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Contamination of healthcare environment by carbapenem-resistant Acinetobacter baumannii

      Abstract

      Acinetobacter baumannii is frequently found on floors, devices, and environmental sites in hospitals and can survive for prolonged periods and accumulate resistance determinants. The infection and presence of carbapenem-resistant A. baumannii (CRAB) in patients is associated with increased mortality, severe clinical outcomes, and longer lengths of stay at hospitals. This review addresses contamination by CRAB in corporal surfaces of patients and healthcare workers and environmental sites at healthcare-related settings. We summarized published data during the last decade on potential reservoirs for CRAB, including contamination frequency and the involved resistance mechanisms, and some measures associated with the elimination of CRAB from hospital surfaces.

      Key Indexing Terms

      Introduction

      Acinetobacter baumannii is a Gram-negative opportunistic pathogen that has emerged as one of the most important causative agents of healthcare-associated infections (HAIs) related to outbreaks worldwide and is considered to be endemic in many hospitals. This microorganism has a significant ability to survive for prolonged periods in the nosocomial environment and is frequently detected on floors, devices, and environmental sites in hospitals.
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      • Seifert H.
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      • Liou M.L.
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      Persistent nasal carriers of Acinetobacter baumannii in long-term-care facilities.
      A. baumannii accumulates resistance determinants, leading to the development of multidrug-resistant (MDR) strains.
      • Kempf M.
      • Rolain J.M.
      Emergence of resistance to carbapenems in Acinetobacter baumannii in Europe: clinical impact and therapeutic options.
      Carbapenems have been used to treat MDR A. baumannii infections.
      • Munoz-Price L.S.
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      • Nordmann P.
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      Eighteen years of experience with Acinetobacter baumannii in a tertiary care hospital.
      Nonetheless, the incidence of carbapenem-resistant A. baumannii (CRAB) has increased over time, leading to limited therapeutic options. This event is considered a sentinel event for emerging antimicrobial resistance.
      • Kempf M.
      • Rolain J.M.
      Emergence of resistance to carbapenems in Acinetobacter baumannii in Europe: clinical impact and therapeutic options.
      Carbapenem resistance is associated with multiple mechanisms including the production of carbapenemases.
      • Butler D.A.
      • Biagi M.
      • Tan X.
      • et al.
      Multidrug resistant Acinetobacter baumannii: resistance by any other name would still be hard to treat.
      The following classes of enzymes involved in carbapenem resistance have been reported: class A, Klebsiella pneumoniae carbapenemase (KPC) and Guiana extended-spectrum β-lactamase (GES); class B, New Delhi metallo-β-lactamase (NDM), Imipenem-hydrolyzing beta-lactamases (IMP), and Verona integron-encoded metallo- β-lactamase (VIM); and class D, oxacillinases (OXA), including OXA-23, OXA-24, OXA-51, and OXA-58.
      • Ramirez M.S.
      • Bonomo R.A.
      • Carbapenemases T.M.E.
      Transforming Acinetobacter baumannii into a yet more dangerous menace.
      ,
      • Nordmann P.
      • Poirel L.
      Epidemiology and diagnostics of carbapenem resistance in gram-negative bacteria.
      The ability for GES to expand their spectrum to hydrolyze carbapenems is notabe, as a result of a single or double amino acid substitutions
      • Castanheira M.
      • Simner P.J.
      • Bradford PA.
      Extended-spectrum β-lactamases: an update on their characteristics, epidemiology and detection.
      ,
      • Sawa T.
      • Kooguchi K.
      • Moriyama K.
      Molecular diversity of extended-spectrum β-lactamases and carbapenemases, and antimicrobial resistance.
      ; the presence of GES enzyme is frequently reported in A. baumannii isolates (5 to 26%).
      • Cicek A.C.
      • Saral A.
      • Iraz M.
      • et al.
      OXA- and GES-type β-lactamases predominate in extensively drug-resistant Acinetobacter baumannii isolates from a Turkish University Hospital.
      • Al-Hassan L.
      • Elbadawi H.
      • Osman E.
      • et al.
      Molecular epidemiology of carbapenem-resistant Acinetobacter baumannii from Khartoum state, Sudan.
      • Zeka A.N.
      • Poirel L.
      • Sipahi O.R.
      • et al.
      GES-type and OXA-23 carbapenemase-producing Acinetobacter baumannii in Turkey.
      • Bogaerts P.
      • Naas T.
      • El Garch F.
      • et al.
      GES extended-spectrum β-lactamases in Acinetobacter baumannii isolates in Belgium.
      Tigecycline and colistin are considered last resort treatment options for CRAB infections. However, these antimicrobial agents have adverse effects, including high toxicity and reduced efficacy in some tissues.
      • Cai Y.
      • Chai D.
      • Wang R.
      • et al.
      Colistin resistance of Acinetobacter baumannii: clinical reports, mechanisms and antimicrobial strategies.
      ,
      • Potron A.
      • Poirel L.
      • Nordmann P.
      Emerging broad-spectrum resistance in pseudomonas aeruginosa and Acinetobacter baumannii: mechanisms and epidemiology.
      Ceftazidime/avibactam has been proposed to manage CRAB infections, with in vitro resistance reported.
      • Savov E.
      • Trifonova A.
      • Kovachka K.
      • et al.
      Antimicrobial in vitro activities of ceftazidime-avibactam, meropenem-vaborbactam and plazomicin against multidrug-resistant Acinetobacter baumannii and pseudomonas aeruginosa - a pilot Bulgarian study.
      Due to the antimicrobial resistance implications in A. baumannii, the understanding of contamination by CRAB in the hospital environment is essential for HAI control. Despite reported evidence, the importance of hospital environmental contamination by pathogens and the subsequent colonization process is still debated. Healthcare workers (HCWs) are important for dissemination in clinical settings.

      World Health Organization. Classifying health workers: mapping occupations to the international standard classification. 2010. Available at: https://www.who.int/hrh/statistics/Health_workers_classification.pdf. Accessed March 26, 2022.

      In this review, we addressed colonization by CRAB on the corporal surfaces of patients and contamination of environmental sites in healthcare-related settings, and the role of HCWs in its dissemination. Data from the literature, related to potential CRAB reservoirs in healthcare settings and patients during the last decade, is summarized. Additionally, the involved carbapenem resistance mechanisms and measures associated with the elimination of CRAB from hospital surfaces are described.

