Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-28T04:34:33.223Z Has data issue: false hasContentIssue false

Carbapenem-Resistant Enterobacteriaceae: A Strategic Roadmap for Infection Control

Published online by Cambridge University Press:  15 March 2017

N. Deborah Friedman*
Affiliation:
Barwon Health, Victoria, Australia
Yehuda Carmeli
Affiliation:
Tel Aviv Sourasky Medical Center, Tel Aviv, Israel National Center for Infection Control, Israel Ministry of Health, Tel Aviv, Israel Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
Aaron Lea Walton
Affiliation:
Barwon Health, Victoria, Australia
Mitchell James Schwaber
Affiliation:
National Center for Infection Control, Israel Ministry of Health, Tel Aviv, Israel Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
*
Address correspondence to A/Prof. N. Deborah Friedman, Departments of Medicine and Infectious Diseases, Barwon Health, Geelong, VIC 3220 Australia (Deborahf@barwonhealth.org.au).

Abstract

The incidence of carbapenem-resistant Enterobacteriaceae (CRE) has increased worldwide with great regional variability. Infections caused by these organisms are associated with crude mortality rates of up to 70%. The spread of CRE in healthcare settings is both an important medical problem and a major global public health threat. All countries are at risk of falling victim to the emergence of CRE; therefore, a preparedness plan is required to avoid the catastrophic natural course of this epidemic. Proactive and adequate preventive measures locally, regionally, and nationally are required to contain the spread of these bacteria. The keys to success in preventing the establishment of CRE endemicity in a region are early detection through targeted laboratory protocols and containment of spread through comprehensive infection control measures. This guideline provides a strategic roadmap for infection control measures based on the best available evidence and expert opinion, to enable preparation of a multifaceted preparedness plan to abort epidemics of CRE.

Infect Control Hosp Epidemiol 2017;38:580–594

Type
Review Article
Copyright
© 2017 by The Society for Healthcare Epidemiology of America. All rights reserved 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1. Surveillance atlas of infectious diseases. The European Centre for Disease Prevention and Control (ECDC) website. http://ecdc.europa.eu/en/healthtopics/antimicrobial_resistance/database/Pages/table_reports.aspx. Published 2015. Accessed October 9, 2016.Google Scholar
2. Munoz-Price, LS, Quinn, JP. Deconstructing the infection control bundles for the containment of carbapenem-resistant Enterobacteriaceae . Curr Opin Infect Dis 2013;26:378387.CrossRefGoogle ScholarPubMed
3. Schwaber, MJ, Klarfeld-Lidji, S, Navon-Venezia, S, Schwartz, D, Leavitt, A, Carmeli, Y. Predictors of carbapenem-resistant Klebsiella pneumoniae acquisition among hospitalized adults and effect of acquisition on mortality. Antimicrob Agents Chemother 2008;52:10281033.CrossRefGoogle ScholarPubMed
4. Ben-David, D, Kordevani, R, Keller, N, Tal, I, Marzel, A, Gal-Mor, O, Maor, Y, Rahav, G. Outcome of carbapenem-resistant Klebsiella pneumoniae bloodstream infections. Clin Microbiol Infect 2012;18:5460.CrossRefGoogle ScholarPubMed
5. Borer, A, Saidel-Odes, L, Riesenberg, K, et al. Attributable mortality rate for carbapenem-resistant Klebsiella pneumoniae bacteremia. Infect Control Hosp Epidemiol 2009;30:972976.CrossRefGoogle ScholarPubMed
6. Patel, G, Huprikar, S, Factor, SH, Jenkins, SG, Calfee, DP. Outcomes of carbapenem-resistant Klebsiella pneumoniae infection and the impact of antimicrobial and adjunctive therapies. Infect Control Hosp Epidemiol 2008;29:10991106.CrossRefGoogle ScholarPubMed
7. Swaminathan, M, Sharma, S, Blash, SP, et al. Prevalence and risk factors for acquisition of carbapenem-resistant Enterobacteriaceae in the setting of endemicity. Infect Control Hosp Epidemiol 2013;34:809817.CrossRefGoogle ScholarPubMed
8. Cornaglia, G, Akova, M, Amicosante, G, et al. Metallo-beta-lactamases as emerging resistance determinants in Gram-negative pathogens: open issues. Int J Antimicrob Agents 2007;29:380388.CrossRefGoogle ScholarPubMed
9. Chitnis, AS, Caruthers, PS, Rao, AK, et al. Outbreak of carbapenem-resistant Enterobacteriaceae at a long-term acute care hospital: sustained reductions in transmission through active surveillance and targeted interventions. Infect Control Hosp Epidemiol 2012;33:984992.Google Scholar
10. Grundmann, H, Livermore, DM, Giske, CG, et al. Carbapenem-non-susceptible Enterobacteriaceae in Europe: conclusions from a meeting of national experts. Euro Surveill 2010;15:19711.Google Scholar
