Carbapenem-resistant enterobacteriaceae: Laboratory detection and infection control practices

Current Infectious Disease Reports

Volumn 15, Issue 6, 2013, Pages 549-558

  Kruse, Eva Brigitta ^a   Aurbach, Ute ^a   Wisplinghoff, Hilmar ^a,b  

^a Dres Med Wisplinghoff und Kollegen   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Antibiotic resistance; Carbapenem resistant Enterobacteriaceae; Carbapenems; Infection control

Indexed keywords

BORONIC ACID DERIVATIVE; CARBAPENEMASE; CHLORHEXIDINE; DIPICOLINIC ACID; DORIPENEM; EDETIC ACID; ERTAPENEM; FROPENEM; IMIPENEM; MEROPENEM;

ACINETOBACTER BAUMANNII; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; AWARENESS; BACTERIAL CLEARANCE; BACTERIUM CULTURE; BACTERIUM DETECTION; BATH; CARBAPENEM RESISTANT ENTEROBACTERIACEAE; CONTACT EXAMINATION; CRITICALLY ILL PATIENT; CULTURE MEDIUM; DISK DIFFUSION; ENTEROBACTERIACEAE; GERMANY; GLOVE; GRAM NEGATIVE BACTERIUM; HAND WASHING; HEALTH EDUCATION; INFECTION CONTROL; INFECTION PREVENTION; KLEBSIELLA PNEUMONIAE; LABORATORY TEST; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRACTICE GUIDELINE; PSEUDOMONAS AERUGINOSA; SCREENING; SENSITIVITY AND SPECIFICITY; ULTRAVIOLET SPECTROPHOTOMETRY; UNITED KINGDOM;

EID: 84890588394     PISSN: 15233847     EISSN: 15343146     Source Type: Journal    
DOI: 10.1007/s11908-013-0373-x     Document Type: Article

References (99)

1. Orsi G, Falcone M, Venditti M. Surveillance and management of multidrug-resistant microorganisms. Expert Rev Anti Infect Ther. 2011;9:653-79.
2. Centers for Disease Control and Prevention (CDC). CDC National Center for Emerging and Zoonotic Infectious Diseases, Division of Healthcare Quality Promotion. Guidance for control of carbapenem-resistant Enterobacteriaceae (CRE). 2012 CRE Toolkit. http://www.cdc.gov/hai/organisms/cre/cre-toolkit/index. html. Accessed 22 Sep 2013.
3. Nordmann P, Naas T, Poirel L. Global spread of carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis. 2011;17:1791-8.
4. Casellas JM. Antibacterial drug resistance in Latin America: consequences for infectious disease control. Rev Panam Salud Publica. 2011;30:519-28.
5. Canton R, Akova M, Carmeli Y, Giske CG, Glupczynski Y, Gniadkowski M, et al. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin Microbiol Infect. 2012;18:413-31.
6. Pitout JD, Laupland KB. Extended-spectrum beta-lactamase producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis. 2008;8:159-66.
7. Papp-Wallace KM, Endimiani A, Taracila MA, Bonomo RA. Carbapenems: past, present, and future. Antimicrob Agents Chemother. 2011;55:4943-60.
8. • Hara G, Gould I, Endimiani A, Pardo P, Daikos G, Hsueh P, et al. Detection, treatment, and prevention of carbapenemase-producing Enterobacteriaceae: recommendations from an International working group. J Chemother. 2013;25:129-40. This is one of the most comprehensive reviews addressing detection, treatment and prevention of CREs authored by an International Working Group of clinical microbiologists, and infectious disease, infection control, and public-health specialists.
9. Queenan AM, Bush K. Carbapenemases: the versatile β-lactamases. Clin Microbiol Rev. 2007;20:440-58.
10. Nordmann P, Gniadkowski M, Giske CG, Poirel L, Woodford N, Miriagou V, et al. Identification and screening of carbapenemase-producing Enterobacteriaceae. Clin Microbiol Infect. 2012;18:432-8.