      Incidence of A. baumannii infections and the impact of carbapenem resistance

      The incidence of HAIs caused by A. baumannii is reported as 25.1 cases per 1000 patients according to 18 healthcare centers studied in Europe, Eastern Mediterranean, and Africa.
      • Ayobami O.
      • Willrich N.
      • Harder T.
      • et al.
      The incidence and prevalence of hospital-acquired (carbapenem-resistant) Acinetobacter baumannii in Europe, eastern Mediterranean and Africa: a systematic review and meta-analysis.
      In intensive care units (ICU), A. baumannii infections are as high as 56.5 cases per 1000 patients, accounting for 20.9% of all HAIs.
      • Ayobami O.
      • Willrich N.
      • Harder T.
      • et al.
      The incidence and prevalence of hospital-acquired (carbapenem-resistant) Acinetobacter baumannii in Europe, eastern Mediterranean and Africa: a systematic review and meta-analysis.
      The Centers for Disease Control and Prevention estimates 8,500 infections in hospitalized patients and 700 deaths caused by carbapenem-resistant Acinetobacter in the United States.
      Centers for Disease Control and Prevention
      Antibiotic Resistance Threats in the United States, 2019.
      During recent years, CRAB prevalence has increased worldwide, and the indiscriminate use of carbapenem is a factor that contributes to the appearance of CRAB and other drug-resistant pathogens.
      • Cheon S.
      • Kim M.J.
      • Yun S.J.
      • et al.
      Controlling endemic multidrug-resistant Acinetobacter baumannii in intensive care units using antimicrobial stewardship and infection control.
      In the US between 2014 and 2018, up to 78% of A. baumannii isolates were resistant to carbapenems, as reported by the SENTRY Antimicrobial Surveillance Program.
      • Flamm R.K.
      • Shortridge D.
      • Castanheira M.
      • et al.
      In vitro activity of minocycline against U.S. Isolates of Acinetobacter baumannii-Acinetobacter calcoaceticus species complex, stenotrophomonas maltophilia, and burkholderia cepacia complex: results from the SENTRY Antimicrobial surveillance program, 2014 to 2018.
      In 2017, Acinetobacter spp. was included on the WHO list of antibiotic-resistant bacteria for research, discovery, and development of new antibiotics.

      World Health Organization. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. 2017. Available at: http://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf. Accessed August 1, 2020.

      CRAB reservoirs

      The colonization by CRAB in patients is associated with increased mortality,
      • Cheng V.C.
      • Chen J.H.
      • So S.Y.
      • et al.
      Use of fluoroquinolones is the single most important risk factor for the high bacterial load in patients with nasal and gastrointestinal colonization by multidrug-resistant Acinetobacter baumannii.
      ,
      • Henig O.
      • Weber G.
      • Hoshen M.B.
      • et al.
      Risk factors for and impact of carbapenem-resistant Acinetobacter baumannii colonization and infection: matched case-control study.
      severe clinical outcomes,

      World Health Organization. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. 2017. Available at: http://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf. Accessed August 1, 2020.

      and a higher length of stay at hospitals.
      • Sheng W.H.
      • Liao C.H.
      • Lauderdale T.L.
      • et al.
      A multicenter study of risk factors and outcome of hospitalized patients with infections due to carbapenem-resistant Acinetobacter baumannii.
      Furthermore, healthcare settings are reservoirs of drug-resistant microorganisms, including methicillin-resistant Staphylococcus aureus, extended-spectrum β-lactamase–producing Enterobacteriaceae, and CRAB, among others.
      • Bedenić B.
      • Beader N.
      • Godič-Torkar K.
      • et al.
      Nursing home as a reservoir of carbapenem-resistant Acinetobacter baumannii.
      Corporal surfaces from HCWs and patients (skin and mucosal surfaces from patients and HCWs, such as palmar surfaces, retroauricular and antecubital creases, nostril, rectum, etc.)
      • Skowron K.
      • Bauza-Kaszewska J.
      • Kraszewska Z.
      • et al.
      Human skin microbiome: impact of intrinsic and extrinsic factors on skin microbiota.
      with predisposing factors (long period hospitalization, catheter insertion, and wounds) are also sites prone to contamination and/or colonization by CRAB, which may contribute to its dissemination (Tables 1 and 2).
      • Bedenić B.
      • Beader N.
      • Godič-Torkar K.
      • et al.
      Nursing home as a reservoir of carbapenem-resistant Acinetobacter baumannii.
      ,
      • Cruz-López F.
      • Villarreal-Treviño L.
      • Morfin-Otero R.
      • et al.
      Dynamics of colonization in patients with health care-associated infections at step-down care units from a tertiary care hospital in Mexico.
      • Hong K.B.
      • Oh H.S.
      • Song J.S.
      • et al.
      Investigation and control of an outbreak of imipenem-resistant Acinetobacter baumannii Infection in a pediatric intensive care unit.
      • Brigante G.
      • Migliavacca R.
      • Bramati S.
      • et al.
      Emergence and spread of a multidrug-resistant Acinetobacter baumannii clone producing both the carbapenemase OXA-23 and the 16S rRNA methylase ArmA.
      • Gao J.
      • Zhao X.
      • Bao Y.
      • et al.
      Antibiotic resistance and OXA-type carbapenemases-encoding genes in airborne Acinetobacter baumannii isolated from burn wards.
      • Cheng V.C.
      • Chen J.H.
      • Ng W.C.
      • et al.
      Emergence of carbapenem-resistant Acinetobacter baumannii in nursing homes with high background rates of MRSA colonization.
      TABLE 1Reports of colonization by CRAB in patients.
      Population characteristicsSampled sitesCRAB recovery (n/N)*Associated resistance determinantStudy length (weeks)Country, yearRefs.
      Patients from a spinal cord injury unitStool