11. Glasner, C, Albiger, B, Buist, G, et al. Carbapenemase-producing Enterobacteriaceae in Europe: a survey among national experts from 39 countries, February 2013. Euro Surveill 2013;18:20525.CrossRefGoogle ScholarPubMed
12. Prabaker, K, Lin, MY, McNally, M, et al. Transfer from high-acuity long-term care facilities is associated with carriage of Klebsiella pneumoniae carbapenemase–producing Enterobacteriaceae: A multihospital study. Infect Control 2012;33:11931199.Google Scholar
13. Bilavsky, E, Schwaber, MJ, Carmeli, Y. How to stem the tide of carbapenemase-producing Enterobacteriaceae?: proactive versus reactive strategies. Curr Opin Infect Dis 2010;23:327331.CrossRefGoogle ScholarPubMed
14. Munoz-Price, LS, Poirel, L, Bonomo, RA, et al. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect Dis 2013;13:785796.CrossRefGoogle ScholarPubMed
15. Cejas, D, Fernández Canigia, L, Rincón Cruz, G, et al. First isolate of KPC-2-producing Klebsiella pneumoniae sequence Type 23 from the Americas. J Clin Microbiol 2014;52:34835485.Google Scholar
16. Pitout, JDD, Nordmann, P, Poirel, L. Carbapenemase-producing Klebsiella pneumoniae, a key pathogen set for global nosocomial dominance. Antimicrob Agents Chemother 2015;59:58735884.CrossRefGoogle ScholarPubMed
17. Bonelli, RR, Meurer Moreira, B, Cristina Picão, R. Antimicrobial resistance among Enterobacteriaceae in South America: History, current dissemination status and associated socioeconomic factors. Drug Resist Updates 2014;17:2436.Google Scholar
18. Guh, AY, Limbago, BM, Kallen, AJ. Epidemiology and prevention of carbapenem-resistant Enterobacteriaceae in the United States. Exp Rev Anti-infect Ther 2014;12:565580.CrossRefGoogle ScholarPubMed
19. Healthcare-associated infections. Tracking CRE. Centers for Disease Control and Prevention website. http://www.cdc.gov/hai/organisms/cre/TrackingCRE.html. Published 2015. Accessed October 15, 2016.Google Scholar
20. Hrabák, J, Papagiannitsis, CC, Študentová, V, Jakubu, V, Fridrichová, M, Zemlickova, H. Carbapenemase-producing Klebsiella pneumoniae in the Czech Republic in 2011. Euro Surveill 2013;18:20626.Google Scholar
21. Miró, E, Agüero, J, Larrosa, MN, et al. Prevalence and molecular epidemiology of acquired AmpC β-lactamases and carbapenemases in Enterobacteriaceae isolates from 35 hospitals in Spain. Eur J Clin Microbiol Infect Dis 2013;32:253259.Google Scholar
22. Jans, B, Daniel Huang, TD, Bauraing, C, et al. Infection due to travel-related carbapenemase-producing Enterobacteriaceae, a largely underestimated phenomenon in Belgium. Acta Clinica Belgica 2015;70:181187.Google Scholar
23. Denisuik, AJ, Lagacé-Wiens, PR, Pitout, JD, et al. Molecular epidemiology of extended-spectrum β-lactamase-, AmpC β-lactamase-and carbapenemase-producing Escherichia coli and Klebsiella pneumoniae isolated from Canadian hospitals over a 5 year period: CANWARD 2007–11. J Antimicrob Chemother 2013;68:i57i65.Google Scholar
24. Kostyanev, T, Tafaj, S, Skenduli, I, et al. First detection of KPC-3-producing Klebsiella pneumoniae in Albania. New Microbes New Infect 2015;4:11.Google Scholar
25. Tängdén, T, Giske, CG. Global dissemination of extensively drug-resistant carbapenemase-producing Enterobacteriaceae: clinical perspectives on detection, treatment and infection control. J Int Med 2015;277:501512.Google Scholar
26. Brink, A, Coetzee, J, Clay, C, et al; L. The spread of carbapenem-resistant Enterobacteriaceae in South Africa: Risk factors for acquisition and prevention. SAMJ: South African Med J 2012;102:599601.CrossRefGoogle ScholarPubMed
27. Saito, R, Takahashi, R, Sawabe, E, et al. First Report of KPC-2 carbapenemase-producing Klebsiella pneumoniae in Japan. Antimicrob Agents Chemother 2014;58:29612963.Google Scholar
28. Markovska, R, Stoeva, T, Schneider, I, et al. Clonal dissemination of multilocus sequence type ST15 KPC 2 producing Klebsiella pneumoniae in Bulgaria. APMIS 2015;23:887894.Google Scholar
29. Rodríguez-Zulueta, P, Silva-Sánchez, J, Barrios, H, et al. First outbreak of KPC-3-producing Klebsiella pneumoniae (ST258) clinical isolates in a Mexican Medical Center. Antimicrob Agents Chemother 2013;57:40864088.Google Scholar
30. Quiñones, D, Hart, M, Espinosa, F, et al. Emergence of Klebsiella pneumoniae clinical isolates producing KPC-2-carbapenemase in Cuba. New Microbes New Infect 2014;2:123126.Google Scholar
31. Pavelkovich, A, Balode, A, Edquist, P, et al. Detection of carbapenemase-producing Enterobacteriaceae in the Baltic Countries and St. Petersburg Area. BioMed Res Int 2014;7 pp. doi. org/10.1155/2014/548960.Google Scholar
32. Ageevets, VA, Partina, IV, Lisitsyna, ES, et al. Emergence of carbapenemase-producing Gram-negative bacteria in Saint Petersburg, Russia. Int J Antimicrob Agents 2014;44:152155.Google Scholar
