Infection control implications of heterogeneous resistance mechanisms in carbapenem-resistant Enterobacteriaceae (CRE)

Expert Review of Anti-Infective Therapy

Volumn 14, Issue 1, 2016, Pages 95-108

  Goodman, K E ^a   Simner, P J ^b   Tamma, P D ^a,b   Milstone, A M ^a,b,c  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

Antibiotic stewardship (AS); Antimicrobial drug resistance; Carbapenem resistant Enterobacteriaceae (CRE); Carbapenemase; Carbapenemase producing Enterobacteriaceae (CPE); Hospital epidemiology; Transmission

Indexed keywords

ANTIBIOTIC AGENT; CARBAPENEM; CARBAPENEMASE; DORIPENEM; ERTAPENEM; IMIPENEM; MEROPENEM; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; BETA LACTAMASE; CARBAPENEM DERIVATIVE;

ANTIBIOTIC RESISTANCE; BACTERIAL COLONIZATION; BACTERIAL TRANSMISSION; BACTERIUM CONTAMINATION; CARBAPENEM RESISTANT ENTEROBACTERIACEAE; CLONE; DRUG EFFECT; DRUG EXPOSURE; ENTEROBACTERIACEAE INFECTION; ENVIRONMENTAL FACTOR; ENZYME SYNTHESIS; GENETIC REASSORTMENT; HEALTH CARE PERSONNEL; HEALTH CARE POLICY; HOSPITAL INFECTION; HOSPITAL PATIENT; HUMAN; INFECTION CONTROL; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN EXPRESSION; REVIEW; CHEMISTRY; COMMUNICABLE DISEASE CONTROL; CROSS INFECTION; DRUG EFFECTS; ENTEROBACTERIACEAE; ENTEROBACTERIACEAE INFECTIONS; ENZYMOLOGY; EPIDEMIOLOGICAL MONITORING; GENE EXPRESSION; GENETICS; HORIZONTAL GENE TRANSFER; METABOLISM; MICROBIOLOGY; MOLECULAR EPIDEMIOLOGY; MUTATION; PLASMID; PROCEDURES; TRANSMISSION; UNITED STATES;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; CARBAPENEMS; COMMUNICABLE DISEASE CONTROL; CROSS INFECTION; ENTEROBACTERIACEAE; ENTEROBACTERIACEAE INFECTIONS; EPIDEMIOLOGICAL MONITORING; GENE EXPRESSION; GENE TRANSFER, HORIZONTAL; HUMANS; MOLECULAR EPIDEMIOLOGY; MUTATION; PLASMIDS; UNITED STATES;

EID: 84954395700     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/14787210.2016.1106940     Document Type: Review

References (120)

1. Hussein K, Sprecher H, Mashiach T, et al. Carbapenem resistance among Klebsiella pneumoniae isolates: risk factors, molecular characteristics, and susceptibility patterns. Infect Control Hosp Epidemiol. 2009;30(7):666-671
2. Castanheira M, Sader HS, Jones RN. Antimicrobial susceptibility patterns of KPC-producing or CTX-M-producing Enterobacteriaceae. Microb Drug Resist. 2010;16(1):61-65
3. Elemam A, Rahimian J, Mandell W. Infection with panresistant Klebsiella pneumoniae: a report of 2 cases and a brief review of the literature. Clin Infect Dis. 2009;49(2):271-274
4. Bratu S, Landman D, Haag R, et al. Rapid spread of carbapenem-resistant Klebsiella pneumoniae in New York City: a new threat to our antibiotic armamentarium. Arch Intern Med. 2005;165 (12):1430-1435
5. Patel G, Huprikar S, Factor S, et al. Outcomes of carbapenem-resistant Klebsiella pneumoniae infection and the impact of antimicrobial and adjunctive therapies. Infect Control Hosp Epidemiol. 2008;29(12):1099-1106
6. Schwaber MJ, Klarfeld-Lidji S, Navon-Venezia S, et al. Predictors of carbapenem-resistant Klebsiella pneumoniae acquisition among hospitalized adults and effect of acquisition on mortality. Antimicrob Agents Chemother. 2008;52 (3):1028-1033
7. Lübbert C, Becker-Rux D, Rodloff AC, et al. Colonization of liver transplant recipients with KPC-producing Klebsiella pneumoniae is associated with high infection rates and excess mortality: a case-control analysis. Infection. 2014;42 (2):309-316
