates due to SARS-CoV-2 alone, this coinfection results in severe morbidity and nearly complete mortality. Coinfection is associated with elevated influenza viral loads in respiratory organs. Remarkably, prior immunity to influenza, but not to SARS-CoV-2, prevents severe disease and mortality. This protection is antibody-dependent. These data experimentally support the necessity of seasonal influenza vaccination for reducing the risk of severe influenza/COVID-19 comorbidity during the COVID-19 pandemic.
MeSH term(s)	Angiotensin-Converting Enzyme 2/metabolism ; Animals ; Antibodies, Viral/immunology ; COVID-19/immunology ; COVID-19/pathology ; COVID-19/virology ; Cell Line ; Coinfection/immunology ; Coinfection/virology ; Disease Models, Animal ; Female ; Humans ; Immunity ; Inflammation/genetics ; Lung/pathology ; Lung/virology ; Male ; Mice, Inbred C57BL ; Mice, Transgenic ; Orthomyxoviridae Infections/immunology ; Orthomyxoviridae Infections/virology ; SARS-CoV-2/immunology ; Up-Regulation/genetics ; Viral Load/immunology ; Mice
Chemical Substances	Antibodies, Viral ; Angiotensin-Converting Enzyme 2 (EC 3.4.17.23)
Language	English
Publishing date	2021-10-05
Publishing country	England
Document type	Journal Article
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-021-26113-1
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Article ; Online: Coinfection by Severe Acute Respiratory Syndrome Coronavirus 2 and Influenza A(H1N1)pdm09 Virus Enhances the Severity of Pneumonia in Golden Syrian Hamsters.

Zhang, Anna Jinxia / Lee, Andrew Chak-Yiu / Chan, Jasper Fuk-Woo / Liu, Feifei / Li, Can / Chen, Yanxia / Chu, Hin / Lau, Siu-Ying / Wang, Pui / Chan, Chris Chung-Sing / Poon, Vincent Kwok-Man / Yuan, Shuofeng / To, Kelvin Kai-Wang / Chen, Honglin / Yuen, Kwok-Yung

Clinical infectious diseases : an official publication of the Infectious Diseases Society of America

2020 Volume 72, Issue 12, Page(s) e978–e992

Abstract: ... coinfection by SARS-CoV-2 and A(H1N1)pdm09 caused more severe disease than monoinfection by either virus ... severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and seasonal influenza viruses are unknown.: Methods: We established ... in hamsters. Prior A(H1N1)pdm09 infection lowered SARS-CoV-2 pulmonary viral loads but enhanced lung damage ...

Abstract	Background: Clinical outcomes of the interaction between the co-circulating pandemic severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and seasonal influenza viruses are unknown. Methods: We established a golden Syrian hamster model coinfected by SARS-CoV-2 and mouse-adapted A(H1N1)pdm09 simultaneously or sequentially. The weight loss, clinical scores, histopathological changes, viral load and titer, and serum neutralizing antibody titer were compared with hamsters challenged by either virus. Results: Coinfected hamsters had more weight loss, more severe lung inflammatory damage, and tissue cytokine/chemokine expression. Lung viral load, infectious virus titers, and virus antigen expression suggested that hamsters were generally more susceptible to SARS-CoV-2 than to A(H1N1)pdm09. Sequential coinfection with A(H1N1)pdm09 one day prior to SARS-CoV-2 exposure resulted in a lower lung SARS-CoV-2 titer and viral load than with SARS-CoV-2 monoinfection, but a higher lung A(H1N1)pdm09 viral load. Coinfection also increased intestinal inflammation with more SARS-CoV-2 nucleoprotein expression in enterocytes. Simultaneous coinfection was associated with delay in resolution of lung damage, lower serum SARS-CoV-2 neutralizing antibody, and longer SARS-CoV-2 shedding in oral swabs compared to that of SARS-CoV-2 monoinfection. Conclusions: Simultaneous or sequential coinfection by SARS-CoV-2 and A(H1N1)pdm09 caused more severe disease than monoinfection by either virus in hamsters. Prior A(H1N1)pdm09 infection lowered SARS-CoV-2 pulmonary viral loads but enhanced lung damage. Whole-population influenza vaccination for prevention of coinfection, and multiplex molecular diagnostics for both viruses to achieve early initiation of antiviral treatment for improvement of clinical outcome should be considered.
MeSH term(s)	Animals ; COVID-19 ; Coinfection ; Cricetinae ; Disease Models, Animal ; Humans ; Influenza A Virus, H1N1 Subtype ; Influenza, Human ; Mesocricetus ; Mice ; SARS-CoV-2
Language	English
Publishing date	2020-11-20
Publishing country	United States
Document type	Journal Article
ZDB-ID	1099781-7
ISSN	1537-6591 ; 1058-4838
ISSN (online)	1537-6591
ISSN	1058-4838
DOI	10.1093/cid/ciaa1747
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Article: The impact of RSV/SARS-CoV-2 co-infection on clinical disease and viral replication: insights from a BALB/c mouse model.

Morris, Dorothea R / Qu, Yue / Thomason, Kerrie S / de Mello, Aline Haas / Preble, Richard / Menachery, Vineet D / Casola, Antonella / Garofalo, Roberto P

bioRxiv : the preprint server for biology

2023

Abstract: RSV and SARS-CoV-2 are prone to co-infection with other respiratory viruses. In this study, we use ... However, SARS-CoV-2 infection followed by RSV results in enhanced SARS-CoV-2-induced disease while protecting ... RSV/SARS-CoV-2 co-infection to evaluate changes to clinical disease and viral replication in vivo ...

Abstract	RSV and SARS-CoV-2 are prone to co-infection with other respiratory viruses. In this study, we use RSV/SARS-CoV-2 co-infection to evaluate changes to clinical disease and viral replication in vivo. To consider the severity of RSV infection, effect of sequential infection, and the impact of infection timing, mice were co-infected with varying doses and timing. Compared with a single infection of RSV or SARS-CoV-2, the co-infection of RSV/SARS-CoV-2 and the primary infection of RSV followed by SARS-CoV-2 results in protection from SARS-CoV-2-induced clinical disease and reduces SARS-CoV-2 replication. Co-infection also augmented RSV replication at early timepoints with only the low dose. Additionally, the sequential infection of RSV followed by SARS-CoV-2 led to improved RSV clearance regardless of viral load. However, SARS-CoV-2 infection followed by RSV results in enhanced SARS-CoV-2-induced disease while protecting from RSV-induced disease. SARS-CoV-2/RSV sequential infection also reduced RSV replication in the lung tissue, regardless of viral load. Collectively, these data suggest that RSV and SARS-CoV-2 co-infection may afford protection from or enhancement of disease based on variation in infection timing, viral infection order, and/or viral dose. In the pediatric population, understanding these infection dynamics will be critical to treat patients and mitigate disease outcomes.
Language	English
Publishing date	2023-05-24
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.05.24.542043
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