33. Chua, KYL, Grayson, ML, Burgess, AN, Lee, JYH, Howden, BP. The growing burden of multidrug-resistant infections among returned Australian travellers. Med J Aust 2014;200:116118.CrossRefGoogle ScholarPubMed
34. Coatsworth, NR, Huntington, PG, Hardiman, RP, Hudson, BJ, Fernandes, CJ. A case of carbapenemase-producing Klebsiella pneumoniae in Australia. Pathology 2012;44:4244.Google Scholar
35. Chang, LWK, Buising, KL, Jeremiah, CJ, et al. Managing a nosocomial outbreak of carbapenem-resistant Klebsiella pneumoniae: an early Australian hospital experience. Int Med J 2015;45:10371043.Google Scholar
36. Sheng, WH, Badal, RE, Hseuh, P-R. Distribution of Extended-spectrum β-lactamases (ESBLs), AmpC β-lactamases, and carbapenemases among Enterobacteriaceae isolates causing intra-abdominal infections in Asia-Pacific: the Study for Monitoring Antimicrobial Resistance Trends (SMART). Antimicrob Agents Chemother 2013;57:29812988.Google Scholar
37. Lixandru, BE, Cotar, AI, Straut, M, et al. Carbapenemase-producing Klebsiella pneumoniae in Romania: a six-month survey. PloS One 2015;10(11). doi. 10.1371/journal.pone.0143214.Google Scholar
38. Zujić Atalić, V, Bedenić, B, Kocsis, E, et al. Diversity of carbapenemases in clinical isolates of Enterobacteriaceae in Croatia—the results of a multicentre study. Clin Microbiol Infect 2014;20:08940903.CrossRefGoogle ScholarPubMed
39. Jones, RN, Flonta, M, Gurler, N, Cepparulo, M, Mendes, RE, Castanheira, M. Resistance surveillance program report for selected European nations 2011 Diagn Microbiol Infect Dis 2014;78:429436.Google Scholar
40. Manenzhe, RI, Zar, HJ, Nicol, MP, Kaba, M. The spread of carbapenemase-producing bacteria in Africa: a systematic review. J Antimicrob Chemother 2015;70:2340.Google Scholar
41. Ogbolu, DO, Webber, MA. High-level and novel mechanisms of carbapenem- resistance in Gram-negative bacteria from tertiary hospitals in Nigeria. Int J Antimicrob Agents 2014;43:412417.Google Scholar
42. Rimrang, B, Chanawong, A, Lulitanond, A, et al. Emergence of NDM-1-and IMP-14a-producing Enterobacteriaceae in Thailand. J Antimicrob Chemother 2012;67:26262630.Google Scholar
43. Mushi, MF, Mshana, SE, Imirzalioglu, C, Bwanga, F. Carbapenemase genes among multidrug-resistant Gram-negative clinical isolates from a tertiary hospital in Mwanza, Tanzania. BioMed Res Int 2014. doi: 10.1155/2014/303104.Google Scholar
44. Peirano, G, Lascols, C, Hackel, M, Hoban, DJ, Pitout, JDD. Molecular epidemiology of Enterobacteriaceae that produce VIMs and IMPs from the SMART surveillance program. Diagn Microbiol Infect Dis 2014;78:277281.Google Scholar
45. Hawser, SP, Bouchillon, SK, Lascols, C, et al. Susceptibility of Klebsiella pneumoniae isolates from intra-abdominal infections, and molecular characterization of ertapenem-resistant isolates. Antimicrob Agents Chemother 2011;55:39173922.Google Scholar
46. Huang, XZ, Frye, JG, Chahine, MA, et al. Characteristics of plasmids in multi-drug-resistant Enterobacteriaceae isolated during prospective surveillance of a newly opened hospital in Iraq. PloS One 2012;7. doi: 10.1371/journal.pone.004036.Google Scholar
47. Jamal, W, Rotimi, VO, Albert, MJ, Khodakhast, F, Nordmann, P, Poirel, L. High prevalence of VIM-4 and NDM-1 metallo-β-lactamase among carbapenem-resistant Enterobacteriaceae . J Med Microbiol 2013;6:12391244.Google Scholar
48. Nastro, M, Monge, R, Zintgraff, J, et al. First nosocomial outbreak of VIM 16 producing Serratia marcescens in Argentina. Clin Microbiol Infect 2013;19:617619.Google Scholar
49. Lascols, C, Hackel, M, Marshall, SH, et al. Increasing prevalence and dissemination of NDM-1 metallo-β-lactamase in India: data from the SMART study (2009). J Antimicrob Chemother 2011;66:19921997.Google Scholar
50. Nordmann, P, Poirel, L, Walsh, TR, Livermore, DM. The emerging NDM carbapenemases. Trends Microbiol 2011;19:588595.CrossRefGoogle ScholarPubMed
51. Barantsevich, EP, Churkina, IV, Barantsevich, NE, Pelkonen, J, Schlyakhto, EV, Woodford, N. Emergence of Klebsiella pneumoniae producing NDM-1 carbapenemase in Saint Petersburg, Russia. J Antimicrob Chemother 2013;68:12041206.Google Scholar
52. Brink, AJ, Coetzee, J, Clay, CG, et al. Emergence of New Delhi metallo-beta-lactamase (NDM-1) and Klebsiella pneumoniae carbapenemase (KPC-2) in South Africa. J Clin Microbiol 2012;50:525527.Google Scholar
53. Tran, HH, Ehsani, S, Shibayama, K, et al. Common isolation of New Delhi metallo-beta-lactamase-1-producing Enterobacteriaceae in a large surgical hospital in Vietnam. Eur J Clin Microbiol Infect Dis 2015;34:12471254.CrossRefGoogle Scholar
54. Berrazeg, M, Diene, SM, Medjahed, L, et al. New Delhi metallo-beta-lactamase around the world: an eReview using Google Maps. Eurosurveillance website. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20809. Published 2014. Accessed September 15, 2016.Google Scholar