11. Giske CG, Sundsfjord AS, Kahlmeter G, Woodford N, Nordmann P, Paterson DL. Redefining extended-spectrum β-lactamase: balancing science and clinical need. J Antimicrob Chemother. 2009;63:1-4.
12. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement. Document M100-S21. Wayne, PA: Clinical and Laboratory Standards Institute; 2011.
13. Cohen Stuart J, Leverstein-Van Hall MA, Dutch Working Party on the Detection of Highly Resistant Microorganisms. Guideline for phenotypic screening and confirmation of carbapenemases in Enterobacteriaceae. Int J Antimicrob Agents. 2010;36(3):205-10.
14. •• Nordmann P, Poirel L. Strategies for identification of carbapenemase-producing Enterobacteriaceae. J Antimicrob Chemother. 2013;68(3):487-9. This paper proposes an interesting strategy for detection of CREs without molecular techniques.
15. Willems E, Verhaegen J, Magerman K, Nys S, Cartuyvels R. Towards a phenotypic screening strategy for emerging β-lactamases in Gram-negative bacilli. Int J Antimicrob Agents. 2013;41(2):99-109.
16. Frawley J, Mangan L, Boo TW. Comparison of four laboratory methods in the detection of carbapenemase-producing Enterobacteriaceae. J Med Microbiol. 2013;62(7):1094-6.
17. Clinical and Laboratory Standards Institute. M100-23: performance standards for antimicrobial susceptibility testing; twenty third informational supplement. Wayne, PA: Clinical and Laboratory Standards Institute; 2013.
18. European Committee on Antimicrobial Susceptibility Testing (EUCAST). Clinical breakpoints. http://www.eucast.org/clinical-breakpoints/. Accessed 22 Sep 2013.
19. Pasteran F, Mendez T, Guerriero L, Rapoport M, Corso A. Sensitive screening tests for suspected class A carbapenemase production in species of Enterobacteriaceae. J Clin Microbiol. 2009;47:1631-9.
20. Lartigue MF, Poirel L, Poyart C, Réglier-Poupet H, Nordmann P. Ertapenem resistance of Escherichia coli. Emerg Infect Dis. 2007;13:315-7.
21. Doumith M, Ellington MJ, Livermore DM, Woodford N. Molecular mechanisms disrupting porin expression in ertapenem-resistant Klebsiella and Enterobacter spp. clinical isolates from the UK. J Antimicrob Chemother. 2009;63:659-67.
22. Endimiani A, Hujer AM, Hujer KM, Gatta JA, Schriver AC, Jacobs MR, et al. Evaluation of a commercial microarray system for detection of SHV-, TEM-, CTX-M-, and KPC-type beta-lactamase genes in Gram-negative isolates. J Clin Microbiol. 2010;48:2618-22.
23. Vading M, Samuelsen Ø, Haldorsen B, Sundsfjord AS, Giske CG. Comparison of disk diffusion, Etest and VITEK2 for detection of carbapenemase-producing Klebsiella pneumoniae with the EUCAST and CLSI breakpoint systems. Clin Microbiol Infect. 2011;17:668-74.
24. Blackburn J, Tsimiklis C, Lavergne V, Pilotte J, Grenier S, Gilbert A, et al. Carbapenem disks on MacConkey agar in screening methods for detection of carbapenem-resistant Gram-negative rods in stools. J Clin Microbiol. 2013;51(1):331-3.
25. Day KM, Pike R, Winstanley TG, Lanyon C, Cummings SP, Raza MW, et al. Use of faropenem as an indicator of carbapenemase activity in the Enterobacteriaceae. J Clin Microbiol. 2013;51(6):1881-6.
26. Anderson KF, Lonsway DR, Rasheed JK, Biddle J, Jensen B, McDougal LK, et al. Evaluation of methods to identify the Klebsiella pneumoniae carbapenemase in Enterobacteriaceae. J Clin Microbiol. 2007;45:2723-5.
