Detection of influenza virus and Streptococcus pneumoniae in air sampled from co-infected ferrets and analysis of their influence on pathogen stability
ABSTRACT Secondary infection with Streptococcus pneumoniae has contributed significantly to morbidity and mortality during multiple influenza virus pandemics and remains a common threat today. During a concurrent infection, both pathogens can influence the transmission of each other, but the mechani...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-08-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msphere.00039-23 |
| _version_ | 1797730249555836928 |
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| author | Andrea J. French Nicole C. Rockey Valerie Le Sage Karina Mueller Brown Meredith J. Shephard Sheila Frizzell Mike M. Myerburg N. Luisa Hiller Seema S. Lakdawala |
| author_facet | Andrea J. French Nicole C. Rockey Valerie Le Sage Karina Mueller Brown Meredith J. Shephard Sheila Frizzell Mike M. Myerburg N. Luisa Hiller Seema S. Lakdawala |
| author_sort | Andrea J. French |
| collection | DOAJ |
| description | ABSTRACT Secondary infection with Streptococcus pneumoniae has contributed significantly to morbidity and mortality during multiple influenza virus pandemics and remains a common threat today. During a concurrent infection, both pathogens can influence the transmission of each other, but the mechanisms behind this are unclear. In this study, condensation air sampling and cyclone bioaerosol sampling were performed using ferrets first infected with the 2009 H1N1 pandemic influenza virus (H1N1pdm09) and secondarily infected with S. pneumoniae strain D39 (Spn). We detected viable pathogens and microbial nucleic acid in expelled aerosols from co-infected ferrets, suggesting that these microbes could be present in the same respiratory expulsions. To assess whether microbial communities impact pathogen stability within an expelled droplet, we performed experiments measuring viral and bacterial persistence in 1 µL droplets. We observed that H1N1pdm09 stability was unchanged in the presence of Spn. Further, Spn stability was moderately increased in the presence of H1N1pdm09, although the degree of stabilization differed between airway surface liquid collected from individual patient cultures. These findings are the first to collect both pathogens from the air and in doing so, they provide insight into the interplay between these pathogens and their hosts. IMPORTANCE The impact of microbial communities on transmission fitness and environmental persistence is under-studied. Environmental stability of microbes is crucial to identifying transmission risks and mitigation strategies, such as removal of contaminated aerosols and decontamination of surfaces. Co-infection with S. pneumoniae is very common during influenza virus infection, but little work has been done to understand whether S. pneumoniae alters stability of influenza virus, or vice versa, in a relevant system. Here, we demonstrate that influenza virus and S. pneumoniae are expelled by co-infected hosts. Our stability assays did not reveal any impact of S. pneumoniae on influenza virus stability, but did show a trend towards increased stability of S. pneumoniae in the presence of influenza viruses. Future work characterizing environmental persistence of viruses and bacteria should include microbially complex solutions to better mimic physiologically relevant conditions. |
| first_indexed | 2024-03-12T11:42:29Z |
| format | Article |
| id | doaj.art-50e982b0e4c84aca8587882e3dfc8ed4 |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-03-12T11:42:29Z |
| publishDate | 2023-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-50e982b0e4c84aca8587882e3dfc8ed42023-08-31T14:26:41ZengAmerican Society for MicrobiologymSphere2379-50422023-08-018410.1128/msphere.00039-23Detection of influenza virus and Streptococcus pneumoniae in air sampled from co-infected ferrets and analysis of their influence on pathogen stabilityAndrea J. French0Nicole C. Rockey1Valerie Le Sage2Karina Mueller Brown3Meredith J. Shephard4Sheila Frizzell5Mike M. Myerburg6N. Luisa Hiller7Seema S. Lakdawala8Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine , Pittsburgh, Pennsylvania, USADepartment of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine , Pittsburgh, Pennsylvania, USADepartment of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine , Pittsburgh, Pennsylvania, USADepartment of Biological Sciences, Carnegie Mellon University , Pittsburgh, Pennsylvania, USADepartment of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine , Pittsburgh, Pennsylvania, USADivision of Pulmonary, Allergy, and Critical Care Medicine, University of Pittsburgh , Pittsburgh, Pennsylvania, USADivision of Pulmonary, Allergy, and Critical Care Medicine, University of Pittsburgh , Pittsburgh, Pennsylvania, USADepartment of Biological Sciences, Carnegie Mellon University , Pittsburgh, Pennsylvania, USADepartment of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine , Pittsburgh, Pennsylvania, USAABSTRACT Secondary infection with Streptococcus pneumoniae has contributed significantly to morbidity and mortality during multiple influenza virus pandemics and remains a common threat today. During a concurrent infection, both pathogens can influence the transmission of each other, but the mechanisms behind this are unclear. In this study, condensation air sampling and cyclone bioaerosol sampling were performed using ferrets first infected with the 2009 H1N1 pandemic influenza virus (H1N1pdm09) and secondarily infected with S. pneumoniae strain D39 (Spn). We detected viable pathogens and microbial nucleic acid in expelled aerosols from co-infected ferrets, suggesting that these microbes could be present in the same respiratory expulsions. To assess whether microbial communities impact pathogen stability within an expelled droplet, we performed experiments measuring viral and bacterial persistence in 1 µL droplets. We observed that H1N1pdm09 stability was unchanged in the presence of Spn. Further, Spn stability was moderately increased in the presence of H1N1pdm09, although the degree of stabilization differed between airway surface liquid collected from individual patient cultures. These findings are the first to collect both pathogens from the air and in doing so, they provide insight into the interplay between these pathogens and their hosts. IMPORTANCE The impact of microbial communities on transmission fitness and environmental persistence is under-studied. Environmental stability of microbes is crucial to identifying transmission risks and mitigation strategies, such as removal of contaminated aerosols and decontamination of surfaces. Co-infection with S. pneumoniae is very common during influenza virus infection, but little work has been done to understand whether S. pneumoniae alters stability of influenza virus, or vice versa, in a relevant system. Here, we demonstrate that influenza virus and S. pneumoniae are expelled by co-infected hosts. Our stability assays did not reveal any impact of S. pneumoniae on influenza virus stability, but did show a trend towards increased stability of S. pneumoniae in the presence of influenza viruses. Future work characterizing environmental persistence of viruses and bacteria should include microbially complex solutions to better mimic physiologically relevant conditions.https://journals.asm.org/doi/10.1128/msphere.00039-23influenzaStreptococcus pneumoniaeaerosolsstabilitysurvivalpersistence |
| spellingShingle | Andrea J. French Nicole C. Rockey Valerie Le Sage Karina Mueller Brown Meredith J. Shephard Sheila Frizzell Mike M. Myerburg N. Luisa Hiller Seema S. Lakdawala Detection of influenza virus and Streptococcus pneumoniae in air sampled from co-infected ferrets and analysis of their influence on pathogen stability mSphere influenza Streptococcus pneumoniae aerosols stability survival persistence |
| title | Detection of influenza virus and Streptococcus pneumoniae in air sampled from co-infected ferrets and analysis of their influence on pathogen stability |
| title_full | Detection of influenza virus and Streptococcus pneumoniae in air sampled from co-infected ferrets and analysis of their influence on pathogen stability |
| title_fullStr | Detection of influenza virus and Streptococcus pneumoniae in air sampled from co-infected ferrets and analysis of their influence on pathogen stability |
| title_full_unstemmed | Detection of influenza virus and Streptococcus pneumoniae in air sampled from co-infected ferrets and analysis of their influence on pathogen stability |
| title_short | Detection of influenza virus and Streptococcus pneumoniae in air sampled from co-infected ferrets and analysis of their influence on pathogen stability |
| title_sort | detection of influenza virus and streptococcus pneumoniae in air sampled from co infected ferrets and analysis of their influence on pathogen stability |
| topic | influenza Streptococcus pneumoniae aerosols stability survival persistence |
| url | https://journals.asm.org/doi/10.1128/msphere.00039-23 |
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