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Semin Respir Crit Care Med 2019; 40(04): 558-568
DOI: 10.1055/s-0039-1696980
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Controlling the Diffusion of Multidrug-Resistant Organisms in Intensive Care Units

Solen Kernéis
1   Faculté de médecine, Université de Paris, Sorbonne Paris cité, Paris, France
2   Assistance Publique Hôpitaux de Paris, Hôpitaux Universitaires Paris Centre-Site Cochin, Antimicrobial Stewardship Team, Paris, France
3   Pharmacoepidemiology and Infectious Diseases, Institut Pasteur, Paris, France
,
Jean-Christophe Lucet
4   Université de Paris, IAME, INSERM, F-75018 Paris, France
5   Assistance Publique Hôpitaux de Paris, Infection Control Unit, Hôpital Bichat, F-75018 Paris, France
› Author Affiliations
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Publication History

Publication Date:
04 October 2019 (online)

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Abstract

The prevalence of multidrug-resistant organisms (MDROs) in intensive care units (ICUs) is increasing worldwide, with very large variations across countries, microorganisms, and settings. Emerging MDR gram-negative bacteria and fungi raise particular concerns that require improved prevention and control strategies. Vertical approaches are mainly based on screening and contact precautions and/or decolonization of MDRO carriers. On the other hand, horizontal strategies are not pathogen-specific and include standard precautions (i.e., hand hygiene), universal decolonization, antimicrobial stewardship, and environmental cleaning. The impacts of the different strategies vary between MDROs and compliance with control measures, and are intermixed in most infection control programs. Based on historical data, hand hygiene remains the cornerstone to prevent transmission of MDROs in ICUs. In the context of high hand hygiene compliance, screening and contact precautions for carriers seem to have a limited additional effect, particularly for MDR gram-negative bacteria. Studies on skin decolonization with chlorhexidine bathing show conflicting results, impairing its widespread adoption. Selective oral and digestive decontaminations have shown positive impact on clinical outcomes in ICUs with low levels of antibiotic resistance, but raised ecological concerns in high-prevalence settings. Antibiotic stewardship programs have been associated with reductions in antimicrobial use, duration of stay, and costs with no negative impact on mortality and should be widely promoted in ICUs. Whatever the strategy, compliance with the recommended measures is of crucial importance and implementation should rely on behavioral approach and change in the institutional and safety culture.

Keywords

multidrug-resistant organisms - intensive care units - infection control
 

  • References

  • 1 Woerther P-L, Lepeule R, Burdet C, Decousser J-W, Ruppé É, Barbier F. Carbapenems and alternative β-lactams for the treatment of infections due to extended-spectrum β-lactamase-producing Enterobacteriaceae: what impact on intestinal colonisation resistance?. Int J Antimicrob Agents 2018; 52 (06) 762-770
    CrossrefPubMedGoogle Scholar
  • 2 Armand-Lefèvre L, Angebault C, Barbier F. , et al. Emergence of imipenem-resistant gram-negative bacilli in intestinal flora of intensive care patients. Antimicrob Agents Chemother 2013; 57 (03) 1488-1495
    CrossrefPubMedGoogle Scholar
  • 3 Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 2013; 13 (11) 790-801
    CrossrefPubMedGoogle Scholar
  • 4 Ruppé É, Lisboa T, Barbier F. The gut microbiota of critically ill patients: first steps in an unexplored world. Intensive Care Med 2018; 44 (09) 1561-1564
    CrossrefPubMedGoogle Scholar