27. Nordmann P, Girlich D, Poirel L. Detection of carbapenemase producers in Enterobaceriaceae using a novel screening medium. J Clin Microbiol. 2012;50:2761-6.
28. Samra Z, Bahar J, Madar-Shapiro L, Aziz N, Israel S, Bishara J. Evaluation of CHROMagar KPC for rapid detection of carbapenem-resistant Enterobacteriaceae. J Clin Microbiol. 2008;46:3110-1.
29. Moran Gilad J, Carmeli Y, Schwartz D, Navon-Venezia S. Laboratory evaluation of the CHROMagar KPC medium for identification of carbapenem-nonsusceptible Enterobacteriaceae. Diagn Microbiol Infect Dis. 2011;70(4):565-7.
30. Withey S, Scopes E. A new screening medium for detection of carbapenem-resistant Enterobacteriaceae. In: Abstracts of the Twenty-first European Congress for Clinical Microbiology and Infectious Diseases, Milan, 2011. Abstract P862.
31. Cohen Stuart J, Voets G, Rottier W, Voskuil S, Scharringa J, van Dijk K, et al. Evaluation of the Oxoid Brilliance™ CRE Agar for the detection of carbapenemase-producing Enterobacteriaceae. Eur J Clin Microbiol Infect Dis. 2013. doi: 10.1007/s10096-013-1896-7.
32. Vrioni G, Daniil I, Voulgari E, Ranellou K, Koumaki V, Ghirardi S, et al. Comparative evaluation of a prototype chromogenic medium (ChromID CARBA) for detecting carbapenemase-producing Enterobacteriaceae in surveillance rectal swabs. J Clin Microbiol. 2012;50(6):1841-6.
33. Panagea T, Galani I, Souli M, Adamou P, Antoniadou A, Giamarellou H. Evaluation of CHROMagar™ KPC for the detection of carbapenemase-producing Enterobacteriaceae in rectal surveillance cultures. Int J Antimicrob Agents. 2011;37:124-8.
34. Girlich D, Poirel L, Nordmann P. Comparison of the SUPERBA, CHROMagr KPC, and Brilliance CRE screening media for detection of Enterobacteriaceae with reduced susceptibility to carbapenems. Diagn Microbiol Infect Dis. 2013;75:214-7.
35. Centers for Disease Control and Prevention (CDC). Modified Hodge test for carbapenemase detection in Enterobacteriaceae. www.cdc.gov/HAI/pdfs/ labSettings/HodgeTest-Carbapenemase-Enterobacteriaceae.pdf. Accessed 22 Sep 2013.
36. Carvalhaes C, Picao R, Nicoletti A, Xavier D, Gales A. Cloverleaf test (modified Hodge test) for detecting carbapenemase production in Klebsiella pneumoniae: be aware of false positive results. J Antimicrob Chemother. 2010;65:249-51.
37. Girlich D, Poirel L, Nordmann P. Value of the modified Hodge test for detection of emerging carbapenemases in Enterobacteriaceae. J Clin Microbiol. 2012;50:477-9.
38. Österblad MH, Jalava P. Evaluation of EDTA and dipicolinic acid, with and without the addition of zinc, in the detection of metallo-lactamases. In: 19th European Congress of Clinical Microbiology and Infectious Diseases (ECCMID). ESCMID; 2009. Abstract P700.
39. Giske CG, Gezelius L, Samuelsen Ø, Warner M, Sundsfjord A, Woodford N. A sensitive and specific phenotypic assay for detection of metallo-β-lactamases and KPC in Klebsiella pneumoniae with the use of meropenem disks supplemented with aminophenylboronic acid, dipicolinic acid and cloxacillin. Clin Microbiol Infect. 2011;17(4):552-6.
40. Tsakris A, Kristo I, Poulou A, Themeli-Digalaki K, Ikonomidis A, Petropoulou D, et al. Evaluation of boronic acid disk tests for differentiating KPC-possessing Klebsiella pneumoniae isolates in the clinical laboratory. J Clin Microbiol. 2009;47:362-7.
