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Co-infections in people with COVID-19: a systematic review and meta-analysis.
Open accessAbstract
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.
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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.
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32 Own result · 28 Not checked yet · 13 Own interpretation · 8 No basis given · 5 Own method
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In the paper
“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”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Abstract > Results
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In the paper
“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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Abstract > Results
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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
“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)”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Abstract > Results
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In the paper
“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%).”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Abstract > Results
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“Other fungal co-infections from respiratory samples were Aspergillus flavus (2 patients), Aspergillus fumigatus and Candida glabrata (one patient each).”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
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In the paper
“Pooled analysis of crude odds ratios for death indicated that COVID-19 patients with a co-infection were more likely to die than patients who did not have a co-infection (pooled OR 5·82, 95% CI 3·4 – 9·9, n=733, 4 studies, I2=85·4%).”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
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“Subgroup analysis did not show a significant difference in proportions between patients on ICU and the mixed hospitalised population (5% (95% CI 1-14, n=42, 2 studies) and 3% (95% CI 1-5%, n=972, 14 studies, I2=62·9%) respectively)”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
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“Excluding three studies which only included paediatric patients resulted in a slight decrease in overall proportion of viral co-infected patients to 2% (95% CI 1-5%, n=886, 13 studies, I2=55·5%).”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
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“For hospitalised patients, the overall proportion of co-infected patients was 12% (95% CI 2-29, n=991, 6 studies, I2=97·3%).”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
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“One study42, which included SARS-CoV-2 positive patients seen in outpatients and the emergency department reported viral co-infection in 23/115 patients (20%).”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
What the sources say
- Not checked yetcites [42] Kim, 2020, Rates of Co-infection Between SARS-CoV-2 and Other Respiratory Pathogens, JAMA source
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“In the risk of bias assessment 11 of the 29 (38%) observational studies were judged to have an element of selection bias as the patients they reported may not have been truly representative of patients with COVID-19.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
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“The one RCT was judged to be at low risk of bias in the domains relating to the randomisation process, deviations from the intended interventions and outcome measurement.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
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“in the studies where the diagnostic method was described, all the M.pneumoniae co-infections were diagnosed serologically through detection of IgM.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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“Specific co-infecting pathogens were identified in 17 studies.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
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In the paper
“In the ascertainment of outcome domain, 21 of 29 studies (72%) were at some risk of bias, which was generally attributable to incomplete follow-up of patients, with most studies reporting that many patients were still hospitalised at the censor date.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
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In the paper
“Viral co-infecting respiratory pathogens were identified in 14 studies5 , 10 , 13 , 20 , 24 , 27 , 29, 30, 31 , 33 , 37, 38, 39 , 42”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
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“The majority of studies were case series reporting the clinical characteristics of patients infected with a previously unencountered virus”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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“Only three of the included studies in our review reported co-infections with fungal pathogens.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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“and details on identified co-infections were generally limited.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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“one study reported the detection of extended spectrum β-lactamase (ESBL)-positive K.pneumoniae, ESBL-positive P.aeruginosa, and carbapenem-resistant K.pneumoniae in patients on ICU.35”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [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
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“We estimated that 3% of patients hospitalised with COVID-19 were also co-infected with another respiratory virus”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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“respiratory syncytial virus (RSV) and influenza A being the most common viral pathogens identified in this review.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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“From available data, we are unable to draw conclusions as to whether patients who have a concurrent viral infection have a worse prognosis than those in whom SARS-CoV-2 is the only detected pathogen.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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“Although there were no specific data on antimicrobial resistance patterns in the bacteria identified in the studies included in this review”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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“there were very few data on the timing of co-pathogen detections”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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In the paper
“most of the studies screened did not report on this.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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“a considerable number of included participants remained hospitalised at the censor date of most studies”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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In the paper
“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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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“patients in the studies included in this review were predominantly hospitalised.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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“but it was not possible to differentiate between these possibilities from the data provided.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
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In the paper
“Many studies of hospitalised patients with COVID-19 note the empiric use of antibiotics in a majority of patients;5 , 10 , 11”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Introduction
What the sources say
- Not checked yetcites [5] Wu, 2020, Risk Factors Associated With Acute Respiratory Distress Syndrome and Death in Patients With Coronavirus Disease 2019 Pneumonia in Wuhan, China, JAMA Intern Med source
- Not checked yetcites [10] Wang, 2020, Clinical Features of 69 Cases with Coronavirus Disease 2019 in Wuhan, China, Clin Infect Dis
- Not checked yetcites [11] Du, 2020, Hospitalization and Critical Care of 109 Decedents with COVID-19 Pneumonia in Wuhan, China
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In the paper
“A low proportion of COVID-19 patients have a bacterial co-infection; less than in previous influenza pandemics.”