  • 5 Magiorakos A-P, 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 (03) 268-281
    CrossrefPubMedGoogle Scholar
  • 6 Lynch III JP, Zhanel GG, Clark NM. Infections due to Acinetobacter baumannii in the ICU: treatment options. Semin Respir Crit Care Med 2017; 38 (03) 311-325
    Article in Thieme ConnectPubMedGoogle Scholar
  • 7 European Centre for Disease Prevention and Control. Surveillance of antimicrobial resistance in Europe 2017. 2018 . Available at: http://ecdc.europa.eu/en/publications-data/surveillance-antimicrobial-resistance-europe-2017 . Accessed June 15, 2019
    PubMed
  • 8 Weiner LM, Webb AK, Limbago B. , et al. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2011–2014. Infect Control Hosp Epidemiol 2016; 37 (11) 1288-1301
    CrossrefPubMedGoogle Scholar
  • 9 Rosenthal VD, Al-Abdely HM, El-Kholy AA. , et al; Remaining authors. International Nosocomial Infection Control Consortium report, data summary of 50 countries for 2010-2015: device-associated module. Am J Infect Control 2016; 44 (12) 1495-1504
    CrossrefPubMedGoogle Scholar
  • 10 Tacconelli E, Cataldo MA, Dancer SJ. , et al; European Society of Clinical Microbiology. ESCMID guidelines for the management of the infection control measures to reduce transmission of multidrug-resistant Gram-negative bacteria in hospitalized patients. Clin Microbiol Infect 2014; 20 (Suppl. 01) 1-55
    CrossrefPubMedGoogle Scholar
  • 11 Livorsi DJ, Chorazy ML, Schweizer ML. , et al. A systematic review of the epidemiology of carbapenem-resistant Enterobacteriaceae in the United States. Antimicrob Resist Infect Control 2018; 7: 55
    CrossrefPubMedGoogle Scholar
  • 12 Lin MY, Lyles-Banks RD, Lolans K. , et al; Centers for Disease Control and Prevention Epicenters Program. The importance of long-term acute care hospitals in the regional epidemiology of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae. Clin Infect Dis 2013; 57 (09) 1246-1252
    CrossrefPubMedGoogle Scholar
  • 13 Won SY, Munoz-Price LS, Lolans K, Hota B, Weinstein RA, Hayden MK. ; Centers for Disease Control and Prevention Epicenter Program. Emergence and rapid regional spread of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae. Clin Infect Dis 2011; 53 (06) 532-540
    CrossrefPubMedGoogle Scholar
  • 14 Albiger B, Glasner C, Struelens MJ, Grundmann H, Monnet DL. ; European Survey of Carbapenemase-Producing Enterobacteriaceae (EuSCAPE) working group. Carbapenemase-producing Enterobacteriaceae in Europe: assessment by national experts from 38 countries, May 2015. Euro Surveill 2015 20. (45): doi:10.2807/1560-7917.ES.2015.20.45.30062
    PubMedGoogle Scholar
  • 15 Rojas LJ, Salim M, Cober E. , et al; Antibacterial Resistance Leadership Group. Colistin resistance in carbapenem-resistant Klebsiella pneumoniae: laboratory detection and impact on mortality. Clin Infect Dis 2017; 64 (06) 711-718
    PubMedGoogle Scholar
  • 16 Ziakas PD, Thapa R, Rice LB, Mylonakis E. Trends and significance of VRE colonization in the ICU: a meta-analysis of published studies. PLoS One 2013; 8 (09) e75658
    CrossrefPubMedGoogle Scholar
  • 17 Arendrup MC, Patterson TF. Multidrug-resistant Candida: epidemiology, molecular mechanisms, and treatment. J Infect Dis 2017; 216 (suppl_3): S445-S451
    CrossrefPubMedGoogle Scholar
  • 18 Jeffery-Smith A, Taori SK, Schelenz S. , et al; Candida auris Incident Management Team. Candida auris: a review of the literature. Clin Microbiol Rev 2017; 31 (01) e00029-17
    CrossrefPubMedGoogle Scholar
  • 19 Bougnoux M-E, Brun S, Zahar J-R. Healthcare-associated fungal outbreaks: new and uncommon species, new molecular tools for investigation and prevention. Antimicrob Resist Infect Control 2018; 7: 45
    CrossrefPubMedGoogle Scholar