      3/20OXA-23 and OXA-694USA, 2015
      • Kanwar A.
      • Domitrovic T.N.
      • Koganti S.
      • et al.
      A cold hard menace: a contaminated ice machine as a potential source for transmission of carbapenem-resistant Acinetobacter baumannii.
      Patients from a medical ICU and a surgical ICU of a tertiary care hospitalTracheal aspirates (intubated) or throat (non-intubated); groin9/10OXA-234Germany, 2015
      • Molter G.
      • Seifert H.
      • Mandraka F.
      • et al.
      Outbreak of carbapenem-resistant Acinetobacter baumannii in the intensive care unit: a multi-level strategic management approach.
      Injured adult patients from 3 hospitalsGroin, pharynx, nasal, perianal, and hairline18/21
      A proportion of the study population showed clinical evidence of CRAB infection (cases not considered colonization).
      OXA-4852Germany, 2016
      • Granzer H.
      • Hagen R.M.
      • Warnke P.
      • et al.
      Molecular epidemiology of carbapenem-resistant Acinetobacter baumannii complex isolates from patients that were injured during the eastern Ukrainian conflict.
      Patients from an adult ICU during a CRAB outbreakRectum2/7
      A proportion of the study population showed clinical evidence of CRAB infection (cases not considered colonization).
      NDM-135France, 2013
      • Decousser J.W.
      • Jansen C.
      • Nordmann P.
      • et al.
      Outbreak of NDM-1-producing Acinetobacter baumannii in France, January to May 2013.
      Patients from an ICU or other wards (NS)Respiratory tract and skin8/21
      A proportion of the study population showed clinical evidence of CRAB infection (cases not considered colonization).
      OXA-2336Italy, 2012
      • Brigante G.
      • Migliavacca R.
      • Bramati S.
      • et al.
      Emergence and spread of a multidrug-resistant Acinetobacter baumannii clone producing both the carbapenemase OXA-23 and the 16S rRNA methylase ArmA.
      Patients from two ICUs of a large general hospitalNS74/391
      A proportion of the study population showed clinical evidence of CRAB infection (cases not considered colonization).
      OXA-2324Italy, 2013
      • Mammina C.
      • Bonura C.
      • Vivoli A.R.
      • et al.
      Co-colonization with carbapenem-resistant Klebsiella pneumoniae and Acinetobacter baumannii in intensive care unit patients.
      Patients from a medical-surgical ICUTracheal/oropharyngeal secretions and rectum52/234
      A proportion of the study population showed clinical evidence of CRAB infection (cases not considered colonization).
      OXA-2352Brazil, 2013
      • Martins N.
      • Martins I.S.
      • de Freitas W.V.
      • et al.
      Imported and intensive care unit-born Acinetobacter baumannii clonal complexes: one-year prospective cohort study in intensive care patients.
      Colonized or infected adult patients from a medical ICUSkin, mucous membranes, open wounds, and secretions38/867OXA-23 and OXA-14348Brazil, 2016
      • Neves F.C.
      • Clemente W.T.
      • Lincopan N.
      • et al.
      Clinical and microbiological characteristics of OXA-23- and OXA-143-producing Acinetobacter baumannii in ICU patients at a teaching hospital, Brazil.
      Patients and environmental surfaces from a medical ICUNares, axillae, groin, rectum, wounds, exit sites of drains, and endotracheal tube aspirates3/7

      OXA-234Singapore, 2018
      • Ng D.H.L.
      • Marimuthu K.
      • Lee J.J.
      • et al.
      Environmental colonization and onward clonal transmission of carbapenem-resistant Acinetobacter baumannii (CRAB) in a medical intensive care unit: the case for environmental hygiene.
      Patients from the CCC, ICU, emergency room, operating room, and other tertiary care hospital wardsSputum, throat swabs, and stool12/15
      A proportion of the study population showed clinical evidence of CRAB infection (cases not considered colonization).
      OXA-23 and ISAba-140Japan, 2016
      • Ushizawa H.
      • Yahata Y.
      • Endo T.
      • et al.
      A epidemiological investigation of a nosocomial outbreak of multidrug-resistant Acinetobacter baumannii in a critical care center in Japan, 2011-2012.
      Patients from an adult ICU or an emergency room ICUThroat and rectum or stools

      158/412

      OXA-23, OXA-24, OXA-58, OXA-66, OXA-68, and NDM-140Indonesia, 2018
      • Saharman Y.R.
      • Karuniawati A.
      • Sedono R.
      • et al.
      Endemic carbapenem-nonsusceptible Acinetobacter baumannii-calcoaceticus complex in intensive care units of the national referral hospital in Jakarta, Indonesia.
      Patients from a neurological ICU of an adult hospitalUrine, throat, groin, axilla, and rectum12/32
      A proportion of the study population showed clinical evidence of CRAB infection (cases not considered colonization).
      OXA-23, VIM, and IMP24Turkey, 2019
      • Metan G.
      • Zarakolu P.
      • Otlu B.
      • et al.
      Emergence of colistin and carbapenem-resistant Acinetobacter calcoaceticus-Acinetobacter baumannii (CCR-Acb) complex in a neurological intensive care unit followed by successful control of the outbreak.
      Newborns from a neonatal ICURectum17/762OXA-23 and NDM-132Turkey, 2016
      • Karaaslan A.
      • Soysal A.
      • Altinkanat Gelmez G.
      • et al.
      Molecular characterization and risk factors for carbapenem-resistant Gram-negative bacilli colonization in children: emergence of NDM-producing Acinetobacter baumannii in a newborn intensive care unit in Turkey.
      Patients from 32 adult ICUsRectum117/493OXA-23, OXA-24/40, IMP, and GES64Kuwait, 2020
      • Al-Hashem G.
      • Rotimi V.O.
      • Albert M.J.
      Antimicrobial resistance of serial isolates of Acinetobacter baumannii colonizing the rectum of adult intensive care Unit patients in a teaching hospital in Kuwait.
      Patients from a medical and a surgical ICUMouth, rectum, and groin32/83OXA-23, OXA-24, and NDM-1.24Morocco, 2017
      • Uwingabiye J.
      • Lemnouer A.
      • Roca I.
      • et al.
      Clonal diversity and detection of carbapenem resistance encoding genes among multidrug-resistant Acinetobacter baumannii isolates recovered from patients and environment in two intensive care units in a Moroccan hospital.
      Patients from an ICURectum9/63OXA-23 and NDM-112Tunisia, 2018
      • Maamar E.
      • Alonso C.A.
      • Ferjani S.
      • et al.
      NDM-1- and OXA-23-producing Acinetobacter baumannii isolated from intensive care unit patients in Tunisia.
      Environmental surfaces from an ICU, two medical wards and two surgical wards of a general hospital.Wound1/21OXA-69, ISAba1, and GES-114Saudi Arabia, 2020
      • Al-Hamad A.
      • Pal T.
      • Leskafi H.
      • et al.
      Molecular characterization of clinical and environmental carbapenem resistant Acinetobacter baumannii isolates in a hospital of the Eastern Region of Saudi Arabia.
      Patients from 6 adult ICUs (trauma, surgical, medical, and neurosurgical units) of a hospitalRectum and respiratory tract from patients17/25 (respiratory tract