8. Livingstone D, Gill MJ, Wise R. Mechanisms of resistance to the carbapenems. J Antimicrob Chemother. 1995;35 (1):1-5
9. Bush K, Jacoby GA. Updated functional classification of beta-lactamases. Antimicrob Agents Chemother. 2010;54 (3):969-976
10. Ambler RP. The structure of beta-lactamases. Philos Trans R Soc Lond B Biol Sci. 1980;289(1036):321-331
11. Muscarella LF. Risk of transmission of carbapenem-resistant Enterobacteriaceae and related "superbugs" during gastrointestinal endoscopy. World J Gastrointest Endosc. 2014;6(10):457-474
12. Laurent C, Rodriguez-Villalobos H, Rost F, et al. Intensive care unit outbreak of extended-spectrum -lactamase-producing Klebsiella pneumoniae controlled by cohorting patients and reinforcing infection control measures. Infect Control Hosp Epidemiol. 2008;29(6):517-524
13. Piednoir E, et al. Long-term clinical and economic benefits associated with the management of a nosocomial outbreak resulting from extended-spectrum beta-lactamase-producing Klebsiella pneumoniae. Crit Care Med. 2011;39(12):2672-2677
14. Oteo J, Perez-Vazquez M, Campos J. Extended-spectrum -lactamase producing Escherichia coli: changing epidemiology and clinical impact. Curr Opin Infect Dis. 2010;23(4):320-326
15. CLSI, C.L.S.I. Performance standards for antimicrobial susceptibility testing: twentieth informational supplement (M100-S20). Wayne (PA): CLSI; 2010
16. CLSI, C.L.S.I. Performance standards for antimicrobial susceptibility testing: twenty-second informational supplement (M100-S22). Wayne, PA: CLSI; 2012
17. CDC, C.f.D.C.a.P. FAQs about choosing and implementing a CRE definition. 2015 Jun 29; Available from: http://www. cdc.gov/hai/organisms/cre/definition.html
18. Chea N, Bulens SN, Kongphet-Tran T, et al. Improved phenotype-based definition for identifying carbapenemase producers among carbapenem-resistant Enterobacteriaceae. Emerg Infect Dis. 2015;21(9):1611-1616
19. Tzouvelekis LS, Markogiannakis A, Piperaki E, et al. Treating infections caused by carbapenemase-producing Enterobacteriaceae. Clin Microbiol Infect. 2014;20(9):862-872
20. Morrill HJ, Pogue JM, Kaye KS, et al. Treatment options for carbapenem-resistant Enterobacteriaceae infections. Open Forum Infect Dis. 2015;2(2):ofv050
21. Rasmussen BA, et al. Characterization of IMI-1 beta-lactamase, a class A carbapenem-hydrolyzing enzyme from Enterobacter cloacae. Antimicrob Agents Chemother. 1996;40(9):2080-2086
22. Conlan S, Deming C, Tsai Y-C, et al. Complete genome sequence of a Klebsiella pneumoniae Isolate with chromosomally encoded carbapenem resistance and colibactin synthesis loci. Genome Announc. 2014;2(6):pii: e01332-14
23. Espedido B, Iredell J, Thomas L, et al. Wide dissemination of a carbapenemase plasmid among gram-negative bacteria: implications of the variable phenotype. J Clin Microbiol. 2005;43(9):4918-4919
24. Hu L, Zhong Q, Shang Y, et al. The prevalence of carbapenemase genes and plasmid-mediated quinolone resistance determinants in carbapenem-resistant Enterobacteriaceae from five teaching hospitals in central China. Epidemiol Infect. 2014;142(9):1972-1977
25. Huang T-D, Berhin C, Bogaerts P, et al. Prevalence and mechanisms of resistance to carbapenems in Enterobacteriaceae isolates from 24 hospitals in Belgium. J Antimicrob Chemother. 2013;68 (8):1832-1837