- Also stated in: § Discussion · hedged
“These analyses, arising from the earliest cases of the SARS-CoV-2 pandemic, suggest that bacterial co-infections are less prevalent in COVID-19 patients than in patients with influenza.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Abstract > Conclusions
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None of the sources cited for this claim have been checked yet.
In the paper
“there is evidence that the inflammatory serological markers that are usually associated with bacterial infection, such as raised procalcitonin and C-reactive protein, may appear in patients with COVID-19 without a corresponding bacterial co-infection occurring.12 , 13”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Introduction
What the sources say
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“In the 2009 influenza pandemic, 1 in 4 severe or fatal cases of influenza A(H1N1)pdm09 had a bacterial infection, with an apparent association with morbidity and mortality.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [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
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“These findings do not support the routine use of antibiotics in the management of confirmed COVID-19 infection.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Abstract > Conclusions
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In the paper
“In a study of patients with SARS, those who tested positive for M.pneumoniae and C.pneumoniae on serology were PCR- negative at the time of respiratory specimen collection.9”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [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
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In the paper
“Our findings are similar to studies reporting the bacteria implicated in secondary infections in patients with MERS-CoV and SARS-CoV.8 , 46 , 47”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [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 yetcites [46] Arabi, 2017, Middle East Respiratory Syndrome, N Engl J Med source
- Not checked yetcites [47] Hwang, 2005, Pulmonary pathology of severe acute respiratory syndrome in Toronto, Mod Pathol source
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In the paper
“The identification of co-infections with gram-negative organisms is consistent with the types of pathogens frequently associated with hospital–acquired pneumonia (HAP) or ICU-HAP as a complication of ICU care49”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [49] Jones, 2010, Microbial etiologies of hospital-acquired bacterial pneumonia and ventilator-associated bacterial pneumonia, Clin Infect Dis source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“and galactomannan testing is not validated for upper respiratory tract specimens.63”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [63] Verweij, 2020, Diagnosing COVID-19-associated pulmonary aspergillosis, Lancet Microbe source
plain- Asserted: passes — The authors put it forward as true.
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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
“and does not necessarily suggest a specific predilection for Gram-negative co-infections in COVID-19.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
hedged- Asserted: passes — The authors put it forward as true.
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In the paper
“Serum galactomannan detection for diagnosis of aspergillosis in COVID-19 patients is less sensitive than in influenza patients for currently unknown reasons”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [63] Verweij, 2020, Diagnosing COVID-19-associated pulmonary aspergillosis, Lancet Microbe source
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“conventional microscopy and culture of respiratory tract sample has only low sensitivity and specificity of around 50%.57”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [57] Hope, 2005, Laboratory diagnosis of invasive aspergillosis, Lancet Infect Dis source
plain- Asserted: passes — The authors put it forward as true.
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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
“this is an unlikely scenario in the context of studies reporting the proportion of patients with co-infections in COVID-19.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
hedged- Asserted: passes — The authors put it forward as true.
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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
“Administration of broad-spectrum antibiotics to a large proportion of the patients included in this review may also have decreased the sensitivity of bacterial culture methods”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
hedgedconditional- Asserted: passes — The authors put it forward as true.
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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
“underestimation of secondary bacterial or fungal infections developing later in the course of the disease is likely.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
hedged- Asserted: passes — The authors put it forward as true.
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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
“Differences between the healthcare systems in China and other parts of the world mean the overall estimate of co-infected patients may not be representative globally.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
hedgedconditional- Asserted: passes — The authors put it forward as true.
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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
“we found that the overall proportion of COVID-19 patients who have a bacterial coinfection is lower than in previous influenza pandemics”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
plain- Asserted: passes — The authors put it forward as true.
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- Rests on an assumption: The pooled proportion of bacterial co-infection is valid despite significant unexplained heterogeneity.
- Rests on an assumption: The previous influenza pandemic co-infection proportions are comparable to COVID-19.
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
“which could have resulted in underestimation of the true numbers of co-infections.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
hedgedconditional- Asserted: passes — The authors put it forward as true.
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- It may state two separate claims as one. 21
- Probably not a substantial claim. 24
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 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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Abstract > Results
plainn = 4- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
- Also stated in: § Results · 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
“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%).”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Abstract > Results
plain- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
- Also stated in: § Results · 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
“Three studies reported fungal co-infections.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Abstract > Results
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
What the sources say
- Not checked yetcites [10] Wang, 2020, Clinical Features of 69 Cases with Coronavirus Disease 2019 in Wuhan, China, Clin Infect Dis
- Not checked yetcites [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 yetcites [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
plainn = 5- Asserted: passes — The authors put it forward as true.
