Table 1.
Characteristics of the included studies. The table shows the main characteristics of the included studies, as reported by the authors. BSI, bloodstream infection; CRBI, catheter-related bloodstream infection; ECMO, extracorporeal membrane oxygenation; ICU, intensive care unit; NA, not available; RT-PCR, real-time polymerase chain reaction.
| Authors (Year) | Design of the Study (Country) |
Setting | Population | Comparison Group (non COVID-19): |
Definitions |
|---|---|---|---|---|---|
| Adler et al. (2020) [38] | Single center retrospective observational study (UK) |
Both ICU and non-ICU | 195 hospitalized patients with COVID-19 (RT-PCR); Age 69 y. [59–81]; Male 60.5% |
NA | Samples unequivocally consistent with contamination were considered negative. Results recorded until 7 days from the positive COVID-19 to exclude hospital-acquired infections |
| Akagi et al. (2021) [45] | Single center retrospective, case–control study (USA) |
Non-ICU | 565 hospitalized patients with COVID-19; Age 64.5 y. ±16.4; Male 57.1% |
NA | Community onset bloodstream infection Positive blood culture with a known pathogen in one or more blood cultures or the same commensal organism in two or more blood cultures drawn within 48 h of hospitalization |
| Bardi et al. (2021) [14] | Single center retrospective observational study (Spain) |
ICU | 140 patients with severe COVID-19 (RT-PCR), admitted to ICU Age 61 y. [57–67], Male 77% |
NA | All infections were defined according to the Centers for Disease Control and Prevention criteria and the Spanish Society of Infectious Diseases and Clinical Microbiology |
| Barry et al. (2021) [49] | Single center case series (Saudi Arabia) |
Both ICU and non-ICU | 605 hospitalized patients with COVID-19 Age 75% < 65 y. Male 61% |
NA | NA |
| Baskaran et al. (2021) [33] | Multicenter retrospective observational study (UK) |
ICU | 254 patients with COVID-19 (RT-PCR) admitted to ICU, Age 59 y. [49–69], Male 64.6% |
NA | Culture results were excluded if they were considered to represent contamination or colonisation |
| Bayo et al. (2020) [28] |
Single center retrospective cohort study (Spain) | Both ICU and non-ICU | 2923 hospitalized patients with COVID-19 (RT-PCR), Age 64.5 [NA] Male 86% |
29,314 hospitalized patients, Age 65.9 [NA] Male 67% |
Blood culture contamination was defined as the presence of one or more of the following organisms found in only one blood culture set and only one of a series of two or three blood culture sets: coagulase-negative staphylococci, Micrococcus spp., viridans group streptococci, Propionibacterium acnes, Corynebacterium spp., and Bacillus spp. |
| Blazoski et al. (2021) [39] | Single center retrospective observational study (USA) |
ICU | 20 patients with COVID-19 admitted to ICU and treated with ECMO; Age 54 ± 8.7 Male 60% |
NA | NA |
| Bonazzetti et al. (2020) [36] | Single center retrospective observational study (Italy) |
ICU | 89 patients with COVID-19 admitted to ICU, Age 61.5 y. [53.1–68.7]; Male 77.5% |
NA | BSIs were defined using the Center for Disease and Control criteria. BSI due to organisms usually associated with contamination had to be confirmed in two sets of blood cultures. ICU-acquired BSI if diagnosed greater than or equal to 48 h after ICU admission |
| Buehler et al. (2021) [37] | Single center prospective observational study (Switzerland) |
ICU | 45 patients with COVID-19 (RT-PCR) admitted to ICU, Age 60 y. [54–69], Male 77.8% |
NA | NA |
| Buetti et al. (2021) [6] | Multicenter prospective observational study (France) |
ICU | 235 patients with COVID-19, admitted to ICU, Age 59.8 y. ± 12.7 Male 80% |
Historical cohort of 235 patients with ARDS, admitted to ICU Age 59.8 y. ± 13.8 Male 80% |
ICU-BSI infection onset occurring >48 h after ICU admission. Typical skin contaminants were included if ≥2 blood cultures showed the same phenotype within a 48-h period or ≥1 blood culture positive for clinical sepsis, no other infectious process, and antibacterial agent treatment initiated by the attending physician Secondary BSI same microorganism in one blood culture and in the suspected source of infection. All catheter-related BSI (CRBSI) were documented by quantitative tip culture |
| Cataldo et al. (2020) [12] | Single center retrospective cohort study (Italy) |
ICU | 57 patients with COVID-19 admitted to ICU, Age 62 y. ± 13, Male 72% | Historical cohort of 75 patients admitted to ICU | NA |