26. Rock C, et al. Frequency of Klebsiella pneumoniae carbapenemase (KPC)-producing and non-KPC-producing Klebsiella species contamination of healthcare workers and the environment. Infect Control Hosp Epidemiol. 2014;35 (4):426-429
27. Woodford N, Reddy S, Fagan EJ, et al. Wide geographic spread of diverse acquired AmpC beta-lactamases among Escherichia coli and Klebsiella spp. in the UK and Ireland. J Antimicrob Chemother. 2007;59(1):102-105
28. Jacoby GA. AmpC beta-lactamases. Clin Microbiol Rev. 2009;22(1):161-182. Table of Contents
29. Doumith M, Ellington MJ, Livermore DM, et al. Molecular mechanisms disrupting porin expression in ertapenemresistant Klebsiella and Enterobacter spp. clinical isolates from the UK. J Antimicrob Chemother. 2009;63(4):659-667
30. Livermore DM, Yang YJ. Beta-lactamase lability and inducer power of newer betalactam antibiotics in relation to their activity against beta-lactamase-inducibility mutants of Pseudomonas aeruginosa. J Infect Dis. 1987;155(4):775-782
31. Girlich D, Poirel L, Nordmann P. Do CTX-M beta-lactamases hydrolyse ertapenem? J Antimicrob Chemother. 2008;62(5):1155-1156
32. Livermore DM, Woodford N. The -lactamase threat in Enterobacteriaceae, Pseudomonas and Acinetobacter. Trends Microbiol. 2006;14(9):413-420
33. Poirel L, Heritier C, Spicq C, et al. In vivo acquisition of high-level resistance to imipenem in Escherichia coli. J Clin Microbiol. 2004;42(8):3831-3833
34. Oteo J, Delgado-Iribarren A, Vega D, et al. Emergence of imipenem resistance in clinical Escherichia coli during therapy. Int J Antimicrob Agents. 2008;32 (6):534-537
35. Kruse EB, Aurbach U, Wisplinghoff H. Carbapenem-resistant Enterobacteriaceae: laboratory detection and infection control practices. Curr Infect Dis Rep. 2013. doi:10.1007/s11908-013-0373-x. Epub ahead of print
36. Hrabak J, Chudackova E, Papagiannitsis CC. Detection of carbapenemases in Enterobacteriaceae: a challenge for diagnostic microbiological laboratories. Clin Microbiol Infect. 2014;20(9):839-853
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(2):477-479
38. Carvalhaes CG, Picao RC, Nicoletti AG, et al. Cloverleaf test (modified Hodge test) for detecting carbapenemase production in Klebsiella pneumoniae: be aware of false positive results. J Antimicrob Chemother. 2010;65(2):249-251
39. Vasoo S, Cunningham SA, Kohner PC, 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):3097-3101
40. Dortet L, Bréchard L, Poirel L, et al. Rapid detection of carbapenemase-producing Enterobacteriaceae from blood cultures. Clin Microbiol Infect. 2014;20 (4):340-344
41. Pasteran F, Veliz O, Ceriana P, et al. Evaluation of the blue-carba test for rapid detection of carbapenemases in gram-negative bacilli. J Clin Microbiol. 2015;53(6):1996-1998
42. Huang TD, Berhin C, Bogaerts P, et al. Comparative evaluation of two chromogenic tests for rapid detection of carbapenemase in Enterobacteriaceae and in Pseudomonas aeruginosa isolates. J Clin Microbiol. 2014;52(8):3060-3063
43. Simner PJ, Gilmour MW, DeGagne P, et al. Evaluation of five chromogenic agar media and the Rosco Rapid Carb screen kit for detection and confirmation of carbapenemase production in gramnegative bacilli. J Clin Microbiol. 2015;53(1):105-112
