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Cited by 250Influenza Virus Research StudiesPneumonia and Respiratory InfectionsRespiratory viral infections research

Bacterial and viral infections associated with influenza

Open access
Joseph, Carol, Togawa, Yu, Shindo, Nahoko·2013·Influenza and Other Respiratory Viruses
DOI 10.1111/irv.12089PMC PMC5909385
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Abstract

Influenza‐associated bacterial and viral infections are responsible for high levels of morbidity and death during pandemic and seasonal influenza episodes. A review was undertaken to assess and evaluate the incidence, epidemiology, aetiology, clinical importance and impact of bacterial and viral co‐infection and secondary infection associated with influenza. A review was carried out of published articles covering bacterial and viral infections associated with pandemic and seasonal influenza between 1918 and 2009 (and published through D ecember 2011) to include both pulmonary and extra‐pulmonary infections. While pneumococcal infection remains the predominant cause of bacterial pneumonia, the review highlights the importance of other co‐ and secondary bacterial and viral infections associated with influenza, and the emergence of newly identified dual infections associated with the 2009 H 1 N 1 pandemic strain. Severe influenza‐associated pneumonia is often bacterial and will necessitate antibiotic treatment. In addition to the well‐known bacterial causes, less common bacteria such as L egionella pneumophila may also be associated with influenza when new influenza strains emerge. This review should provide clinicians with an overview of the range of bacterial and viral co‐ or secondary infections that could present with influenza illness.

AI snapshot

Written from the paper’s full text.

TL;DR

This narrative review summarizes bacterial and viral co-infections and secondary infections associated with pandemic and seasonal influenza from 1918 through 2009. It concludes that severe influenza-associated pneumonia is often bacterial, with *Streptococcus pneumoniae* remaining the predominant pathogen, followed by *Staphylococcus aureus* and *Haemophilus influenzae*, and that prevention and treatment must address both influenza and bacterial complications.

Key findings

  • Across pandemics, bacterial co/secondary infection was common and often fatal: in 37 large US army camps in 1918, secondary bacterial infection occurred in approximately 17% of influenza cases, of which approximately 35% were fatal; US military mean influenza attack rate was 23%, pneumonia developed in 16% of influenza cases, and 34% of pneumonia cases were fatal.
  • In the 1957 H2N2 pandemic, a Dutch study of 158 deaths recovered *S aureus* and pneumococci from 59% and 15% of lung cultures, respectively; a British study of 140 hospitalized pneumonia cases isolated *S aureus* from 27%, pneumococci from 15%, and *H influenzae* from 4%, with mortality 47% in the staphylococcal group versus 16% in the non-staphylococcal group.
  • In the 2009 H1N1 pandemic, a New York City study of the first 47 deaths found invasive bacterial co-infection in 13 (28%), most commonly *S pneumoniae* in 8 (17%) and *S pyogenes* in 3 (6%); a US multi-centre review of 77 deaths found concurrent bacterial infection in 22 (29%), including 10 caused by *S pneumoniae*.
  • In Argentina, among 199 confirmed H1N1 cases tested for 33 additional microbial agents, at least one additional potential pathogen was detected in 152 samples, including *S pneumoniae* (41%), *H influenzae* (68.4%), *S aureus* (23%), and MRSA (4%); *S pneumoniae* was present in 56.4% of severe cases versus 25% of mild cases (P = 0.0004).

Methods

  • Narrative review of published articles on bacterial and viral infections associated with pandemic and seasonal influenza between 1918 and 2009, with articles published through December 2011, covering pulmonary and extra-pulmonary infections.
  • Searched PubMed/National Library of Medicine using terms including “influenza” and “secondary infection,” “influenza” and “pneumonia,” and “influenza” and “co-infection,” plus reference lists of identified articles.
  • Included human studies published in English from 1918 to end of 2011 in which pathogens were identified; abstracts and titles were reviewed and relevant studies selected.

Limitations

  • The paper states that literature on viral co-infections during pandemic periods is sparse compared with bacterial infections, and that there are no reports documenting solely viral co-infections during the 1957 and 1968 pandemics.
  • The paper notes that bacterial co-infections associated with the 2009 H1N1 pandemic have not been well described because of lack of data.
  • Evident from the text: this is a narrative review without a described formal quality appraisal or meta-analysis, and the search was limited to English-language human studies published through 2011, with many findings drawn from heterogeneous surveillance, autopsy, case-report, and observational data.

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

Integrity signals

Registry

Crossref · 10.1111/irv.12089

Cites

81 of 81 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 122 cited sources checked · 0 supported · 0 flagged

  • Findingnone given

    Newly identified dual infections were associated with the 2009 H1N1 pandemic strain.