| Cates et al. (2020) [16] | Multicenter retrospective observational study (USA) |
Both ICU and non-ICU | 3948 hospitalized patients with COVID-19 (RT-PCR), Age 70 y. [61–77], Male 94% |
5453 hospitalized patients with influenza A or B (RT-PCR or other), Age 69 [61–75], Male 93.8% |
ICD-10-CM codes |
| Chen et al. (2020) [30] | Single center retrospective observational study (China) |
Both ICU and non-ICU | 408 hospitalized patients with COVID-19 (PCR), Age 48 y. [34–60], Male 48% |
NA | BSI non-skin flora commensal on one or more blood culture to define a bloodstream infection as that caused by a common skin colonizer. Two or more blood cultures drawn from different sites were required plus a clinical evaluation. Co-infections if present at the time of admission (initial 48 h), secondary infections if emerged during the course of hospitalization |
| Cheng et al. (2020) [47] | Single center retrospective observational study (China) |
NA | 212 hospitalized patients with COVID-19; Age 53.1 y. ± 16.6; Male 60% |
NA | According to the diagnostic standard of nosocomial infection formulated by the China’s Ministry of Health in 2001 |
| Contou et al. (2020) [53] | Single center retrospective observational study (France) |
ICU | 92 patients with COVID-19 (RT-PCR) admitted to ICU, Age 61 y. [55–70], Male 79% |
NA | A patient was considered as co-infected when at least one of the performed microbiological investigations isolated a pathogenic bacterium |
| D’Onofrio et al. (2020) [22] |
Single center prospective and retrospective observational study (Belgium) |
Both ICU and non-ICU | 110 patients hospitalized with COVID-19 (RT-PCR), Age 73 y. [60–82], Male 63% |
103 hospitalized patients with influenza, Age 76 y. [57–84], Male 51% |
Blood cultures were drawn at admission (<24 h) |
| Engsbro et al. (2020) [27] | Single center prospective observational cohort study (Denmark) | Both ICU and non-ICU | 227 hospitalized patients with COVID-19 (RT-PCR); Age 66.3 y. ± 17, Male 51% |
2097 hospitalized patients | Bloodstream infections were categorized as community-acquired or hospital-acquired if cultures were drawn within or after 48 h of admission. Clinical significance assessed by microbiologist |
| Fakih et al. (2021) [18] | Retrospective study (USA) | Both ICU and non-ICU | 18,048 hospitalized patients with COVID-19 |
Hospitalized patients | NA |
| Garcia-Vidal et al. (2021) [43] |
Single center observational cohort study (Spain) | Both ICU and non-ICU | 989 hospitalized adults with COVID-19 (RT- PCR), tested for BSI Age 62 y. [48–74], Male 56% |
NA | BSI Non-skin flora commensal on one or more blood culture or common skin colonizer in two or more blood cultures from different sites, plus clinical suspect. Community-acquired diagnosis within the first 24 h of admission Hospital-acquired >48 h after admission |
| Giacobbe et al. (2020) [50] |
Single center retrospective observational study (Italy) |
ICU | 78 patients with COVID-19 (RT-PCR) admitted to ICU, Age 66 y. [57–70], Male 77% |
NA | ICU-acquired BSI At least one positive blood culture for bacteria or fungi, drawn at >48 h after ICU admission. For other common skin contaminants, at least two consecutive blood cultures were positive for the same pathogen. In patients with multiple blood cultures that were positive for the same organism, novel BSI events were considered as independent if occurring at least 30 days after the previous event. Polymicrobial infections were considered as separate BSI events, one for each causative organism isolated from the blood culture |
| Gidaro et al. (2020) [35] | Multicenter retrospective cohort study (Italy) |
Both ICU and non-ICU | 1077 hospitalized patients with COVID-19 | 1082 hospitalized patients | CRBSI diagnosed with blood culture performed by the catheter that showed microbial growth at least 2 h earlier than growth detected in blood collected simultaneously from a peripheral vein |
| Girona-Alarcon et al. (2020) [26] | Single center prospective observational study (Spain) |
ICU | 16 patients with COVID-19 (PCR) admitted to ICU Age 32 y. [23.3–41.5] Male 56.3% |
NA | |
| Grasselli et al. (2021) [55] |
Multicenter retrospective analysis of prospectively collected data (Italy) |
ICU | 774 patients with COVID-19 admitted to ICU; Age 62 y. [54–68] Male 77% |