      8/25 (rectum)
      ND20USA, 2016
      • Shimose L.A.
      • Masuda E.
      • Sfeir M.
      • et al.
      Carbapenem-resistant acinetobacter baumannii: concomitant contamination of air and environmental surfaces.
      Mechanically ventilated patients from 30 acute care facilities and 10 LTC facilitiesSputum and perianal region76/358ND2USA, 2012
      • Thom K.A.
      • Maragakis L.L.
      • Richards K.
      • et al.
      Assessing the burden of Acinetobacter baumannii in Maryland: a statewide cross-sectional period prevalence survey.
      Mechanically ventilated patients from an ICURectum and respiratory45/360ND92USA, 2016
      • Munoz-Price L.S.
      • Rosa R.
      • Castro J.G.
      • et al.
      Evaluating the impact of antibiotic exposures as time-dependent variables on the acquisition of carbapenem-resistant Acinetobacter baumannii.
      Liver transplant patients from a tertiary hospitalInguinal-rectal area, axilla, and throat83/181ND8Brazil, 2017
      • Freire M.P.
      • Villela Soares Oshiro I.C.
      • Bonazzi P.R.
      • et al.
      Surveillance culture for multidrug-resistant gram-negative bacteria: performance in liver transplant recipients.
      Mechanically ventilated patients from a medical centerMouth, rectum, and skin32/34ND36Israel, 2016
      • Nutman A.
      • Lerner A.
      • Schwartz D.
      • et al.
      Evaluation of carriage and environmental contamination by carbapenem-resistant Acinetobacter baumannii.
      Adult patients who had a CRAB clinical culture during a prior hospitalizationMouth, rectum, and skin12/38N.D.120Israel, 2019
      • Nutman A.
      • Lerner A.
      • Fallach N.
      • et al.
      Likelihood of persistent carriage of carbapenem-resistant Acinetobacter baumannii on readmission in previously identified carriers.
      Patients from a medical ICUThroat or trachea, skin, and urine98/1115
      A proportion of the study population showed clinical evidence of CRAB infection (cases not considered colonization).
      N.D.176Korea, 2017
      • An J.H.
      • Kim Y.H.
      • Moon J.E.
      • et al.
      Active surveillance for carbapenem-resistant Acinetobacter baumannii in a medical intensive care unit: can it predict and reduce subsequent infections and the use of colistin?.
      Residents from 28 nursing homesRectum, axilla, and nasal fossae92/1408ND8Hong Kong, 2016
      • Cheng V.C.
      • Chen J.H.
      • Ng W.C.
      • et al.
      Emergence of carbapenem-resistant Acinetobacter baumannii in nursing homes with high background rates of MRSA colonization.
      Patients from an ICUNS22/40
      A proportion of the study population showed clinical evidence of CRAB infection (cases not considered colonization).
      N.D.20Taiwan, 2014
      • Liu W.L.
      • Liang H.W.
      • Lee M.F.
      • et al.
      The impact of inadequate terminal disinfection on an outbreak of imipenem-resistant Acinetobacter baumannii in an intensive care unit.
      Patients from two general wards of a general hospitalNS6/12ND24Taiwan, 2017
      • Wang C.H.
      • Li J.F.
      • Huang L.Y.
      • et al.
      Outbreak of imipenem-resistant Acinetobacter baumannii in different wards at a regional hospital related to untrained bedside caregivers.
      Neonate patients from a NICUTrachea257/3,367
      A proportion of the study population showed clinical evidence of CRAB infection (cases not considered colonization).
      N.D.28Thailand, 2020
      • Thatrimontrichai A.
      • Pannaraj P.S.
      • Janjindamai W.
      • et al.
      Intervention to reduce carbapenem-resistant Acinetobacter baumannii in a neonatal intensive care unit.
      Patients with CRAB positive cultures from an adult ICUTracheal aspirate, rectum, sternal skin, and urine129/160ND280Thailand, 2013
      • Apisarnthanarak A.
      • Warren D.K.
      Screening for carbapenem-resistant Acinetobacter baumannii colonization sites: an implication for combination of horizontal and vertical approaches.
      Abbreviations: CCC, critical care center; CCU, coronary care unit; CRAB, carbapenem-resistant A. baumannii; GES: Guiana extended-spectrum-lactamase; ICU, intensive care unit; IMP, imipenem; ISAba, insertion sequence in A. baumannii; LTC, long-term care; MDRO: multidrug-resistant microorganisms; ND, not determined; NDM, New Delhi metallo-beta-lactamase; NICU, neonatal intensive care unit; NIU, neonatal intermediate unit; NS, not specified; OXA, oxacillinase, VIM, Verona integron encoded-metallo-beta-lactamase.
      a A proportion of the study population showed clinical evidence of CRAB infection (cases not considered colonization).
      TABLE 2CRAB contamination reports in the environment of healthcare settings and healthcare workers.
      Population/surface characteristicsSampled sitesCRAB recovery in environmental samples or HCWs (n/N)Associated resistance determinantStudy length (weeks)Country, yearRefs.
      Nurses and environmental surfaces from a spinal cord injury unitNurses' hands

      Sinks, high touch surfaces, ice machine drain, water outlet, ice outlet, ice, and water
      1/15 nurses