55. Zowawi, HM, Sartor, AL, Balkhy, HH, et al. Molecular characterization of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae in the countries of the Gulf Cooperation Council: dominance of OXA-48 and NDM producers. Antimicrob Agents Chemother 2014;58:30853090.Google Scholar
56. Bastian, S, Nordmann, P, Creton, E, et al. First case of NDM-1-producing Klebsiella pneumoniae in Caribbean islands. Int J Infect Dis 2015;34:5354.Google Scholar
57. Torres-González, P, Bobadilla-del Valle, M, Tovar-Calderón, E, et al. Outbreak caused by Enterobacteriaceae harboring NDM-1 metallo-β-lactamase carried in an IncFII plasmid in a tertiary care hospital in Mexico City. Antimicrob Agents Chemother 2015;59:70807083.Google Scholar
58. Hrabák, J, Študentová, V, Adámková, V, et al. Report on a transborder spread of carbapenemase-producing bacteria by a patient injured during Euromaidan, Ukraine. New Microbes New Infect 2015;8:2830.Google Scholar
59. Poirel, L, Héritier, C, Tolün, V, Nordmann, P. Emergence of oxacillinase-mediated resistance to imipenem in Klebsiella pneumoniae . Antimicrob Agents Chemother 2004;48:1522.Google Scholar
60. Poirel, L, Potron, A, Nordmann, P. OXA-48-like carbapenemases: the phantom menace. J Antimicrob Chemother 2012;67:15971606.CrossRefGoogle ScholarPubMed
61. Izdebski, R, Bojarska, K, Baraniak, A, et al. NDM-1-or OXA-48-producing Enterobacteriaceae colonising Polish tourists following a terrorist attack in Tunis, March 2015. Euro Surveill 2015;20(23):21150.Google Scholar
62. Fursova, NK, Astashkin, EI, Knyazeva, AI, et al. The spread of bla OXA-48 and bla OXA-244 carbapenemase genes among Klebsiella pneumoniae, Proteus mirabilis and Enterobacter spp. isolated in Moscow, Russia. Ann Clin Microbiol Antimicrob 2015;14:1.Google Scholar
63. Al-Agamy, MH, Shibl, AM, Elkhizzi, NA, Meunier, D, Turton, JF, Livermore, DM. Persistence of Klebsiella pneumoniae clones with OXA-48 or NDM carbapenemases causing bacteraemias in a Riyadh hospital. Diagn Microbiol Infect Dis 2013;76:214216.CrossRefGoogle ScholarPubMed
64. Matar, GM, Cuzon, G, Araj, F, et al. Oxacillinase-mediated resistance to carbapenems in Klebsiella pneumoniae from Lebanon. Clin Microbiol Infect 2008;14:887888.Google Scholar
65. Cuzon, G, Naas, T, Lesenne, A, Benhamou, M, Nordmann, P. Plasmid-mediated carbapenem-hydrolysing OXA-48 β-lactamase in Klebsiella pneumoniae from Tunisia. Int J Antimicrob Agents 2010;36:9193.Google Scholar
66. Lafeuille, E, Decré, D, Mahjoub-Messai, F, Bidet, P, Arlet, G, Bingen, E. OXA-48 carbapenemase-producing Klebsiella pneumoniae isolated from Libyan patients. Microbial Drug Resist 2013;19:491497.Google Scholar
67. Brink, AJ, Coetzee, J, Corcoran, C, et al. Emergence of OXA-48 and OXA-181 carbapenemases among Enterobacteriaceae in South Africa and evidence of in vivo selection of colistin resistance as a consequence of selective decontamination of the gastrointestinal tract. J Clin Microbiol 2013;51:369372.Google Scholar
68. Lascols, C, Peirano, G, Hackel, M, Laupland, KB, Pitout, JD. Surveillance and molecular epidemiology of Klebsiella pneumoniae that produce carbapenemases; the first report of OXA-48-like enzymes in North America. Antimicrob Agents Chemother 2013;57:130136.Google Scholar
69. Williamson, DA, Heffernan, H, Sidjabat, H, et al. Intercontinental transfer of OXA-181-producing Klebsiella pneumoniae into New Zealand. J Antimicrob Chemother 2011;66:28882890.Google Scholar
70. Biedenbach, D, Bouchillon, S, Hackel, M, et al. Dissemination of NDM metallo-β-lactamase genes among clinical isolates of Enterobacteriaceae collected during the SMART global surveillance study from 2008 to 2012. Antimicrob Agents Chemother 2015;59:826830.Google Scholar
71. Teo, JW, Kurup, A, Lin, RT, Hsien, KT. Emergence of clinical Klebsiella pneumoniae producing OXA-232 carbapenemase in Singapore. New Microbes New Infect 2013;1:1315.Google Scholar
72. Jao, Y, Lee, PS, Hung, CT, et al. First report of OXA-48 carbapenemase-producing Escherichia coli in Taiwan. Antimicrob Resist Infect Control 2015;4(Suppl 1):126.Google Scholar
73. Djahmi, N, Dunyach-Remy, C, Pantel, A, Dekhil, M, Sotto, A, Lavigne, JP. Epidemiology of carbapenemase-producing Enterobacteriaceae and Acinetobacter baumannii in Mediterranean countries. BioMed Res Int 2014;2014:305784.CrossRefGoogle ScholarPubMed
74. Samuelsen, Ø, Naseer, U, Karah, N, et al. Identification of Enterobacteriaceae isolates with OXA-48 and coproduction of OXA-181 and NDM-1 in Norway. J Antimicrob Chemother 2013;68:16821685.Google Scholar
75. Walkty, A, Gilmour, M, Simner, P, et al. Isolation of multiple carbapenemase-producing Gram-negative bacilli from a patient recently hospitalized in Nigeria. Diagn Microbiol Infect Dis 2015;81:296298.Google Scholar