    “the emergence of newly identified dual infections associated with the 2009 H1N1 pandemic strain”
    Quote in the paperSubstantial claim
  • Findingcitation

    Influenza A is the dominant strain associated with co/secondary bacterial infection.

    “Influenza A is the dominant strain associated with co/secondary bacterial infection”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [15] Peltola VT, Murti KG, McCullers JA. Influenza virus neuraminidase contributes to secondary bacterial pneumonia. J Infect Dis 2005; 192: 249– 257. 15962219 PMC2715995 source

      Not checked in the free run.

  • Findingcitation

    Recent re-analyses of post-mortem lung cultures from 1918 showed evidence of bacterial infection in >90% of the specimens.

    “Recent re‐analyses of post‐mortem lung cultures from 1918 showed evidence of bacterial infection in >90% of the specimens.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [18] Morens DM, Taubenberger JK, Fauci AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 2008; 198: 962– 970. 18710327 PMC2599911 source

      Not checked in the free run.

    • cites [20] Chien YW, Klugman KP, Morens D. Bacterial pathogens and death during the 1918 influenza pandemic. N Engl J Med 2009; 361: 2582– 2583. 20032332 source

      Not checked in the free run.

  • Findingcitation

    Influenza B can also cause severe secondary bacterial infection during seasonal influenza episodes, especially within younger age groups.

    “Influenza B, although generally regarded as having less impact on morbidity and mortality in healthy persons can also cause severe secondary bacterial infection during seasonal influenza episodes, especially within younger age groups.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [5] Finelli L, Fiore A, Dhara R et al Influenza‐associated pediatric mortality in the United States: increase of staphylococcus aureus coinfection. Pediatrics 2008; 122: 805– 811. 18829805 source

      Not checked in the free run.

    • cites [16] Aebi T, Weisser M, Bucher E, Hirsch HH, Marsch S, Siegemund M. Co‐infection of Influenza B and Streptococci causing severe pneumonia and septic shock in healthy women. BMC Infect Dis 2010; 10: 308. 20979628 PMC2988048 source

      Not checked in the free run.

    • cites [17] Scaber J, Saeed S, Ihekweazu C, Efstratiou A, McCarthy N, O'Moore E. Group A streptococcal infections during the seasonal influenza outbreak 2010/11 in South East England. Euro Surveill 2011; 16(5): pii=19780. 21315058 source

      Not checked in the free run.

  • Findingcitation

    Morbidity and mortality are greater in cases of influenza-associated bacterial infection compared with bacterial pneumonia without influenza infection.

    “Morbidity and mortality are recognised to be greater in cases of influenza‐associated bacterial infection compared with bacterial pneumonia without influenza infection”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] Seki M, Kosai K, Yanagihara K et al Disease severity in patients with simultaneous influenza and bacterial pneumonia. Intern Med 2007; 46: 953– 958. 17603232 source

      Not checked in the free run.

  • Classified as probably not a substantial claim. 8
  • May combine two claims. 41

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Findingnone given

    Pneumococcal infection remains the predominant cause of bacterial pneumonia.

    “While pneumococcal infection remains the predominant cause of bacterial pneumonia, the review highlights the importance of other co‐ and secondary bacterial and viral infections associated with influenza”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingcitation

    In the US military, the mean influenza attack rate during the 1918/1919 pandemic was 23%, the mean percentage of influenza cases that developed pneumonias was 16%, and the mean percentage of pneumonia cases that were fatal was 34%.

    “Overall, it has been estimated that in the US military, the mean influenza attack rate during the course of the 1918/1919 pandemic was 23%, the mean percentage of influenza cases that developed pneumonias was 16% and the mean percentage of pneumonia cases that were fatal was 34%.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [4] Brundage JF. Interactions between influenza and bacterial respiratory pathogens: implications for pandemic preparedness. Lancet Infect Dis 2006; 6: 303– 312. 16631551 PMC7106411 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Over a period of 2 months in 1918 at 37 large American army camps, secondary bacterial infection occurred in approximately 17% of those diagnosed with influenza, of which approximately 35% were fatal.

    “Over a period of 2 months in 1918 at 37 large American army camps, secondary bacterial infection occurred in approximately 17% of those diagnosed with influenza of which approximately 35% were fatal.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [4] Brundage JF. Interactions between influenza and bacterial respiratory pathogens: implications for pandemic preparedness. Lancet Infect Dis 2006; 6: 303– 312. 16631551 PMC7106411 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    In American civilian populations, attack rates and deaths were similar among younger adults and overall were approximately 28% for influenza with 30% of associated pneumonias being fatal.