      2/10 samples
      OXA-23 and OXA-694USA, 2015
      • Kanwar A.
      • Domitrovic T.N.
      • Koganti S.
      • et al.
      A cold hard menace: a contaminated ice machine as a potential source for transmission of carbapenem-resistant Acinetobacter baumannii.
      Environmental surfaces near patients from an ICU and semi-intensive therapy/care of a tertiary hospitalBed headboard, drug carts, crash carts, ventilator monitors, manifolds, floors, patient call buttons, and telephones2/45OXA-234Italy, 2014
      • Dettori M.
      • Piana A.
      • Deriu M.G.
      • et al.
      Outbreak of multidrug-resistant Acinetobacter baumannii in an intensive care unit.
      Environmental surfaces from an adult ICUNurse gloves, floor, bedrails, bedside tables, Ambu bags, monitors, valves, pumps, door handles, ventilators, stethoscopes, nursing tables, equipment, and medical carts70/886OXA-2336Brazil, 2017
      • Raro O.H.F.
      • Gallo S.W.
      • Ferreira C.A.S.
      • et al.
      Carbapenem-resistant Acinetobacter baumannii contamination in an intensive care unit.
      CCC, ICU, emergency room, operating room, and other wards (NS) of a tertiary care hospitalStainless steel sinks, bedrails, locker handles, stethoscopes, mobile medical carts, mobile carts with a suction bottle, and pulse oximetry17/82OXA-23 and ISAba-140Japan, 2016
      • Ushizawa H.
      • Yahata Y.
      • Endo T.
      • et al.
      A epidemiological investigation of a nosocomial outbreak of multidrug-resistant Acinetobacter baumannii in a critical care center in Japan, 2011-2012.
      Environmental surfaces and HCWs from an ICU of a tertiary care hospitalComputer keyboards, bedrails, nurse supply carts, ventilator panels, ventilator airflow sensors, bedside cabinets, curtains, and mattresses.

      Nurses, doctors, and cleaning staff hands and/or gloves.
      32/1550 samples

      4/15 HCWs
      OXA-23 and ISAba-112 (non-continuous)China, 2015
      • Ye D.
      • Shan J.
      • Huang Y.
      • et al.
      A gloves-associated outbreak of imipenem-resistant Acinetobacter baumannii in an intensive care unit in Guangdong, China.
      Environmental surfaces from an adult ICU or an emergency room ICUWashbasins, bedrails, bedside cabinet tables, ventilators, monitor screens, infusion pumps, and mattresses6/400

      OXA-23, OXA-24, OXA-58, OXA-66, OXA-68, and NDM-140 (non-continuous)Indonesia, 2018
      • Saharman Y.R.
      • Karuniawati A.
      • Sedono R.
      • et al.
      Endemic carbapenem-nonsusceptible Acinetobacter baumannii-calcoaceticus complex in intensive care units of the national referral hospital in Jakarta, Indonesia.
      Environmental surfaces from a medical ICU of a hospitalPhysiological monitor terminals, bedside rails, automatic door buttons, infusion pumps, resuscitation bags, ventilator panels, suction bottles, stethoscopes, tables, and sinks11/233