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It 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
“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).”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
plain- Asserted: passes — The authors put it forward as true.
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It 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
“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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
plainn = 652- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“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).”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
plaincorrelational- Asserted: passes — The authors put it forward as true.
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It 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
“There were no data in the remaining studies relating to the time from admission to detection of co-infection.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It 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
“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)”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
plainn = 3- Asserted: passes — The authors put it forward as true.
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It 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
“We found only one report of MRSA and no cases of co-infection with S.pneumoniae nor S.pyogenes.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
plainSingle case- Asserted: passes — The authors put it forward as true.
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It 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
“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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
plainn = 4- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
In the paper
“A highly resistant Acinetobacter baumannii was isolated in a further study.23”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [23] Chen, 2020, Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study, Lancet source
plain- Asserted: passes — The authors put it forward as true.
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Probably 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
“More than three-quarters of the studies we included were from China describing patients at the start of the pandemic.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
plain- Asserted: passes — The authors put it forward as true.
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It 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
“with little evidence of S.aureus, S.pneumoniae or S.pyogenes having a major role.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
plain- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
- Rests on an assumption: The pooled proportion of bacterial co-infection is valid despite significant unexplained heterogeneity.
In the paper
“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”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [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
plainn = 3,800- Asserted: passes — The authors put it forward as true.
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Probably 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
“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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Methods > Search strategy and selection criteria
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“We conducted this systematic review meta-analysis in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.15”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Methods > Search strategy and selection criteria
What the sources say
- Not checked yetcites [15] Moher, 2009, Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement, BMJ source
plain- Asserted: passes — The authors put it forward as true.
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Probably 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
“Two reviewers (LL and BL/VB) independently extracted data from individual studies using a predefined template.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Methods > Data extraction and analysis
plain- Asserted: passes — The authors put it forward as true.
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- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“Furthermore, co-infection has been associated with more severe outcomes in pandemic and seasonal influenza.7”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Introduction
What the sources say
- Not checked yetcites [7] Joseph, 2013, Bacterial and viral infections associated with influenza, Influenza Other Respir Viruses source
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“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”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Introduction
What the sources say
- Not checked yetcites [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 yetcites [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
plain- Asserted: passes — The authors put it forward as true.
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- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
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It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“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”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [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 yetcites [44] Chertow, 2013, Bacterial coinfection in influenza: a grand rounds review, JAMA source
- Not checked yetcites [45] Klein, 2016, The frequency of influenza and bacterial coinfection: a systematic review and meta-analysis, Influenza Other Respir Viruses source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“The study protocol is registered with the National Institute for Health Research international prospective register of systematic reviews (PROSPERO).18”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Methods > Data extraction and analysis
What the sources say
- Not checked yetcites [18] Lansbury, 2020, Co-infections in people with COVID-19: a systematic review and meta-analysis, PROSPERO
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“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”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Methods > Data extraction and analysis
What the sources say
- Not checked yetcites [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
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably 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
“As we anticipated a high level of heterogeneity, an a priori decision was made not to abandon meta-analyses due to high heterogeneity.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Methods > Data extraction and analysis
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim.
In the paper
“This, on its own, is not a highly specific test and may result in overestimation of infections.48”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [48] Sobieszczanska, 2014, Relevance of serology for Mycoplasma pneumoniae infection among children with persistent cough, Adv Clin Exp Med source
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
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It may state two separate claims as one.
In the paper
“The Cochrane Risk of Bias Tool (version 2) was used to assess risk of bias in randomised controlled trials (RCTs).17”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Methods > Data extraction and analysis
What the sources say
- Not checked yetcites [17] Sterne, 2019, RoB 2: a revised tool for assessing risk of bias in randomised trials, BMJ source
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“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”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [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 yetcites [51] Blaize, 2020, Fatal Invasive Aspergillosis and Coronavirus Disease in an Immunocompetent Patient, Emerg Infect Dis source
- Not checked yetcites [52] Koehler, 2020, COVID-19 Associated Pulmonary Aspergillosis, Mycoses source
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“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”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [55] Koehler, 2019, Intensive care management of influenza-associated pulmonary aspergillosis, Clin Microbiol Infect source
- Not checked yetcites [56] Schauwvlieghe, 2018, Invasive aspergillosis in patients admitted to the intensive care unit with severe influenza: a retrospective cohort study, Lancet Respir Med source
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
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- Based: passes — The paper gives a reason why it holds.