  • 20 Eyre DW, Sheppard AE, Madder H. , et al. A Candida auris outbreak and its control in an intensive care setting. N Engl J Med 2018; 379 (14) 1322-1331
    CrossrefPubMedGoogle Scholar
  • 21 Chow NA, Gade L, Tsay SV. , et al; US Candida auris Investigation Team. Multiple introductions and subsequent transmission of multidrug-resistant Candida auris in the USA: a molecular epidemiological survey. Lancet Infect Dis 2018; 18 (12) 1377-1384
    CrossrefPubMedGoogle Scholar
  • 22 Vincent J-L, Rello J, Marshall J. , et al; EPIC II Group of Investigators. International study of the prevalence and outcomes of infection in intensive care units. JAMA 2009; 302 (21) 2323-2329
    CrossrefPubMedGoogle Scholar
  • 23 Weiner LM, Fridkin SK, Aponte-Torres Z. , et al. Vital signs: preventing antibiotic-resistant infections in hospitals - United States, 2014. MMWR Morb Mortal Wkly Rep 2016; 65 (09) 235-241
    CrossrefPubMedGoogle Scholar
  • 24 Shorr AF. Review of studies of the impact on Gram-negative bacterial resistance on outcomes in the intensive care unit. Crit Care Med 2009; 37 (04) 1463-1469
    CrossrefPubMedGoogle Scholar
  • 25 Barbier F, Pommier C, Essaied W. , et al; OUTCOMEREA Study Group. Colonization and infection with extended-spectrum β-lactamase-producing Enterobacteriaceae in ICU patients: what impact on outcomes and carbapenem exposure?. J Antimicrob Chemother 2016; 71 (04) 1088-1097
    CrossrefPubMedGoogle Scholar
  • 26 Ajao AO, Harris AD, Roghmann M-C. , et al. Systematic review of measurement and adjustment for colonization pressure in studies of methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci, and Clostridium difficile acquisition. Infect Control Hosp Epidemiol 2011; 32 (05) 481-489
    CrossrefPubMedGoogle Scholar
  • 27 Lucet J-C, Paoletti X, Lolom I. , et al. Successful long-term program for controlling methicillin-resistant Staphylococcus aureus in intensive care units. Intensive Care Med 2005; 31 (08) 1051-1057
    CrossrefPubMedGoogle Scholar
  • 28 Kaier K, Meyer E, Dettenkofer M, Frank U. Epidemiology meets econometrics: using time-series analysis to observe the impact of bed occupancy rates on the spread of multidrug-resistant bacteria. J Hosp Infect 2010; 76 (02) 108-113
    CrossrefPubMedGoogle Scholar
  • 29 Septimus E, Weinstein RA, Perl TM, Goldmann DA, Yokoe DS. Approaches for preventing healthcare-associated infections: go long or go wide?. Infect Control Hosp Epidemiol 2014; 35 (07) 797-801
    CrossrefPubMedGoogle Scholar
  • 30 Landelle C, Marimuthu K, Harbarth S. Infection control measures to decrease the burden of antimicrobial resistance in the critical care setting. Curr Opin Crit Care 2014; 20 (05) 499-506
    CrossrefPubMedGoogle Scholar
  • 31 Pittet D, Hugonnet S, Harbarth S. , et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Infection Control Programme. Lancet 2000; 356 (9238): 1307-1312
    CrossrefPubMedGoogle Scholar
  • 32 WHO. WHO guidelines on hand hygiene in health care. Available at: https://www.who.int/gpsc/5may/tools/9789241597906/en/ . Available June 18, 2019
    PubMed
  • 33 Gould DJ, Moralejo D, Drey N, Chudleigh JH, Taljaard M. Interventions to improve hand hygiene compliance in patient care. Cochrane Database Syst Rev 2017; 9: CD005186
    CrossrefPubMedGoogle Scholar
  • 34 Derde LPG, Cooper BS, Goossens H. , et al; MOSAR WP3 Study Team. Interventions to reduce colonisation and transmission of antimicrobial-resistant bacteria in intensive care units: an interrupted time series study and cluster randomised trial. Lancet Infect Dis 2014; 14 (01) 31-39
    CrossrefPubMedGoogle Scholar