    “In American civilian populations, attack rates and deaths were similar among younger adults and overall were approximately 28% for influenza with 30% of associated pneumonias being fatal.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [21] Frost WH. The epidemiology of influenza. JAMA 1919; 73: 313– 318.

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    The three influenza pandemics of the 20th century (1918 H1N1, 1957 H2N2 and 1968 H3N2) are all associated with secondary bacterial pneumonia.

    “The three influenza pandemics of the 20th century (1918 H1N1, 1957 H2N2 and 1968 H3N2) are all associated with secondary bacterial pneumonia.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [18] Morens DM, Taubenberger JK, Fauci AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 2008; 198: 962– 970. 18710327 PMC2599911 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Excess respiratory deaths were recorded in the second wave of the 1969/70 pandemic and increased by approximately 55%, and circulatory system deaths by 4%.

    “However, excess respiratory deaths were recorded in the second wave of the pandemic in 1969/70 and increased by approximately 55% and circulatory system deaths by 4%.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [29] Tillett HE, Smith JW, Gooch CD. Excess deaths attributable to influenza in England and Wales: age at death and certified cause. Int J Epidemiol 1983; 12: 344– 352. 6629624 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Children had the highest rates of clinical influenza infection, whereas young adults had the highest influenza pneumonia rates and associated fatality rates.

    “Children had the highest rates of clinical influenza infection, whereas young adults had the highest influenza pneumonia rates and associated fatality rates.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [20] Chien YW, Klugman KP, Morens D. Bacterial pathogens and death during the 1918 influenza pandemic. N Engl J Med 2009; 361: 2582– 2583. 20032332 source

      Not checked in the free run.

    • cites [22] Frost WH. Statistics of influenza morbidity with special reference to certain factors in case incidence and case‐fatality. Public Health Rep. 1920; 35: 584– 597. [cited 2008 May 30]. Available from http://www.pubmedcentral.nih.gov/picrender.fcgi?artid=1996797&blobtype=pdf.

      Not checked in the free run.

    • cites [23] Britten RH. The incidence of epidemic influenza, 1918–19. Public Health Rep 1932; 47: 303– 339. [cited 2008 May 30]. Available from http://www.pubmedcentral.nih.gov/picrender.fcgi?artid=1996206&blobtype=pdf.19315333

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    In a British study of 140 hospitalised cases of pneumonia in 1957, S aureus was isolated from 27%, pneumococci from 15%, and H influenzae from 4%.

    “A British study of 140 hospitalised cases of pneumonia over a two‐month period in 1957, a high proportion of whom also had evidence of confirmed influenza A infection, showed that S aureus was isolated from 27% of the cases and pneumococci and H influenzae from 15% and 4%, respectively.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [26] Robertson L, Caley JP, Moore J. Importance of staphylococcus aureus in pneumonia in the 1957 epidemic of influenza A. Lancet 1958; 2: 233– 236. 13564806 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    In a study of 68 autopsy reports from 457 pandemic influenza deaths in the UK, 28 (41%) reported bacterial secondary infection as the significant complication; pneumococcus was the most common agent identified (25%).

    “In a study of 68 autopsy reports from a total of 457 pandemic influenza deaths in the UK, 28 (41%) reported that bacterial secondary infection was the significant complication; pneumococcus was the most common agent identified (25%).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [33] Lucas S. Predictive clinicopathological features derived from systematic autopsy examination of patients who died with A/H1N1 influenza infection in the UK 2009–10 pandemic. Health Technol Assess 2010; 14: 83– 114. 21208548

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    In that New York City study, S pneumoniae was most commonly identified [8 patients (17%)], followed by S pyogenes [3 patients (6%)].

    “S pneumoniae was most commonly identified [8 patients (17%)], followed by S pyogenes [3 patients (6%)].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [13] Lee EH, Wu C, Lee EU et al for the New York City Department of Health and Mental Hygiene 2009 H1N1 Influenza Investigation Team. Fatalities associated with the 2009 H1N1 influenza a virus in New York City. Clin Infect Dis 2010; 50: 1498– 1504. 20420514 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    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).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [34] Palacios G, Hornig M, Cisterna D et al Streptococcus pneumoniae coinfection is correlated with the severity of h1n1 pandemic influenza. PLoS ONE 4: e8540. 20046873 PMC2795195 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    In the 1969/70 second wave, deaths in the elderly increased by 10%, in those aged 40-60 years by 8%, and in younger adults by 4%.

    “Deaths in the elderly increased by 10%, in those aged 40–60 years by 8% and in younger adults by 4%.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [29] Tillett HE, Smith JW, Gooch CD. Excess deaths attributable to influenza in England and Wales: age at death and certified cause. Int J Epidemiol 1983; 12: 344– 352. 6629624 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    In an analysis of 631 patients admitted to hospital in the UK during the 2009 pandemic with confirmed pandemic influenza, 102 cases had radiological evidence of pneumonia and mortality in cases with radiographic pneumonia was significantly higher than in cases without (P = 0·0008).

