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Cited by 275Influenza Virus Research StudiesPneumonia and Respiratory InfectionsRespiratory viral infections research

Streptococcus pneumoniae coinfection is correlated with the severity of H1N1 pandemic influenza

Open access
Palacios, Gustavo, Hornig, Mady, Cisterna, Daniel, Savji, Nazir, Bussetti, Ana Valeria, Kapoor, Vishal, Hui, Jeffrey, Tokarz, Rafal +3 more·2009·PLoS ONE
DOI 10.1371/journal.pone.0008540PMC PMC2795195
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Abstract

BACKGROUND: Initial reports in May 2009 of the novel influenza strain H1N1pdm estimated a case fatality rate (CFR) of 0.6%, similar to that of seasonal influenza. In July 2009, however, Argentina reported 3056 cases with 137 deaths, representing a CFR of 4.5%. Potential explanations for increased CFR included virus reassortment or genetic drift, or infection of a more vulnerable population. Virus genomic sequencing of 26 Argentinian samples representing both severe and mild disease indicated no evidence of reassortment, mutations associated with resistance to antiviral drugs, or genetic drift that might contribute to virulence. Furthermore, no evidence was found for increased frequency of risk factors for H1N1pdm disease. METHODS/PRINCIPAL FINDINGS: We examined nasopharyngeal swab samples (NPS) from 199 cases of H1N1pdm infection from Argentina with MassTag PCR, testing for 33 additional microbial agents. The study population consisted of 199 H1N1pdm-infected subjects sampled between 23 June and 4 July 2009. Thirty-nine had severe disease defined as death (n = 20) or hospitalization (n = 19); 160 had mild disease. At least one additional agent of potential pathogenic importance was identified in 152 samples (76%), including Streptococcus pneumoniae (n = 62); Haemophilus influenzae (n = 104); human respiratory syncytial virus A (n = 11) and B (n = 1); human rhinovirus A (n = 1) and B (n = 4); human coronaviruses 229E (n = 1) and OC43 (n = 2); Klebsiella pneumoniae (n = 2); Acinetobacter baumannii (n = 2); Serratia marcescens (n = 1); and Staphylococcus aureus (n = 35) and methicillin-resistant S. aureus (MRSA, n = 6). The presence of S. pneumoniae was strongly correlated with severe disease. S. pneumoniae was present in 56.4% of severe cases versus 25% of mild cases; more than one-third of H1N1pdm NPS with S. pneumoniae were from subjects with severe disease (22 of 62 S. pneumoniae-positive NPS, p = 0.0004). In subjects 6 to 55 years of age, the adjusted odds ratio (OR) of severe disease in the presence of S. pneumoniae was 125.5 (95% confidence interval [CI], 16.95, 928.72; p<0.0001). CONCLUSIONS/SIGNIFICANCE: The association of S. pneumoniae with morbidity and mortality is established in the current and previous influenza pandemics. However, this study is the first to demonstrate the prognostic significance of non-invasive antemortem diagnosis of S. pneumoniae infection and may provide insights into clinical management.

AI snapshot

Written from the paper’s full text.

TL;DR

In 199 Argentine H1N1pdm cases, *Streptococcus pneumoniae* coinfection was strongly associated with severe disease, especially in subjects aged 6–55 years (adjusted OR 125.5). The study suggests non-invasive antemortem detection of *S. pneumoniae* may have prognostic value for H1N1pdm severity.

Key findings

  • Among 199 H1N1pdm-positive nasopharyngeal swab samples, at least one additional potential pathogen was detected in 152 (76%); *S. pneumoniae* was found in 62 (35.5%).
  • *S. pneumoniae* was present in 56.4% of severe cases versus 25.0% of mild cases; 22 of 62 *S. pneumoniae*-positive samples were from severe cases (p = 0.0004). In subjects aged 6–55 years, the adjusted odds ratio for severe disease with *S. pneumoniae* was 125.5 (95% CI 16.95–928.72; p < 0.0001).
  • *H. influenzae* was common overall (104/199, 52.3%) but less frequent in severe disease (9/39, 23.1%) than mild disease (95/160, 59.4%; p < 0.0001). RSV A was more common in severe cases (6/39, 15.4%) than mild cases (5/160, 3.1%; p = 0.0085).
  • Of 45 subjects with bacterial respiratory pathogens other than *S. pneumoniae* or *H. influenzae*, 44 had mild disease (97.8%; p = 0.0004). Among 96 subjects receiving oseltamivir alone, 10 (10.4%) had severe disease, whereas 13 of 14 patients (92.9%) receiving antibiotics without antiviral medication had severe disease (p < 0.0001).