76. Carbapenem-resistant Enterobacteriaceae. California Department of Public Health website. http://www.cdph.ca.gov/programs/hai/Pages/Carbapenem-ResistantEnterobacteriaceae.aspx. Accessed September 25, 2016.Google Scholar
77. Centers for Disease Control and Prevention. Guidance for control of infections with carbapenem-resistant or carbapenemase-producing Enterobacteriaceae in acute care facilities. Morb Mortal Wkly Rep 2009;58:256260.Google Scholar
78. Carmeli, Y, Akova, M, Cornaglia, G, et al. Controlling the spread of carbapenemase-producing Gram-negatives: therapeutic approach and infection control. Clin Microbiol Infect 2010;16:102111.CrossRefGoogle ScholarPubMed
79. 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;46:31103111.Google Scholar
80. Carrer, A, Fortineau, N, Nordmann, P. Use of ChromID extended-spectrum beta-lactamase medium for detecting carbapenemase-producing Enterobacteriaceae . J Clin Microbiol 2010;48:19131914.Google Scholar
81. Adler, A, Navon-Venezia, S, Moran-Gilad, J, Marcos, E, Schwartz, D, Carmeli, Y. Laboratory and clinical evaluation of screening agar plates for detection of carbapenem-resistant Enterobacteriaceae from surveillance rectal swabs. J Clin Microbiol 2011;49:22392242.Google Scholar
82. Nordmann, P, Cuzon, G, Naas, T. The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect Dis 2009;9:228236.Google Scholar
83. Wertheim, HF, Vos, MC, Boelens, HA, et al. Low prevalence of methicillin-resistant Staphylococcus aureus (MRSA) at hospital admission in the Netherlands: the value of search and destroy and restrictive antibiotic use. J Hosp Infect 2004;56:321325.Google Scholar
84. Kluytmans–VandenBergh, MFQ, Kluytmans, JAJW, Voss, A. Dutch guideline for preventing nosocomial transmission of highly resistant microorganisms (HRMO). Infection 2005;33:309313.Google Scholar
85. Akova, M, Daikos, GL, Tzouvelekis, L, Carmeli, Y. Interventional strategies and current clinical experience with carbapenemase-producing Gram-negative bacteria. Clin Micro Infect 2012;18:439448.CrossRefGoogle ScholarPubMed
86. McGrath, EJ, Chopra, T, Abdel-Haq, N, et al. An outbreak of carbapenem-resistant Acinetobacter baumannii infection in a neonatal intensive care unit: investigation and control. Infect Control Hosp Epidemiol 2011;32:3441.Google Scholar
87. Schwaber, MJ, Carmeli, Y. An ongoing national intervention to contain the spread of carbapenem-resistant Enterobacteriaceae . Clin Infect Dis 2014;58:697703.Google Scholar
88. Kotsanas, D, Wijesooriya, WR, Korman, TM, et al. “Down the drain”: carbapenem-resistant bacteria in intensive care unit patients and handwashing sinks. Med J Aust 2013;198:267269.Google Scholar
89. Needleman, J, Buerhaus, P, Mattke, S, Stewart, M, Zelevinsky, K. Nurse-staffing levels and the quality of care in hospitals. N Engl J Med 2002;346:17151722.Google Scholar
90. Fedorowsky, R, Peles-Bortz, A, Masarwa, S, Liberman, D, Rubinovitch, B, Lipkin, V. Carbapenem-resistant Enterobacteriaceae carriers in acute care hospitals and postacute-care facilities: The effect of organizational culture on staff attitudes, knowledge, practices, and infection acquisition rates. Am J Infect Control 2015;43:935939.Google Scholar
91. Siegel, JD, Rhinehart, E, Jackson, M, Chiarello, L. 2007 guideline for isolation precautions: preventing transmission of infectious agents in health care settings. Am J Infect Control. 2007(35):S65S164.Google Scholar
92. Wiener-Well, Y, Rudensky, B, Yinnon, AM, et al. Carriage rate of carbapenem-resistant Klebsiella pneumoniae in hospitalised patients during a national outbreak. J Hosp Infect 2010;74:344349.Google Scholar
93. Löfmark, S, Sjöström, K, Mäkitalo, B, Edquist, P, Tegmark Wisell, K, Giske, CG. Carbapenemase-producing Enterobacteriaceae in Sweden 2007–2013: Experiences from seven years of systematic surveillance and mandatory reporting. Drug Resist Updates (2015).Google Scholar
94. Matthaiou, DK, Michalopoulos, A, Rafailidis, PI, et al. Risk factors associated with the isolation of colistin-resistant Gram-negative bacteria: a matched case-control study. Crit Care Med 2008;36:807811.Google Scholar
95. Lerner, A, Romano, J, Chmelnitsky, I, Navon-Venezia, S, Edgar, R, Carmeli, Y. Rectal swabs are suitable for quantifying the carriage load of KPC-producing carbapenem-resistant Enterobacteriaceae . Antimicrob Agents Chemother 2013;57:14741479.Google Scholar
96. Thurlow, CJ, Prabaker, K, Lin, MY, Lolans, K, Weinstein, RA, Hayden, MK. Anatomic sites of patient colonization and environmental contamination with Klebsiella pneumoniae carbapenemase—producing Enterobacteriaceae at long-term acute care hospitals. Infect Control Hosp Epidemiol 2013;34:5661.Google Scholar
