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Cited by 1,619COVID-19 Clinical Research StudiesPneumonia and Respiratory InfectionsRespiratory viral infections research

Co-infections in people with COVID-19: a systematic review and meta-analysis.

Open access
Lansbury, Louise, Lim, Benjamin, Baskaran, Vadsala, Lim, Wei Shen·2020·Journal of Infection
DOI 10.1016/j.jinf.2020.05.046PMC PMC7255350
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Abstract

Objectives In previous influenza pandemics, bacterial co-infections have been a major cause of mortality. We aimed to evaluate the burden of co-infections in patients with COVID-19. Methods We systematically searched Embase, Medline, Cochrane Library, LILACS and CINAHL for eligible studies published from 1 January 2020 to 17 April 2020. We included patients of all ages, in all settings. The main outcome was the proportion of patients with a bacterial, fungal or viral co-infection. . Results Thirty studies including 3834 patients were included. Overall, 7% of hospitalised COVID-19 patients had a bacterial co-infection (95% CI 3-12%, n=2183, I2=92·2%). A higher proportion of ICU patients had bacterial co-infections than patients in mixed ward/ICU settings (14%, 95% CI 5-26, I2=74·7% versus 4%, 95% CI 1-9, I2= 91·7%). The commonest bacteria were Mycoplasma pneumonia, Pseudomonas aeruginosa and Haemophilus influenzae. The pooled proportion with a viral co-infection was 3% (95% CI 1-6, n=1014, I2=62·3%), with Respiratory Syncytial Virus and influenza A the commonest. Three studies reported fungal co-infections. Conclusions A low proportion of COVID-19 patients have a bacterial co-infection; less than in previous influenza pandemics. These findings do not support the routine use of antibiotics in the management of confirmed COVID-19 infection.

AI snapshot

Written from the paper’s full text.

TL;DR

This systematic review and meta-analysis found that bacterial co-infections were uncommon in hospitalised COVID-19 patients, with a pooled proportion of 7%, and viral co-infections in 3%. The authors conclude these findings do not support routine empirical antibiotics for confirmed COVID-19.

Key findings

  • Among 30 studies and 3834 patients, the pooled proportion of laboratory-confirmed bacterial co-infection in hospitalised COVID-19 patients was 7% (95% CI 3–12%, n=2183, I²=92.2%).
  • Bacterial co-infections were higher in ICU-only studies than in mixed ward/ICU studies: 14% (95% CI 5–26%, n=204, I²=74.7%) versus 4% (95% CI 1–9%, n=1979, I²=91.7%).
  • The pooled proportion with viral co-infection was 3% (95% CI 1–6%, n=1014, I²=62.3%); RSV and influenza A were the commonest. The commonest bacteria were *Mycoplasma pneumoniae* (42% of 27 confirmed bacterial detections), *Pseudomonas aeruginosa* (12%), and *Haemophilus influenzae* (12%).
  • Co-infected patients were more likely to die than non-co-infected patients (pooled OR 5.82, 95% CI 3.4–9.9, n=733, 4 studies, I²=85.4%).

Methods

  • Systematic review and meta-analysis searching Embase, Medline, Cochrane Library, LILACS, and CINAHL from 1 January 2020 to 17 April 2020, with no language restriction; single case reports and studies with fewer than ten participants were excluded.
  • Included 30 studies (29 observational studies and 1 RCT) with 3834 patients; most data were from adults, with three small paediatric-only studies (n=86), and 23 of 30 studies were from China.
  • Pooled proportions were estimated using a random-effects model (DerSimonian Laird weights) with Freeman-Tukey double arcsine transformation, exact binomial 95% CIs, and heterogeneity assessed by I²; analyses used Stata 16.0.