Methods

  • Nasopharyngeal swab samples from 199 H1N1pdm-infected subjects in Argentina, collected 23 June–4 July 2009; 39 had severe disease (death n = 20 or hospitalization n = 19) and 160 had mild disease.
  • H1N1pdm was confirmed by WHO-approved real-time PCR; samples were tested by MassTag PCR for 33 additional viral and bacterial respiratory pathogens.
  • Group comparisons used Mann-Whitney U and Fisher’s exact tests; multivariable logistic regression stratified by age risk category adjusted for RSV A, total number of agents detected, and presence of a medical risk factor.

Limitations

  • The paper states that information on passive tobacco smoke exposure, older siblings, and personal/familial atopic background was unavailable, and that underreporting of milder infections could not be excluded as an explanation for Argentina’s elevated case fatality rate.
  • Evident from the text: the observational design cannot establish causality, and severe and mild samples were randomly selected from different repositories (1769 severe cases vs. 1282 mild cases), which may introduce selection or confounding.
  • Evident from the text: missing data for age (181/199), sex (184/199), and antimicrobial use (120/199), plus the very wide adjusted OR confidence interval (16.95–928.72), suggest limited precision and possible sparse-data instability.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0008540

Cites

14 of 14 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 12 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The significance of the relationship between S. pneumoniae and severe disease was restricted to patients in the low risk age group (6-55 years).

    “The significance of the relationship between S. pneumoniae and severe disease was restricted to patients in the low risk age group (p<0.0001; Table 3 ).”
    • Also stated in: § Discussion · plain
      “The risk associated with S. pneumoniae is particularly prominent in 6-to-55 year-old individuals.”
    Quote in the paperSubstantial claim
  • Findingown data

    More than one-third of H1N1pdm NPS samples positive for S. pneumoniae were from subjects with severe disease (22 of 62, p = 0.0004).

    “more than one-third of H1N1pdm NPS with S. pneumoniae were from subjects with severe disease (22 of 62 S. pneumoniae-positive NPS, p = 0.0004).”
    • Also stated in: § MassTag PCR assays · plain
      “more than one-third of H1N1pdm NPS with S. pneumoniae were from subjects with severe disease (22 of 62 S. pneumoniae-positive NPS, p = 0.0004; Table 2 ).”
    Quote in the paperSubstantial claim
  • Findingown data

    Results of the logistic regression analysis were not significant for subjects with high age-associated risk (<6 or >55 years of age).

    “Results of the logistic regression analysis were not significant for subjects with high age-associated risk (<6 or >55 years of age).”
    Quote in the paperSubstantial claim
  • Findingown data

    The presence of S. pneumoniae in NPS was associated with severe H1N1pdm disease.

    “The presence of S. pneumoniae was strongly correlated with severe disease.”
    • Also stated in: § MassTag PCR assays · plain
      “The presence of S. pneumoniae was associated with severe disease.”
    Quote in the paperSubstantial claim
  • Findingown data

    In subjects 6 to 55 years of age, the adjusted odds ratio of severe disease in the presence of S. pneumoniae was 125.5 (95% CI 16.95, 928.72; p<0.0001).

    “In subjects 6 to 55 years of age, the adjusted odds ratio (OR) of severe disease in the presence of S. pneumoniae was 125.5 (95% confidence interval [CI], 16.95, 928.72; p<0.0001).”
    • Also stated in: § MassTag PCR assays · plain
      “In the low age risk category (subjects aged 6 to 55 years), the adjusted OR for the contribution of S. pneumoniae-positivity to severe disease outcomes in this logistic regression model was 125 (95% CI, 16.95, 928.72; p<0.0001, Table 4 .”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. 14
  • May combine two claims. 7
  • The quote only partly states this claim. 1

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    There was a trend toward a higher prevalence of severe disease in males (20 of 80, 25.0%) compared with females (15 of 104, 14.4%; p = 0.09).

    “There was a trend toward a higher prevalence of severe disease in males (20 of 80, or 25.0%) as compared with females (15 of 104, or 14.4%; p = 0.09).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Risk of severe disease was diminished in subjects who received only oseltamivir: 10 of 96 (10.4%) had severe disease, whereas 13 of 14 (92.9%) who received antibiotics without antiviral medication had severe disease (p<0.0001).