97. Schwaber, MJ, Lev, B, Israeli, A, et al. Containment of a country-wide outbreak of carbapenem-resistant Klebsiella pneumoniae in Israeli Hospitals via a nationally implemented intervention. Clin Infect Dis 2011;52:848855.Google Scholar
98. WHO guidelines on hand hygiene in health care. World Health Organization website. http://apps.who.int/iris/bitstream/10665/44102/1/9789241597906_eng.pdf. Accessed January 21, 2017.Google Scholar
99. Sax, H, Allegranzi, B, Uckay, I, Larson, E, Boyce, J, Pittet, D. ‘My five moments for hand hygiene’: a user-centred design approach to understand, train, monitor and report hand hygiene. J Hosp Infect 2007;67:921.Google Scholar
100. Lledo, W, Hernandez, M, Lopez, E, et al. Guidance for control of infections with carbapenem-resistant or carbapenemase-producing Enterobacteriaceae in acute care facilities. Morbid Mortal Wkly Rep 2009;58:256260.Google Scholar
101. Schechner, V, Kotlovsky, T, Tarabeia, J, et al. Predictors of rectal carriage of carbapenem-resistant Enterobacteriaceae (CRE) among patients with known CRE carriage at their next hospital encounter. Infect Control Hosp Epidemiol 2011;32:497503.Google Scholar
102. Ben-David, D, Masarwa, S, Navon-Venezia, S, et al. Carbapenem-resistant Klebsiella pneumoniae in post-acute-care facilities in Israel. Infect Control Hosp Epidemiol 2011;32:845853.Google Scholar
103. Lewis, JD, Enfield, KB, Mathers, AJ, Giannetta, ET, Sifri, CD. The limits of serial surveillance cultures in predicting clearance of colonization with carbapenemase-producing Enterobacteriaceae . Infect Control Hosp Epidemiol 2015;36:13.Google Scholar
104. Feldman, N, Adler, A, Molshatzki, N, et al. Gastrointestinal colonization by KPC-producing Klebsiella pneumoniae following hospital discharge: duration of carriage and risk factors for persistent carriage. Clin Microbiol Infect 2013;19:E190E196.Google Scholar
105. Oren, I, Sprecher, H, Finkelstein, R, et al. Eradication of carbapenem-resistant Enterobacteriaceae gastrointestinal colonization with nonabsorbable oral antibiotic treatment: a prospective controlled trial. Am J Infect Control 2013;41:11671172.CrossRefGoogle ScholarPubMed
106. Facility guidance for control of carbapenem-resistant Enterobacteriaceae (CRE)—November 2015 update CRE toolkit. Centers for Disease Control and Prevention website. https://www.cdc.gov/hai/organisms/cre/cre-toolkit/. Published 2015. Accessed October 2, 2016.Google Scholar
107. Carbapenemase-producing Enterobacteriaceae: early detection, management and control toolkit for acute trusts. Public Health England website. https://www.gov.uk/government/publications/carbapenemase-producing-enterobacteriaceae-early-detection-management-and-control-toolkit-for-acute-trusts. Published 2014. Accessed October 2, 2016.Google Scholar
108. Ben-David, D, Masarwa, S, Adler, A, Mishali, H, Carmeli, Y, Schwaber, MJ. A national intervention to prevent the spread of carbapenem-resistant Enterobacteriaceae in Israeli post-acute care hospitals. Infect Control Hosp Epidemiol 2014;35:802809.Google Scholar
109. Hand hygiene in outpatient and home-based care and long-term care facilities. World Health Organization website. http://www.who.int/gpsc/en/. Published 2016. Accessed October 2, 2016.Google Scholar
110. Rogers, BA, Aminzadeh, Z, Hayashi, Y, Paterson, DL. Country-to-country transfer of patients and the risk of multi-resistant bacterial infection. Clin Infect Dis 2011;53:4956.Google Scholar
111. Lerner, A, Solter, E, Rachi, E, et al. Detection and characterization of carbapenemase-producing Enterobacteriaceae in wounded Syrian patients admitted to hospitals in northern Israel. Eur J Clin Microbiol Infect Dis 2015:16.Google Scholar
112. Reichel, M, Schlicht, A, Ostermeyer, C, Kampf, G. Efficacy of surface disinfectant cleaners against emerging highly resistant Gram-negative bacteria. BMC Infect Dis 2014;14:292.Google Scholar
113. Jawad, A, Seifert, H, Snelling, AM, et al. Survival of Acinetobacter baumannii on dry surfaces: comparison of outbreak and sporadic isolates. J Clin Microbiol 1998;36:19381941.Google Scholar
114. Olson, B, Weinstein, RA, Nathan, C. Epidemiology of endemic Pseudomonas aeruginosa: why infection control efforts have failed. J Infect Dis 1984;150:808816.Google Scholar
115. Simor, AE, Lee, M, Vearncombe, M. An outbreak due to multiresistant Acinetobacter baumannii in a burn unit: risk factors for acquisition and management. Infect Control Hosp Epidemiol 2002;23:261267.Google Scholar
116. 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 Micro Infect 2011;17:12011208.Google Scholar