44. CLSI, C.a.L.S.I. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-fifth Informational Supplement, in M100-S25. Wayne (PA); 2015 Jan
45. Giani T, et al. Epidemic diffusion of KPC carbapenemase-producing Klebsiella pneumoniae in Italy: results of the first countrywide survey, 15 May to 30 June 2011. Euro Surveill. 2013;18(22):pii 20489
46. 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(9):845-853
47. 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(8):809-817
48. 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(4):344-349
49. Marchaim D, Chopra T, Bhargava A, et al. Recent exposure to antimicrobials and carbapenem-resistant Enterobacteriaceae: the role of antimicrobial stewardship. Infect Control Hosp Epidemiol. 2012;33(8):817-830
50. 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 (10):984-992
51. Shapiro RS. Antimicrobial-induced DNA damage and genomic instability in microbial pathogens. PLoS Pathog. 2015;11(3):e1004678
52. Cirz RT, Chin JK, Andes DR, et al. Inhibition of mutation and combating the evolution of antibiotic resistance. PLoS Biol. 2005;3(6):e176
53. Thi TD, Lopez E, Rodriguez-Rojas A, et al. Effect of recA inactivation on mutagenesis of Escherichia coli exposed to sublethal concentrations of antimicrobials. J Antimicrob Chemother. 2011;66 (3):531-538
54. Smith BT, Walker GC. Mutagenesis and more: umuDC and the Escherichia coli SOS response. Genetics. 1998;148 (4):1599-1610
55. Queenan AM, Bush K. Carbapenemases: the versatile beta-lactamases. Clin Microbiol Rev. 2007;20(3):440-458. table of contents
56. Warner DM, Yang Q, Duval V, et al. Involvement of MarR and YedS in carbapenem resistance in a clinical isolate of Escherichia coli from China. Antimicrob Agents Chemother. 2013;57(4):1935-1937
57. Chia JH, Siu LK, Su LH, et al. Emergence of carbapenem-resistant Escherichia coli in Taiwan: resistance due to combined CMY-2 production and porin deficiency. J Chemother. 2009;21 (6):621-626
58. Yang Q, Wang H, Sun H, et al. Phenotypic and genotypic characterization of Enterobacteriaceae with decreased susceptibility to carbapenems: results from large hospital-based surveillance studies in China. Antimicrob Agents Chemother. 2010;54(1):573-577
59. Tamma PD, et al. Carbapenem therapy is associated with improved survival compared with piperacillin-tazobactam for patients with extended-spectrum betalactamase bacteremia. Clin Infect Dis. 2015;60(9):1319-1325
60. Treviño M, Moldes L, Martínez-Lamas L, et al. Carbapenem-resistant Enterobacter cloacae and the emergence of metallo-lactamase-producing strains in a thirdlevel hospital (Santiago de Compostela, NW Spain). Eur J Clin Microbiol Infect Dis. 2009;28(10):1253-1258
61. Kim J, Lee JY, Kim SI, et al. Rates of fecal transmission of extended-spectrum -lactamase-producing and Carbapenem-resistant Enterobacteriaceae among patients in intensive care units in Korea. Ann Lab Med. 2014;34(1):20-25
62. Grobner S, et al. Emergence of carbapenem-non-susceptible extended-spectrum beta-lactamase-producing Klebsiella pneumoniae isolates at the university hospital of Tubingen, Germany. J Med Microbiol. 2009;58(Pt 7):912-922
63. Garcia-Fernandez A, Miriagou V, Papagiannitsis CC, et al. An ertapenemresistant extended-spectrum-beta-lactamase-producing Klebsiella pneumoniae clone carries a novel OmpK36 porin variant. Antimicrob Agents Chemother. 2010;54(10):4178-4184
