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Antimicrobial Agents and Chemotherapy, July 2005, p. 3018-3020, Vol. 49, No. 7
0066-4804/05/$08.00+0     doi:10.1128/AAC.49.7.3018-3020.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Emergence of KPC-Possessing Klebsiella pneumoniae in Brooklyn, New York: Epidemiology and Recommendations for Detection

Simona Bratu,1 Mohamad Mooty,1 Satyen Nichani,1 David Landman,1 Carl Gullans,2 Barbara Pettinato,3 Usha Karumudi,1 Pooja Tolaney,1 and John Quale1*

Department of Medicine, SUNY-Downstate Medical Center,1 Department of Microbiology, Kings County Hospital,2 Department of Pathology Services, Coney Island Hospital, Brooklyn, New York3

Received 14 February 2005/ Returned for modification 24 March 2005/ Accepted 3 April 2005


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ABSTRACT
 
Among 257 isolates of Klebsiella pneumoniae collected in Brooklyn, NY, 24% were found to possess blaKPC. Clinical microbiology laboratories that used automated broth microdilution systems reported 15% of the KPC-possessing isolates as susceptible to imipenem. The imipenem MIC was found to be markedly affected by the inoculum. For accurate detection of KPC-possessing K. pneumoniae, particular attention should be paid to proper inoculum preparation for broth-based susceptibility methods. In addition, using ertapenem or meropenem for class reporting of carbapenem susceptibility will improve detection.


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TEXT
 
Carbapenem resistance among Klebsiella pneumoniae isolates had been distinctly unusual. Recently, carbapenem resistance mediated by the KPC ß-lactamases has been documented in isolates of Klebsiella spp. (1, 6, 7, 9), Enterobacter spp. (2, 4), and Salmonella (5). Accurate detection of these isolates will be crucial for controlling their spread. In this study, we examined the accuracy of the clinical laboratories and various susceptibility test methods in the detection of KPC-possessing isolates.

(This report was presented in part at the 105th General Meeting of the American Society for Microbiology, Atlanta, GA, abstr. C-359, 2005.)

During September and October 2004, isolates of Escherichia coli, Enterobacter spp., and K. pneumoniae were gathered from four hospitals in Brooklyn, NY. Isolates of E. coli and Enterobacter spp. for which the ceftazidime MIC was ≥1 µg/ml and all isolates of K. pneumoniae were screened for the presence of blaKPC. The methods used for PCR screening and blaKPC identification, ribotyping, and isoelectric focusing were as previously described (1, 2). KPC possession was confirmed by a second, independent PCR test; previously characterized clinical isolates (1) were used as positive and negative controls.

In the central research laboratory, the MICs of carbapenems were determined by the broth microdilution method in cation-supplemented Mueller-Hinton broth using inocula of ~5 x 104 and 5 x 105 CFU/ml for all KPC-possessing isolates. Carbapenem susceptibility testing was also performed using the disk diffusion (3) and Etest methodologies with Mueller-Hinton agar. Susceptibility results were defined according to established breakpoints (3).

Carbapenem susceptibility results were correlated with results reported by the clinical microbiology laboratories, all of which used the MicroScan System (Dade Microscan WalkAway System; Dade International Inc., West Sacramento, CA). All of the clinical laboratories used Prompt Inoculation System-D (3M Company, St. Paul, MN) for inoculum preparation. Selected isolates underwent repeated carbapenem susceptibility testing, using the MicroScan System, with inocula prepared using (i) Prompt Inoculation System-D and (ii) the CLSI (formerly NCCLS)-recommended protocol (3).

A total of 642 isolates of E. coli were gathered during the surveillance. None of the 55 isolates for which the ceftazidime MIC was >1 µg/ml possessed blaKPC. Seventy-nine isolates of Enterobacter spp. were collected during the 2-month surveillance; none of the 29 ceftazidime-resistant isolates carried blaKPC.

A total of 257 single-patient isolates of K. pneumoniae were gathered during the surveillance study; 109 (42%) were considered to possess extended-spectrum ß-lactamases. All 257 isolates were screened for the presence of blaKPC, and 62 (24%) were found to carry the gene. Fifty-nine possessed blaKPC-2, and 3 possessed blaKPC-3. All demonstrated a ß-lactamase with a pI value of 6.7 by isoelectric focusing; ß-lactamases with pIs of 5.4 and 7.6 were also identified in many isolates. Ribotyping revealed that 88% of the 62 isolates belonged to a single ribotype.

The clinical laboratories identified 15% of the 62 KPC-possessing isolates as susceptible to imipenem (Table 1). Of 42 isolates that also had meropenem susceptibility determined, 12% were reported as susceptible to this antibiotic. All were found to be resistant to ceftazidime.