  • 35 von Lengerke T, Ebadi E, Schock B. , et al. Impact of psychologically tailored hand hygiene interventions on nosocomial infections with multidrug-resistant organisms: results of the cluster-randomized controlled trial PSYGIENE. Antimicrob Resist Infect Control 2019; 8: 56
    CrossrefPubMedGoogle Scholar
  • 36 Teltsch DY, Hanley J, Loo V, Goldberg P, Gursahaney A, Buckeridge DL. Infection acquisition following intensive care unit room privatization. Arch Intern Med 2011; 171 (01) 32-38
    PubMedGoogle Scholar
  • 37 Kluytmans van den Bergh MFQ, Bruijning Verhagen PCJ, Vandenbroucke Grauls CMJE. , et al. Contact precautions in single-bed or multiple-bed rooms for patients with extended-spectrum beta-lactamase-producing Enterobacteriaceae in Dutch hospitals: a cluster-randomised, crossover, non-inferiority study. Lancet Infect Dis 2019 . doi: 10.1016/S1473-3099(19)30262-2. [Epub ahead of print]
    PubMedGoogle Scholar
  • 38 Mitchell BG, Dancer SJ, Anderson M, Dehn E. Risk of organism acquisition from prior room occupants: a systematic review and meta-analysis. J Hosp Infect 2015; 91 (03) 211-217
    CrossrefPubMedGoogle Scholar
  • 39 Magiorakos AP, Burns K, Rodríguez Baño J. , et al. Infection prevention and control measures and tools for the prevention of entry of carbapenem-resistant Enterobacteriaceae into healthcare settings: guidance from the European Centre for Disease Prevention and Control. Antimicrob Resist Infect Control 2017; 6: 113
    CrossrefPubMedGoogle Scholar
  • 40 Harris AD, Pineles L, Belton B. , et al; Benefits of Universal Glove and Gown (BUGG) Investigators. Universal glove and gown use and acquisition of antibiotic-resistant bacteria in the ICU: a randomized trial. JAMA 2013; 310 (15) 1571-1580
    PubMedGoogle Scholar
  • 41 Huskins WC, Huckabee CM, O'Grady NP. , et al; STAR*ICU Trial Investigators. Intervention to reduce transmission of resistant bacteria in intensive care. N Engl J Med 2011; 364 (15) 1407-1418
    CrossrefPubMedGoogle Scholar
  • 42 Jain R, Kralovic SM, Evans ME. , et al. Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections. N Engl J Med 2011; 364 (15) 1419-1430
    CrossrefPubMedGoogle Scholar
  • 43 Hayden MK, Lin MY, Lolans K. , et al; Centers for Disease Control and Prevention Epicenters Program. Prevention of colonization and infection by Klebsiella pneumoniae carbapenemase-producing enterobacteriaceae in long-term acute-care hospitals. Clin Infect Dis 2015; 60 (08) 1153-1161
    CrossrefPubMedGoogle Scholar
  • 44 Climo MW, Yokoe DS, Warren DK. , et al. Effect of daily chlorhexidine bathing on hospital-acquired infection. N Engl J Med 2013; 368 (06) 533-542
    CrossrefPubMedGoogle Scholar
  • 45 Huang SS, Septimus E, Kleinman K. , et al; CDC Prevention Epicenters Program; AHRQ DECIDE Network and Healthcare-Associated Infections Program. Targeted versus universal decolonization to prevent ICU infection. N Engl J Med 2013; 368 (24) 2255-2265
    CrossrefPubMedGoogle Scholar
  • 46 Noto MJ, Domenico HJ, Byrne DW. , et al. Chlorhexidine bathing and health care-associated infections: a randomized clinical trial. JAMA 2015; 313 (04) 369-378
    CrossrefPubMedGoogle Scholar
  • 47 Frost SA, Alogso M-C, Metcalfe L. , et al. Chlorhexidine bathing and health care-associated infections among adult intensive care patients: a systematic review and meta-analysis. Crit Care 2016; 20 (01) 379
    CrossrefPubMedGoogle Scholar
  • 48 Afonso E, Blot K, Blot S. Prevention of hospital-acquired bloodstream infections through chlorhexidine gluconate-impregnated washcloth bathing in intensive care units: a systematic review and meta-analysis of randomised crossover trials. Euro Surveill 2016; 21 (46) 30400
    PubMedGoogle Scholar
  • 49 Frost SA, Hou YC, Lombardo L. , et al. Evidence for the effectiveness of chlorhexidine bathing and health care-associated infections among adult intensive care patients: a trial sequential meta-analysis. BMC Infect Dis 2018; 18 (01) 679
