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Table 1 Summary of study characteristics of the 38 included studies

From: Antimicrobial resistance (AMR) in COVID-19 patients: a systematic review and meta-analysis (November 2019–June 2021)

First Author

Location

Hospital setting

Study type

Microbiological detection and/or identification

Antimicrobial susceptibility testing method

Chowdhary [31]

New Delhi, India

ICU

Retro-spective Cohort

MALDI-ToF MS

CLSI Broth Microdilution Method M27-A3/S4

Bogossian [44]

Brussels, Belgium

ICU

Retro-spective Case Control

Routine surveillance swabs: chromID® CARBA SMART agar, MacConkey agar containing ceftazidime chromID® VRE agar, MALDI-ToF MS

EUCAST: VITEK 2 and disk diffusion Carbapenemases OXA-48, KPC, NDM, VIM and IMP; VanA, VanB were detected

via PCR analysis or Coris Resist-5 O.O.K.N.V. antigenic. MDR Pseudomonas spp. and

Acinetobacter spp. were defined as recommended considering antimicrobial resistance phenotype

Ramadan [33]

Assiut, Egypt

Tertiary hospitals: Alrahji Liver Hospital and Assiut University Hospital

Prospective Cohort

MALDI-ToF MS

Detection of antibiotic resistance genes by Monoplex PCR Technique (mecA, NDM-1, KPC, TEM, CTX-M, SHV)

Amarsy [45]

Nantes, France

ICU

Retro-spective Cohort

Blood cultures and respiratory cultures

Detection of resistance genes by Illumina WGS

Perez [19]

New Jersey, USA

ICU, Medical-surgical unit, progressive care unit

Retro-spective Cohort

Clinical specimens, colonization screening

CRAB definition:

Detection using RT-PCR for carbapenemase genes

Salehi [22]

Tehran, Iran

Three tertiary care training hospitals

Cross-Sectional

Budding yeasts and pseudohyphae in KOH 10% preparation and culture

CLSI M60 and M59 supplements

Cataldo [46]

Rome, Italy

ICU

Retro-spective Cohort

Blood cultures

NA

Posteraro [47]

Basel, Switzerland

COVID care unit

Case Report

MALDI-ToF MS

Sensititre YeastOne® method confirmed by the CLSI M27-A3 reference method

Nori [3]

New York, City, NY, USA

ICU

Retro-spective Observa-tional

Respiratory cultures, blood cultures

NA

Mahmoudi [48]

Hamedan, Iran

Nahavand Hospitals

Cross-Sectional

Blood and endotracheal aspirate samples

CLSI

Li  [22]

Wuhan, China

Hospital (designated for COVID patients)

Retro-spective Cross-Sectional

Qualified sputum, endotracheal aspirate, bronchoalveolar lavage fluid, blood samples, or qualified urine

CLSI

Contou [18]

Argenteuil, France

COVID ICU

Retro-spective Cross-Sectional

Blood cultures, cultures of the respiratory tract secretions

Panel RP2 plus (Film Array Biomerieux®), Panel Pneumonia Plus (Film Array Biomerieux®)

Mo [22]

Brooklyn, New York

Community Teaching Hospital

Case Series (Retro-spective Observa-tional)

NA

NA

Garcia-Menino [8]

Oviedo, Spain

ICU

Case Series (Retro-spective Observa-tional)

MALDI TOF/MS -

Microscan System (BeckmanCoulter, Brea, CA, USA); results interpreted according to EUCAST

Sharifipour [20]

Qom, Iran,

ICU

Prospective Cohort

Samples were cultured on Blood Agar, Chocolate Agar, Eosin Methylene Blue (EMB), and MacConkey Agar

CLSI

Walpole [50]

United Kingdom

ICU

Case Report

Sputum sample

NA

Razazi [10]

France

ICU

Retro-spective Cohort

Bacterial co-infection at ICU admission evidenced by detection of bacteria in sputum or blood samples, in the absence of other sources of infection, or by a positive pneumococcal or L. pneumophila serotype 1 urinary antigen test

Susceptibility profiles of recovered microorganisms were recorded

Guisado-Gil [17]

Seville, Spain

ICU

Retro-spective Cohort

Blood cultures obtained > 48 h after admission

EUCAST. MDR categorization according to the Germany Society for Hygiene and Microbiology

Montrucchio [51]

Turin, Italy

ICU

Case Series (Retro-spective Observa-tional)