Limitations

  • Stated: more than three-quarters of included studies were from China early in the pandemic; most were case series with limited co-infection details, few data on timing of co-pathogen detection, and possible under-investigation of secondary infections.
  • Stated: broad-spectrum antibiotic use may have reduced bacterial culture sensitivity and underestimated co-infections; some reported bacteria may have been colonisers rather than causative pathogens; healthcare-system differences may limit global representativeness, and most included patients were hospitalised.
  • Stated: there was significant unexplained heterogeneity, especially for bacterial co-infections; many participants remained hospitalised at censor date, likely underestimating later secondary infections; publication bias was not assessed. Evident from the text: the pooled estimates rely heavily on observational case series with risk-of-bias concerns in selection and outcome ascertainment.

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

Integrity signals

Registry

Crossref · 10.1016/j.jinf.2020.05.046

Cites

66 of 66 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 42 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Thirty studies including 3834 patients were included in the review.

    “Thirty studies including 3834 patients were included.”
    • Also stated in: § Results · plain
      “Data on 3834 patients from 29 observational studies and one RCT were included”
    • Also stated in: § Results · plain
      “leaving 30 studies which were included in the analyses”
    Quote in the paperSubstantial claim
  • Findingown data

    Overall, 7% of hospitalised COVID-19 patients had a laboratory-confirmed bacterial co-infection (95% CI 3-12%, n=2183, I2=92·2%).

    “Overall, 7% of hospitalised COVID-19 patients had a bacterial co-infection (95% CI 3-12%, n=2183, I2=92·2%).”
    • Also stated in: § Results · plain
      “For hospitalised COVID-19 patients, the overall pooled proportion of patients who had laboratory-confirmed bacterial co-infections was 7% (95% confidence intervals (CI) 3 to 12, n=2183, 18 studies, 19 datasets, I2 92·2%).”
    • Also stated in: § Discussion · hedged
      “Our meta-analysis indicated that overall 7% of hospitalised COVID-19 patients had a bacterial co-infection, increasing to 14% in studies that only included ICU patients.”
    Quote in the paperSubstantial claim
  • Findingown data

    A higher proportion of ICU patients had bacterial co-infections than patients in mixed ward/ICU settings (14%, 95% CI 5-26, I2=74·7% versus 4%, 95% CI 1-9, I2=91·7%, p=0·05).

    “A higher proportion of ICU patients had bacterial co-infections than patients in mixed ward/ICU settings (14%, 95% CI 5-26, I2=74·7% versus 4%, 95% CI 1-9, I2= 91·7%).”
    • Also stated in: § Results · plain
      “Subgroup analysis of studies with separate data for ICU patients only showed that a greater proportion of them had bacterial co-infections than patients from mixed hospitalised/ICU studies (14% (95% CI 5-26), n=204, I2=74.7% versus 4% (95% CI 1-9), n=1979, I2 91·7% respectively, p=0·05)”
    Quote in the paperSubstantial claim
  • Findingown data

    The pooled proportion of hospitalised COVID-19 patients with a viral co-infection was 3% (95% CI 1-6, n=1014, I2=62·3%).

    “The pooled proportion with a viral co-infection was 3% (95% CI 1-6, n=1014, I2=62·3%), with Respiratory Syncytial Virus and influenza A the commonest.”
    • Also stated in: § Results · hedged
      “From pooled analysis, an estimated 3% of patients had a confirmed viral co-infection (95% CI 1-6, n=1014, 16 studies, I2=62·3%).”
    Quote in the paperSubstantial claim
  • Findingown data

    Other fungal co-infections from respiratory samples were Aspergillus flavus (2 patients), Aspergillus fumigatus and Candida glabrata (one patient each).

    “Other fungal co-infections from respiratory samples were Aspergillus flavus (2 patients), Aspergillus fumigatus and Candida glabrata (one patient each).”
    Quote in the paperNot a substantial claim
  • May combine two claims. 21
  • Classified as probably not a substantial claim. 24

  • May combine two claims.

    Findingown data

    The most frequently detected bacterial pathogen was Mycoplasma pneumoniae, followed by Pseudomonas aeruginosa, Haemophilus influenzae and Klebsiella pneumoniae.