      OXA-234Singapore, 2018
      • Ng D.H.L.
      • Marimuthu K.
      • Lee J.J.
      • et al.
      Environmental colonization and onward clonal transmission of carbapenem-resistant Acinetobacter baumannii (CRAB) in a medical intensive care unit: the case for environmental hygiene.
      Environmental surfaces near patients infected by A baumannii from trauma, surgery, and neurosurgical ICUsVentilators, bedrails, bedside curtains, monitors, and tables18/22OXA-2348Taiwan, 2013
      • Ho C.M.
      • Ho M.W.
      • Chi C.Y.
      • et al.
      Repeated colonization by multi-drug-resistant Acinetobacter calcoaceticus-A. baumannii complex and changes in antimicrobial susceptibilities in surgical intensive care units.
      Isolates from HCWs and environmental surfaces of ICUs wards (surgery, medical, cardiovascular surgery, and CCU)IV catheters, IV solutions, ventilators, laryngoscopy knives, incubators, taps, sinks, drug containers, monitors, tables, feeding pumps, MVE, intubation tubes, resuscitation equipment, and blood gas devices HCW hands42/233 samples 3/18 HCWsOXA-2368Turkey, 2014
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      Environmental surfaces from a medical and a surgical ICUFloors, bed sheets, medical ventilators, pillows, monitors, patient trolleys, and IV solution stands36/72OXA-23, OXA-24, and NDM-124Morocco, 2017
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      Clonal diversity and detection of carbapenem resistance encoding genes among multidrug-resistant Acinetobacter baumannii isolates recovered from patients and environment in two intensive care units in a Moroccan hospital.
      Environmental surfaces from the ICU, infectious disease, medical, and pediatric wards of 2 teaching hospitalsHandles, bed sheets, medical equipment, and bedrails61/67NDM-1 and OXA-23200Algeria, 2015
      • Zenati K.
      • Touati A.
      • Bakour S.
      • et al.
      Characterization of NDM-1- and OXA-23-producing Acinetobacter baumannii isolates from inanimate surfaces in a hospital environment in Algeria.
      Environmental surfaces from an ICU, two medical wards and two surgical wards of a general hospital.Alcohol dispenser, nurse desk, and computer keyboard3/30OXA-69, ISAba1, and GES-114Saudi Arabia, 2020
      • Al-Hamad A.
      • Pal T.
      • Leskafi H.
      • et al.
      Molecular characterization of clinical and environmental carbapenem resistant Acinetobacter baumannii isolates in a hospital of the Eastern Region of Saudi Arabia.
      Environmental surfaces from 6 adult ICUs (trauma, surgical, medical, and neurosurgical units) of a hospitalBedrails, bedside tables, ventilator panels, IV pumps, and unit air samples758/1690ND20USA, 2016
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      • et al.
      Carbapenem-resistant acinetobacter baumannii: concomitant contamination of air and environmental surfaces.
      Mattresses from an adult ICU, a CCU, and other clinical units (NS)Mattresses19/51ND12Brazil, 2016
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      • dos Santos S.G.
      • Oliveira AC.
      Recovery of resistant bacteria from mattresses of patients under contact precautions.
      Air from two ICUs of a medical centerAir samples24/186ND32Turkey, 2016
      • Yakupogullari Y.
      • Otlu B.
      • Ersoy Y.
      • et al.
      Is airborne transmission of Acinetobacter baumannii possible: a prospective molecular epidemiologic study in a tertiary care hospital.
      Environmental surfaces from two general wards of a general hospitalOxygen humidifiers, bedrails, and table surfaces8/60ND24Taiwan, 2017
      • Wang C.H.
      • Li J.F.
      • Huang L.Y.
      • et al.
      Outbreak of imipenem-resistant Acinetobacter baumannii in different wards at a regional hospital related to untrained bedside caregivers.
      Environmental surfaces from an ICUBedrails, bedside sinks, bedside tables, and monitors12/22ND20Taiwan, 2014
      • Liu W.L.
      • Liang H.W.
      • Lee M.F.
      • et al.
      The impact of inadequate terminal disinfection on an outbreak of imipenem-resistant Acinetobacter baumannii in an intensive care unit.
      Abbreviations: CCC, critical care center; CCU, coronary care unit; CRAB, carbapenem-resistant A. baumannii; GES: Guiana extended-spectrum-lactamase; GNB, Gram-negative bacilli; HCW, healthcare workers; ICU, intensive care unit; ISAba, insertion sequence in A. baumannii; IV, intravenous; LTC, long-term care; MDRO, multidrug-resistant microorganisms; MVE, mechanical ventilator equipment; ND, not determined; NDM, New Delhi metallo-β-lactamase; NS, not specified; OXA, oxacillinase.
      The CRAB contamination rate is higher among hospitalized patients (up to 80% of CRAB detection), as shown by rectal and nasal swab cultures. CRAB recovery from hands and gloves of HCWs, and from skin and mucosa of patients (pharynx, nasal, rectum, groin, axilla, and mouth) has been previously reported.
      • Bedenić B.
      • Beader N.
      • Godič-Torkar K.
      • et al.
      Nursing home as a reservoir of carbapenem-resistant Acinetobacter baumannii.
      ,
      • Cruz-López F.
      • Villarreal-Treviño L.
      • Morfin-Otero R.
      • et al.
      Dynamics of colonization in patients with health care-associated infections at step-down care units from a tertiary care hospital in Mexico.
      Additionally, diverse studies have shown that A. baumannii is one of the most abundant pathogens across workplaces, devices, and floors in hospitals.
      • Liou M.L.
      • Chen K.H.
      • Yeh H.L.
      • et al.
      Persistent nasal carriers of Acinetobacter baumannii in long-term-care facilities.
      ,
      • Tang C.Y.
      • Yiu S.M.
      • Kuo H.Y.
      • et al.
      Application of 16S rRNA metagenomics to analyze bacterial communities at a respiratory care centre in Taiwan.
      Up to 93% of hospital environmental surfaces are contaminated by CRAB.
      • Gao J.
      • Zhao X.
      • Bao Y.
      • et al.
      Antibiotic resistance and OXA-type carbapenemases-encoding genes in airborne Acinetobacter baumannii isolated from burn wards.
      ,
      • Cheng V.C.
      • Chen J.H.
      • Ng W.C.
      • et al.
      Emergence of carbapenem-resistant Acinetobacter baumannii in nursing homes with high background rates of MRSA colonization.
      Hospital environments, medical equipment, and medical devices have been reported as sites contaminated by CRAB, so they are all considered potential reservoirs for this pathogen.
      • Bedenić B.
      • Beader N.
      • Godič-Torkar K.
      • et al.
      Nursing home as a reservoir of carbapenem-resistant Acinetobacter baumannii.
      ,
      • Cruz-López F.
      • Villarreal-Treviño L.
      • Morfin-Otero R.
      • et al.
      Dynamics of colonization in patients with health care-associated infections at step-down care units from a tertiary care hospital in Mexico.
      • Hong K.B.
      • Oh H.S.
      • Song J.S.
      • et al.
      Investigation and control of an outbreak of imipenem-resistant Acinetobacter baumannii Infection in a pediatric intensive care unit.
      • Brigante G.
      • Migliavacca R.
      • Bramati S.
      • et al.
      Emergence and spread of a multidrug-resistant Acinetobacter baumannii clone producing both the carbapenemase OXA-23 and the 16S rRNA methylase ArmA.
      • Gao J.
      • Zhao X.
      • Bao Y.
      • et al.
      Antibiotic resistance and OXA-type carbapenemases-encoding genes in airborne Acinetobacter baumannii isolated from burn wards.
      • Cheng V.C.
      • Chen J.H.
      • Ng W.C.
      • et al.
      Emergence of carbapenem-resistant Acinetobacter baumannii in nursing homes with high background rates of MRSA colonization.
      CRAB isolates have also been recovered from bed headboard, monitor screens, bedrails, bedside tables, infusion pumps, medical ventilators, bed sheets, pillows, sinks, floors, and another high touch contact nosocomial environmental spots (Table 2).
      • Cruz-López F.
      • Villarreal-Treviño L.
      • Morfin-Otero R.
      • et al.
      Dynamics of colonization in patients with health care-associated infections at step-down care units from a tertiary care hospital in Mexico.
      ,
      • Hong K.B.
      • Oh H.S.
      • Song J.S.
      • et al.
      Investigation and control of an outbreak of imipenem-resistant Acinetobacter baumannii Infection in a pediatric intensive care unit.
      ,
      • Gao J.
      • Zhao X.
      • Bao Y.
      • et al.
      Antibiotic resistance and OXA-type carbapenemases-encoding genes in airborne Acinetobacter baumannii isolated from burn wards.
      Transient presence of CRAB has been found to last from 6 days to 5 weeks in patients and on environmental surfaces, which could represent a risk for HAI development and/or contamination to other patients, HCWs, and other hospital areas.
      • Maamar E.
      • Alonso C.A.
      • Ferjani S.
      • et al.
      NDM-1- and OXA-23-producing Acinetobacter baumannii isolated from intensive care unit patients in Tunisia.
      ,
      • Tsiatsiou O.
      • Iosifidis Ε.
      • Katragkou A.
      • et al.
      Successful management of an outbreak due to carbapenem-resistant Acinetobacter baumannii in a neonatal intensive care unit.

