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Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza
Open accessAbstract
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.
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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.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results > MassTag PCR assays
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Discussion · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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 ).”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Abstract > Methods/Principal Findings
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § MassTag PCR assays · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Results of the logistic regression analysis were not significant for subjects with high age-associated risk (<6 or >55 years of age).”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results > MassTag PCR assays
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Abstract > Methods/Principal Findings
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § MassTag PCR assays · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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 .”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Abstract > Methods/Principal Findings
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § MassTag PCR assays · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“S. pneumoniae was present in 56.4% of severe cases versus 25% of mild cases;”
- Also stated in: § MassTag PCR assays · plain
“S. pneumoniae was detected in 56.4% of severe cases, but only 25.0% of mild cases;”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Abstract > Methods/Principal Findings
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § MassTag PCR assays · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Of the 45 subjects with one or more bacterial respiratory pathogens other than S. pneumoniae or H. influenzae in their NPS samples, 44 had mild disease (97.8%; p = 0.0004).”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results > MassTag PCR assays
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The presence of a risk-associated medical condition was associated with increased risk of severe disease (OR [95% CI], 15.31 [1.21, 193.49], p = 0.0358);”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results > MassTag PCR assays
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“At least one additional agent of potential pathogenic importance was identified in 152 samples (76%)”
- Also stated in: § MassTag PCR assays · plain
“MassTag PCR detected H1N1pdm and at least one additional potential respiratory pathogen in 152 of 199 samples (76.4%).”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Abstract > Methods/Principal Findings
Strength:plain· not yet calibratedn = 199Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes- Also stated in: § MassTag PCR assays · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The presence of RSV A, though relatively infrequent, was more common in severe (6 of 39 cases, 15.4%) than in mild disease (5 of 160 cases, 3.1%; p = 0.0085).”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results > MassTag PCR assays
Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes
- Probably not a substantial claim. 14
- It may state two separate claims as one. 7
- The quote only partly states this claim. 1
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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).”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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).”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results
Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results > MassTag PCR assays
Strength:plain· not yet calibratedn = 199Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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).”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results
Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“including Streptococcus pneumoniae (n = 62)”
- Also stated in: § MassTag PCR assays · plain
“Co-infecting agents included S. pneumoniae (n = 62);”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Abstract > Methods/Principal Findings
Strength:plain· not yet calibratedn = 199Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesThe quote only partly states this claim.
- Also stated in: § MassTag PCR assays · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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).”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Abstract > Background
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
- Also stated in: § Introduction · plain
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“after ensuring that relationships among included variables were low (nonsignificant contingency coefficients ranging from 0.001 to 0.255).”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results > MassTag PCR assays
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
In the paper
“Secondary bacterial infections have been implicated in morbidity and mortality in H1N1 influenza [3].”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Discussion
What the sources say
- Not checked yetcites [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
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
In the paper
“Analysis of lung tissue sections from fatal 1918 influenza case materials frequently revealed histopathologic findings consistent with acute bacterial pneumonia [3].”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Discussion
What the sources say
- Not checked yetcites [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
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results > MassTag PCR assays
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
- Also stated in: § Statistics · plain
In the paper
“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.”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Discussion
What the sources say
- Not checked yetcites [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
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“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].”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Discussion
What the sources say
- Not checked yetcites [5] R Perez-Padilla, 2009, Pneumonia and respiratory failure from swine-origin influenza A (H1N1) in Mexico., N Engl J Med source
Strength:plain· not yet calibratedn = 18Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“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].”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Results
What the sources say
- Not checked yetcites [7] 2009, CDC protocol of real-time RTPCR for influenza A (H1N1).
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
- Also stated in: § Subjects and Specimens · plain
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Both INEI and CU maintain approved Institutional Review Board (IRB) protocols for receipt and analysis of deidentified samples and their associated deidentified clinical data.”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Materials and Methods > Data Collection
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Materials and Methods > Subjects and Specimens
Strength:plain· not yet calibratedn = 1,769Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“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].”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Discussion
What the sources say
- Not checked yetcites [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
Strength:plain· not yet calibratedn = 1,918Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“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].”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Discussion
What the sources say
- Not checked yetcites [4] S Hackett, 2009, Clinical characteristics of paediatric H1N1 admissions in Birmingham, UK., Lancet source
Strength:plain· not yet calibratedn = 63Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“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.”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Introduction
What the sources say
- Not checked yetcites [1] C Fraser, 2009, Pandemic potential of a strain of influenza A (H1N1): early findings., Science source
Strength:hedged· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
- Also stated in: § Background · hedged
In the paper
“Madhi and colleagues demonstrated that vaccination against S. pneumoniae reduces the frequency of pneumonia associated with influenza A, RSV and parainfluenza viruses [10].”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Discussion
What the sources say
- Not checked yetcites [10] SA Madhi, 2004, A role for Streptococcus pneumoniae in virus-associated pneumonia., Nat Med source
Strength:boosted· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Materials and Methods > Data Collection
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“First, S. pneumoniae is important in the pathogenesis and prognosis of H1N1pdm-associated disease.”
§ Streptococcus pneumoniae Coinfection Is Correlated with the Severity of H1N1 Pandemic Influenza > Discussion
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
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.”
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?
In the citing paper
“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 citing paper
“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 the citing paper
“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]
In the citing paper
“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 citing paper
“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]
In the citing paper
“In Argentina, nasopharyngeal swab samples from 199 cases of confirmed H1N1 pandemic infection were tested for 33 additional microbial agents using MassTag PCR methods. At least one additional agent of potential pathogenic importance was detected in 152 samples, including S pneumoniae (41%); H influenzae (68·4%); S aureus (23%); and methicillin‐resistant S aureus (MRSA, 4%).”
From Bacterial and viral infections associated with influenza (2013) · cites this paper as [34]
In the citing paper
“In Argentina, 20 of 199 persons investigated with pandemic disease were co‐infected with another respiratory virus including RSV (A or B), rhinovirus and coronavirus. Seven of these cases were classed as having severe disease (hospitalisation or death with no other risk factors related to underlying disease) and 13, mild disease (ambulatory cases).”
From Bacterial and viral infections associated with influenza (2013) · cites this paper as [34]
In the citing paper
“Staphylococcus aureus is a Gram-positive cocci that has been found to complicate influenza infection; increasingly so in more recent years/pandemics (Hers et al., 1958; Palacios et al., 2009).”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Palacios et al., 2009
In the citing paper
“Although not the most common bacteria found, S. pneumoniae was the most strongly associated with severe disease (Palacios et al., 2009).”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Palacios et al., 2009
In the citing paper
“Palacios et al. (2009) examined nasopharyngeal swab samples from almost 200 cases of pandemic influenza. H. influenzae was found in 52%, S. pneumoniae was found in 31% and S. aureus in 18% of samples.”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Palacios et al., 2009
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Incorrect overall percentage for S. pneumoniae
MinorTable 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
“| S. pneumoniae | 22 (56.4)* | 40 (25.0) | 62 (35.5) |”
Citations
Cites
Influenza-Associated Hospitalizations in the United States
Thompson, W. W. (2004) · JAMA · doi:10.1001/jama.292.11.1333 · Cited by 2,213
Pandemic Potential of a Strain of Influenza A (H1N1): Early Findings
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Cited by
Sorted by citations
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Metadata
- 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)
- 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
- gold
- doi.org
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
A language model drew the claims from the paper on 2026-10-09, under version 3 of the claim definition (model deepseek-v4.1-flash, prompt extract-v3).
A second model labelled each claim on 2026-10-09 (model jev-1.13-20260917, definition revision gold-guideline-v0.2).
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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