Influenza A virus infection predisposes hosts to secondary infection with different Streptococcus pneumoniae serotypes with similar outcome but serotype-specific manifestation.
Open accessAbstract
Influenza A virus (IAV) and Streptococcus pneumoniae are major causes of respiratory tract infections, particularly during coinfection. The synergism between these two pathogens is characterized by a complex network of dysregulated immune responses, some of which last until recovery following IAV infection. Despite the high serotype diversity of S. pneumoniae and the serotype replacement observed since the introduction of conjugate vaccines, little is known about pneumococcal strain dependency in the enhanced susceptibility to severe secondary S. pneumoniae infection following IAV infection. Thus, we studied how preinfection with IAV alters host susceptibility to different S. pneumoniae strains with various degrees of invasiveness using a highly invasive serotype 4 strain, an invasive serotype 7F strain, and a carrier serotype 19F strain. A murine model of pneumococcal coinfection during the acute phase of IAV infection showed a significantly increased degree of pneumonia and mortality for all tested pneumococcal strains at otherwise sublethal doses. The incidence and kinetics of systemic dissemination, however, remained bacterial strain dependent. Furthermore, we observed strain-specific alterations in the pulmonary levels of alveolar macrophages, neutrophils, and inflammatory mediators ultimately affecting immunopathology. During the recovery phase following IAV infection, bacterial growth in the lungs and systemic dissemination were enhanced in a strain-dependent manner. Altogether, this study shows that acute IAV infection predisposes the host to lethal S. pneumoniae infection irrespective of the pneumococcal serotype, while the long-lasting synergism between IAV and S. pneumoniae is bacterial strain dependent. These results hold implications for developing tailored therapeutic treatment regimens for dual infections during future IAV outbreaks.
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In a mouse model, carrier strain serotype 19F caused pneumonia in 91% and bacteraemia in 0% in single infection; co-infection with influenza increased these to 100% and 33%, and mortality rose from 0% to 63%.
“In comparison, individual infection with a carrier strain (of lower invasive potential) of serotype 19F, caused pneumonia in 91% of cases and bacteraemia in 0%. When co-infecting with influenza and 19F these figures increased to 100 and 33%. Mortality rose from 0% during individual infection to 63% during co-infection (Sharma-Chawla et al., 2016).”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Sharma-Chawla et al., 2016
More virulent pneumococcal serotypes caused a greater burden of disease in both co-infected mice and mice infected with S. pneumoniae alone.
“More virulent pneumococcal serotypes caused a greater burden of disease in both the co-infected mice and those infected with S. pneumoniae alone.”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Sharma-Chawla et al., 2016
In a mouse model, more cases of pneumonia and bacteraemia were observed in mice infected with both influenza A and S. pneumoniae than in mice infected with these pathogens individually, for all S. pneumoniae serotypes tested.
“More cases of pneumonia and bacteraemia were observed in mice infected with both influenza A and S. pneumoniae than in mice infected with these pathogens individually. This was the case for all S. pneumoniae serotypes tested.”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Sharma-Chawla et al., 2016
In a mouse model, highly invasive pneumococcal serotype 4 caused pneumonia in 58% and bacteraemia in 21% in single infection; co-infection with influenza increased these to 100% and 90%, respectively, and mortality increased from 0% to 79%.
“The highly invasive pneumococcal serotype 4 caused pneumonia in 58% of mice and bacteraemia in 21% in a single infection model. When co-infecting with influenza these figures increased to 100 and 90% for pneumonia and bacteraemia, respectively. Mortality rates increased from 0% for individual infection to 79% during co-infection.”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Sharma-Chawla et al., 2016
Even after influenza is cleared, S. pneumoniae bacterial clearance is affected.
“Even after influenza is cleared, S. pneumoniae bacterial clearance is affected.”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Sharma-Chawla et al., 2016
The reduction in alveolar macrophages during S. pneumoniae and influenza co-infection likely hinders bacterial clearance, leading to increased bacterial load and prolonged inflammatory response increasing morbidity.