41. Miriagou V, Pappagianistis CC, Tzelepi E, Bou Casals J, Legakis NJ, Tzouvelekis LS. Detection of VIM-1 production in Proteus mirabilis by an imipenem dipicolinic acid double disk synergy test. J Clin Microbiol. 2010;4:667-8.
42. Seah C, Low DE, Patel SN, Melano RG. Comparative evaluation of a chromogenic agar medium, the modified Hodge test, and a battery of meropenem-inhibitor discs for detection of carbapenemase activity in Enterobacteriaceae. J Clin Microbiol. 2011;49:1965-9.
43. Poirel L, Potron A, Nordmann P. OXA-48-like carbapenemases: the phantom menace. J Antimicrob Chemother. 2012;67:1597-606.
44. Miriagou V, Tzelepi E, Kotsakis SD, Daikos GL, Bou Casals J, Tzouvelekis LS. Combined disc methods for the detection of KPC- and/or VIM-positive Klebsiella pneumoniae: improving reliability for the double carbapenemase producers. Clin Microbiol Infect. 2013;19(9):E412-5.
45. Dortet L, Poirel L, Nordmann P. Rapid identification of Carbapenemase types in Enterobacteriaceae and Pseudomonas spp. by using a biochemical test. Antimicrob Agents Chemother. 2012;12:6437-40.
46. Nordmann P, Poirel L, Dortet L. Rapid detection of Carbapenemase- producing Enterobacteriaceae. Emerg Infect Dis. 2012;18(9):1503-7.
47. Vasoo S, Cunningham SA, Kohner PC, Simner PJ, Mandrekar JN, Lolans K, et al. Comparison of a novel rapid chromogenic biochemical assay, the Carba NP test with the modified Hodge test for detection of carbapenemase producing Gram-negative bacilli. J Clin Microbiol. 2013;51(9):3097-101.
48. Bernabeu S, Poirel L, Nordmann P. Spectrophotometry-based detection of carbapenemase producers in Enterobacteriaceae. Diagn Microbiol Infect Dis. 2012;74:88-90.
49. Wang L, Han C, Sui W, Wang M, Xinxin L. MALDI-TOF MS applied to indirect carbapenemase detection: a validated procedure to clearly distinguish between carbapenemase-positive and carbapenemase-negative bacterial strains. Anal Bioanal Chem. 2013;405:5259-66.
50. Burckhardt I, Zimmermann S. Using matrix-assisted laser desorption ionization-time of flight mass spectrometry to detect carbapenem resistance within 1 to 2.5 hours. J Clin Microbiol. 2011;49(9):3321-4.
51. Hrabák J, Walková R, Studentová V, Chudácková E, Bergerová T. Carbapenemase activity detection by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol. 2011;49(9):3222-7.
52. Cuzon G, Naas T, Bogaerts P, Glupczynski Y, Nordmann P. Evaluation of a DNA microarray for the rapid detection of extended-spectrum b-lactamases (TEM, SHV and CTX-M), plasmid-mediated cephalosporinases (CMY-2-like, DHA, FOX, ACC-1, ACT/MIR and CMY-1-like/MOX) and carbapenemases (KPC, OXA-48, VIM, IMP and NDM). J Antimicrob Chemother. 2012;67:1865-9.
53. Kaase M, Szabados F, Wassill L, Gatermann SG. Detection of carbapenemases in Enterobacteriaceae by a commercial multiplex PCR. J Clin Microbiol. 2012;50:3115-8.
54. Spanu T, Fiori B, D'Inzeo T, Canu G, Campoli S, Giani T, et al. Evaluation of the new NucliSENS EasyQ KPC test for rapid detection of Klebsiella pneumoniae carbapenemase genes (blaKPC). J Clin Microbiol. 2012;50:2783-5.