MALDI-ToF MS

EUCAST: Microscan WalkAway plus System, MASTDISCS® Combi Carba plus disk system

Mady [23]

Riyadh, Saudi Arabia

ICU

Case Series (Retro-spective Observa-tional)

Blood and respiratory cultures

Not described

Tiri [52]

Terni, Italy

ICU

Retro-spective Observa-tional Cohort

MALDI-ToF MS

VITEK2; Immunochromatography for OXA-48-like, OXA-163, KPC, NDM, VIM

Kokkoris [53]

Athens, Greece

ICU

Case Series (Retro-spective Observatio-nal Cohort)

Blood specimen

NA

Perrotta [54]

FG, Italy

ICU

Case Report

NA

NA

Baiou [55]

Doha, Qatar

ICU

Retro-spective Case–Control

MALDI-ToF MS

BD Phoenix according to CLSI standards

Segrelles-Calvo [56]

Madrid, Spain

ICU, RICU

Prospective Observa-tional Cohort

Aspergillus galactomannan antigen on BAL

Not described

Martinez-Guerra [57]

Mexico City, Mexico

COVID-19 dedicated facility

Prospective Cohort

MALDI-Tof MS

VITEK2; AmpC producers considered with known chromosomal AmpC Beta-Lactamases, ESBL considered in those resistant to 3rd generation cephalosporins and monobactams, CRE considered with resistance to carbapenems in VITEK and confirmed with modified CIM test, MDR P. aeruginosa considered in isolates with resistance to at least one agent in three or more antibiotic categories

Karruli [58]

Naples, Italy

ICU

Retro-spective Observa-tional Cohort

Microbiological sampling of blood, urine, and airways

MDR defined according to Magiorakos et al. [59] criteria

Gomez-Simmonds [60]

New York City, USA

ICU

Retro-spective Observational Cohort

Surveillance using MicroScan

Xpert Carba-R, BMD, E-test, WGS

Cultrera [61]

Ferrara, Italy

ICU

Retro-spective Observational Cohort

MALDI-ToF MS

VITEK2

Khurana [62]

New Delhi, India

COVID-19 dedicated facility

Retro-spective Observational Cohort

VITEK2 and BioFire FilmArray Respiratory Panel

VITEK2 AST card interpreted by CLSI guidelines

Posteraro [47]

Rome, Italy

ICU

Retro-spective Observa-tional Cohort

Positive blood culture using BacT/ALERT VIRTUO and MALDI Biotyper

VITEK2 and Sensititre YeastOne® following EUCAST breakpoints

Pascale [63]

Bologna, Italy

ICU and non-ICU settings

Cross-Sectional

Active surveillance of blood and respiratory cultures

CRE defined as per EUCAST criteria; WGS

Baskaran [64]

England

ICU

Multicentre Retro–spective Observa-tional Cohort

Standard culture, respiratory viral PCR and urinary antigen tests

NA

Moretti [65]

Brussels, Belgium

ICU

Retro-spective Observational Cohort

Endotracheal aspiration or BAL with > 105 and > 104 CFU/mL

Not described. MDR or extreme-drug resistant (XDR) based on European Center of Disease Prevention and Control (ECDC)

Grasselli [66]

Genoa, Italy

ICU

Retro-spective Observa-tional Cohort

Routine microbiological surveillance: perineal swabs, nasal swabs, tracheal aspirate, urine culture

Not described

Magnasco [67]

Genoa, Italy

ICU

Retro-spective Observa-tional Cross-Sectional

Blood, respiratory and urinary samples using VITEK MS

VITEK2; Sensititre YeastOne® Panel (antifungal)

Bentivegna [68]

Rome, Italy

COVID-19 Depart-ment

Case–Control

NA

NA

Suarez-de-la-Rica [69]

Madrid, Spain

CCU

Retro-spective Observational Cohort

Conventional culture

Not described

  1. Abbreviations: Bronchoalveolar Lavage (BAL), Clinical and Laboratory Standards Institute (CLSI), Critical Care Unit (CCU), European Committee on Antimicrobial Susceptibility Testing (EUCAST), intensive care unit (ICU), multi-drug resistant (MDR), matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS), polymerase chain reaction (PCR), whole-genome sequencing (WGS), carbapenem resistant Acinetobacter baumannii (CRAB), respiratory intensive care unit (RICU), real-time polymerase chain reaction (RT-PCR), oropharyngeal candidiasis (OPC)