    “The commonest bacteria were Mycoplasma pneumonia, Pseudomonas aeruginosa and Haemophilus influenzae.”
    • Also stated in: § Results · plain
      “The most frequently detected bacterial pathogen was Mycoplasma pneumoniae (42% of 27 confirmed bacterial pathogen detections), followed by Pseudomonas aeruginosa (12%, including one patient with bacteraemia) and Haemophilus influenzae (12%).”
    • Also stated in: § Discussion · plain
      “the most commonly detected bacterial pathogen was M.pneumoniae, followed by P.aeruginosa, H.influenzae and K.pneumoniae.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Respiratory Syncytial Virus was the most prevalent viral co-infecting pathogen, followed by influenza A.

    “with Respiratory Syncytial Virus and influenza A the commonest.”
    • Also stated in: § Results · plain
      “respiratory syncytial virus (RSV) was the most prevalent respiratory virus (16·9% of detections), followed by influenza A (15·5%).”
    Quote in the paperNot a substantial claim

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

    Findingown data

    Three studies reported fungal co-infections.

    “Three studies reported fungal co-infections.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingcitation

    Four fungal pathogens were identified from three studies; Candida albicans was isolated from the respiratory tract in five patients and urinary tract of a sixth.

    “Four fungal pathogens were identified from three studies.10 , 23 , 35 Candida albicans was isolated from the respiratory tract in five patients and urinary tract of a sixth.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [10] Wang, 2020, Clinical Features of 69 Cases with Coronavirus Disease 2019 in Wuhan, China, Clin Infect Dis

      Not checked in the free run.

    • cites [23] Chen, 2020, Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study, Lancet source

      Not checked in the free run.

    • cites [35] Yang, 2020, Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: a single-centered, retrospective, observational study, Lancet Respir Med source

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    Sensitivity analysis excluding one study which only included children did not significantly affect the overall proportion of patients with bacterial co-infection, nor did it decrease heterogeneity (6%, 95% CI 2-12, I2=92·4%), although the difference between ICU and mixed hospital population failed to reach statistical significance (p=0·08).

    “Sensitivity analysis excluding one study which only included children did not significantly affect the overall proportion of patients with bacterial co-infection, nor did it decrease the heterogeneity (6% (95% CI 2-12), I2=92·4%), although the difference between ICU patients and a mixed hospital population failed to reach statistical significance (p=0·08).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In a sensitivity analysis excluding the study of older adults diagnosed by inflammatory biomarkers, the proportion of co-infected patients fell to 7% (95% CI 2-12, n=652, I2=79·5%), similar to the proportion with specific bacterial co-infections.

    “In a sensitivity analysis excluding this study, the proportion of co-infected patients fell to 7% (95% CI 2-12, n=652, I2=79·5%), similar to the proportion of patients with specific bacterial co-infections.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingcitation

    One study reported that bacterial infection was a predictor of death in older patients on univariate analysis (HR 7·01, 95% CI 3·65-13·5, p<001), but not on multivariate analysis (adjusted HR 1·52, 95% CI 0·71-3·24, p=0·28).

    “One study reported that bacterial infection was a predictor of death in older patients based on univariate regression analysis (hazard ratio (HR) 7·01 (95% CI 3·65-13·5, p<001), but it was not a significant predictor on multivariate analysis (adjusted HR 1·52 (95% CI 0·71-3·24, p=0·28).”
    Quote in the paperNot a substantial claim

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

    Findingown data

    There were no data in the remaining studies relating to the time from admission to detection of co-infection.

    “There were no data in the remaining studies relating to the time from admission to detection of co-infection.”
    Quote in the paperNot a substantial claim

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

    Findingreasoning

    In the missing outcome and selection of reported result domains there were some concerns due to lack of information on how secondary infections were ascertained and continued hospitalisation of some participants at censor date.

    “In the missing outcome and selection of reported result domains there were some concerns due to lack of information on how secondary infections were ascertained and continued hospitalisation of some participants at the censor date.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Other bacteria detected included Enterobacter species (three patients), Acinetobacter baumannii and Chlamydia species (two patients each), and Enterococcus faecium, MRSA, and Serratia marcescens (one patient each).