      Measures for preventing or reducing colonization by A. baumannii in healthcare settings

      Different strategies to reduce A. baumannii infections have been described, including the implementation of antimicrobial stewardship programs. In a study by Cheon et al. nosocomial MDR A. baumannii was reduced 10-fold after decreasing carbapenem use.
      • Cheon S.
      • Kim M.J.
      • Yun S.J.
      • et al.
      Controlling endemic multidrug-resistant Acinetobacter baumannii in intensive care units using antimicrobial stewardship and infection control.
      Thus, a coordinated effort between healthcare facilities authorities, HCWs, and laboratory surveillance programs is needed to reduce CRAB's impact.
      Diverse protocols have been applied as preventive measures for the presence of antimicrobial-resistant microorganisms, including CRAB. Among them, active surveillance cultures (ASCs) have been used to identify and monitor contamination in patients, HCWs
      • An J.H.
      • Kim Y.H.
      • Moon J.E.
      • et al.
      Active surveillance for carbapenem-resistant Acinetobacter baumannii in a medical intensive care unit: can it predict and reduce subsequent infections and the use of colistin?.
      ,
      • Thatrimontrichai A.
      • Apisarnthanarak A.
      Active surveillance culture program in asymptomatic patients as a strategy to control multidrug-resistant gram-negative organisms: what should be considered?.
      and environmental sites.
      • Hong K.B.
      • Oh H.S.
      • Song J.S.
      • et al.
      Investigation and control of an outbreak of imipenem-resistant Acinetobacter baumannii Infection in a pediatric intensive care unit.
      ,
      • Gao J.
      • Zhao X.
      • Bao Y.
      • et al.
      Antibiotic resistance and OXA-type carbapenemases-encoding genes in airborne Acinetobacter baumannii isolated from burn wards.
      ,
      • Nutman A.
      • Lerner A.
      • Schwartz D.
      • et al.
      Evaluation of carriage and environmental contamination by carbapenem-resistant Acinetobacter baumannii.
      • Ho C.M.
      • Ho M.W.
      • Chi C.Y.
      • et al.
      Repeated colonization by multi-drug-resistant Acinetobacter calcoaceticus-A. baumannii complex and changes in antimicrobial susceptibilities in surgical intensive care units.
      • Rosa R.
      • Arheart K.L.
      • Depascale D.
      • et al.
      Environmental exposure to carbapenem-resistant Acinetobacter baumannii as a risk factor for patient acquisition of A. baumannii.
      Different conditions can be used for ASCs. For example, culture media used and sampling sites can be standardized to improve infection control or spread prevention. Additionally, the utility of ASCs for carriage detection should be determined for specific processes, such as during patient admission or ward transference. Other aspects to consider for ASCs include sampling frequency, patients with medical devices and catheters, HCW monitoring frequency, and the subjects that should be included in the surveillance.
      • Hong K.B.
      • Oh H.S.
      • Song J.S.
      • et al.
      Investigation and control of an outbreak of imipenem-resistant Acinetobacter baumannii Infection in a pediatric intensive care unit.
      ,
      • Gao J.
      • Zhao X.
      • Bao Y.
      • et al.
      Antibiotic resistance and OXA-type carbapenemases-encoding genes in airborne Acinetobacter baumannii isolated from burn wards.
      ,
      • Thom K.A.
      • Maragakis L.L.
      • Richards K.
      • et al.
      Assessing the burden of Acinetobacter baumannii in Maryland: a statewide cross-sectional period prevalence survey.
      • Wang C.H.
      • Li J.F.
      • Huang L.Y.
      • et al.
      Outbreak of imipenem-resistant Acinetobacter baumannii in different wards at a regional hospital related to untrained bedside caregivers.
      • Apisarnthanarak A.
      • Warren D.K.
      Screening for carbapenem-resistant Acinetobacter baumannii colonization sites: an implication for combination of horizontal and vertical approaches.
      • Ye D.
      • Shan J.
      • Huang Y.
      • et al.
      A gloves-associated outbreak of imipenem-resistant Acinetobacter baumannii in an intensive care unit in Guangdong, China.
      • Ho C.M.
      • Ho M.W.
      • Chi C.Y.
      • et al.
      Repeated colonization by multi-drug-resistant Acinetobacter calcoaceticus-A. baumannii complex and changes in antimicrobial susceptibilities in surgical intensive care units.
      • Rosa R.
      • Arheart K.L.
      • Depascale D.
      • et al.
      Environmental exposure to carbapenem-resistant Acinetobacter baumannii as a risk factor for patient acquisition of A. baumannii.
      • Lim C.J.
      • Cheng A.C.
      • Kennon J.
      • et al.
      Prevalence of multidrug-resistant organisms and risk factors for carriage in long-term care facilities: a nested case-control study.
      • Roy S.
      • Viswanathan R.
      • Singh A.
      • et al.
      Gut colonization by multidrug-resistant and carbapenem-resistant Acinetobacter baumannii in neonates.
      ASCs, contact precautions, and preventive isolation can be applied to avoid pathogen dissemination from patients colonized with CRAB.
      • Perencevich E.N.
      • Fisman D.N.
      • Lipsitch M.
      • et al.
      Projected benefits of active surveillance for vancomycin-resistant enterococci in intensive care units.
      Nevertheless, the success of these methods strongly depends on the cohort and the adherence to precautions.
      • An J.H.
      • Kim Y.H.
      • Moon J.E.
      • et al.
      Active surveillance for carbapenem-resistant Acinetobacter baumannii in a medical intensive care unit: can it predict and reduce subsequent infections and the use of colistin?.
      ,
      • Choi W.S.
      • Kim S.H.
      • Jeon E.G.
      • et al.
      Nosocomial outbreak of carbapenem-resistant Acinetobacter baumannii in intensive care units and successful outbreak control program.
      Prevention measures for dissemination of antimicrobial-resistant pathogens include cleaning techniques for environmental surfaces and antiseptic baths. The effectiveness of cleaning techniques is associated with diverse aspects, including disinfectant products (chlorhexidine, chlorine solution, aerosolized hydrogen peroxide (aHP), etc.), concentration, and action time.
      • Robustillo-Rodela A.
      • Pérez-Blanco V.
      • Espinel Ruiz M.A.
      • et al.
      Successful control of 2 simultaneous outbreaks of OXA-48 carbapenemase-producing Enterobacteriaceae and multidrug-resistant Acinetobacter baumannii in an intensive care unit.
      • Lerner A.O.
      • Abu-Hanna J.
      • Carmeli Y.
      • et al.
      Environmental contamination by carbapenem-resistant Acinetobacter baumannii: the effects of room type and cleaning methods.
      • Fan C.Y.
      • Lee W.T.
      • Hsu T.C.
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      Effect of chlorhexidine bathing on colonization or infection with Acinetobacter baumannii: a systematic review and meta-analysis.
      • Mendoza-Olazarán S.
      • Camacho-Ortiz A.
      • Martínez-Reséndez M.F.
      • et al.
      Influence of whole-body washing of critically ill patients with chlorhexidine on Acinetobacter baumannii isolates.
      • Lai N.M.
      • Lai N.A.
      • O’Riordan E.
      • et al.
      Skin antisepsis for reducing central venous catheter-related infections.
      An 85% reduction of CRAB contamination was observed after sodium hypochlorite disinfection (24/59 sampled objects were contaminated before disinfection with sodium hypochlorite, and contamination persisted in 3/52 sampled objects after disinfection process); and a 78% reduction after aHP disinfection (59/74 sampled objects were contaminated before disinfection, and 12/68 objects remained contaminated after disinfection).
      • Lerner A.O.
      • Abu-Hanna J.
      • Carmeli Y.
      • et al.
      Environmental contamination by carbapenem-resistant Acinetobacter baumannii: the effects of room type and cleaning methods.
      Daily chlorhexidine baths reduced CRAB acquisition rates by 52% at the ICU (44 cases per 1000 at-risk patient days before chlorhexidine baths and 21.2 cases per 1000 at-risk patient-days after baths introduction, p < 0.001).
      • Chung Y.K.
      • Kim J.S.
      • Lee S.S.
      • et al.
      Effect of daily chlorhexidine bathing on acquisition of carbapenem-resistant Acinetobacter baumannii (CRAB) in the medical intensive care unit with CRAB endemicity.
      It has been suggested that cleaning does not reduce the contamination rates in environments, possibly by insufficient frequency of disinfection; however, favorable results are obtained by training HCWs and cleaning staff.
      • Lerner A.O.
      • Abu-Hanna J.
      • Carmeli Y.
      • et al.
      Environmental contamination by carbapenem-resistant Acinetobacter baumannii: the effects of room type and cleaning methods.
      ,
      • Lerner A.O.
      • Abu-Hanna J.
      • Carmeli Y.
      • et al.
      Environmental contamination by carbapenem-resistant Acinetobacter baumannii: the effects of room type and cleaning methods.
      ,
      • Muscarella L.F.
      Risk of transmission of carbapenem-resistant Enterobacteriaceae and related “superbugs” during gastrointestinal endoscopy.
      A study reported a significant reduction (p < 0.0001) of CRAB recovery from environmental objects after a training of intensive cleaning manual procedure with sodium hypochlorite. Before training, 78% of sampled objects (62/82) were contaminated by CRAB, while 39% of sampled objects were contaminated (75/191) after training.
      • Lerner A.O.
      • Abu-Hanna J.
      • Carmeli Y.
      • et al.
      Environmental contamination by carbapenem-resistant Acinetobacter baumannii: the effects of room type and cleaning methods.
      Effective actions for control of dissemination and development of infections by CRAB have been reported, including the assignment of specific units or beds for CRAB-colonized patients, closure of contaminated units, contact precautions, environmental contamination surveillance, environmental disinfection, and evaluation of hygiene protocol adherence.
      • Choi W.S.
      • Kim S.H.
      • Jeon E.G.
      • et al.
      Nosocomial outbreak of carbapenem-resistant Acinetobacter baumannii in intensive care units and successful outbreak control program.
      ,
      • Ben-Chetrit E.
      • Wiener-Well Y.
      • Lesho E.
      • et al.
      An intervention to control an ICU outbreak of carbapenem-resistant Acinetobacter baumannii: long-term impact for the ICU and hospital.

