Screening for carbapenem-resistant Enterobacteriaceae: Who, When, and How?

Figures & data

Table 1. Plasmid-encoded carbapenemases of primary concern.⁷

Molecular Class	Functional Group	Enzyme	Endemic region
A^a	2f	KPC	Argentina, China, Colombia, Greece, Israel, Italy, North America, Poland
		GES	Brazil
B^b	3	NDM	China, India, Kenya
		IMP	China, Greece, Japan, India
		VIM	Brazil, France, Germany, Greece, India, Ireland, Italy, Japan, Lebanon, Poland, Portugal, UK
D^a	2d	OXA	Africa, Belgium, Canada, Germany, Israel, Lebanon, Middle East, Morocco, Switzerland, Turkey

Notes. Key: KPC-Klebsiella pneumoniae carbapenemase; GES-Guiana extended spectrum; NDM-New Delhi metallo-β-lactamase, IMP-active on imipenem; VIM-Verona integron-encoded metallo-ß-lactamase; GIM-German imipenemase; SPM-Sao Paulo metallo-ß-lactamase; OXA-oxacillin-hydrolyzing.

^a Class A and D ß-lactamases have serine at active site and are inhibited by clavulanic acid.

^b Class B ß-lactamases (metallo-enzymes) utilize zinc at active site and are inhibited by EDTA.

Figure 1. CRE screening in acute care facilities.

Table 2. CLSI and EUCAST carbapenem susceptibility testing breakpoints (µg/ml)^a.

	CLSI			EUCAST
	S	I	R	Clinical S/I	Screening for CPO
Doripenem	≤ 1	2	≥ 4	≤ 1	—
Imipenem	≤ 1	2	≥ 4	≤ 2	>1
Meropenem	≤ 1	2	≥ 4	≤ 2	>0 .12
Ertapenem	≤ 0.5	1	≥ 2	≤ 0.5	>0 .12

Notes.

^a S, susceptible; I, intermediate, R, resistant.^40,45

Table 3. Evaluations of culture-based CRE screening methods on rectal or perirectal swabs.

Method	No. of specimens tested	Carbapenemases (no. isolates)	Sensitivity (%)	Specificity (%)	References
CDC protocol	177	KPC (85)/VIM (1)	98.8	80.2	^55
	200	KPC (63)/VIM (29)	89.1	86.4	^58
	149	KPC (33)	65.6	49.6	^57
	126	KPC (46)	78.3	100	^56
	302	OXA-48 (33)	57.6	95.2	^59
MacConkey agar with carbapenem disk	139	KPC (33)	75.8	89.6	^51
	122	KPC (41)	92.7	95.9	^61
	187	KPC (54)	87	100	^62
	150	KPC (47)	83	73.8	^63
	189	KPC (60)/VIM (9)/KPC & VIM (26)/OXA-48 (3)	96.9	98.9	^64
MacConkey agar with imipenem	139	KPC (33)	84.9	94.3	^51
	755	KPC (64)	87.5	99.4	^65
	177	KPC (85)/VIM (1)	89.5	31.9	^55
	126	KPC (33)/VIM (13)	78.3	97.5	^66
MacConkey agar with meropenem	200	KPC (63)/VIM (29)	89.1	85.2	^58
CHROMagar KPC	139	KPC (33)	84.9	88.7	^51
	122	KPC (41)	100	98.4	^61
	95	KPC (66)	77.3	100	^70
	150	KPC (47)	76	75.7	^63
	126	KPC (33)/VIM (13)	97.8	98.7	^66
chromID Carba	177	KPC (85)/VIM (1)	96.5	91.2	^55
	200	KPC (63)/VIM (29)	92.4	96.9	^58
	302	OXA-48 (33)	57.6	98.9	^59
chromID OXA-48	302	OXA-48 (33)	75.8	99.3	^59
Brilliance CRE	77	OXA-48 (10)	80	86.6	^83
HardyChrom	126	KPC (46)	76.1	100	^56
Supercarba	77	OXA-48 (10)	80	98.5	^83
SpectraCRE	150	KPC (47)	97.8	86.4	^63

Queenan AM, Bush K. Carbapenemases: the versatile β-lactamases. Clin Microbiol Rev 2007; 20:440-58, table of contents; PMID:17630334; https://doi.org/10.1128/CMR.00001-07

 PubMed Web of Science ®Google Scholar

Papadimitriou-Olivgeris M, Bartzavali C, Christofidou M, Bereksi N, Hey J, Zambardi G, Spiliopoulou I. Performance of chromID(R) CARBA medium for carbapenemases-producing Enterobacteriaceae detection during rectal screening. Eur J Clin Microbiol Infect Dis 2014; 33:35-40; PMID:23912722; https://doi.org/10.1007/s10096-013-1925-6