    “Other bacteria detected were Enterobacter species (three patients), Acinetobacter baumannii and Chlamydia species (two patients each), and Enterococcus faecium, methicillin resistant Staphylococcus aureus (MRSA), and Serratia marscecens (one patient each)”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    We found only one report of MRSA and no cases of co-infection with S. pneumoniae nor S. pyogenes.

    “We found only one report of MRSA and no cases of co-infection with S.pneumoniae nor S.pyogenes.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Klebsiella pneumoniae was isolated from four patients, including a carbapenem resistant isolate and an extended spectrum beta lactamase positive isolate.

    “Klebsiella pneumoniae was isolated from four patients, including a carbapenem resistant isolate from one patient with hospital-acquired pneumonia (HAP) and bacteraemia, and an extended spectrum beta lactamase positive isolate from another patient with HAP.”
    Quote in the paperNot a substantial claim

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

    Findingcitation

    A highly resistant Acinetobacter baumannii was isolated in a further study.

    “A highly resistant Acinetobacter baumannii was isolated in a further study.23”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [23] Chen, 2020, Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study, Lancet source

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    More than three-quarters of the studies included were from China describing patients at the start of the pandemic.

    “More than three-quarters of the studies we included were from China describing patients at the start of the pandemic.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    There is little evidence of S. aureus, S. pneumoniae or S. pyogenes having a major role.

    “with little evidence of S.aureus, S.pneumoniae or S.pyogenes having a major role.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The pooled proportion of bacterial co-infection is valid despite significant unexplained heterogeneity.

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

    Findingcitation

    More than 3,800 patients were included in this review, which is only a small representation of the total number of SARS-CoV-2 infections, around 3 million cases worldwide.

    “Although there were more than 3,800 patients included in this review, this is only a small representation of the total number of SARS-CoV-2 infections, which currently stands at around 3 million cases worldwide.65”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [65] World Health Organization. Coronavirus disease 2019 (COVID-19) Situation Report – 99 Available from:https://www.who.int/docs/default-source/coronaviruse/situation-reports/20200428-sitrep-99-covid-19.pdf?sfvrsn=119fc381_2. Accessed 13 May 2020

      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

    Two independent reviewers screened abstracts and reviewed full texts, with disagreements resolved by consensus.

    “Two independent reviewers (LL and BL/VB) screened the abstracts of identified studies and reviewed the full texts of those which were potentially eligible, with disagreements resolved by consensus.”
    Quote in the paperNot a substantial claim

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

    Study design and conductcitation

    The review was conducted in accordance with PRISMA guidelines.

    “We conducted this systematic review meta-analysis in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.15”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [15] Moher, 2009, Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement, BMJ source

      Not checked in the free run.

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

    Study design and conductnone given

    Two reviewers independently extracted data using a predefined template.

    “Two reviewers (LL and BL/VB) independently extracted data from individual studies using a predefined template.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    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”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [7] Joseph, 2013, Bacterial and viral infections associated with influenza, Influenza Other Respir Viruses source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    There is evidence that co-infections do not occur in patients infected with MERS-CoV and occur rarely in patients infected with SARS-CoV-1.

    “there is evidence that co-infections do not occur in patients infected with MERS-CoV8 and occur rarely in patients infected with SARS-CoV-1.9”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [8] Assiri, 2013, Epidemiological, demographic, and clinical characteristics of 47 cases of Middle East respiratory syndrome coronavirus disease from Saudi Arabia: a descriptive study, Lancet Infect Dis source

      Not checked in the free run.

    • cites [9] Zahariadis, 2006, Risk of ruling out severe acute respiratory syndrome by ruling in another diagnosis: variable incidence of atypical bacteria coinfection based on diagnostic assays, Can Resp J

      Not checked in the free run.

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

    Premisecitation

    The bacteria most commonly associated with influenza infection are those which commonly colonise the nasopharynx, such as Streptococcus pneumoniae, Staphylococcus aureus, and Streptococcus pyogenes, with secondary infection usually occurring in the first 6 days of influenza.