    “An analysis of 631 patients admitted to hospital over the five‐month pandemic period in 2009 in the UK with confirmed pandemic influenza infection reported that 102 cases had radiological evidence of pneumonia and that mortality in cases with radiographic pneumonia was significantly higher than in cases without (P = 0·0008).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [32] Nguyen‐Van‐Tam JS, Openshaw PJ, Hashim A et al Risk factors for hospitalisation and poor outcome with pandemic A/H1N1 influenza: United Kingdom first wave (May‐September 2009). Thorax 2010; 65: 645– 651. 20627925 PMC2921287

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    In that UK analysis, four cases of pneumonia (4%) had positive bacteriological findings, three of whom died - two children with MRSA and one adult with S pneumoniae in sputum.

    “Four cases of pneumonia (4%) had positive bacteriological findings, three of whom died – two children with methicillin‐resistant Staphylococcus aureus (MRSA) and one adult with S pneumoniae in sputum.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [32] Nguyen‐Van‐Tam JS, Openshaw PJ, Hashim A et al Risk factors for hospitalisation and poor outcome with pandemic A/H1N1 influenza: United Kingdom first wave (May‐September 2009). Thorax 2010; 65: 645– 651. 20627925 PMC2921287

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    In Argentina, among 199 cases of confirmed H1N1 pandemic infection, 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 MRSA (4%).

    “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%).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [34] Palacios G, Hornig M, Cisterna D et al Streptococcus pneumoniae coinfection is correlated with the severity of h1n1 pandemic influenza. PLoS ONE 4: e8540. 20046873 PMC2795195 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    In the United States, those aged 5-19 years experienced the largest relative increase in pneumococcal hospitalisations during the 2009 pandemic influenza period compared with seasonal baseline estimates, and this mirrored temporal and geographical influenza activity.

    “In the United States, those aged 5–19 years experienced overall the largest relative increase in pneumococcal hospitalisations during the 2009 pandemic influenza period compared with seasonal baseline estimates for this age group and mirrored both temporal and geographical influenza activity across the country.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [35] Weinberger DM, Simonson L, Jordan R, Steiner C, Miller M, Viboud C. Impact of the 2009 influenza pandemic on pneumococcal pneumonia hospitalizations in the United States. J Infect Dis 2012; 205: 458– 465. 22158564 PMC3276240

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Of 128 patients with pneumonia during the 1968 pandemic influenza period, 26% were proven staphylococcal pneumonia cases and a high correlation between pneumonia and influenza infection was documented.

    “Of 128 patients with pneumonia during the pandemic influenza period, 26% were proven staphylococcal pneumonia cases and a high correlation between pneumonia and influenza infection was documented.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [27] Schwarzmann SW, Adler JL, Sullivan RJ, Marine WM. Bacterial pneumonia during the Hong Kong influenza epidemic of 1968–1969. Arch Intern Med 1971; 127: 1037– 1041. 5578560

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Death rates in the 2009 H1N1 pandemic, although low, were more prevalent in younger age groups than the elderly.

    “Death rates although low, were more prevalent in younger age groups than the elderly”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingcitation

    Different pneumococcal strains may increase the duration of pneumococcal carriage and enhance the bacterial pneumonia.

    “Different strains may increase the duration of pneumococcal carriage and enhance the bacterial pneumonia.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [10] McCullers JA, McCauley JL, Browell S, Iverson AR, Boyd KL, Normark BH. Influenza enhances susceptibility to natural acquisition of and disease due to Streptococcus pneumoniae in ferrets. J Infect Dis 2010; 202: 1287– 1295. 20822454 PMC3249639 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    A US study of 173 cases of pandemic H1N1 found co-infection with other viruses in 20 cases (11·6%), rhinovirus being the most common agent.

    “A US study of 173 cases of pandemic H1N1 found co‐infection with other viruses in 20 cases (11·6%), rhinovirus being the most common agent.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [44] Esper F. Rate and Influence of Respiratory Virus Coinfection on Pandemic (H1N1) Influenza Disease. Infectious Diseases Society of America 48th annual meeting, Vancouver. Oral abstract session, 23 October 2010.

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    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 were severe and 13 mild.

    “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).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [34] Palacios G, Hornig M, Cisterna D et al Streptococcus pneumoniae coinfection is correlated with the severity of h1n1 pandemic influenza. PLoS ONE 4: e8540. 20046873 PMC2795195 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    A significant fall in influenza-associated pneumonia hospitalisations was observed among vaccinated children and unvaccinated adults; the vaccine acted to prevent the secondary pneumococcal pneumonia that followed influenza infection.

