ESKAPE bacteria characterization reveals the presence of Acinetobacter baumannii and Pseudomonas aeruginosa outbreaks in COVID-19/VAP patients

Published:August 21, 2022DOI:


      • ESKAPE bacteria was related in COVID-19/VAP patients.
      • MDR and XDR ESKAPE bacteria were identified.
      • Clonal dispersion of A. baumannii was detected in COVID-19/VAP patients.



      A decrease of detection of outbreaks by multidrug-resistant bacteria in critical areas has been reduced due to COVID-19 pandemic. Therefore, molecular epidemiological surveillance should be a primary tool to reveal associations not evident by classical epidemiology. The aim of this work was to demonstrate the presence of hidden outbreaks in the first wave of the COVID-19 pandemic and to associate their possible origin.


      A population of 96 COVID-19 patients was included in the study (April to June 2020) from Hospital Juárez de México. Genetic identification and antimicrobial susceptibility testing of VAP causative agents isolated from COVID-19 patients was performed. Resistance phenotypes were confirmed by PCR. Clonal association of isolates was performed by analysis of intergenic regions obtained. Finally, the association of clonal cases of VAP patients was performed by timelines.


      ESKAPE and non-ESKAPE bacteria were identified as causative agents of VAP. ESKAPE bacteria were classified as MDR and XDR. Only A. baumannii and P. aeruginosa were identified as clonally distributed in 13 COVID-19/VAP patients. Time analysis showed that cross-transmission existed between patients and care areas.


      Acinetobacter baumannii and Pseudomonas aeruginosa were involved in outbreaks non-detected in COVID-19/VAP patients in the first wave of COVID-19 pandemic.

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      1. World Health Organization. (2022). COVID-19 weekly epidemiological update, edition 76, 25 January 2022. Accessed Ferbuary 28, 2022.—25-january-2022