    “The bacteria most commonly associated with influenza infection have been reported to be those which commonly colonise the nasopharynx, such as Streptococcus pneumoniae, Staphylococcus aureus, and Streptococcus pyogenes, with secondary infection usually occurring in the first 6 days of influenza.43, 44, 45”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [43] MacIntyre, 2018, The role of pneumonia and secondary bacterial infection in fatal and serious outcomes of pandemic influenza a(H1N1)pdm09, BMC Infect Dis source

      Not checked in the free run.

    • cites [44] Chertow, 2013, Bacterial coinfection in influenza: a grand rounds review, JAMA source

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    • cites [45] Klein, 2016, The frequency of influenza and bacterial coinfection: a systematic review and meta-analysis, Influenza Other Respir Viruses source

      Not checked in the free run.

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    Study design and conductcitation

    The study protocol is registered with PROSPERO.

    “The study protocol is registered with the National Institute for Health Research international prospective register of systematic reviews (PROSPERO).18”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [18] Lansbury, 2020, Co-infections in people with COVID-19: a systematic review and meta-analysis, PROSPERO

      Not checked in the free run.

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

    Study design and conductcitation

    Risk of bias in observational studies was assessed using a modification of the Newcastle-Ottawa Scale.

    “For observational studies, we assessed the risk of bias in the domains of study group selection and ascertainment of co-infection using a modification of the Newcastle-Ottawa Scale.16”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [16] Wells G, Shea B, O'Connell D, Peterson J, V Welch, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analysesAvailable from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed 13 May 2020

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    An a priori decision was made not to abandon meta-analyses due to high heterogeneity.

    “As we anticipated a high level of heterogeneity, an a priori decision was made not to abandon meta-analyses due to high heterogeneity.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    IgM serology alone is not a highly specific test and may result in overestimation of infections.

    “This, on its own, is not a highly specific test and may result in overestimation of infections.48”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [48] Sobieszczanska, 2014, Relevance of serology for Mycoplasma pneumoniae infection among children with persistent cough, Adv Clin Exp Med source

      Not checked in the free run.

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

    Study design and conductcitation

    Risk of bias in randomised controlled trials was assessed using the Cochrane Risk of Bias Tool version 2.

    “The Cochrane Risk of Bias Tool (version 2) was used to assess risk of bias in randomised controlled trials (RCTs).17”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [17] Sterne, 2019, RoB 2: a revised tool for assessing risk of bias in randomised trials, BMJ source

      Not checked in the free run.

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

    Premisecitation

    At the time of writing, there are an increasing number of reports from Europe of patients with probable or possible COVID-19 associated pulmonary aspergillosis.

    “at the time of writing there are an increasing number of reports from Europe of patients with probable or possible COVID-19 associated pulmonary aspergillosis.50, 51, 52, 53, 54”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [50] Alanio A, Dellière S, Fodil S, Bretagne S, B.M. High Prevalence of Putative Invasive Pulmonary Aspergillosis in Critically Ill COVID-19 Patients (April 14, 2020) Available from: SRN:https://ssrn.com/abstract=3575581 or http://dx.doi.org/10.2139/ssrn.3575581. Accessed 13 May 2020 source

      Not checked in the free run.

    • cites [51] Blaize, 2020, Fatal Invasive Aspergillosis and Coronavirus Disease in an Immunocompetent Patient, Emerg Infect Dis source

      Not checked in the free run.

    • cites [52] Koehler, 2020, COVID-19 Associated Pulmonary Aspergillosis, Mycoses source

      Not checked in the free run.

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

    Premisecitation

    Patients with acute respiratory distress syndrome caused by influenza have been reported to be at increased risk of invasive aspergillosis, even in the absence of predisposing immunocompromising conditions.

    “Patients with acute respiratory distress syndrome caused by influenza have been reported to be at increased risk of invasive aspergillosis (IA), even in the absence of predisposing immunocompromising conditions.55 , 56”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [55] Koehler, 2019, Intensive care management of influenza-associated pulmonary aspergillosis, Clin Microbiol Infect source

      Not checked in the free run.

    • cites [56] Schauwvlieghe, 2018, Invasive aspergillosis in patients admitted to the intensive care unit with severe influenza: a retrospective cohort study, Lancet Respir Med source

      Not checked in the free run.