    “A significant fall in influenza‐associated pneumonia hospitalisations was observed among vaccinated children and unvaccinated adults; the vaccine acted to prevent the secondary pneumococcal pneumonia that followed influenza infection.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [51] Simonson L, Taylor RJ, Young‐Xu Y, Haber M, May L, Klugman KP. Impact of pneumococcal conjugate vaccination of infants on pneumonia and influenza hospitalization and mortality in all age groups in the United States. mBio 2011; 2(1): e00309– e00310. 21264063 PMC3025524

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Kallen reported 51 cases of influenza-related S aureus, 37 of which were MRSA infections in young adults; where outcome was known, deaths occurred in 24 of 47 cases.

    “Kallen who reported 51 cases of influenza‐related S aureus, 37 of which were MRSA infections in young adults. Where outcome of illness was known, deaths occurred in 24 of 47 cases.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [56] Kallen AJ, Brunkard J, Moore Z et al Staphylococcus aureus community‐acquired pneumonia during the 2006 to 2007 influenza season. Ann Emerg Med 2009; 53: 358– 365. 18534715

      Not checked in the free run.

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

    Findingcitation

    Finelli notes that the proportion of influenza-related S aureus paediatric deaths increased fivefold between 2004 and 2007.

    “Finelli notes that the proportion of influenza‐related S aureus paediatric deaths increased fivefold between 2004 and 2007.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [5] Finelli L, Fiore A, Dhara R et al Influenza‐associated pediatric mortality in the United States: increase of staphylococcus aureus coinfection. Pediatrics 2008; 122: 805– 811. 18829805

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Other US studies of the 2003/04 season noted a rise in reports of community-acquired S aureus infections in children and young adults, a significant proportion being MRSA infections.

    “Other US studies of that season also noted a rise in reports of community‐acquired S aureus infections in children and young adults, a significant proportion being MRSA infections.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [54] Hageman JC, Uyeki TM, Francis JS et al Severe community‐acquired pneumonia due to staphylococcus aureus, 2003–04 influenza season. Emerg Infect Dis 2006; 12: 894– 899. 16707043 PMC3373026

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    A review of influenza surveillance data in the United States from 2004 to 2007 revealed that 23 to 38% of annually reported paediatric deaths attributable to influenza were from influenza B, and many fatal cases had evidence of bacterial co-infection.

    “A review of influenza surveillance data in the United States from 2004 to 2007 revealed that anywhere from 23 to 38% of the annually reported paediatric deaths attributable to influenza were from influenza B, and many of the fatal cases had evidence of bacterial co‐infection.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [5] Finelli L, Fiore A, Dhara R et al Influenza‐associated pediatric mortality in the United States: increase of staphylococcus aureus coinfection. Pediatrics 2008; 122: 805– 811. 18829805

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    A description of 19 cases of invasive Group A streptococcal infection in South East England during the seasonal outbreak of influenza in 2010/2011 included four cases of influenza B infection, of which three were fatal.

    “A description of 19 cases of invasive Group A streptococcal (iGAS) infection in South East England during the seasonal outbreak of influenza in 2010/2011 included four cases of influenza B infection, of which three were fatal.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [17] Scaber J, Saeed S, Ihekweazu C, Efstratiou A, McCarthy N, O'Moore E. Group A streptococcal infections during the seasonal influenza outbreak 2010/11 in South East England. Euro Surveill 2011; 16(5): pii=19780. 21315058

      Not checked in the free run.

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

    Findingnone given

    A similar finding of 3% was obtained from community-based virological surveillance data in England and Wales for the 2010/11 winter season.

    “while a similar finding of 3% was obtained from the community‐based virological surveillance data in England and Wales for the 2010/11 winter season”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation

    Secondary bacterial infections are facilitated by virus-induced cytopathology and resulting immunological impairment, which may be caused in part by overproduction of inflammatory cytokines.

    “Secondary bacterial infections are facilitated by virus‐induced cytopathology and resulting immunological impairment, which may be caused in part by the overproduction of inflammatory cytokines.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [6] Beadling C, Slifka MK. How do viral infections predispose patients to bacterial infections? Curr Opin Infect Dis 2004; 17: 185– 191. 15166819

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationnone given

    Less common bacteria such as Legionella pneumophila may also be associated with influenza when new influenza strains emerge.

    “In addition to the well‐known bacterial causes, less common bacteria such as Legionella pneumophila may also be associated with influenza when new influenza strains emerge.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation

    The fatal outcome of influenza pneumonia was determined partly by virally depressed local and general pulmonary resistance and partly by the virulence and nature of the invading bacteria.