        • Maes M
        • Higginso E
        • Pereira-Dias J
        • et al.
        Ventilator-associated pneumonia in critically ill patients with COVID-19.
        Crit Care. 2021; 25: 25
        • Zhou F
        • Yu T
        • Du R
        • et al.
        Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retro- spective cohort study.
        Lancet. 2020; 395: 1054-1062
        • Giacobbe D
        • Battaglini D
        • Enrile E
        • et al.
        Incidence and prognosis of ventilator-associated pneumonia in critically ill patients with COVID-19: a multicenter study.
        J Clin Med. 2021; 10: 555
        • Nseir S
        • Martin-Loeches I
        • Povoa P
        • et al.
        Relationship between ventilator-associated pneumonia and mortality in COVID-19 patients: a planned ancillary analysis of the coVAPid cohort.
        Crit Care. 2021; 25: 284
        • Ścisło L
        • Walewska E
        • Bodys-Cupak I
        • Gniadek A
        • Kózka M.
        Nutritional status disorders and selected risk factors of Ventilator-Associated Pneumonia (VAP) in Patients Treated in the Intensive Care Ward-a retrospective study.
        Int J Environ Res. 2022; 19: 602
        • Meawed T
        • Ahmed S
        • Mowafy S
        • Samir G M
        • Anis R.
        Bacterial and fungal ventilator associated pneumonia in critically ill COVID-19 patients during the second wave.
        J Infect Public Health. 2021; 14: 375-1380
        • Rouzé A
        • Martin-Loeches I
        • Povoa P
        • Makris D
        • Artigas A
        • Bouchereau M.
        Relationship between SARS-CoV-2 infection and the incidence of ventilator-associated lower respiratory tract infections: a European multicenter cohort study.
        Intensive Care Med. 2021; 47: 188-198
        • Hughes S
        • Troise O
        • Donaldson H
        • Mughal N
        • Moore L.
        Bacterial and fungal coinfection among hospitalized patients with COVID-19: a retrospective cohort study in a UK secondary-care setting.
        Clin Microbiol Infect. 2020; 26: 1395-1399
        • Mulani M
        • Kamble E
        • Kumkar S
        • Tawre M
        • Pardesi
        Emerging strategies to combat ESKAPE pathogens in the Era of antimicrobial resistance: a review.
        Front Microbiol. 2019; 10: 539
        • Santajit S
        • Indrawattana N.
        Mechanisms of antimicrobial resistance in ESKAPE pathogens.
        Biomed Res. Int. 2016; 2475067
        • Sosa-Hernández O
        • Matías-Téllez B
        • Estrada-Hernández A
        • Cureño-Díaz M
        • Bello-López J.
        Incidence and costs of ventilator-associated pneumonia in the adult intensive care unit of a tertiary referral hospital in Mexico.
        Am. J infect. Control. 2019; 47: e21-e25
        • Fattorini L
        • Creti R
        • Palma C
        • Pantosti A
        Unit of Antibiotic Resistance and Special Pathogens, & Unit of Antibiotic Resistance and Special Pathogens of the Department of Infectious Diseases, Istituto Superiore di Sanità, Rome. Bacterial coinfections in COVID-19: an underestimated adversary.
        Ann Ist Super Sanita. 2020; 56: 359-364
        • Dettori M
        • Piana A
        • Deriu M
        • et al.
        Outbreak of multidrug-resistant Acinetobacter baumannii in an intensive care unit.
        New Microbiol. 2014; 37: 185-191
        • Ababneh Q
        • Abulaila S
        • Jaradat Z.
        Isolation of extensively drug resistant Acinetobacter baumannii from environmental surfaces inside intensive care units.
        Am. J. Infect. Control. 2021; S0196-6553 (00589-7)
        • Durán-Manuel E
        • Cruz-Cruz C
        • Ibáñez-Cervantes G
        • et al.
        Clonal dispersion of Acinetobacter baumannii in an intensive care unit designed to patients COVID-19.
        J Infect Dev Ctries. 2021; 15: 58-68
        • Morgan D
        • Liang S
        • Smith C
        • et al.
        Frequent multidrug-resistant Acinetobacter baumannii contamination of gloves, gowns, and hands of healthcare workers.
        Infect Control Hosp Epedemiol. 2010; 31: 716-721
        • Tajeddin E
        • Rashidan M
        • Razaghi M
        • et al.
        The role of the intensive care unit environment and health-care workers in the transmission of bacteria associated with hospital acquired infections.
        J Infect Public Health. 2016; 9: 13-23
        • Agodi A
        • Barchitta M
        • Cipresso R
        • Giaquinta L
        • Romeo M
        • Denaro C
        Pseudomonas aeruginosa carriage, colonization, and infection in ICU patients.
        Intensive Care Med. 2007; 33: 1155-1161
        • Weber D
        • Rutala W
        • Miller M
        • Huslage K
        • Sickbert-Bennett E.
        Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species.
        Am J Infect Control. 2010; 38: S25-S33
        • Kalantar M
        • Jarineshi H
        • Mehrvarz S
        • Danial Z
        • Rasouli H
        • Rashidi A.
        Bacterial contamination of ventilators in the Intensive Care Unit.
        Trauma Mon. 2018; 23: 5
        • Cureño-Díaz M
        • Durán-Manuel E
        • Cruz-Cruz C
        • et al.
        Impact of the modification of a cleaning and disinfection method of mechanical ventilators of COVID-19 patients and ventilator-associated pneumonia: one year of experience.
        Am J Infect Control. 2021; 49: 1474-1480
        • Johanson W
        • Pierce A
        • Sanford J
        • Thomas G.
        Nosocomial respiratory infection with gram negative bacilli: the significance of colonization of respiratory tract.
        Ann Intern Med. 1972; 77: 701-706
        • Gupta R
        • Sharma S
        • Parwez Saxena S
        Changing panorama for surveillance of device-associated healthcare infections: challenges faced in implementation of current guidelines.
        Indian J Med Microbiol. 2018; 36: 18-25
        • Mehta A
        • Bhagat R.
        Preventing ventilator-associated infections.
        Clin Chest Med. 2016; 37: 683-692
        • DeSantis T
        • Brodie E
        • Moberg J
        • et al.
        Highdensity universal16S rRNA microarray analysis reveals broader diversity than typical clone library when sampling the environment.
        Microb Ecol. 2007; 53: 371-383
        • Jiménez Pearson M
        • Galas M
        • Corso A
        • et al.
        Consenso latinoamericano para definir, categorizar y notificar patógenos multirresistentes, con resistencia extendida o panresistentes.
        Am J Public Health. 2019; 43: e65
      2. Clinical and Laboratory standard institute (CLSI). Performance standards for antimicrobial susceptibility testing, 31th ed. CLSI Supplement M100. (ISBN: 978-1-68440-105-5). 2021.