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

    Interpretationreasoning

    With the emergence of the COVID-19 pandemic during the winter months, it is unsurprising that studies in this review were also detecting viral co-infection in patients with COVID-19.

    “With the emergence of the COVID-19 pandemic during the winter months, it is unsurprising that studies in our review were also detecting viral co-infection in patients with COVID-19.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Detection of galactomannan from bronchoalveolar lavage fluid has been shown to be a useful and rapid tool for identification of invasive aspergillosis in both immunocompromised and immunocompetent patients.

    “Detection of galactomannan (a polysaccharide antigen found primarily in the cells walls of Aspergillus species) from bronchoalveolar lavage fluid (BALF), has been shown to be a useful and rapid tool for identification of IA in both immunocompromised and immunocompetent patients.58, 59, 60, 61”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [58] D'Haese, 2012, Detection of galactomannan in bronchoalveolar lavage fluid samples of patients at risk for invasive pulmonary aspergillosis: analytical and clinical validity, J Clin Microbiol source

      Not checked in the free run.

    • cites [59] Meersseman, 2008, Galactomannan in bronchoalveolar lavage fluid: a tool for diagnosing aspergillosis in intensive care unit patients, Am J Respir Crit Care Med source

      Not checked in the free run.

    • cites [60] Patterson, 2016, Practice Guidelines for the Diagnosis and Management of Aspergillosis: 2016 Update by the Infectious Diseases Society of America, Clin Infect Dis source

      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

    The study's strengths include use of a comprehensive search strategy to identify potentially eligible studies from multiple databases and handsearching relevant journals for recently published articles up to the search cut-off date.

    “The strengths of our study include our use of a comprehensive search strategy to identify potentially eligible studies from multiple databases as well as handsearching relevant journals for recently published articles up to our search cut-off date.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Influenza has dual seasonality in China, with incidence in northern China following a winter pattern typically seen in northern hemisphere countries, whereas in southern China the virus is prevalent throughout the year.

    “Influenza has been shown to have dual seasonality in China, with the incidence in northern China following a winter pattern typically seen in northern hemisphere countries, whereas in southern China the virus is prevalent throughout the year.64”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [64] Shu, 2010, Dual seasonal patterns for influenza, China, Emerg Infect Dis source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The usefulness of standard publication bias tests for proportional meta-analyses has been questioned, with funnel plots and statistical tests potentially yielding misleading results.

    “the usefulness of standard publication bias tests for proportional meta-analyses has been questioned, with funnel plots and statistical tests potentially yielding misleading results.66”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [66] Hunter, 2014, In meta-analyses of proportion studies, funnel plots were found to be an inaccurate method of assessing publication bias, J Clin Epidemiol source

      Not checked in the free run.

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

    Interpretationreasoning

    This unexplained heterogeneity may be due to differences between studies in disease severity, patient comorbidities, treatment differences such as corticosteroid administration, use of antibiotics prior to and during hospitalisation, or other unidentified covariates.

    “This unexplained heterogeneity may be due to differences between studies in disease severity, patient comorbidities, treatment differences (such as corticosteroid administration), use of antibiotics prior to and during hospitalisation, or other unidentified covariates.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    It is possible that patients with a suspected secondary infection may not have had thorough microbiological investigations given the unprecedented circumstances and enormous strain on the hospital systems.

    “It is possible that patients with a suspected secondary infection may not have had thorough microbiological investigations given the unprecedented circumstances and enormous strain on the hospital systems.”
    Quote in the paperNot a substantial claim

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

    Study design and conductcitation

    The review did not assess publication bias.

    “We did not assess publication bias in this review”
    Quote in the paperNot a substantial claim

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

    Interpretationnone given

    Some of the bacteria reported may have been merely colonising a normally non-sterile site rather than being causative agents of secondary infections.

    “some of the bacteria reported may have been merely colonising a normally non-sterile site rather than being causative agents of secondary infections”
    Quote in the paperNot a substantial claim
38 of 38

  • The paper relies on this without support.