    “The fatal outcome of influenza pneumonia was therefore determined partly by virally depressed local and general pulmonary resistance and partly by the virulence and nature of the invading bacteria.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [12] Brundage JF, Shanks GD. Deaths from Bacterial Pneumonia during 1918–19 Influenza Pandemic. Emerg Infect Dis 2008; 14: 8. PMC2600384 18680641 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    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.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [34] Palacios G, Hornig M, Cisterna D et al Streptococcus pneumoniae coinfection is correlated with the severity of h1n1 pandemic influenza. PLoS ONE 4: e8540. 20046873 PMC2795195 source

      Not checked in the free run.

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

    Premisecitation

    Maxwell first noted that bacterial pneumonia could occur during interepidemic periods when sporadic cases of influenza were investigated.

    “Maxwell first noted that bacterial pneumonia could occur during interepidemic periods when sporadic cases of influenza were investigated.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [46] Maxwell ES, Ward TG, Van Metre TE jr. The relation of influenza virus and bacteria in the etiology of pneumonia. J Clin Invest 1949; 28: 307– 318. 16695680 PMC439604 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Much of the 2009 pandemic occurred outside the regular season for pneumococcal disease in temperate regions, which may help explain the lack of a marked increase in risk of pneumococcal infection at this time.

    “The fact that much of the 2009 pandemic occurred outside the regular season for pneumococcal disease in temperate regions may help to explain the lack of a marked increase in risk of pneumococcal infection at this time.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [40] Kuster SP, Tuite AR, Kwong JC, McGeer A, the Toronto Invasive Bacterial Diseases Network, Fisman D. Evaluation of coseasonality of influenza and invasive pneumococcal disease: results from prospective surveillance. PLoS Med 2011; 8: e1001042. 21687693 PMC3110256

      Not checked in the free run.

  • May combine two claims.

    Interpretationnone given

    The overall conclusion from epidemiological and clinical studies of the 2009 H1N1 pandemic is that worldwide incidence was low and infection was mostly mild.

    “The overall conclusion to date from epidemiological and clinical studies of the 2009 H1N1 pandemic is that worldwide incidence was low and infection was mostly mild.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation

    No national relative increase in pneumococcal hospitalisations occurred in persons aged <5 years or aged 65 years or more, suggesting that the pandemic influenza virus was the likely cause of the increase in the younger age group.

    “No national relative increase occurred in persons aged <5 years or aged 65 years or more, suggesting that the pandemic influenza virus was the likely cause of the increase in the younger age group.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [35] Weinberger DM, Simonson L, Jordan R, Steiner C, Miller M, Viboud C. Impact of the 2009 influenza pandemic on pneumococcal pneumonia hospitalizations in the United States. J Infect Dis 2012; 205: 458– 465. 22158564 PMC3276240

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In a study of 126 HIV patients with respiratory symptoms, among 30 co-infected with pandemic H1N1, illness opportunistic infections were more severe, with longer hospital stays, higher hospitalisation rates, and increased deaths.

    “In Mexico, a study of 126 HIV patients with respiratory symptoms found that in the 30 patients co‐infected with pandemic H1N1 virus, illness opportunistic infections were more severe and involved longer hospital stays (P = 0·0013), higher hospitalisation rates (P < 0·0001) and increased deaths (P = 0·026).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [63] Ormsby CE, De la Rosa‐Zamboni D, Vazquez‐Pérez J et al Severe 2009 pandemic influenza A (H1N1) infection and increased mortality in patients with late and advanced HIV disease. AIDS 2011; 4: 435– 439. 21139486

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Sweden, influenza and pneumococcal polysaccharide vaccines together reduced hospital admissions for influenza, pneumonia and invasive pneumococcal disease by 32, 22 and 54%, respectively.

    “In Sweden, influenza and pneumococcal polysaccharide vaccines together reduced hospital admissions for influenza, pneumonia and invasive pneumococcal disease by 32, 22 and 54%, respectively.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [75] Hedlund J, Christenson B, Lundbergh P, Ortqvist A. Effects of a large‐scale intervention with influenza and 23‐valent pneumococcal vaccines in elderly people: a 1‐year follow‐up. Vaccine 2003; 21: 3906– 3911. 12922125

      Not checked in the free run.

  • May combine two claims.

    Interpretationnone given

    This review has documented the adverse impact of co/secondary bacterial infection with influenza infection, and the higher rates of severe morbidity or mortality that subsequently occur in all age groups.

    “This review has documented the adverse impact of co/secondary bacterial infection with influenza infection, and the higher rates of severe morbidity or mortality that subsequently occur in all age groups.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    Deaths do result from influenza B infection, and awareness is growing of the role influenza B co-infection may play in severity of influenza-related illness.