        • Pierce VM
        • Simner PJ
        • Lonsway DR
        • et al.
        Modified carbapenem inactivation method for phenotypic detection of carbapenemase production among enterobacteriaceae.
        J Clin Microbiol. 2017; 55: 2321-2333
        • Cortés-Ortíz IA
        • Juárez-Gómez JC
        • Cu-Quijano C
        • et al.
        Klebsiella pneumoniae blaNDM-1carrying a class 1 integron causing a hospital outbreak in a Mexican attention center.
        J Inf Dev Ctries. 2021; 15: 657-664
        • Dallenne C
        • Da Costa A
        • Decré D
        • Favier C
        • Arlet G
        Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae.
        J Antimicrob Chemother. 2010; 65: 490-495
        • Nordmann P
        • Poirel L
        • Carrër A
        • Toleman MA
        • Walsh TR.
        How to detect NDM-1 producers.
        J Clin Microbiol. 2011; 49: 718-721
        • Girlich D
        • Bernabeu S
        • Grosperrin V
        • et al.
        Evaluation of the amplidiag CarbaR+MCR kit for accurate detection of carbapenemase-producing and colistin-resistant bacteria.
        J Clin Microbiol. 2019; 57: e01800-e01818
        • Alsehlawi ZS
        • Alshara JM
        • Had ZJ
        • Almohana AM.
        First report of the blaOxa-23 gene in a clinical isolates of Acinetobacter baumannii in Najaf hospitals-Iraq.
        Int J Recent Sci Res. 2014; 5: 1407-1411
        • Versalovic J
        • Koeuth T
        • Lupski JR.
        Distribution of repetitive DNA sequences in eubacteria and. Application to fingerprinting of bacterial genomes.
        Nucleic Acids Res. 1991; 19: 6823-6831
        • Tenover FC
        • Arbeit RD
        • Goering RV
        • et al.
        Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing.
        J Clin Microbiol. 1995; 33: 2233-2239
        • Prokop M
        • van Everdingen W
        • van Rees Vellinga T
        • Quarles van Ufford H
        • Stöger L
        • et al.
        CO-RADS: a categorical CT assessment scheme for patients suspected of having COVID-19-Definition and evaluation.
        Radiology. 2020; 296: E97-E104
        • Magiorakos AP
        • Srinivasan A
        • Carey RB
        • et al.
        Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance.
        Clin Microbiol Infect. 2012; 18: 268-281
        • Harrison AG
        • Lin T
        • Wang P.
        Mechanisms of SARS-CoV-2 transmission and pathogenesis.
        Trends Immunol. 2020; 41: 1100-1115
        • Awadasseid A
        • Wu Y
        • Tanaka Y
        • Zhang W.
        Current advances in the development of SARS-CoV-2 vaccines.
        Int J Biol Sci. 2021; 17: 8-19
        • Raman R
        • Patel K J
        • Ranjan K.
        COVID-19: unmasking emerging SARS-CoV-2 variants, vaccines and therapeutic strategies.
        Biomolecules. 2021; 11: 993
        • Mukherjee S
        • Pahan K.
        Is COVID-19 Gender-sensitive?.
        J Neuroimmune Pharmacol. 2021; 16: 38-47
        • Grasselli G
        • Greco M
        • Zanella A
        • Albano G
        • Antonelli M
        • Bellani G.
        Risk factors associated with mortality among patients with COVID-19 in intensive care units in Lombardy, Italy.
        JAMA Intern Med. 2020; 180: 1345-1355
        • Parra-Bracamonte GM
        • Lopez-Villalobos N
        • Parra-Bracamonte FE.
        Clinical characteristics and risk factors for mortality of patients with COVID-19 in a large data set from Mexico.
        Ann Epidemiol. 2020; 52: 93-98.e2
        • Zhou F
        • Yu T
        • Du R
        • et al.
        Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study.
        Lancet. 2020; 395: 1054e62
        • Li G
        • Fan Y
        • Lai Y
        • Han T
        • Li Z
        • Zhou P.
        Coronavirus infections and immune responses.
        J Med Virol. 2020; 92: 424-432
        • Opal SM
        • Girard TD
        • Ely EW
        The immunopathogenesis of sepsis in elderly patients.
        Clin Infect Dis. 2005; 41: S504e12
        • Póvoa H
        • Chianca GC
        • Iorio N.
        COVID-19: An Alert to Ventilator-Associated Bacterial Pneumonia.
        Infect Dis Ther. 2020; 9: 417-420
        • Perez S
        • Innes GK
        • Walters MS
        • et al.