    “Risk of severe disease was diminished in subjects who received only oseltamivir. Of 96 subjects receiving oseltamavir alone, 10 (10.4%) had severe disease. In contrast, 13 of 14 patients (92.9%) who received antibiotics without antiviral medication had severe disease (p<0.0001).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    H. influenzae was detected in 104 of 199 H1N1pdm cases (52.3%) and was not increased among severe cases.

    “H. influenzae infection was frequent in the study population – 104 of all 199 cases (52.3%) harbored the agent – but was not increased among subjects with severe disease.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Five patients had medical conditions associated with increased risk of severe disease following influenza infection; four of these (80%) had severe disease and one had mild disease (p = 0.0056).

    “Five patients had medical conditions associated with increased risk of severe disease following influenza infection (asthma, malnutrition, pregnancy, obesity, immunosuppression; n = 1 each). Four of these patients (80%) had severe disease; 1 had mild disease (p = 0.0056).”
    Quote in the paperNot a substantial claim

  • The quote only partly states this claim.

    Findingown data

    S. pneumoniae was detected in 62 of 199 H1N1pdm NPS samples (35.5%).

    “including Streptococcus pneumoniae (n = 62)”
    • Also stated in: § MassTag PCR assays · plain
      “Co-infecting agents included S. pneumoniae (n = 62);”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Virus genomic sequencing of 26 Argentinian samples representing both severe and mild disease indicated no evidence of reassortment, mutations associated with resistance to antiviral drugs, or genetic drift that might contribute to virulence.

    “Virus genomic sequencing of 26 Argentinian samples representing both severe and mild disease indicated no evidence of reassortment, mutations associated with resistance to antiviral drugs, or genetic drift that might contribute to virulence.”
    • Also stated in: § Introduction · plain
      “Complete genome sequencing of 26 samples representing both severe and mild cases of disease from Argentina did not reveal evidence consistent with development of a more virulent phenotype (data not shown).”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductown data

    Relationships among included variables in the logistic regression model were low (nonsignificant contingency coefficients ranging from 0.001 to 0.255).

    “after ensuring that relationships among included variables were low (nonsignificant contingency coefficients ranging from 0.001 to 0.255).”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Secondary bacterial infections have been implicated in morbidity and mortality in H1N1 influenza.

    “Secondary bacterial infections have been implicated in morbidity and mortality in H1N1 influenza [3].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [3] DM Morens, 2008, Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness., J Infect Dis source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Analysis of lung tissue sections from fatal 1918 influenza case materials frequently revealed histopathologic findings consistent with acute bacterial pneumonia.

    “Analysis of lung tissue sections from fatal 1918 influenza case materials frequently revealed histopathologic findings consistent with acute bacterial pneumonia [3].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] DM Morens, 2008, Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness., J Infect Dis source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductown data

    The multivariable logistic regression model was adjusted for RSV A coinfection, total number of agents detected, and presence of a medical risk factor.

    “A model adjusting for the presence in NPS of RSV A, the total number of agents detected in NPS, and the presence of a medical risk factor implicated in severe H1N1 outcomes was derived”
    • Also stated in: § Statistics · plain
      “The model was adjusted for RSV A coinfection, the total number of bacterial or viral agents detected in NPS, and the presence of a medical risk factor.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Recent postmortem analyses indicated lower respiratory tract infection in 22 out of 77 lethal 2009 H1N1pdm cases in the United States (29%), with S. pneumoniae implicated in 10 of these cases.

    “recent postmortem analyses indicated lower respiratory tract infection in 22 out of 77 lethal 2009 H1N1pdm cases in the United States (29%) [9]; S. pneumoniae was implicated in 10 of these cases.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [9] 2009, Bacterial coinfections in lung tissue specimens from fatal cases of 2009 pandemic influenza A (H1N1) - United States, May-August 2009., MMWR Morb Mortal Wkly Rep

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    A case series of the first 18 H1N1pdm-infected patients hospitalized in Mexico City reported no evidence of coinfection with other common respiratory viruses.

    “A case series of the first 18 H1N1pdm-infected patients hospitalized in Mexico City reported no evidence of coinfection with other common respiratory viruses [5].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [5] R Perez-Padilla, 2009, Pneumonia and respiratory failure from swine-origin influenza A (H1N1) in Mexico., N Engl J Med source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductcitation

    The presence of H1N1pdm was confirmed for all samples with the WHO-approved Real Time PCR H1N1pdm assay prior to MassTag PCR studies.