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  		TABLE 1. Results of carbapenem susceptibility testing of 62 KPC-possessing K. pneumoniae isolates according to various testing procedures

A variety of carbapenem susceptibility testing methods were evaluated in the research laboratory. A pronounced inoculum effect was observed when the broth microdilution method was used for imipenem; using ~104 CFU/ml, only 19% were considered resistant (Table 1). Although only 5% were susceptible to meropenem using the lower inocula, 77% were considered intermediate. An inoculum effect was not observed for ertapenem. Virtually all isolates were found resistant to the three carbapenems when agar diffusion (Etest and disk diffusion) techniques were employed.

Ten isolates that were reported susceptible to imipenem by the clinical microbiology laboratories were reexamined. When the inocula were prepared using Prompt Inoculation System-D, 3 of the 10 were found susceptible and 7 intermediate to imipenem. Using the same system, two were susceptible and eight resistant to meropenem. When the inocula were prepared according to CLSI procedures, 2 were susceptible and 8 intermediate to imipenem; all 10 were found resistant to meropenem.

All of the 62 KPC-possessing K. pneumoniae isolates were resistant to piperacillin-tazobactam and ciprofloxacin (Table 2). Among commonly used antibiotics, gentamicin retained the greatest activity; nearly one-fourth were resistant to polymyxin B.


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  		TABLE 2. Susceptibility results involving 62 KPC-possessing K. pneumoniae isolates

Numerous reports describing KPC-possessing isolates from the northeastern United States have surfaced (1, 2, 4, 7, 8, 9). Despite heightened awareness and enhanced infection control efforts, medical centers in our region continue to struggle with KPC-possessing K. pneumoniae. In this report, a startling 24% of K. pneumoniae isolates harbored the KPC carbapenem-hydrolyzing ß-lactamase. Accurate detection of KPC-possessing K. pneumoniae will be the crucial first step in controlling its spread.

It was anticipated that carbapenem susceptibility results could be used to identify KPC-possessing K. pneumoniae. However, the MICs of imipenem were highly dependent on the inoculum employed in the susceptibility test procedure. While ~95% of isolates were correctly identified as resistant using agar-based diffusion tests, many isolates were considered susceptible or intermediate to imipenem in broth-based tests, especially when the inocula were lower than recommended. This pronounced inoculum effect likely explains the results obtained from the clinical laboratories, which reported 15% of the KPC-possessing isolates of K. pneumoniae as susceptible to imipenem. All of the participating clinical laboratories used Prompt Inoculation System-D for inoculum preparation. As noted by the manufacturer, an adequate sample may not be obtained when the bacterial colonies (such as K. pneumoniae) are extremely mucoid, and other methods for inoculum preparation should be considered.

An inoculum effect was also observed with meropenem, although fewer isolates were categorized as susceptible. No inoculum effect was observed with ertapenem, suggesting that susceptibility testing of this antibiotic may be the preferred method for detecting KPC-possessing isolates.

Based on our results, several recommendations can be offered to clinical microbiology laboratories to improve detection of KPC-possessing K. pneumoniae. First, a correct inoculum of any mucoid lactose-fermenting gram-negative bacillus undergoing identification and susceptibility testing should be assured. If the proper inoculum cannot be assured using an inoculation wand method, inoculum preparation using the CLSI procedures (3) should be employed. Alternatively, an agar diffusion test could be employed for mucoid isolates. Secondly, K. pneumoniae intermediate or resistant to ertapenem or meropenem should be considered resistant to all carbapenems, regardless of the other susceptibility results.

Precisely why some isolates demonstrate an inoculum effect with imipenem while others are highly resistant even with a low inoculum is an area of active investigation. Most of these isolates possess other ß-lactamases (1, 9), perhaps contributing to differing levels of resistance. Also, porin defects have been found in some (7, 8) but not all (9) KPC-possessing Klebsiella spp. Finally, an inoculum effect with imipenem has also been observed in KPC-possessing Enterobacter spp. (2). Since these ß-lactamases reside on transmissible plasmids and have been found in other genera (4, 5, 6, 8), an examination of detection methods with other bacteria is warranted.


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ACKNOWLEDGMENTS
 
This work was supported by a grant from Merck & Co., Inc.


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FOOTNOTES
 
* Corresponding author. Mailing address: SUNY Downstate, Box 77 Division of Infectious Diseases, 450 Clarkson Avenue, Brooklyn, NY 11203. Phone: (718) 270-2148. Fax: (718) 270-2465. E-mail: jquale{at}downstate.edu. Back


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Antimicrobial Agents and Chemotherapy, July 2005, p. 3018-3020, Vol. 49, No. 7
0066-4804/05/$08.00+0     doi:10.1128/AAC.49.7.3018-3020.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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