      Centers for Disease Control and Prevention. Management of multidrug-resistant organisms in healthcare settings. 2015. Available at: https://www.cdc.gov/infectioncontrol/guidelines/mdro/prevention-control.html. Accessed August 20, 2020.

      • Cho O.H.
      • Bak M.H.
      • Baek E.H.
      • et al.
      Successful control of carbapenem-resistant Acinetobacter baumannii in a Korean university hospital: a 6-year perspective.
      • Apisarnthanarak A.
      • Pinitchai U.
      • Thongphubeth K.
      • et al.
      A multifaceted intervention to reduce pandrug-resistant Acinetobacter baumannii colonization and infection in 3 intensive care units in a Thai tertiary care center: a 3-year study.
      Apisarnthanarak et el reported the effectiveness of an intervention strategy on ICU included: strict contact isolation of patients colonized or infected by pandrug-resistant A. baumannii (including carbapenem resistance), ASCs (rectal swabs and tracheal aspirates), hand hygiene adherence, environmental disinfection with sodium hypochlorite, and antimicrobial stewardship program previously established for carbapenem, third-generation cephalosporins, β-lactam inhibitors, and glycopeptides. In the study, the rate of colonization/infection by pandrug-resistant A. baumannii was 3.6 cases per 1000 patient-days before intervention and 1.2 cases per 1000 patient-days after intervention (p < 0.001).
      • Apisarnthanarak A.
      • Pinitchai U.
      • Thongphubeth K.
      • et al.
      A multifaceted intervention to reduce pandrug-resistant Acinetobacter baumannii colonization and infection in 3 intensive care units in a Thai tertiary care center: a 3-year study.

      Conclusions

      Several studies have suggested the potential role of the healthcare environments as CRAB reservoirs and the probable dissemination of this and other MDR pathogens by HCWs and patients. The presence of microorganisms in corporal surfaces is considered a preceding step for HAI development; thus, eradicating environmental reservoirs could break transmission routes and control infection development. However, CRAB contamination rates in the environment and/or among HCWs is probably higher than originally thought because the search for reservoirs has not been routinely established. Reinforced measures are necessary to prevent nosocomial environment contamination by CRAB. These measures should be based on the knowledge of favorable conditions for this pathogen, the material of colonized surfaces, and hygiene and disinfection protocols. Education for HCWs should not be limited to disinfection techniques but also the knowledge of the role of surfaces and objects as reservoirs for pathogens and their contribution to dissemination in the hospital environment.

      Source of funding

      The present investigation has not received specific grants from agencies of the public sector, commercial sector, or non-profit entities

      CRediT authorship contribution statement

      Flora Cruz-López: Conceptualization, Formal analysis, Data curation, Writing – original draft. Adrián Martínez-Meléndez: Conceptualization, Data curation, Writing – original draft. Licet Villarreal-Treviño: Writing – review & editing. Rayo Morfín-Otero: Writing – review & editing. Héctor Maldonado-Garza: Writing – review & editing. Elvira Garza-González: Writing – review & editing.

      Conflicts of Interest

      The authors report no conflicts of interest.

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