117. Weber, DJ, Rutala, WA, Kanamori, H, Gergen, MF, Sickbert-Bennett, EE. Carbapenem-Resistant Enterobacteriaceae: frequency of hospital room contamination and survival on various inoculated surfaces. Infect Control Hosp Epidemiol 2015;36:590593.CrossRefGoogle ScholarPubMed
118. Cochard, H, Aubier, B, Quentin, R, van der Mee-Marquet, N. Extended-spectrum β-lactamase-producing Enterobacteriaceae in French nursing homes: an association between high carriage rate among residents, environmental contamination, poor conformity with good hygiene practice, and putative resident-to-resident transmission. Infect Control Hosp Epidemiol 2014;35:384389.Google Scholar
119. Public Health Agency of Canada. Guidance: Infection prevention and control measures for health workers in all health settings. Carbapenem-resistant Gram-negative bacilli. http://www.phac-aspc.gc.ca/nois-sinp/guide/ipcm-mpci/ipcm-mpci-eng.php. Published 2010. Accessed October 15, 2016.Google Scholar
120. Harris, AD, Perencevich, EN, Johnson, JK, et al. Patient-to-patient transmission is important in extended-spectrum β-lactamase–producing Klebsiella pneumoniae acquisition. Clin Infect Dis 2007;45:13471350.Google Scholar
121. Hilty, M, Betsch, BY, Bögli-Stuber, K, et al. Transmission dynamics of extended-spectrum β-lactamase–producing Enterobacteriaceae in the tertiary care hospital and the household setting. Clin Infect Dis 2012;55:967975.Google Scholar
122. Rodríguez-Baño, J, Navarro, MD, Romero, L, et al. Epidemiology and clinical features of infections caused by extended-spectrum beta-lactamase-producing Escherichia coli in nonhospitalized patients. J Clin Microbiol 2004;42:10891094.Google Scholar
123. 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:cis770.Google Scholar
124. Weinstein, RA. Insights into the epidemiology and control of infection with vancomycin-resistant enterococci. Clin Infect Dis 2000;31:10581065.Google Scholar
125. Donlan, RM. Biofilms: microbial life on surfaces. Emerg Infect Dis 2002;8:881890.Google Scholar
126. de Jager, P, Chirwa, T, Naidoo, S, Perovic, O, Thomas, J. Nosocomial outbreak of New Delhi metallo-β-lactamase-1-producing Gram-negative bacteria in South Africa: a case-control study. PloS One 2015;10:e0123337.Google Scholar
127. Gould, CV, Umscheid, CA, Agarwal, RK, Kuntz, G, Pegues, DA. and Healthcare Infection Control Practices Advisory Committee Guideline for prevention of catheter-associated urinary tract infections 2009. Infect Control Hosp Epidemiol 2010;31:319326.Google Scholar
128. Vernon, MO, Hayden, MK, Trick, WE, Hayes, RA, Blom, DW, Weinstein, RA. Chlorhexidine gluconate to cleanse patients in a medical intensive care unit: the effectiveness of source control to reduce the bioburden of vancomycin-resistant enterococci. Arch Intern Med 2006;166:306312.Google Scholar
129. Climo, MW, Yokoe, DS, Warren, DK, et al. Effect of daily chlorhexidine bathing on hospital-acquired infection. N Engl J Med 2013;368:533542.Google Scholar
130. Munoz-Price, LS, Hota, B, Stemer, A, Weinstein, RA. Prevention of bloodstream infections by use of daily chlorhexidine baths for patients at a long-term acute care hospital. Infect Control Hosp Epidemiol 2009;30:10311035.Google Scholar
131. Derde, LPG, Cooper, BS, Goossens, H, et al. 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;14:3139.Google Scholar
132. Hayden, MK, Lin, MY, Lolans, K, et al. Prevention of colonization and infection by Klebsiella pneumoniae carbapenemase–producing Enterobacteriaceae in long-term acute-care hospitals. Clin Infect Dis 2015;60:11531161.Google Scholar
133. de Smet, AMGA, Kluytmans, JAJW, Cooper, BS, et al. Decontamination of the digestive tract and oropharynx in ICU patients. N Engl J Med 2009;360:2031.Google Scholar
134. Shibli, AB, Milbrandt, EB, Baldisseri, M. Dirty mouth? Should you clean it out? Decontamination for the prevention of pneumonia and mortality in the ICU. Crit Care 2010;14:314.Google Scholar
135. Zuckerman, T, Benyamini, N, Sprecher, H, et al. SCT in patients with carbapenem- resistant Klebsiella pneumoniae: A single center experience with oral gentamicin for the eradication of carrier state. Bone Marrow Transplant 2010. doi: 10.1038/bmt.2010.279.Google Scholar
136. Manges, AR, Steiner, TS, Wright, AJ. Fecal microbiota transplantation for the intestinal decolonization of extensively antimicrobial-resistant opportunistic pathogens: a review. Infect Dis 2016;10:16.Google Scholar
137. Fournier, S, Monteil, C, Lepainteur, M, et al. Long-term control of carbapenemase-producing Enterobacteriaceae at the scale of a large French multihospital institution: a nine-year experience, France, 2004 to 2012. Euro Surveill 2014;19.Google Scholar
138. Österblad, M, Kirveskari, J, Hakanen, AJ, Tissari, P, Vaara, M, Jalava, J. Carbapenemase-producing Enterobacteriaceae in Finland: the first years (2008–11). J Antimicrob Chemother 2012;67:28602864.Google Scholar