55. McEwan A, Derome A, Meunier D, Burns P, Woodford N, Dogson A. Evaluation of the NucliSENS EasyQ KPC assay for detection of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae. J Clin Microbiol. 2013;6:1948-50.
56. Cuzón G, Naas T, Bogaerts P, Glupczynski Y, Nordmann P. Probe ligation and real-time detection of KPC, OXA-48, VIM, IMP, and NDM carbapenemase genes. Diagn Microbiol Infect Dis. 2013;76(4):502-5.
57. Centers for Disease Control and Prevention (CDC). Vital signs: carbapenem-resistant Enterobacteriaceae. MMWR Morb Mortal Wkly Rep. 2013;62(9):165-70.
58. European Centre for Disease Prevention and Control (ECDC). European Antimicrobial Resistance Surveillance Network (EARS-net) interactive database. http://www.ecdc.europa.eu/en/healthtopics/antimicrobial-resistance/database/ Pages/table-reports.aspx. Accessed 19 Aug 2013.
59. Swaminathan M, Sharma S, Poliansky Blash S, Patel G, Banach DB, Phillips M, et al. Prevalence and risk factors for acquisition of carbapenem-resistant Enterobacteriaceae in the setting of endemicity. Infect Control Hosp Epidemiol. 2013;34(8):809-17.
60. Lewis JD, Bishop M, Heon B, Mathers AJ, Enfield KB, Sifri CD. Admission surveillance for carbapenemase-producing Enterobacteriaceae at a long-term acute care hospital. Infect Control Hosp Epidemiol. 2013;34(8):832-4.
61. Burns K, Morris D, Murchan S, Cunney R, Smyth E, Power M, et al. Carbapenemase-producing Enterobacteriaceae in Irish critical care units: results of a pilot prevalence study, June 2011. J Hosp Infect. 2013;83(1):71-3.
62. Drew RJ, Turton JF, Hill RL, Livermore DM, Woodford N, Paulus S, et al. Emergence of carbapenem-resistant Enterobacteriaceae in a UK paediatric hospital. J Hosp Infect. 2013;84(4):300-4.
63. Calfee D, Jenkins SG. Use of active surveillance cultures to detect asymptomatic colonization with carbapenem-resistant Klebsiella pneumoniae in intensive care unit patients. Infect Control Hosp Epidemiol. 2008;29(10):966-8.
64. Gagliotti C, Ciccarese V, Sarti M, Giordani S, Barozzi A, Braglia C, et al. Active surveillance for asymptomatic carriers of carbapenem-producing Klebsiella pneumoniae in a hospital setting. J Hosp Infect. 2013;83(4):330-2.
65. Won SY, Munoz-Price LS, Lolans K, Hota B, Weinstein RA, Hayden MK. Emergence and rapid regional spread of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae. Clin Infect Dis. 2011;53(6):532-40.
66. Carmeli Y, Akova M, Cornaglia G, Daikos GL, Garau J, Harbarth S, et al. Controlling the spread of carbapenemase-producing Gram-negatives: therapeutic approach and infection control. Clin Microbiol Infect. 2010;16(2):102-11.
67. Magiorakos AP, Struelens M, Jasir A; European Centre for Disease Prevention and Control (ECDC). Risk assessment on the spread of carbapenemase-producing Enterobacteriaceae (CPE) through patient transfer between healthcare facilities, with special emphasis on cross-border transfer. http://ecdc.europa.eu/en/publications/Publications/110913-Risk-assessment- resistant-CPE.pdf. Accessed 22 Sep 2013.
68. Glasner C, Albiger B, Buist G, Tanbić-Andrasević A, Canton R, Carmeli Y, et al. Carbapenemase-producing Enterobacteriaceae in Europe: a survey among national experts from 39 countries, February 2013. Euro Surveill. 2013;18(28).
69. Siegel JD, Rhinehart E, Jackson M, Chiarello L. Management of multidrug-resistant organisms in health care settings, 2006. Am J Infect Control. 2007;35(10):S165-93.