NA | Infections were considered as ICU acquired infections whether they occurred ≥48 h from ICU admission |
| Haedo et al. (2020) [24] | Single center secondary analysis of a prospective observational study (Argentina) |
Both ICU and non-ICU | 53 hospitalized patients with COVID-19 (RT-PCR) |
NA | NA |
| Hughes et al. (2020) [10] |
Multicenter retrospective observational study (UK) | Both ICU and non-ICU | 836 hospitalized patients with confirmed SARS-CoV-2 (RT- PCR), Age 69.5 y. [55–81], Male 62% |
Historical cohort of 216 hospitalized patients positive to influenza A or B Age 36 y. [22–65], Male 42% |
Commensal Pathogens not warranting targeted therapy; Community acquired infection Less than 120 h from admission; Hospital acquired infection More than 120 h from admission |
| Karaba et al. (2020) [13] | Multicenter retrospective observational study (USA) |
Both ICU and non-ICU | 1016 hospitalized patients with COVID-19 (NAAT), Age 61 [48–74], Male 54% |
NA | BSI Organisms recovered from blood culture and deemed not to be a contaminant. Co-infections were considered present at the time of admission (initial 48 h) |
| Karami et al. (2021) [17] | Multicenter retrospective observational study (The Netherlands) |
Both ICU and non-ICU | 925 hospitalized patients with COVID-19 (PCR), Age 70 y. [59–77], Male 64% |
NA | Bacterial co-infection was defined as the isolation of a bacterium from a blood culture. Typical contaminants were excluded. The early phase was defined as the first 7 calendar days of admission. |
| Karruli et al. (2021) [42] | Single center retrospective observational study (Italy) |
ICU | 32 patients with COVID-19 admitted to ICU; Age 68 y. [55.2–75]; Male 71.9% |
NA | Infections were diagnosed based on the current US Centers for Disease Control and Prevention National Health care Safety Network criteria. Multidrug resistance was defined according to the Magiorakos et al. criteria. |
| Kokkoris et al. (2021) [15] | Single center retrospective observational study (Greece) |
ICU | 50 patients with COVID-19, admitted to ICU Age 64 y. Male 76% |
NA | ICU-acquired BSI pathogen isolation from ≥1 blood specimen obtained at more than 48 h after ICU admission. In patients with ≥2 BSIs, only the first BSI was included, unless the subsequent episode was fungal |
| Kumar et al. (2020) [41] | Single center retrospective observational study (USA) |
Both ICU and non-ICU | 1565 hospitalized patients with COVID-19 | NA | Hospital acquired BSI if cultures were positive and obtained after 3 days of hospital admission |
| Lardaro et al. (2021) [34] | Multicenter retrospective observational study (USA) |
Both ICU and non-ICU | 542 hospitalized patients with COVID-19 (RT-PCR), Age 62.8 y. ± 16.5, Male 49.6% |
NA | True positive bacteremia At least two of four bottles grew bacteria. The growth of bacteria outside of typical skin flora was generally considered true positive |
| Lendorf et al. (2020) [25] | Single center retrospective observational study (Denmark) |
Both ICU and non-ICU | 110 hospitalized patients with COVID-19 (RT-PCR) Age 68 y. (56–78) Male 60% |
NA | Samples were acquired within 3 days of hospitalization. Clinically relevant if likely to contribute to symptomatology and guided treatment |
| Marcus et al. (2021) [44] | Single center retrospective observational study (USA) |
ICU | 17 patients with COVID-19 admitted to ICU and treated with ECMO; Age 42 y. [35–49], Male 76% |
22 patients with influenza admitted to ICU and treated with ECMO; Age 45 y. [35–55], Male 68% |
BSI Positive cultures during ECMO course or within 48 h of decannulation that were determined to be pathogenic by the patient’s treatment team |
| Martinez-Guerra et al. (2021) [48] | Single center prospective cohort study (Mexico) |
Both ICU and non-ICU | 794 hospitalized patients with COVID-19 (RT-PCR) (data presented on 656 patients with complete follow-up) Age 52 y. [43–62] Male 61.6% |
NA | NA |
| Nori et al. (2021) [54] | Multicenter retrospective observational study (USA) |
Both ICU and non-ICU | 152 hospitalized patients with COVID-19 (PCR) Age 62 y. [52.5–72] Male 59% |
NA | All cases were reviewed by an infectious diseases specialist to determine the presence of true clinical coinfection and the source. National Healthcare Safety Network criteria were used for central-line–associated bloodstream infections |