    “Although less common than influenza A‐associated mortality, deaths do result from influenza B infection, and awareness is growing of the role influenza B co‐infection may play in severity of influenza‐related illness.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation

    HIV or active tuberculosis co-infection could be associated with increased mortality risk.

    “signifying that these conditions could be associated with increased mortality risk”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [61] Archer B, Cohen C, Naidoo D et al Interim report on pandemic H1N1 influenza virus infection in South Africa, April to October 2009: epidemiology and factors associated with fatal cases. Euro Surveill 2009; 14(42): pii=19369. 19883549

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    The South Africa study concluded that a significant proportion of viral pneumonia is due to bacterial co-infection and is preventable by a bacterial vaccine.

    “The study concluded that a significant proportion of viral pneumonia is due to bacterial co‐infection and is preventable by a bacterial vaccine.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [52] Madhi SA, Klugman KP and the Vaccine Trialist Group. A role for Streptococcus pneumoniae in virus‐associated pneumonia. Nat Med August 2004; 10(8): 811– 813. 15247911 PMC7095883 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Viral and bacterial vaccines, antiviral and antibiotic therapies all contribute to reducing the global burden of influenza-associated pneumonias.

    “Control and prevention, through viral and bacterial vaccines, and prophylaxis and treatment, through the application of antiviral and antibiotic therapies all contribute to reducing the global burden of these infections.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Bacterial co-infections associated with the influenza A H1N1 pandemic have not been well described yet because of lack of data.

    “bacterial co‐infections associated with the influenza A H1N1 pandemic have not been well described yet because of lack of data.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [65] Rizzo C, Caporali MG, Rota MC. Pandemic influenza and pneumonia due to legionella pneumophila: a frequently underestimated coinfection. Clin Infect Dis 2010; 51: 115. 20518675 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Interventions through vaccination have been shown to be cost saving and of cost benefit in influenza epidemic and pandemic settings.

    “Interventions through vaccination have been shown to be cost saving and of cost benefit in influenza epidemic and pandemic settings,78”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [78] Rubin JL, McGarry LJ, Klugman KP, Strutton DR, Gilmore KE, Weinstein MC. Public health and economic impact of vaccination with 7‐valent pneumococcal vaccine (PCV7) in the context of the annual influenza epidemic and a severe influenza pandemic. BMC Infect Dis 2010; 10: 14. 20092638 PMC2823614

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Influenza-related bacterial infections overall may account for up to 30% of CAP cases, mainly in the elderly.

    “The articles in this review suggest that influenza‐related bacterial infections overall may account for up to 30% of CAP cases, mainly in the elderly.42”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [42] Gupta RK, George R, Nguyen‐Van‐Tam JS. Bacterial pneumonia and pandemic influenza planning. Emerg Infect Dis 2008; 14: 1187– 1192. 18680640 PMC2600366

      Not checked in the free run.

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

    Premisecitation

    The Global Alliance on Vaccines and Immunisation estimates that the incidence of severe pneumonia and associated mortality in children in developing countries may be reduced by 50% through global coverage of conjugate Hib and pneumococcal vaccines.

    “The recent initiative of the Global Alliance on Vaccines and Immunisation, which supports global coverage of conjugate Hib and pneumococcal vaccines in childhood programmes, estimates that the incidence of severe pneumonia and associated mortality in children in developing countries may be reduced by 50% through this programme.69”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [69] Scott JAG, English M. What are the implications for childhood pneumonia of successfully introducing Hib and pneumococcal vaccines in developing Countries? PLoS Med 2008; 5: e86. 19226734 PMC2292749

      Not checked in the free run.

    • Rests on an assumption: In the developing world, the percentage of CAP cases due to influenza-related bacterial infections is much higher, children are the main sufferers, and pneumonic infections are the leading cause of death in children aged <5 years.

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

    Interpretationreasoning

    Many of these deaths are preventable through immunisation, treatment and access to health care.

    “Many of these deaths are preventable through immunisation, treatment and access to health care.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: In the developing world, the percentage of CAP cases due to influenza-related bacterial infections is much higher, children are the main sufferers, and pneumonic infections are the leading cause of death in children aged <5 years.

  • May combine two claims.

    Premisecitation

    Of 70 paediatric deaths related to the 2009 pandemic, 45 (64%) had received antiviral therapy but only seven (10%) within 48 hours of onset.

    “Of 70 paediatric deaths related to the 2009 pandemic and investigated in one study, 45 (64%) had received antiviral therapy but only seven (10%) within 48 hours of onset.14”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [14] Sachedina N, Donaldson LJ. Paediatric mortality related to pandemic influenza A H1N1 infection in England: an observational population‐based study. http://www.thelancet.com Vol 376; November 2010; 1846– 1852. 21030071

      Not checked in the free run.