70. Savard P, Carroll KC, Wilson LE, Perl TM. The challenges of carbapenemase-producing Enterobacteriaceae and infection prevention: protecting patients in the chaos. Infect Control Hosp Epidemiol. 2013;34(7):730-9.
71. Munoz-Price LS, Quinn JP. Deconstructing the infection control bundles for the containment of carbapenem-resistant Enterobacteriaceae. Curr Opin Infect Dis. 2013;26:378-87.
72. Mattner F, Bange FC, Meyer E, Seifert H, Wichelhaus TA, Chaberny IF. Preventing the spread of multidrug-resistant gram-negative pathogens: recommendations of an expert panel of the German Society for Hygiene and Microbiology. Dtsch Arztebl Int. 2012;109(3):39-45.
73. Robert-Koch-Institut, Kommission für Krankenhaushygiene und Infektionsprävention (KRINKO). Hygienemaßnahmen bei Infektionen oder Besiedlung mit multiresistenten gramnegativen Stäbchen. http://www.rki.de/DE/Content/Infekt/Krankenhaushygiene/Kommission/Downloads/ Gramneg-Erreger.pdf. Accessed 22 Sep 2013.
74. Public Health England. Guidance on carbapenemase producers. http://www.hpa.org.uk/web/HPAweb&Page&HPAwebAutoListName/Page/ 1294740725255. Accessed 22 Sep 2013.
75. Akova M, Daikos GL, Tzouvelekis L, Carmeli Y. Interventional strategies and current clinical experience with carbapenemase-producing Gram-negative bacteria. Clin Microbiol Infect. 2012;18:439-48.
76. WHO. WHO guidelines on hand hygiene in health care. http://whqlibdoc.who. int/publications/2009/9789241597906-eng.pdf. Accessed 22 Sep 2013.
77. Zimmerman FS, Assous MV, Bdolah-Abram T, Lachish T, Yinnon AM, Wiener-Well Y. Duration of carriage of carbapenem-resistant Enterobacteriaceae following hospital discharge. Am J Infect Control. 2013;41:190-4.
78. • Tschudin-Sutter S, Frei R, Dangel M, Stranden A, Widmer AF. Rate of transmission of extended-spectrum beta-lactamase-producing Enterobacteriaceae without contact isolation. Clin Infect Dis. 2012;55(11):1505-11. This study questions the (generally agreed) value of single room isolation.
79. Guet-Revillet H, Le Monnier A, Breton N, Descamps P, Lecuyer H, Alaabouche I, et al. Environmental contamination with extended-spectrum β-lactamases: is there any difference between Escherichia coli and Klebsiella spp? Am J Infect Control. 2012;40(9):845-8.
80. Oostdijk EA, de Smet AM, Kesecioglu J, Bonten MJ, Dutch SOD-SDD Trialists Group. The role of intestinal colonization with gram-negative bacteria as a source for intensive care unit-acquired bacteremia. Crit Care Med. 2011;39:961-6.
81. Brun-Buisson C, Razazi K, Derde LP, Bonten MJ. Control of colonisation with extended-spectrum β-lactamase-producing bacteria: reply to Zandstra et al. Intensive Care Med. 2013;39(3):540.
82. Saidel-Odes L, Polachek H, Peled N, Riesenberg K, Schlaeffer F, Trabelsi Y, et al. A randomized, double-blind, placebo-controlled trial of selective digestive decontamination using oral gentamicin and oral polymyxin E for eradication of carbapenem-resistant Klebsiella pneumoniae carriage. Infect Control Hosp Epidemiol. 2012;33(1):14-9.
83. Zandstra D, Abecasis F, Taylor N, Damjanovic V, Silvestri L, van Saene HK. For control of colonisation with extended-spectrum β-lactamase- producing bacteria, SDD does work. Intensive Care Med. 2013;39(3):539.