64. Lartigue M-F, Poirel L, Poyart C, et al. Ertapenem resistance of Escherichia coli. Emerg Infect Dis. 2007;13(2):315-317
65. Armand-Lefevre 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(3):1488-1495
66. Cheng VC, et al. Proactive infection control measures to prevent nosocomial transmission of carbapenem-resistant Enterobacteriaceae in a non-endemic area. Chin Med J (Engl). 2013;126(23):4504-4509
67. Huang T-W, Chen T-L, Chen Y-T, et al. Copy number change of the NDM-1 sequence in a multidrug-resistant Klebsiella pneumoniae clinical isolate. PLoS One. 2013;8(4):e62774
68. Schechner V, Kotlovsky T, Kazma M, et al. Asymptomatic rectal carriage of blaKPC producing carbapenem-resistant Enterobacteriaceae: who is prone to become clinically infected? Clin Microbiol Infect. 2013;19(5):451-456
69. Shanthi M, Sowmiya M, Malathi J, et al. Clonal diversity of New Delhi metallobetalactamase-1 producing Enterobacteriaceae in a tertiary care centre. Indian J Med Microbiol. 2013;31 (3):237-241
70. Temkin E, Adler A, Lerner A, et al. Carbapenem-resistant Enterobacteriaceae: biology, epidemiology, and management. Ann N Y Acad Sci. 2014;1323:22-42
71. Bilavsky E, Schwaber MJ, Carmeli Y. How to stem the tide of carbapenemaseproducing enterobacteriaceae: Proactive versus reactive strategies. Curr Opin Infect Dis. 2010;23(4):327-331
72. Sistanizad M, et al. Carbapenem restriction and its effect on bacterial resistance in an intensive care unit of a teaching hospital. Iran J Pharm Res. 2013;12 (3):503-509
73. Stoesser N, Giess A, Batty EM, et al. Genome sequencing of an extended series of NDM-producing Klebsiella pneumoniae isolates from neonatal infections in a Nepali hospital characterizes the extent of community-versus hospitalassociated transmission in an endemic setting. Antimicrob Agents Chemother. 2014;58(12):7347-7357
74. Bonten MJ. Colonization pressure: a critical parameter in the epidemiology of antibiotic-resistant bacteria. Crit Care. 2012;16(4):142
75. Merrer J, Santoli F, Vecchi CA-D, et al. "Colonization pressure" and risk of acquisition of methicillin-resistant staphylococcus aureus in a medical intensive care unit. Infect Control Hosp Epidemiol. 2000;21(11):718-723
76. Popoola VO, Carroll KC, Ross T, et al. Impact of colonization pressure and strain type on methicillin-resistant Staphylococcus aureus transmission in children. Clin Infect Dis. 2013;57 (10):1458-1460
77. Williams VR, Callery S, Vearncombe M, et al. The role of colonization pressure in nosocomial transmission of methicillinresistant Staphylococcus aureus. Am J Infect Control. 2009;37(2):106-110
78. Schwaber MJ, Carmeli Y. An ongoing national intervention to contain the spread of carbapenem-resistant enterobacteriaceae. Clin Infect Dis. 2014;58 (5):697-703
79. 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(7):848-855
80. Sypsa V, Psichogiou M, Bouzala G-A, et al. Transmission dynamics of carbapenemase-producing Klebsiella pneumoniae and anticipated impact of infection control strategies in a surgical unit. PLoS One. 2012;7(7):e41068
81. CDC, C.f.D.C.a.P. CRE toolkit: Guidance for control of carbapenemresistant enterobacteriaceae (CRE). Atlanta (GA): CDC; 2012
82. Palmore TN, Henderson DK. Managing transmission of carbapenem-resistant enterobacteriaceae in healthcare settings: a view from the trenches. Clin Infect Dis. 2013;57(11):1593-1599.