    This is the first systematic review to evaluate the burden of co-infections in patients with confirmed SARS-CoV-2 infection.

    “To our knowledge, our study is the first systematic review to evaluate the burden of co-infections in patients with confirmed SARS-CoV-2 infection.”

  • The paper relies on this without support.

    The pooled proportion of bacterial co-infection is valid despite significant unexplained heterogeneity.

    “There was significant heterogeneity among studies, particularly in the meta-analyses of bacterial co-infections which was not accounted for by age group or setting.”

  • The paper relies on this without support.

    The previous influenza pandemic co-infection proportions are comparable to COVID-19.

    “we found that the overall proportion of COVID-19 patients who have a bacterial coinfection is lower than in previous influenza pandemics”
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?

  • ICU patients have a higher proportion of bacterial infections compared with patients in mixed wards/ICU settings.

    “Compared with patients in mixed wards/intensive care unit (ICU) settings, ICU patients have a higher proportion of bacterial infections (Lansbury et al., 2020).”

    From Oral Microbiome and SARS-CoV-2: Beware of Lung Co-infection (2020) · cites this paper as Lansbury et al., 2020

  • Bacterial co-infection occurred in 7% of hospitalized COVID-19 patients.

    “In addition, bacterial co-infection occurred in 7% of hospitalized COVID-19 patients.”

    From Oral Microbiome and SARS-CoV-2: Beware of Lung Co-infection (2020) · cites this paper as Lansbury et al., 2020

Self-check

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

Each contradiction between two passages listed here was confirmed by an independent check.

  • Ruan study's death percentage contradicts its counts

    Minor

    The table lists 68 deceased among 150 participants, which is 45.3%, rather than the stated 16.2%.

    Reported 16.2 · recomputed 45.333333

  • Tagarro study is classified as both paediatric and adult

    Minor

    The results identify study 31 as one of three studies exclusively involving children, but Table 1 labels its age group Adult.

2 of 2

Cites

Flagged first, then by citations

6 of the 72 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

  1. Mo, 2020, Clinical characteristics of refractory COVID-19 pneumonia in Wuhan, China. Clin Infect Dis.

Cited by

Sorted by citations

Related

Authors
Lansbury, L., Lim, B., Baskaran, V., & Lim, W. S.
Affiliations
  • University of Nottingham (GB)
  • University of Cambridge (GB)
  • Nottingham University Hospitals NHS Trust (GB)
Corresponding author
  • Lansbury, Louise
  • Lim, Benjamin
  • Baskaran, Vadsala
  • Lim, Wei Shen
ORCID
Venue
Journal of Infection
Publisher
Elsevier BV
Published
2020-08
Volume
81
Issue
2
Pages
266-275
ISSN
0163-4453 (ISSN-L)
DOI
10.1016/j.jinf.2020.05.046
PMC
PMC7255350
OpenAlex
W3029242200
Semantic Scholar
178ec3f24c4d80e4010688e584fffe519bccb407
Cited by
1,619
References
72
Citations by year
2026: 67 · 2025: 88 · 2024: 170 · 2023: 304 · 2022: 393 · 2021: 463 · 2020: 132
FWCI
15.26
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Infection (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Repository@Nottingham (University of Nottingham) (acceptedVersion, other-oa)
  • Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by-nc-nd)
Funders
National Institute for Health and Care Research
Topics
  • Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
  • Health Sciences › Medicine › Epidemiology › Pneumonia and Respiratory Infections
  • Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
Keywords
COVID-19 pandemic, bacterial co-infection, viral coinfection, fungal co-infection, Mycoplasma pneumoniae pneumonia, Pseudomonas aeruginosa, Haemophilus influenzae, respiratory syncytial virus, influenza A virus, intensive care unit patients, antibiotic use, hospitalized patients
MeSH terms
Betacoronavirus, COVID-19, SARS-CoV-2, Bacterial Infections, Humans, Mycoses, Pneumonia, Viral, Virus Diseases, Coronavirus Infections, Pandemics, Coinfection

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.

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.

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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