    CrossrefPubMedGoogle Scholar
  • 50 Pittet D, Angus DC. Daily chlorhexidine bathing for critically ill patients: a note of caution. JAMA 2015; 313 (04) 365-366
    CrossrefPubMedGoogle Scholar
  • 51 de Smet AMGA, Kluytmans JA, Cooper BS. , et al. Decontamination of the digestive tract and oropharynx in ICU patients. N Engl J Med 2009; 360 (01) 20-31
    CrossrefPubMedGoogle Scholar
  • 52 de Jonge E, Schultz MJ, Spanjaard L. , et al. Effects of selective decontamination of digestive tract on mortality and acquisition of resistant bacteria in intensive care: a randomised controlled trial. Lancet 2003; 362 (9389): 1011-1016
    CrossrefPubMedGoogle Scholar
  • 53 Krueger WA, Lenhart F-P, Neeser G. , et al. Influence of combined intravenous and topical antibiotic prophylaxis on the incidence of infections, organ dysfunctions, and mortality in critically ill surgical patients: a prospective, stratified, randomized, double-blind, placebo-controlled clinical trial. Am J Respir Crit Care Med 2002; 166 (08) 1029-1037
    CrossrefPubMedGoogle Scholar
  • 54 Oostdijk EAN, Kesecioglu J, Schultz MJ. , et al. Effects of decontamination of the oropharynx and intestinal tract on antibiotic resistance in ICUs: a randomized clinical trial. JAMA 2014; 312 (14) 1429-1437
    CrossrefPubMedGoogle Scholar
  • 55 Plantinga NL, de Smet AMGA, Oostdijk EAN. , et al. Selective digestive and oropharyngeal decontamination in medical and surgical ICU patients: individual patient data meta-analysis. Clin Microbiol Infect 2018; 24 (05) 505-513
    CrossrefPubMedGoogle Scholar
  • 56 Timsit J-F, Bassetti M. Antipathy against SDD is justified: yes. Intensive Care Med 2018; 44 (07) 1165-1168
    CrossrefPubMedGoogle Scholar
  • 57 Wittekamp BH, Plantinga NL, Cooper BS. , et al. Decontamination strategies and bloodstream infections with antibiotic-resistant microorganisms in ventilated patients: a randomized clinical trial. JAMA 2018; 320 (20) 2087-2098
    CrossrefPubMedGoogle Scholar
  • 58 Halaby T, Al Naiemi N, Kluytmans J, van der Palen J, Vandenbroucke-Grauls CMJE. Emergence of colistin resistance in Enterobacteriaceae after the introduction of selective digestive tract decontamination in an intensive care unit. Antimicrob Agents Chemother 2013; 57 (07) 3224-3229
    CrossrefPubMedGoogle Scholar
  • 59 Lübbert C, Faucheux S, Becker-Rux D. , et al. Rapid emergence of secondary resistance to gentamicin and colistin following selective digestive decontamination in patients with KPC-2-producing Klebsiella pneumoniae: a single-centre experience. Int J Antimicrob Agents 2013; 42 (06) 565-570
    CrossrefPubMedGoogle Scholar
  • 60 Daneman N, Sarwar S, Fowler RA, Cuthbertson BH. ; SuDDICU Canadian Study Group. Effect of selective decontamination on antimicrobial resistance in intensive care units: a systematic review and meta-analysis. Lancet Infect Dis 2013; 13 (04) 328-341
    CrossrefPubMedGoogle Scholar
  • 61 Tacconelli E, Mazzaferri F, Marie de Smet AM. , et al. ESCMID-EUCIC clinical guidelines on decolonization of multidrug-resistant Gram-negative bacteria carriers. Clin Microbiol Infect 2019; 25 (07) 807-817
    CrossrefPubMedGoogle Scholar
  • 62 Huttner B, Haustein T, Uçkay I. , et al. Decolonization of intestinal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae with oral colistin and neomycin: a randomized, double-blind, placebo-controlled trial. J Antimicrob Chemother 2013; 68 (10) 2375-2382
    PubMedGoogle Scholar
  • 63 Dinh A, Fessi H, Duran C. , et al. Clearance of carbapenem-resistant Enterobacteriaceae vs vancomycin-resistant enterococci carriage after faecal microbiota transplant: a prospective comparative study. J Hosp Infect 2018; 99 (04) 481-486