 PubMed Web of Science ®Google Scholar

Vrioni G, Daniil I, Voulgari E, Ranellou K, Koumaki V, Ghirardi S, Kimouli M, Zambardi G, Tsakris A. Comparative evaluation of a prototype chromogenic medium (ChromID CARBA) for detecting carbapenemase-producing Enterobacteriaceae in surveillance rectal swabs. J Clin Microbiol 2012; 50:1841-6; PMID:22461675; https://doi.org/10.1128/JCM.06848-11

 PubMed Web of Science ®Google Scholar

Lolans K, Calvert K, Won S, Clark J, Hayden MK. Direct ertapenem disk screening method for identification of KPC-producing Klebsiella pneumoniae and Escherichia coli in surveillance swab specimens. J Clin Microbiol 2010; 48:836-41; PMID:20071553; https://doi.org/10.1128/JCM.01988-09

 PubMed Web of Science ®Google Scholar

Vasoo S, Cunningham SA, Kohner PC, Mandrekar JN, Lolans K, Hayden MK, Patel R. Rapid and direct real-time detection of blaKPC and blaNDM from surveillance samples. J Clin Microbiol 2013; 51:3609-15; PMID:23966498; https://doi.org/10.1128/JCM.01731-13

 PubMed Web of Science ®Google Scholar

Zarakolu P, Day KM, Sidjabat HE, Kamolvit W, Lanyon CV, Cummings SP, Paterson DL, Akova M, Perry JD. Evaluation of a new chromogenic medium, chromID OXA-48, for recovery of carbapenemase-producing Enterobacteriaceae from patients at a university hospital in Turkey. Eur J Clin Microbiol Infect Dis 2015; 34:519-25; PMID:25308827; https://doi.org/10.1007/s10096-014-2255-z

 PubMed Web of Science ®Google Scholar

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; 49:2239-42; PMID:21471338; https://doi.org/10.1128/JCM.02566-10

 PubMed Web of Science ®Google Scholar

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; PMID:18632915; https://doi.org/10.1128/JCM.00249-08

 PubMed Web of Science ®Google Scholar

Hindiyeh M, Smollen G, Grossman Z, Ram D, Davidson Y, Mileguir F, Vax M, Ben David D, Tal I, Rahav G, et al. Rapid detection of blaKPC carbapenemase genes by real-time PCR. J Clin Microbiol 2008; 46:2879-83; PMID:18614657; https://doi.org/10.1128/JCM.00661-08

 PubMed Web of Science ®Google Scholar

Vasoo S, Lolans K, Li H, Prabaker K, Hayden MK. Comparison of the CHROMagar KPC, Remel Spectra CRE, and a direct ertapenem disk method for the detection of KPC-producing Enterobacteriaceae from perirectal swabs. Diagn Microbiol Infect Dis 2014; 78:356-9; PMID:24439449; https://doi.org/10.1016/j.diagmicrobio.2013.08.016

 PubMed Web of Science ®Google Scholar

Pournaras S, Zarkotou O, Poulou A, Kristo I, Vrioni G, Themeli-Digalaki K, Tsakris A. A combined disk test for direct differentiation of carbapenemase-producing enterobacteriaceae in surveillance rectal swabs. J Clin Microbiol 2013; 51:2986-90; PMID:23843486; https://doi.org/10.1128/JCM.00901-13

 PubMed Web of Science ®Google Scholar

Schechner V, Straus-Robinson K, Schwartz D, Pfeffer I, Tarabeia J, Moskovich R, Chmelnitsky I, Schwaber MJ, Carmeli Y, Navon-Venezia S. Evaluation of PCR-based testing for surveillance of KPC-producing carbapenem-resistant members of the Enterobacteriaceae family. J Clin Microbiol 2009; 47:3261-5; PMID:19675211; https://doi.org/10.1128/JCM.02368-08

 PubMed Web of Science ®Google Scholar

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; PMID:21177079; https://doi.org/10.1016/j.ijantimicag.2010.10.010

 PubMed Web of Science ®Google Scholar

Singh K, Mangold KA, Wyant K, Schora DM, Voss B, Kaul KL, Hayden MK, Chundi V, Peterson LR. Rectal screening for Klebsiella pneumoniae carbapenemases: comparison of real-time PCR and culture using two selective screening agar plates. J Clin Microbiol 2012; 50:2596-600; PMID:22622443; https://doi.org/10.1128/JCM.00654-12

 PubMed Web of Science ®Google Scholar

Girlich D, Bouihat N, Poirel L, Benouda A, Nordmann P. High rate of faecal carriage of extended-spectrum β-lactamase and OXA-48 carbapenemase-producing Enterobacteriaceae at a university hospital in Morocco. Clin Microbiol Infect 2014; 20:350-4; PMID:23927757; https://doi.org/10.1111/1469-0691.12325

 PubMed Web of Science ®Google Scholar