49 of 49

  • The paper relies on this without support.

    There are few review articles on the topic of bacterial and viral infections associated with influenza.

    “As there are few review articles on this topic, it also aims to integrate some newly published reports.”

  • The paper relies on this without support.

    The annual increase in influenza activity during winter months is usually accompanied by an increase in cases of community-acquired pneumonia.

    “The annual increase in influenza activity during winter months is usually accompanied by an increase in cases of community‐acquired pneumonia (CAP).”

  • The paper relies on this without support.

    The most common causes of community-acquired pneumonia are S pneumoniae, S aureus and H influenzae.

    “The most common causes of CAP are Streptococcus pneumoniae (S pneumoniae), Staphylococcus aureus (S aureus) and Haemophilus influenzae (H influenzae).”

  • The paper relies on this without support.

    Reports from past influenza pandemics show an extremely high frequency of lung colonisation by bacterial species commonly found in the nasopharynx.

    “Reports from past influenza pandemics show an extremely high frequency of lung colonisation by bacterial species that are commonly found in the nasopharynx.”

  • The paper relies on this without support.

    The 2009 pandemic first appeared in some countries during their normal seasonal activity.

    “The 2009 pandemic first appeared in some countries during their normal seasonal activity.”

  • The paper relies on this without support.

    In the developing world, the percentage of CAP cases due to influenza-related bacterial infections is much higher, children are the main sufferers, and pneumonic infections are the leading cause of death in children aged <5 years.

    “In the developing world, this percentage is much higher, but children are the main sufferers, and pneumonic infections are the leading cause of death in children aged <5 years.”
6 of 6

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?

  • Co-infection has been associated with more severe outcomes in pandemic and seasonal influenza.

    “Furthermore, co-infection has been associated with more severe outcomes in pandemic and seasonal influenza.7”

    From Co-infections in people with COVID-19: a systematic review and meta-analysis. (2020) · cites this paper as [7]

  • S. pneumoniae is the most common bacterium found in viral secondary bacterial infections and is particularly associated with high mortality and morbidity during influenza epidemics and pandemics.

    “Streptococcus pneumoniae is the most common bacteria found in viral secondary bacterial infections, and is particularly associated with causing high mortality and morbidity during influenza epidemics and pandemics (Brundage, 2006; Joseph et al., 2013).”

    From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Joseph et al., 2013

  • Influenza with secondary bacterial infection of S. pneumoniae, H. influenzae and/or Staphylococcus sp. was associated with major outbreaks of purulent bronchitis in 1916 and 1917.

    “Influenza with secondary bacterial infection of S. pneumoniae (and other Streptococcus sp.), H. influenzae and/or Staphylococcus sp. was associated with major outbreaks of purulent bronchitis in 1916 and 1917 (Brundage, 2006; Joseph et al., 2013).”

    From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Joseph et al., 2013

  • Influenza infection appears to prime host airways for bacterial infection and modifies and impairs immune responses in a number of ways.

    “Influenza infection appears to prime the host airways for bacterial infection, whilst modifying and impairing immune responses in a number of ways (Joseph et al., 2013).”

    From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Joseph et al., 2013

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Authors
Joseph, C., Togawa, Y., & Shindo, N.
Affiliations
  • World Health Organization (CH)
  • Okayama University (JP)
Corresponding author
Shindo, Nahoko
ORCID
Shindo, Nahoko
Venue
Influenza and Other Respiratory Viruses
Publisher
Wiley
Published
2013-08-27
Volume
7
Issue
s2
Pages
105-113
ISSN
  • 1750-2640 (ISSN-L)
  • 1750-2659
DOI
10.1111/irv.12089
PMC
PMC5909385
OpenAlex
W2014317349
Semantic Scholar
02d5bc03c7036037c6889da969cc82b4441afae7
Cited by
250
References
81
Citations by year
2026: 8 · 2025: 14 · 2024: 19 · 2023: 29 · 2022: 29 · 2021: 39 · 2020: 42 · 2019: 10 · 2018: 20 · 2017: 15 · 2016: 7 · 2015: 12 · 2014: 5 · 2013: 1
FWCI
0.99
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • Influenza and Other Respiratory Viruses (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
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
influenza, bacterial co-infection, viral coinfection, secondary infection, bacterial pneumonia, pneumococcal infection, 2009 H1N1 pandemic, Legionella pneumophila, influenza-associated pneumonia, etiology
MeSH terms
Bacterial Infections, Humans, Influenza, Human, Incidence, Prevalence, Coinfection

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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.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-09.

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