    CrossrefPubMedGoogle Scholar
  • 64 Bilinski J, Grzesiowski P, Sorensen N. , et al. Fecal microbiota transplantation in patients with blood disorders inhibits gut colonization with antibiotic-resistant bacteria: results of a prospective, single-center study. Clin Infect Dis 2017; 65 (03) 364-370
    CrossrefPubMedGoogle Scholar
  • 65 Huttner BD, de Lastours V, Wassenberg M. , et al; R-Gnosis WP3 study group. A 5-day course of oral antibiotics followed by faecal transplantation to eradicate carriage of multidrug-resistant Enterobacteriaceae: a randomized clinical trial. Clin Microbiol Infect 2019; 25 (07) 830-838
    CrossrefPubMedGoogle Scholar
  • 66 Nseir S, Blazejewski C, Lubret R, Wallet F, Courcol R, Durocher A. Risk of acquiring multidrug-resistant Gram-negative bacilli from prior room occupants in the intensive care unit. Clin Microbiol Infect 2011; 17 (08) 1201-1208
    CrossrefPubMedGoogle Scholar
  • 67 Boyce JM. New approaches to decontamination of rooms after patients are discharged. Infect Control Hosp Epidemiol 2009; 30 (06) 515-517
    CrossrefPubMedGoogle Scholar
  • 68 Mitchell BG, Hall L, White N. , et al. An environmental cleaning bundle and health-care-associated infections in hospitals (REACH): a multicentre, randomised trial. Lancet Infect Dis 2019; 19 (04) 410-418
    CrossrefPubMedGoogle Scholar
  • 69 Passaretti CL, Otter JA, Reich NG. , et al. An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms. Clin Infect Dis 2013; 56 (01) 27-35
    CrossrefPubMedGoogle Scholar
  • 70 Anderson DJ, Chen LF, Weber DJ. , et al; CDC Prevention Epicenters Program. Enhanced terminal room disinfection and acquisition and infection caused by multidrug-resistant organisms and Clostridium difficile (the Benefits of Enhanced Terminal Room Disinfection study): a cluster-randomised, multicentre, crossover study. Lancet 2017; 389 (10071): 805-814
    CrossrefPubMedGoogle Scholar
  • 71 Anderson DJ, Moehring RW, Weber DJ. , et al; CDC Prevention Epicenters Program. Effectiveness of targeted enhanced terminal room disinfection on hospital-wide acquisition and infection with multidrug-resistant organisms and Clostridium difficile: a secondary analysis of a multicentre cluster randomised controlled trial with crossover design (BETR Disinfection). Lancet Infect Dis 2018; 18 (08) 845-853
    CrossrefPubMedGoogle Scholar
  • 72 Carling PC. Wastewater drains: epidemiology and interventions in 23 carbapenem-resistant organism outbreaks. Infect Control Hosp Epidemiol 2018; 39 (08) 972-979
    CrossrefPubMedGoogle Scholar
  • 73 Kizny Gordon AE, Mathers AJ, Cheong EYL. , et al. The hospital water environment as a reservoir for carbapenem-resistant organisms causing hospital-acquired infections-a systematic review of the literature. Clin Infect Dis 2017; 64 (10) 1435-1444
    CrossrefPubMedGoogle Scholar
  • 74 Dyar OJ, Huttner B, Schouten J, Pulcini C. ; ESGAP (ESCMID Study Group for Antimicrobial stewardshiP). What is antimicrobial stewardship?. Clin Microbiol Infect 2017; 23 (11) 793-798
    CrossrefPubMedGoogle Scholar
  • 75 Kaki R, Elligsen M, Walker S, Simor A, Palmay L, Daneman N. Impact of antimicrobial stewardship in critical care: a systematic review. J Antimicrob Chemother 2011; 66 (06) 1223-1230
    CrossrefPubMedGoogle Scholar
  • 76 Barlam TF, Cosgrove SE, Abbo LM. , et al. Implementing an antibiotic stewardship program: guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clin Infect Dis 2016; 62 (10) e51-e77
    CrossrefPubMedGoogle Scholar
  • 77 Davey P, Marwick CA, Scott CL. , et al. Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst Rev 2017; 2: CD003543
    CrossrefPubMedGoogle Scholar