Probably 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
“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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“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”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [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 yetcites [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 yetcites [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
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably 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
“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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“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”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [64] Shu, 2010, Dual seasonal patterns for influenza, China, Emerg Infect Dis source
boosted- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“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”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
What the sources say
- Not checked yetcites [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
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
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
“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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
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
“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.”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: fails — It may be too vague to check against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may be too vague to check against evidence.
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
“We did not assess publication bias in this review”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably 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
“some of the bacteria reported may have been merely colonising a normally non-sterile site rather than being causative agents of secondary infections”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Discussion
hedged- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
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”
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
“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
In the citing paper
“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.
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
“Ruan41 | China | Retrospective database, Died vs discharged | 150 (68 deceased, 82 survivors) | Not specified | n/a | n/aa | 16·2%”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
Reported 16.2 · recomputed 45.333333
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
“only three small studies reporting data exclusively from children (n=86).13 , 31 , 39”
§ Co-infections in people with COVID-19: a systematic review and meta-analysis > Results
“Tagarro31 | Spain | Case series Hosp/non-hosp/PIC | 41 | Adult”
Citations
Cites
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Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China
Huang, C., Wang, Y., Li, X., Ren, L., Zhao, J., Hu, Y., Zhang, L., Fan, G., Xu, J., Gu, X., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30183-5 · Cited by 48,884
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859
RoB 2: a revised tool for assessing risk of bias in randomised trials
Sterne, J. A. C., Savović, J., Page, M. J., Elbers, R. G., Blencowe, N. S., Boutron, I., Cates, C. J., Cheng, H.-Y., Corbett, M. S., Eldridge, S. M., et al. (2019) · BMJ · doi:10.1136/bmj.l4898 · Cited by 34,787
Clinical characteristics of coronavirus disease 2019 in China
Guan, W.-J., Ni, Z.-Y., Hu, Y., Liang, W.-H., Ou, C.-Q., He, J.-X., Liu, L., Shan, H., Lei, C.-L., Hui, D. S. C., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2002032 · Cited by 30,246
A novel coronavirus from patients with pneumonia in China, 2019
Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., Shi, W., Lu, R., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2001017 · Cited by 28,244
Zhou, F., Yu, T., Du, R., Fan, G., Liu, Y., Liu, Z., Xiang, J., Wang, Y., Song, B., Gu, X., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30566-3 · Cited by 27,263
Chen, N., Zhou, M., Dong, X., Qu, J., Gong, F., Han, Y., Qiu, Y., Wang, J., Liu, Y., Wei, Y., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30211-7 · Cited by 21,415
(2014) · Medical Entomology and Zoology · Cited by 17,633
Lu, R., Zhao, X., Li, J., Niu, P., Yang, B., Wu, H., Wang, W., Song, H., Huang, B., Zhu, N., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30251-8 · Cited by 11,907
Research works printed but not linked: 1
- Mo, 2020, Clinical characteristics of refractory COVID-19 pneumonia in Wuhan, China. Clin Infect Dis.
Cited by
Sorted by citations
Langford, B. J., So, M., Raybardhan, S., Leung, V., Westwood, D. J., MacFadden, D. R., Soucy, J.-P. R., & Daneman, N. (2020) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2020.07.016 · Cited by 1,589
Antibiotic prescribing in patients with COVID-19: rapid review and meta-analysis
Langford, B. J., So, M., Raybardhan, S., Leung, V., Soucy, J.-P. R., Westwood, D. J., Daneman, N., & MacFadden, D. R. (2021) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2020.12.018 · Cited by 934
Considerations for diagnostic COVID-19 tests
Vandenberg, O., Martiny, D., Rochas, O., van Belkum, A., & Kozlakidis, Z. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-020-00461-z · Cited by 820
Abaleke, E., Abbas, M. A., Abbasi, S., Abbott, A., Abdelaziz, A., Abdelbadiee, S., Abdelfattah, M., Abdul, B., Rasheed, A. A., Kadir, R. A., et al. (2021) · The Lancet · doi:10.1016/s0140-6736(21)00149-5 · Cited by 561
Musuuza, J., Watson, L., Parmasad, V., Putman-Buehler, N., Christensen, L., & Safdar, N. (2021) · PLoS ONE · doi:10.1371/journal.pone.0251170 · Cited by 565
Metadata
- 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
- Venue
- Journal of Infection
- Publisher
- Elsevier BV
- Published
- 2020-08
- Volume
- 81
- Issue
- 2
- Pages
- 266-275
- ISSN
- 0163-4453 (ISSN-L)
- 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
- bronze
- doi.org
- 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.
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.
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