        Increase in hospital-acquired carbapenem-resistant Acinetobacter baumannii infection and colonization in an acute care hospital during a surge in COVID-19 admissions - New Jersey, February-July 2020.
        MMWR Morb Mortal Wkly Rep. 2020; 69: 1827-1831
        • Zangrillo A
        • Beretta L
        • Scandroglio AM
        • Monti G
        • Fominskiy E
        • Colombo S.
        Characteristics, treatment, outcomes and cause of death of invasively ventilated patients with COVID-19 ARDS in Milan, Italy.
        Criticl Care Resusc. 2020; 22: 200-211
        • Sader HS
        • Castanheira M
        • Arends S
        • Goossens H
        • Flamm RK.
        Geographical and temporal variation in the frequency and antimicrobial susceptibility of bacteria isolated from patients hospitalized with bacterial pneumonia: results from 20 years of the SENTRY Antimicrobial Surveillance Program (1997-2016).
        J Antimicrob Chemother. 2019; 74: 1595-1606
        • Chen N
        • Zhou M
        • Dong X
        • Qu J
        • Gong F
        • Han Y.
        Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study.
        Lancet. 2020; 395: 507-513
        • Lai CC
        • Wang CY
        • Hsueh PR.
        Co-infections among patients with COVID-19: the need for combination therapy with non-anti-SARS-CoV-2 agents?.
        J Microbiol Immunol Infect. 2020; 53: 505-512
        • Rawson TM
        • Moore L
        • Castro-Sanchez E
        • Charani E
        • Davies F
        • Satta G.
        COVID-19 and the potential long-term impact on antimicrobial resistance.
        J Antimicrob Chemother. 2020; 75: 1681-1684
        • Huemer M
        • Mairpady Shambat S
        • Brugger SD
        • Zinkernagel AS
        Antibiotic resistance and persistence-Implications for human health and treatment perspectives.
        EMBO Rep. 2020; 21: e51034
        • Ceccato A
        • Di Giannatale P
        • Nogas S
        • Torres A.
        Safety considerations of current drug treatment strategies for nosocomial pneumonia.
        ExperT Opin Drug Saf. 2021; 20: 181-190
        • Gales AC
        • Seifert H
        • Gur D
        • Castanheira M
        • Jones RN
        • Sader HS.
        Antimicrobial Susceptibility of Acinetobacter calcoaceticus-Acinetobacter baumannii Complex and Stenotrophomonas maltophilia clinical isolates: results from the SENTRY Antimicrobial Surveillance Program (1997-2016).
        Open Forum Infect Dis. 2019; 6: S34-S46
        • Garza-González E
        • Bocanegra-Ibarias P
        • Bobadilla-Del-Valle M
        • Ponce-de-León-Garduño LA
        • Esteban-Kenel V
        Drug resistance phenotypes and genotypes in Mexico in representative gram-negative species: results from the infivar network.
        PloS One. 2021; 16e0248614
        • Xu C
        • Bilya SR
        • Xu W
        adeABC efflux gene in Acinetobacter baumannii.
        New Microbes New Infections. 2019; 30100549
        • Lee CR
        • Lee JH
        • Park M
        • Park KS
        • Bae IK
        • Kim YB.
        Biology of Acinetobacter baumannii: pathogenesis, antibiotic resistance mechanisms, and prospective treatment options.
        Front Cell Infect Microbiol. 2017; 7: 55
        • Sosa-Hernández O
        • Matías-Téllez B
        • Silva-López YE
        • Alarcón-Hernández V
        • Bello-López JM
        • Cureño-Díaz MA
        Economic and epidemiological impact of an improvement plan for the decrease of ventilator-associated pneumonia in a tertiary hospital in Mexico.
        J Patient Saf. 2021; 17: e1889-e1893
        • Rangel K
        • Chagas T
        • De-Simone SG.
        Acinetobacter baumannii infections in times of COVID-19 pandemic.
        Pathogens. 2021; 10: 1006
        • Eckardt P
        • Canavan K
        • Guran R
        • George E
        • Miller N
        • Avendano DH
        Containment of a carbapenem-resistant Acinetobacter baumannii complex outbreak in a COVID-19 intensive care unit.
        Am J Infect Control. 2022; 50: 477-481
        • Ruiz-Garbajosa P
        • Cantón R.
        COVID-19: Impact on prescribing and antimicrobial resistance.
        Revi Esp Quimioter. 2021; 34: 63-68
        • Ukuhor HO.
        The interrelationships between antimicrobial resistance, COVID-19, past, and future pandemics.
        J Iinfect Public Health. 2021; 14: 53-60