Table 2.
Summary of Included Studies Involving Patients With COVID-19 and Community-Acquired (CA) Bacterial Coinfections or Hospital-Acquired (HA) Secondary Bacterial Infections
| Study | Study Type/Date | Total COVID-19 Patients, No. | Coinfection or Secondary Infection Type a /Acquisition Setting | Time of Infection Diagnosis a | Rate of Secondary Bacterial Infection or Coinfection b | Mortality Outcomes in COVID-19 Patients With Secondary Bacterial Infection or Coinfection c | Other Outcomes Reported in COVID-19 Patients With Secondary Bacterial Infection or Coinfection c |
|---|---|---|---|---|---|---|---|
| Observational studies, United States | |||||||
| Singh et al, 2021 33 | Analysis of respiratory samples, 1 laboratory, USA (March–August 2020) | 4,259 | CA and HA respiratory bacterial infections/outpatient and inpatient | NR | Bacterial, 33.2% | NR | NR |
| Kubin et al, 2021 21 | Retrospective cohort, 1 hospital, USA (March–May 2020) |
3,028 | CA and HA bacterial/fungal infection/outpatient and inpatient | ≤72 h of hospitalization or ≤5 d prior to admission from outpatient/ED visit (CA infection); after hospital day 3 (HA infection) | Overall bacterial/fungal infection, 516 (17.0%) of 3,028; CA infection, 183 (6.0%) of 3,028; HA infection, 350 (11.6%) of 3,028 |
Mortality rate, 168 (33%) of 516 | Hospital LOS, ICU admission rate, MV rate |
| Cusumano et al, 2020 25 | Retrospective case series, 2 hospitals, USA (March–May 2020) |
2,679; 42 with S. aureus bacteremia | CA and HA Staphylococcus aureus bacteremia/outpatient and inpatient | On admission; ≥4 d after admission (HA bacteremia) |
S. aureus bacteremia, 42 (1.6%) of 2,679; HA-bacteremia, 28 (66.7%) of 42 |
14-d mortality rate, 23 (54.8%) of 42; 30-d mortality rate, 28 (66.7%) of 42 | Hospital LOS |
| Observational studies, Europe | |||||||
| Amin-Chowdhury et al, 2020 46 | Prospective national cohort study, England (February–June 2020) | 160,886 | Bacterial coinfection with IPD/outpatient and inpatient | Coinfection, ≤2 d of positive COVID test | Coinfection, 40 (0.025%) of 160,886 | Mortality rate (<28 d), 25 (63.2%) of 40 | NR |
| Russell et al, 2021 41 | Prospective cohort, 260 hospitals, UK (February–June 2020) | 48,902 | CA and HA-acquired bacterial infection/outpatient and inpatient | ≤2 d of admission (coinfection) and ≥3 d (HA infection) | Respiratory or BSI, 1,107 (2.3%) of 48,902g; unrelated infections, 1,002 (2.0%) of 48,902g; 70.6% of infections were HA |
No association between respiratory infection or BSI and mortality in ICU patients | NR |
| Calderón-Parra et al, 2021 53 | Retrospective cohort SEMI-COVID-19 registry, 150 hospitals, Spain (March–June 2020) | 13,932 | CA and HA bacterial infection/outpatient and inpatient | NR | NR | NR d | NR d |
| Sharov et al, 2020 26 | Two sampling sets, Russia (March–May 2020) |
Set 1: 147 of 3,382 patients with COVID-19-related pneumonia; Set 2: 1,204 patients with pneumonia and COVID-19 | CA and HA bacterial pneumonia/outpatient and inpatient | At admission, day 4, and day 10 of hospitalization or with clinical deterioration | Set 1: bacterial pneumonia, 61 (41.5%) of 147. Set 2: 433 (36.0%) of 1,204; HA, 239 (55.2%) of 433 | Set 1: 91.7% of lethal COVID-19 cases associated with secondary bacterial pneumonia. Set 2: patients with diagnosed bacterial pneumonia, 57 (17.7%) of 322 |
NR |
| Garcia-Vidal et al, 2021 15 | Retrospective cohort, 1 hospital, Spain (February–April 2020) |
989 | CA bacterial infection/outpatient | ≤24 h of admission | CA bacterial infections, 25 (2.5%) of 989; bacterial pneumonia, 21 (2.1%) of 989 | Mortality rate, 5 (16.1%) of 31 patients with CA coinfections | Hospital LOS, ICU admission rate, ICU LOS |
| HA bacterial infection/inpatient | ≥48 h after admission; mean time to diagnosis, 10.6 d | HA bacterial infections, 38 (3.8%) of 989 | Mortality rate, 8 (18.6%) of 43 patients with HA superinfections | Hospital LOS, ICU admission rate, ICU LOS | |||
| Hughes et al, 2021 23 | Retrospective cohort, 2 hospitals, UK (February–April 2020) |
836 | CA bacterial infection/outpatient | <5 d from admission (CA infection) | 27 (3.2%) of 836 early bacterial infections (0–5 d after admission); bacterial CA pathogens, 14 (35.9%) of 39 among 112 respiratory samples taken |
Relative risk of death of patients with true pathogens in blood against baseline of admitted patients, 1.51 (P = .3543) | |
| HA bacterial infection/inpatient | >5 d from admission (HA infection) | 51 (6.1%) of 836 bacterial infections throughout admission; bacterial HA pathogens, 25 (64.1%) of 39 among 112 respiratory samples taken |
|||||
| Rouze et al, 2021 39 | Retrospective cohort, 36 ICUs, EU (March–May 2020) | 568 | CA and HA pneumonia infection/outpatient and inpatient | ≤48 h intubation (n=359) | Overall pneumonia, 55 (9.7%) of 568; pneumonia with <48 h hospital stay, 29 (8.1%) of 359 | 28-d mortality rate, 24 (43.6%) of 55; increased adjusted HR for 28-d mortality, 1.57 (95% CI, 1.01–2.44; P =.043) | ICU LOS, ICU LOS, MV duration, ICU mortality |