  • 78 Karanika S, Paudel S, Grigoras C, Kalbasi A, Mylonakis E. Systematic review and meta-analysis of clinical and economic outcomes from the implementation of hospital-based antimicrobial stewardship programs. Antimicrob Agents Chemother 2016; 60 (08) 4840-4852
    CrossrefPubMedGoogle Scholar
  • 79 Lindsay PJ, Rohailla S, Taggart LR. , et al. Antimicrobial stewardship and intensive care unit mortality: a systematic review. Clin Infect Dis 2019; 68 (05) 748-756
    CrossrefPubMedGoogle Scholar
  • 80 Perozziello A, Routelous C, Charani E. , et al; CEFECA Study Group. Experiences and perspectives of implementing antimicrobial stewardship in five French hospitals: a qualitative study. Int J Antimicrob Agents 2018; 51 (06) 829-835
    CrossrefPubMedGoogle Scholar
  • 81 Charani E, Castro-Sanchéz E, Bradley S, Nathwani D, Holmes AH, Davey P. Implementation of antibiotic stewardship in different settings - results of an international survey. Antimicrob Resist Infect Control 2019; 8: 34
    CrossrefPubMedGoogle Scholar
  • 82 Bauer KA, Perez KK, Forrest GN, Goff DA. Review of rapid diagnostic tests used by antimicrobial stewardship programs. Clin Infect Dis 2014; 59 (Suppl. 03) S134-S145
    CrossrefPubMedGoogle Scholar
  • 83 Huang H-B, Peng J-M, Weng L, Wang C-Y, Jiang W, Du B. Procalcitonin-guided antibiotic therapy in intensive care unit patients: a systematic review and meta-analysis. Ann Intensive Care 2017; 7 (01) 114
    CrossrefPubMedGoogle Scholar
  • 84 Garnier M, Rozencwajg S, Pham T. , et al. Evaluation of early antimicrobial therapy adaptation guided by the BetaLACTA® test: a case-control study. Crit Care 2017; 21 (01) 161
    CrossrefPubMedGoogle Scholar
  • 85 Zahar J-R, Blot S, Nordmann P. , et al. Screening for intestinal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae in critically ill patients: expected benefits and evidence-based controversies. Clin Infect Dis 2019; 68 (12) 2125-2130
    CrossrefPubMedGoogle Scholar
  • 86 Birgand G, Armand-Lefevre L, Lepainteur M. , et al. Introduction of highly resistant bacteria into a hospital via patients repatriated or recently hospitalized in a foreign country. Clin Microbiol Infect 2014; 20 (11) O887-O890
    CrossrefPubMedGoogle Scholar
  • 87 Schwaber MJ, Carmeli Y. An ongoing national intervention to contain the spread of carbapenem-resistant enterobacteriaceae. Clin Infect Dis 2014; 58 (05) 697-703 . doi: 10.1093/cid/cit795 [Erratum in: Clin Infect Dis. 2014 Jul 15;59(2):323. PubMed PMID: 24304707]
    CrossrefPubMedGoogle Scholar
  • 88 Fournier S, Desenfant L, Monteil C, Nion-Huang M, Richard C, Jarlier V. ; The Ap-Hp Outbreaks Control Group. Efficiency of different control measures for preventing carbapenemase-producing enterobacteria and glycopeptide-resistant Enterococcus faecium outbreaks: a 6-year prospective study in a French multihospital institution, January 2010 to December 2015. Euro Surveill 2018 23. (08): doi:10.2807/1560-7917.ES.2018.23.8.17-00078
    PubMedGoogle Scholar
  • 89 Lee BY, Bartsch SM, Hayden MK. , et al. How Introducing a Registry with Automated Alerts for Carbapenem-Resistant Enterobacteriaceae (CRE) May Help Control CRE Spread in a Region. Clin Infect Dis 2019 . pii: ciz300. doi: 10.1093/cid/ciz300. [Epub ahead of print]
    PubMedGoogle Scholar
  • 90 Slayton RB, Toth D, Lee BY. , et al. Vital signs: estimated effects of a coordinated approach for action to reduce antibiotic-resistant infections in health care facilities - United States. MMWR Morb Mortal Wkly Rep 2015; 64 (30) 826-831
    CrossrefPubMedGoogle Scholar
  • 91 Ostrowsky BE, Trick WE, Sohn AH. , et al. Control of vancomycin-resistant Enterococcus in health care facilities in a region. N Engl J Med 2001; 344 (19) 1427-1433
    CrossrefPubMedGoogle Scholar