83. Guet-Revillet H, Le Monnier A, Breton N, et al. Environmental contamination with extended-spectrum -lactamases: Is there any difference between Escherichia coli and Klebsiella spp? Am J Infect Control. 2012;40(9):845-848
84. Freeman JT, Nimmo J, Gregory E, et al. Predictors of hospital surface contamination with Extended-spectrum -lactamase-producing Escherichia coli and Klebsiella pneumoniae: patient and organism factors. Antimicrob Resist Infect Control. 2014;3(1):5
85. Lerner A, Adler A, Abu-Hanna J, et al. Environmental contamination by carbapenem-resistant Enterobacteriaceae. J Clin Microbiol. 2013;51(1):177-181
86. Otter JA, French GL. Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor. J Clin Microbiol. 2009;47(1):205-207
87. Havill NL, Boyce JM, Otter JA. Extended survival of carbapenem-resistant Enterobacteriaceae on dry surfaces. Infect Control Hosp Epidemiol. 2014;35 (4):445-447
88. Snitkin ES, Zelazny AM, Thomas PJ, et al. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med. 2012;4(148):148ra116
89. Naas T, Cuzon G, Babics A, et al. Endoscopy-associated transmission of carbapenem-resistant Klebsiella pneumoniae producing KPC-2 beta-lactamase. J Antimicrob Chemother. 2010;65 (6):1305-1306
90. Kola A, Piening B, Pape U-F, et al. An outbreak of carbapenem-resistant OXA-48-producing Klebsiella pneumonia associated to duodenoscopy. Antimicrob Resist Infect Control. 2015;4:8
91. Centers for Disease Control and Prevention. Notes from the Field: New Delhi metallo-beta-lactamase-producing Escherichia coli associated with endoscopic retrograde cholangiopancreatography-Illinois, 2013. MMWR Morb Mortal Wkly Rep. 2014;62(51-52):1051
92. Harris AD, Johnson JK, Thom KA, et al. Risk factors for development of intestinal colonization with imipenem-resistant Pseudomonas aeruginosa in the intensive care unit setting. Infect Control Hosp Epidemiol. 2011;32(7):719-722
93. Marchaim D, Perez F, Lee J, et al. "Swimming in resistance": Co-colonization with carbapenem-resistant Enterobacteriaceae and Acinetobacter baumannii or Pseudomonas aeruginosa. Am J Infect Control. 2012;40(9):830-835
94. Mathers AJ, Cox HL, Kitchel B, et al. Molecular dissection of an outbreak of carbapenem-resistant enterobacteriaceae reveals Intergenus KPC carbapenemase transmission through a promiscuous plasmid. MBio. 2011;2(6):e00204-11
95. Li P, Yang C, Xie J, et al. Acinetobacter calcoaceticus from a fatal case of pneumonia harboring bla NDM-1 on a widely distributed plasmid. BMC Infect Dis. 2015;15:131
96. Epson EE, Pisney LM, Wendt JM, et al. Carbapenem-resistant Klebsiella pneumoniae producing New Delhi Metallo-Lactamase at an Acute Care Hospital, Colorado, 2012. Infect Control Hosp Epidemiol. 2014;35(04):390-397
97. Lachish T, Elimelech M, Arieli N, et al. Emergence of New Delhi metallo-lactamase in Jerusalem, Israel. Int J Antimicrob Agents. 2012;40(6):566-567
98. Goren MG, Carmeli Y, Schwaber MJ, et al. Transfer of carbapenem-resistant plasmid from Klebsiella pneumoniae ST258 to Escherichia coli in patient. Emerg Infect Dis. 2010;16(6):1014-1017
99. Kitchel B, Rasheed JK, Patel JB, et al. Molecular epidemiology of KPC-producing Klebsiella pneumoniae isolates in the United States: clonal expansion of multilocus sequence type 258. Antimicrob Agents Chemother. 2009;53(8):3365-3370
100. Munoz-Price LS, Poirel L, Bonomo RA, et al. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect Dis. 2013;13 (9):785-796
101. Bowers JR, Kitchel B, Driebe EM, et al. Genomic analysis of the emergence and rapid global dissemination of the clonal group 258 Klebsiella pneumoniae pandemic. PLoS One. 2015;10(7):e0133727