| Baskaran et al, 2021 36 | Retrospective cohort, 7 ICUs, England, (February–May) | 254 | CA and HA infection/outpatient and inpatient | <48 h (CA infection), >48 h (HA infection) | Overall bacterial infection, 83 (32.7%) of 254g; bacterial CA, 14 (5.5%) of 254; bacterial/fungal HA, 77 (30.3%) of 254 | Mortality rate, 8 of 43 (18.6%); P = .047 vs patients w/o HA infection |
ICU LOS |
| Foschi et al, 2021 32 | Retrospective cohort, Italy, ICUs, (March–December 2020) | 178 critically ill | CA and HA respiratory bacterial infection, mostly HA/outpatient and inpatient | NR | Respiratory bacterial infections, 79 (34.3%) of 230 samples among 178 patients | NR | NR |
| Søgaard et al, 2020 16 | Retrospective cohort, 1 hospital, Switzerland (February–May 2020) | 162 | CA and HA respiratory tract infection/outpatient and inpatient | ≤48 h of admission (CA infection) | Bacterial CA pneumonia and bacteremia, 1 (0.6%) of 162; bacterial HA infection, 23 (13.6%) of 162 | NR | NR |
| Observational studies, Asia | |||||||
| Tan et al, 2020 59 | Antibiotic use point prevalence survey, 2 hospitals, Singapore (April 2020) | 577 (554 confirmed, 23 suspected) | CA and HA infection/outpatient and inpatient | NR | NR | NR d | NR d |
| Chen et al, 2021 27 | Retrospective cohort, 1 hospital, China (January–March 2020) | 408 | CA and HA infection/outpatient and inpatient | <48 h (CA infection); >48 h (HA infection) | Bacterial/viral CA, 33 (8.1%) of 408; bacterial/fungal HA, 21 (5.1%) of 408 | NR d | NR d |
| Nasir et al, 2021 24 | Retrospective case-control study, 1 hospital, Pakistan, (February–June 2020) | 100: 50 cases with and 50 controls w/o bacterial infection | CA and HA bacterial infection/outpatient and inpatient | NR | 28% CA bacterial infections and 72% HA bacterial infections. Most common infection: HA pneumonia, 28 (56%) of 50; CA pneumonia, 8 (16%) of 50 |
Mortality rate, 21 (42%) of 50, vs 18% w/o bacterial infection (P < .05) |
Hospital LOS, ICU admission rate, MV rate |
| Meta-analyses and reviews | |||||||
| Langford et al, 2021 52 | Systematic review/meta-analysis, 154 studies (December 2019–May 2020) | 35,263 | Coinfection and secondary bacterial infection/outpatient and inpatient | NR | Bacterial coinfection, 8.6% from 31 studies pooled | NR | NR |
| Lansbury et al, 2020 34 | Systematic review/meta-analysis, 30 studies (January–April 2020) | 3,834 | Coinfection and secondary infection/outpatient and inpatient | NR | Bacterial, 7% for hospitalized patients; 14% for ICU patients | Crude pooled OR for death patients with vs w/o coinfection, 5.82 (95% CI, 3.4–9.9) | NR |
| Vazzana et al, 2021 64 | Systematic review/meta-analysis, 355 studies (December 2019–April 2020) |
3,492 | CA and HA bacterial infection/outpatient and inpatient | NR | Secondary bacterial infections, 4.8%–19.5% from 8 studies pooled | Risk of severe course and/or fatal outcomes was significantly increased in patients with evidence of bacterial infection (OR, 20.8; 95% CI, 11.6–37.4) | NR |
| Langford et al, 2020 22 | Systematic review/meta-analysis, 24 studies (December 2019–March 2020) | 3,338 | Coinfection and secondary bacterial infection/outpatient and inpatient | On presentation (coinfection); emerging during illness or hospital stay (secondary infection) | Overall bacterial, 6.9%; CA, 3.5%; HA, 14.3% | NR | NR |
| Rawson et al, 2020 31 | Systematic review, 9 studies (January–April 2020) | 806 (infection rates); 2010 (antimicrobial prescribing) | CA and HA bacterial and fungal infection/outpatient and inpatient | NR | Bacterial/fungal infection, 62 (8%) of 806 | NR | NR |
Note. BSI, bloodstream infections; CA, community acquired; CABP, community-acquired bacterial pneumonia; CPE, carbapenemase-producing Enterobacterales; CRKp, carbapenem-resistant Klebsiella pneumoniae; CRPA, carbapenem-resistant Pseudomonas aeruginosa; ED, emergency department; EU, European Union; HA, hospital-acquired; HAP, hospital-acquired pneumonia; ICU, intensive care unit; IPD, invasive pneumonococcal disease; LOS, length of stay; MDR, multidrug resistant; MV, mechanical ventilation; NR, not reported; OBD, occupied bed days; OR, odds ratio; patients, patients; VAP, ventilator-associated pneumonia; w/o, without.
a
Based on published information, including clinical details, or on the time of infection diagnosis: outpatient/≤3 d of hospitalization = community acquired infection; ≥4 d of hospitalization = hospital-acquired infection, unless otherwise stated in the source.
b
Rates were reported per total number of patients with COVID-19.
c
Data for hospital LOS, ICU admission rates in patients with COVID-19 who secondary bacterial infections or coinfections.
d
Outcomes were reported in total patient population.