“This reduction is likely to hinder bacterial clearance, hence the increased bacterial load found during co-infection during this study, and results in prolonged inflammatory response increasing morbidity.”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Sharma-Chawla et al., 2016
S. pneumoniae and influenza co-infection results in a reduction in local alveolar macrophages due to increased death of these macrophages by apoptosis and necrosis.
“Additionally it has recently been shown that S. pneumoniae and influenza co-infection results in a reduction in the number of local alveolar macrophages, this due to increased death of these macrophages by apoptosis and necrosis (Sharma-Chawla et al., 2016).”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Sharma-Chawla et al., 2016
The Sharma-Chawla et al. study highlighted serotype-dependent differences in S. pneumoniae co-infection.
“This study has highlighted some serotype dependent differences”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Sharma-Chawla et al., 2016
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- van den Boogaard FE, van Gisbergen KP, Vernooy JH, Medema JP, Roelofs JJ, van Zoelen MA, Endeman H, Biesma DH, Boon L, van 't Veer C, de Vos AF, van der Poll T. 2016. Granzyme A impairs host defense during Streptococcus pneumoniae pneumonia. Am J Physiol Lung Cell Mol Physiol doi:10.1152/ajplung.00116.2016:ajplung 00116 02016. · DOI
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Secondary bacterial infections associated with influenza pandemics
Morris, D. E., Cleary, D. W., & Clarke, S. C. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01041 · Cited by 576 · see citing works
Laws, H.-J., Baumann, U., Bogdan, C., Burchard, G., Christopeit, M., Hecht, J., Heininger, U., Hilgendorf, I., Kern, W., Kling, K., et al. (2020) · Bundesgesundheitsblatt - Gesundheitsforschung - Gesundheitsschutz · doi:10.1007/s00103-020-03123-w · Cited by 88 · see citing works
- Authors
- Sharma-Chawla, N., Sender, V., Kershaw, O., Gruber, A. D., Volckmar, J., Henriques-Normark, B., Stegemann-Koniszewski, S., & Bruder, D.
- Affiliations
- Helmholtz Centre for Infection Research (DE)
- Karolinska Institutet (SE)
- Freie Universität Berlin (DE)
- Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden
- Immune Regulation Group, Helmholtz Centre for Infection Research, Braunschweig, Germany
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 2016-12
- Volume
- 84
- Issue
- 12
- Pages
- 3445-3457
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- PMC
- PMC5116722
- OpenAlex
- W2523421524
- Cited by
- 63
- References
- 55
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 4 · 2023: 5 · 2022: 10 · 2021: 6 · 2020: 11 · 2019: 7 · 2018: 7 · 2017: 6 · 2016: 1
- FWCI
- 6.56
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Infection and Immunity (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HZI (Helmholtz Centre for Infection Research) (submittedVersion, cc-by-nc-sa)
- Funders
- Deutsche Forschungsgemeinschaft (IRTG1273, SFB854)
- Knut och Alice Wallenbergs Stiftelse
- Helmholtz-Gemeinschaft (W2/W3-029)
- Stockholms Läns Landsting (ALF)
- Swedish Research Council
- Swedish Foundation for Strategic Research
- Topics
- Health Sciences › Medicine › Epidemiology › Pneumonia and Respiratory Infections
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
- Keywords
- influenza A virus, Streptococcus pneumoniae, secondary infection, serotype 4, serotype 7F, serotype 19F, systemic dissemination, alveolar macrophages, neutrophils, lung inflammation, immunopathology, respiratory infections, mouse model
- MeSH terms
- Animals, Female, Immunity, Innate, Orthomyxoviridae Infections, Influenza A virus, Pneumococcal Infections, Streptococcus pneumoniae, Viral Load, Mice, Coinfection, Serogroup
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