    “Prior to initiating MassTag PCR studies, the presence of H1N1pdm was confirmed for all samples with the WHO-approved Real Time PCR H1N1pdm assay [7].”
    • Also stated in: § Subjects and Specimens · plain
      “following testing for H1N1pdm by the WHO-approved Real Time PCR test [7].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [7] 2009, CDC protocol of real-time RTPCR for influenza A (H1N1).

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    Both INEI and CU maintain approved Institutional Review Board (IRB) protocols for receipt and analysis of deidentified samples and their associated deidentified clinical data.

    “Both INEI and CU maintain approved Institutional Review Board (IRB) protocols for receipt and analysis of deidentified samples and their associated deidentified clinical data.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    Samples for this study were randomly selected from repository specimens collected during standard H1N1pdm surveillance in Argentina.

    “39 NPS specimens were selected randomly from a total of 1769 severe cases, and studied along with 160 NPS selected randomly from among 1282 H1N1pdm-infected ambulatory (mild) cases.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Agents recovered by postmortem cultures of lung samples from 96 fatal 1918 influenza pandemic cases included S. pneumoniae (23.2%), S. haemolyticus (18.0%), S. aureus (7.7%) and H. influenzae (4.7%).

    “Agents recovered by postmortem cultures of lung samples from 96 fatal 1918 influenza pandemic cases included S. pneumoniae (23.2%), S. haemolyticus (18.0%), S. aureus (7.7%) and H. influenzae (4.7%) [3].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] DM Morens, 2008, Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness., J Infect Dis source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In the first wave of pediatric H1N1pdm admissions in Birmingham, UK, only low rates of bacterial infection were found (10 out of 63 children, 15.8%).

    “In the first wave of pediatric H1N1pdm admissions in Birmingham, UK, only low rates of bacterial infection were found (10 out of 63 children, 15.8%) [4].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [4] S Hackett, 2009, Clinical characteristics of paediatric H1N1 admissions in Birmingham, UK., Lancet source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The CFR of the novel H1N1pdm strain was estimated to be 0.6% based on early data.

    “the CFR was estimated to be 0.6% [1].”
    • Also stated in: § Background · hedged
      “Initial reports in May 2009 of the novel influenza strain H1N1pdm estimated a case fatality rate (CFR) of 0.6%, similar to that of seasonal influenza.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [1] C Fraser, 2009, Pandemic potential of a strain of influenza A (H1N1): early findings., Science source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Vaccination against S. pneumoniae reduces the frequency of pneumonia associated with influenza A, RSV and parainfluenza viruses.

    “Madhi and colleagues demonstrated that vaccination against S. pneumoniae reduces the frequency of pneumonia associated with influenza A, RSV and parainfluenza viruses [10].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [10] SA Madhi, 2004, A role for Streptococcus pneumoniae in virus-associated pneumonia., Nat Med source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Information about other potential factors associated with risk of severe H1N1 disease, including passive tobacco smoke exposure, older siblings, or personal and/or familial atopic background, was unavailable.

    “Information about other potential factors associated with risk of severe H1N1 disease, including presence of passive tobacco smoke exposure, older siblings, or personal and/or familial atopic background, was unavailable.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    S. pneumoniae is important in the pathogenesis and prognosis of H1N1pdm-associated disease.

    “First, S. pneumoniae is important in the pathogenesis and prognosis of H1N1pdm-associated disease.”
    Quote in the paperSubstantial claim
21 of 21

  • The paper relies on this without support.

    Detection of S. pneumoniae in NPS indicates a clinically relevant infection rather than incidental colonization.

    “In our study of Argentinean victims of H1N1pdm, the presence of S. pneumoniae in NPS predicts severe disease outcome.”
    “First, S. pneumoniae is important in the pathogenesis and prognosis of H1N1pdm-associated disease.”

  • The paper relies on this without support.

    The association between S. pneumoniae and severe H1N1pdm disease is not confounded by antimicrobial treatment.

    “Risk of severe disease was diminished in subjects who received only oseltamivir. Of 96 subjects receiving oseltamavir alone, 10 (10.4%) had severe disease. In contrast, 13 of 14 patients (92.9%) who received antibiotics without antiviral medication had severe disease (p<0.0001).”

  • The paper relies on this without support.

    The 90.97% prediction accuracy of the logistic regression model is not due to overfitting.