84. Razazi K, Derde LP, Verachten M, Legrand P, Lesprit P, Brun-Buisson C. Clinical impact and risk factors for colonization with extended-spectrum β-lactamase-producing bacteria in the intensive care unit. Intensive Care Med. 2012;38(11):1769-78.
85. Halaby T, Al Naiemi N, Kluytmans J, van der Palen J, Vandenbroucke-Grauls CM. Emergence of colistin resistance in Enterobacteriaceae after the introduction of selective digestive tract decontamination in an intensive care unit. Antimicrob Agents Chemother. 2013;57(7):3224-9.
86. •• Climo MW, Yokoe DS, Warren DK, Perl TM, Bolon M, Herwaldt LA, et al. Effect of daily chlorhexidine bathing on hospital-acquired infection. N Engl J Med. 2013;368:533-42. This is one of the most important studies on the use of chlorhexidine bathing in preventing hospital infection.
87. Milstone AM, Elward A, Song X, Zerr DM, Orscheln R, Speck K, et al. Daily chlorhexidine bathing to reduce bacteraemia in critically ill children: a multicentre, cluster-randomised, crossover trial. Lancet. 2013;381(9872):1099- 106.
88. Derde LP, Dautzenberg MJ, Bonten MJ. Chlorhexidine body washing to control antimicrobial-resistant bacteria in intensive care units: a systematic review. Intensive Care Med. 2012;38:931-9.
89. 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(8):1201-8.
90. •• Ajao AO, Johnson JK, Harris AD, Zhan M, McGregor JC, Thom KA, et al. Risk of acquiring extended-spectrum β-lactamase-producing Klebsiella species and Escherichia coli from prior room occupants in the intensive care unit. Infect Control Hosp Epidemiol. 2013;34(5):453-8. This is one of the major studies about the limitations of the influence of the environment in ESBL transmission.
91. Hilty M, Betsch BY, Bögli-Stuber K, Heiniger N, Stadler M, Küffer M, et al. Transmission dynamics of extended-spectrum β-lactamase-producing Enterobacteriaceae in the tertiary care hospital and the household setting. Clin Infect Dis. 2012;55(7):967-75.
92. Blazejewski C, Guerry MJ, Preau S, Durocher A, Nseir S. New methods to clean ICU rooms. Infect Disord Drug Targets. 2011;11(4):365-75.
93. Best EL, Sandoe JA, Wilcox MH. Potential for aerosolization of Clostridium difficile after flushing toilets: the role of toilet lids in reducing environmental contamination risk. J Hosp Infect. 2012;80(1):1-5.
94. Johnson DL, Mead KR, Lynch RA, Hirst DV. Lifting the lid on toilet plume aerosol: a literature review with suggestions for future research. Am J Infect Control. 2013;41(3):254-8.
95. Marchaim D, Chopra T, Bhargava A, Bogan C, Dhar S, Hayakawa K, et al. Recent exposure to antimicrobials and carbapenem-resistant Enterobacteriaceae: the role of antimicrobial stewardship. Infect Control Hosp Epidemiol. 2012;33(8):817-30.
96. Martin ET, Tansek R, Collins V, Hayakawa K, Abreu-Lanfranco O, Chopra T, et al. The carbapenem-resistant Enterobacteriaceae score: a bedside score to rule out infection with carbapenem-resistant Enterobacteriaceae among hospitalized patients. Am J Infect Control. 2013;41:180-2.
97. Dellit TH, Owens RC, McGowan JE, Gerding DN, Weinstein RA, Burke JP, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis. 2007;44:159-77.
98. Society for Healthcare Epidemiology of America; Infectious Diseases Society of America; Pediatric Infectious Diseases Society. Policy statement on antimicrobial stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Infectious Diseases Society (PIDS). Infect Control Hosp Epidemiol. 2012;33(4):322-7.
99. Centers for Disease Control and Prevention (CDC). Guidance for control of infections with carbapenem-resistant or Carbapenemase-producing Enterobacteriaceae in acute care facilities. MMWR Morb Mortal Wkly Rep. 2009;58(10):256-60.