102. Leavitt A, Chmelnitsky I, Colodner R, et al. Ertapenem resistance among extended-spectrum-beta-lactamasewww producing Klebsiella pneumoniae isolates. J Clin Microbiol. 2009;47(4):969-974
103. Oregon Health Authority. Guidance for control of carbapenem-resistant Enterobacteriaceae (CRE): 2013 Oregon toolkit. C.f.P.H. Practice, editor. Oregon: Center for Public Health Practice Acute and Communicable Disease Prevention Program; 2013
104. Herbert S, Halvorsen DS, Leong T, et al. Large outbreak of infection and colonization with gram-negative pathogens carrying the Metallo-Lactamase gene bla IMP-4 at a 320-bed tertiary hospital in Australia. Infect Control Hosp Epidemiol. 2007;28(1):98-101
105. Ruppé E, Armand-Lefèvre L, Estellat C, et al. High rate of acquisition but short duration of carriage of multidrug-resistant Enterobacteriaceae after travel to the tropics. Clin Infect Dis. 2015;61(4):593-600
106. Feldman N, Adler A, Molshatzki N, et al. Gastrointestinal colonization by KPCproducing Klebsiella pneumoniae following hospital discharge: duration of carriage and risk factors for persistent carriage. Clin Microbiol Infect. 2013;19 (4):E190-6
107. Zimmerman FS, Assous MV, Bdolah-Abram T, et al. Duration of carriage of carbapenem-resistant Enterobacteriaceae following hospital discharge. Am J Infect Control. 2013;41(3):190-194
108. O'Fallon E, Gautam S, D'Agata EM. Colonization with multidrug-resistant gram-negative bacteria: prolonged duration and frequent cocolonization. Clin Infect Dis. 2009;48(10):1375-1381
109. 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 (5):497-503
110. Sassone-Corsi M, Raffatellu M. No vacancy: how beneficial microbes cooperate with immunity to provide colonization resistance to pathogens. J Immunol. 2015;194(9):4081-4087
111. Spees AM, Lopez CA, Kingsbury DD, et al. Colonization resistance: battle of the bugs or Menage a Trois with the host? PLoS Pathog. 2013;9(11):e1003730
112. Nord CE, Sillerstrom E, Wahlund E. Effect of tigecycline on normal oropharyngeal and intestinal microflora. Antimicrob Agents Chemother. 2006;50 (10):3375-3380
113. Wei Y, Gong J, Zhu W, et al. Fecal microbiota transplantation restores dysbiosis in patients with methicillin resistant Staphylococcus aureus enterocolitis. BMC Infect Dis. 2015;15:265
114. Morgan DJ, Liang S, Smith C, et al. Frequent multidrug-resistant Acinetobacter baumannii contamination of gloves, gowns, and hands of healthcare workers. Infect Control Hosp Epidemiol. 2010;31(7):716-721
115. Morgan DJ, Rogawski E, Thom KA, et al. Transfer of multidrug-resistant bacteria to healthcare workers' gloves and gowns after patient contact increases with environmental contamination. Crit Care Med. 2012;40(4):1045-1051
116. Hong JH, Clancy CJ, Cheng S, et al. Characterization of porin expression in Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae identifies isolates most susceptible to the combination of colistin and carbapenems. Antimicrob Agents Chemother. 2013;57 (5):2147-2153
117. Kazi M, Shetty A, Rodrigues C. The carbapenemase menace: do dual mechanisms code for more resistance? Infect Control Hosp Epidemiol. 2015;36(1):116-117
118. Barnes SL, Morgan DJ, Harris AD, et al. Preventing the transmission of multidrugresistant organisms: modeling the relative importance of hand hygiene and environmental cleaning interventions. Infect Control Hosp Epidemiol. 2014;35 (9):1156-1162
119. Doan TN, Kong DCM, Kirkpatrick CMJ, et al. Optimizing hospital infection control: the role of mathematical modeling. Infect Control Hosp Epidemiol. 2014;35(12):1521-1530
120. Haverkate MR, et al. Modeling spread of KPC-producing bacteria in long-term Acute Care Hospitals in the Chicago region, USA. Infect Control Hosp Epidemiol. 2015;36(10):1148-1154.