    “Indeed, severity of disease in this low risk group can be predicted with 90.97% accuracy via a multivariable logistic regression model that considers the presence of S. pneumoniae together with viruses other than influenza and a risk-associated medical condition.”
3 of 3

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Bacterial co-infection was detected in ~30% of cases in the 2009 H1N1 pandemic, with high mortality rates despite administration of appropriate antibiotics.

    “Bacterial co-infection was also detected in ~30% of cases in the 2009 H1N1 pandemic, with high mortality rates despite administration of appropriate antibiotics”

    From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [16]

  • In the Argentina study, the presence of S pneumoniae was strongly correlated with severe disease and was present in 56·4% of severe cases versus 25% of mild cases (P = 0·0004).

    “The presence of S pneumoniae was strongly correlated with severe disease and was present in 56·4% of severe cases versus 25% of mild cases (P = 0·0004).”

    From Bacterial and viral infections associated with influenza (2013) · cites this paper as [34]

  • In subjects 6-55 years of age, the adjusted odds ratio of severe disease in the presence of S pneumoniae was highly significant (P = 0·0001).

    “In subjects 6–55 years of age, the adjusted odds ratio (OR) of severe disease in the presence of S pneumoniae was highly significant (P = 0·0001).”

    From Bacterial and viral infections associated with influenza (2013) · cites this paper as [34]

  • The Argentina study demonstrated that the presence of S pneumoniae in nasopharyngeal swab samples could predict severe disease outcome, with risk more acute in persons aged 6-55 years.

    “This study demonstrated that the presence of S pneumoniae in nasopharyngeal swab samples could predict severe disease outcome, the risk being more acute in persons aged between 6 and 55 years.”

    From Bacterial and viral infections associated with influenza (2013) · cites this paper as [34]

  • In the low-risk age group, severity of disease could be predicted with 90·97% accuracy via a multivariable logistic regression model.

    “In this low‐risk age group, severity of disease could be predicted with 90·97% accuracy via a multivariable logistic regression model.”

    From Bacterial and viral infections associated with influenza (2013) · cites this paper as [34]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

  • Incorrect overall percentage for S. pneumoniae

    Minor

    Table 2 reports 62 S. pneumoniae-positive subjects among 199 subjects as 35.5%. The overall percentage is 31.2%; 35.5% instead matches the proportion of S. pneumoniae-positive subjects who had severe disease (22 of 62).

    Reported 35.5 · recomputed 31.155779

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Authors
Palacios, G., Hornig, M., Cisterna, D., Savji, N., Bussetti, A. V., Kapoor, V., Hui, J., Tokarz, R., Briese, T., Baumeister, E., & Lipkin, W. I.
Affiliations
  • Columbia University (US)
  • Administración Nacional de Laboratorios e Institutos de Salud (AR)
Corresponding author
  • Palacios, Gustavo
  • Lipkin, W. Ian
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2009-12-31
Volume
4
Issue
12
Pages
e8540
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0008540
PMC
PMC2795195
OpenAlex
W2098792130
Semantic Scholar
73eb67835207270107c1e76b4675a92b3b58a575
Cited by
275
References
14
Citations by year
2026: 2 · 2025: 4 · 2024: 5 · 2023: 9 · 2022: 14 · 2021: 16 · 2020: 16 · 2019: 9 · 2018: 12 · 2017: 11 · 2016: 10 · 2015: 19 · 2014: 17 · 2013: 37 · 2012: 32
FWCI
21.13
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by)
  • Americanae (AECID Library) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Greater South Information System
  • Columbia Academic Commons (Columbia University)
Funders
  • U.S. Department of Defense
  • National Institutes of Health (n01ai30027-9-0-2, AI57158)
  • National Institute of Allergy and Infectious Diseases (U54 AI 57158, R01AI051292, R01 AI30027, AI051292, U54AI057158, N01 AI030027)
Topics
  • Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
  • Health Sciences › Medicine › Epidemiology › Pneumonia and Respiratory Infections
  • Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
Keywords
Streptococcus pneumoniae, co-infection, H1N1 pandemic influenza, 2009 H1N1 influenza, disease severity, case fatality rate, Haemophilus influenzae, Staphylococcus aureus, methicillin-resistant Staphylococcus aureus, respiratory pathogens, Argentina, viral coinfection, bacterial co-infection
MeSH terms
Adolescent, Adult, Argentina, Child, Disease Outbreaks, Female, Humans, Influenza, Human, Male, Middle Aged, Pneumococcal Infections, Risk Factors, Bodily Secretions, Streptococcus pneumoniae, Polymerase Chain Reaction, Influenza A Virus, H1N1 Subtype, Young Adult

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