| Ripa et al. (2021) [52] | Single center prospective observational study (Italy) |
Both ICU and non-ICU | 731 hospitalized patients with COVID-19 (RT-PCR), Age 64 [55–76], Male 67.9% |
NA | BSI Single positive blood culture for a likely pathogen or two or more positive blood cultures for common skin colonizers without a concomitant microbiologically documented lower respiratory tract infection due to the same pathogen. Patients with more than one positive blood culture within 7 days from the first positive blood culture were considered to have a single episode of BSI with multiple isolates |
| Rothe et al. (2021) [40] | Single center retrospective observational study (Germany) |
Both ICU and non-ICU | 140 hospitalized patients with COVID-19 (RT-PCR or serological); Age 63.5 y. (range 17–99); Male 64% |
NA | In case of coagulase-negative staphylococci, the isolates were considered clinically significant (true bacteraemia) if two or more bottles yielded the same microorganism. |
| Søgaard et al. (2021) [29] | Single center retrospective observational study (Switzerland) |
Both ICU and non-ICU | 162 hospitalized patients with COVID-19 (RT-PCR), Age 64.4 y. [50.4–74.2] Male 61.1% |
NA | Community-acquired bloodstream infection pathogen from a blood culture taken within 48 h of hospitalization. Hospital-acquired bloodstream infection pathogen from a blood culture taken 48 h or more after hospitalization. |
| Soriano et al. (2021) [31] | Single center restrospective observational study (Spain) |
ICU | 83 patients with COVID-19 (RT-PCR) admitted to ICU, Age 61.2 y. ± 10.4, Male 79.5% |
NA | NA |
| Suarez de la Rica et al.(2021) [32] | Single center retrospective study (Spain) |
ICU | 107 patients with COVID-19 (RT-PCR), admitted to ICU, Age 62.2 y. ± 10.6, Male 71% |
NA | Nosocomial bacteremia positive blood cultures recovered at least 48 h after the hospital admission. Coagulase-negative staphylococci considered as contaminants (only one positive blood culture) were excluded |
| Thelen et al. (2021) [20] | Multicenter retrospective cohort study (The Netherlands) |
Both ICU and non-ICU | 678 hospitalized patients with COVID-19 (RT-PCR), Age 70 y. [58–78], Male 65% |
653 patients with influenza A or B (RT-PCR) | Bacteria were categorized as likely contaminants if they were affiliated to groups that represent commensal skin microbiota and were defined in the patient’s medical record as a contaminant by the Department of Medical Microbiology. Blood cultures were collected within a time interval of 48 h before and after the RT-PCR test |
| Vaughn et al. (2020) [11] | Multicenter retrospective observational study (USA) |
Both ICU and non-ICU | 1705 hospitalized patients with COVID-19, Age y. 64.7 [53–76.7], Male 52% |
NA | Community onset bacterial coinfections were identified by blood culture positive for a typically pathogenic bacterium |
| Wang et al. (2021) [19] |
Multicenter retrospective observational cohort study (UK) |
Both ICU and non-ICU | 1396 hospitalized patients with COVID-19 (RT-PCR), Age 67.4 y. ± 16.2, Male 64.7% |
NA | Microbiological specimens taken within 48 h of admission. Two senior consultant microbiologists reviewed the clinical significance of the test results and the likelihood of contamination or colonization based on the nature of the isolated organisms |
| Wendel Garcia et al. (2020) [46] | Multicenter prospective observational cohort study (EU) |
ICU | 639 patients with COVID-19 admitted to ICU (data presented on 398 patients who reached the outcome of discharged/dead) Age 63 [53–71]; Male 75% |
NA | Bacteraemia and fungaemia were defined as positive blood cultures for a bacterial or fungal pathogen |
| Zhang et al. (2020) [51] | Multicenter retrospective cohort study (China) |
Both ICU and non-ICU | 38 patients with severe or critical COVID-19, Age 64.76 y. ± 13.76, Male 84% |
NA | Secondary infection clinical symptoms or positive radiologic evidence and a positive laboratory-confirmed aetiologic result (culture positive or mNGS positive confirming by RT–PCR) after 48 h of admission. The final diagnosis of causative agents was made according to the clinical physician expert groups’ discussion results |
| Zhou et al. (2020) [23] | Multicenter retrospective observational study (China) |
Both ICU and non-ICU | 195 patients with COVID-19 (RT-PCR), admitted to ICU, Age 66 y. [56–76], Male 66.7% |
NA | NA |