139. Gupta, N, Limbago, BM, Patel, JB, Kallen, AJ. Carbapenem-resistant Enterobacteriaceae: epidemiology and prevention. Clin Infect Dis 2011;53:6067.CrossRefGoogle ScholarPubMed
140. Canadian Integrated Program for Antimicrobial Resistance (CIPARS). Public Health Agency of Canada website. http://www.phac-aspc.gc.ca/cipars-picra/index-eng.php. Published 2007. Accessed October 19, 2016.Google Scholar
141. What is AGAR? Australasian Group on Antimicrobial Resistance (AGAR) website. http://www.agargroup.org/whatis. Published 2004. Accessed October 19, 2016.Google Scholar
142. WHO. WHO global strategy for containment of antimicrobial resistance. Geneva: WHO; 2001.Google Scholar
143. WHO. The evolving threat of antimicrobial resistance: options for action. Geneva: WHO; 2012.Google Scholar
144. Dumartin, C, Rogues, AM, Amadeo, B, et al. Antibiotic usage in southwestern French hospitals: trends and association with antibiotic stewardship measures. J Antimicrob Chemother 2011;66:16311637.Google Scholar
145. Colligan, C, Sneddon, J, Bayne, G, Malcolm, W, Walker, G, Nathwani, D. Six years of a national antimicrobial stewardship programme in Scotland: where are we now? Antimicrob Resist Infect Control 2015;4:15.Google Scholar
146. Howard, P, Pulcini, C, Levy Hara, G, et al. An international cross-sectional survey of antimicrobial stewardship programmes in hospitals. J Antimicrob Chemother 2015;70:12451255.Google Scholar
147. Jamtvedt, G, Young, JM, Kristoffersen, DT, O’Brien, MA, Oxman, AD. Audit and feedback: effects on professional practice and health care outcomes. Cochrane Database Syst Rev 2006;2(2).Google Scholar
148. Chen, JH, Siu, LK, Fung, CP, et al. Contribution of outer membrane protein K36 to antimicrobial resistance and virulence in Klebsiella pneumoniae . J Antimicrob Chemother 2010;65:986990.Google Scholar
149. Giske, CG, Fröding, I, Hasan, CM, et al. Diverse sequence types of Klebsiella pneumoniae contribute to the dissemination of blaNDM-1 in India, Sweden, and the United Kingdom. Antimicrob Agents Chemother 2012;56:27352738.Google Scholar
150. Deshpande, LM, Jones, RN, Fritsche, TR, Sader, HS. Occurrence and characterization of carbapenemase-producing Enterobacteriaceae: report from the SENTRY Antimicrobial Surveillance Program (2000–2004). Microbiol Drug Resist 2006;12:223230.Google Scholar
151. Sievert, DM, Ricks, P, Edwards, JR, et al , and for the National Healthcare Safety Network (NHSN) Team and Participating NHSN Facilities. 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, 2009–2010. Infect Control Hosp Epidemiol 2013;34:114.Google Scholar
152. Central Asian and Eastern European surveillance of antimicrobial resistance. World Health Organization Europe website. http://www.euro.who.int/__data/assets/pdf_file/0006/285405/CAESAR-Surveillance-Antimicrobial-Resistance2014.pdf?ua=1. Published 2014. Accessed October 2, 2016.Google Scholar
153. Study for monitoring antimicrobial resistant trends (SMART)- IFPM. International Federation of Pharmaceutical Manufacturers website. http://partnerships.ifpma.org/partnership/study-formonitoring-antimicrobial-resistance-trends-smart. Published 2016. Accessed January 23, 2017.Google Scholar
154. Walsh, TR, Weeks, J, Livermore, DM, Toleman, MA. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect Dis 2011;11:355362.Google Scholar
155. Scotta, C, Juan, C, Cabot, G, et al. Environmental microbiota represents a natural reservoir for dissemination of clinically relevant metallo-β-lactamases. Antimicrob Agents Chemother 2011;55:53765379.Google Scholar
156. Chagas, TP, Seki, LM, da Silva, DM, Asensi, MD. Occurrence of KPC-2-producing Klebsiella pneumoniae strains in hospital wastewater. J Hosp Infect 2011;77:281.Google Scholar
157. Knaizeh, EG, Workman, SN. Carbapenemase-producing Enterobacteriaceae detected in sewage on the island of Barbados. Presented at Caribbean Public Health Agency 59th Annual Scientific Meeting, May 2014. Caribbean Public Health Agency website. http://conference.carpha.org/Portals/0/docs/CARPHA_CHRC_Programme.pdf. Published 2014. Accessed October 10, 2016.Google Scholar
158. Abdallah, HM, Reuland, EA, Wintermans, BB, et al. Extended-spectrum β-lactamases and/or carbapenemases-producing Enterobacteriaceae isolated from retail chicken meat in Zagazig, Egypt. PloS One 2015;10:e0136052.Google Scholar
159. Zurfluh, K, Poirel, L, Nordmann, P, Klumpp, J, Stephan, R. First detection of Klebsiella variicola producing OXA-181 carbapenemase in fresh vegetable imported from Asia to Switzerland. Antimicrob Resist Infect Control 2015;4:13.Google Scholar
160. Schwaber, MJ, Carmeli, Y. Carbapenem-resistant Enterobacteriaceae: a potential threat. JAMA 2008;300:29112913.Google Scholar