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Journal of Clinical Microbiology, July 2005, p. 3110-3113, Vol. 43, No. 7
0095-1137/05/$08.00+0     doi:10.1128/JCM.43.7.3110-3113.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

AmpC Disk Test for Detection of Plasmid-Mediated AmpC ß-Lactamases in Enterobacteriaceae Lacking Chromosomal AmpC ß-Lactamases

Jennifer A. Black, Ellen Smith Moland, and Kenneth S. Thomson*

Center for Research in Antiinfectives and Biotechnology, Department of Medical Microbiology and Immunology, Creighton University School of Medicine, Omaha, Nebraska

Received 22 February 2005/ Returned for modification 7 March 2005/ Accepted 14 March 2005


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ABSTRACT
 
Although plasmid-mediated AmpC ß-lactamases were first reported in the late 1980s, many infectious disease personnel remain unaware of their clinical importance. These enzymes are typically produced by isolates of Escherichia coli, Klebsiella spp., Proteus mirabilis, and Salmonella spp. and are associated with multiple antibiotic resistance that leaves few therapeutic options. Plasmid-mediated AmpC ß-lactamases have been associated with false in vitro susceptibility to cephalosporins. Many laboratories do not test for this resistance mechanism because current tests are inconvenient, subjective, lack sensitivity and/or specificity, or require reagents that are not readily available. In this study a new test, the AmpC disk test, based on filter paper disks impregnated with EDTA, was found to be a highly sensitive, specific, and convenient means of detection of plasmid-mediated AmpC ß-lactamases in organisms lacking a chromosomally mediated AmpC ß-lactamase. Using cefoxitin insusceptibility as a screen, the test accurately distinguished AmpC and extended-spectrum ß-lactamase production and differentiated AmpCs from non-ß-lactamase mechanisms of cefoxitin insusceptibility, such as reduced outer membrane permeability. The test is a potentially useful diagnostic tool. It can provide important infection control information and help to ensure that infected patients receive appropriate antibiotic therapy.


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INTRODUCTION
 
ß-Lactamase production is the most common mechanism of ß-lactam drug resistance in gram-negative bacteria. Newer ß-lactamases that hydrolyze cephamycins, oxyimino and zwitterionic cephalosporins, monobactams, or carbapenems are of increasing concern because they restrict therapeutic options, cause treatment failures, and are increasing in occurrence (5, 9, 14, 15). Many clinical laboratories currently test Escherichia coli and Klebsiella spp. for production of extended-spectrum ß-lactamases (ESBLs) but do not attempt to detect plasmid-mediated AmpC ß-lactamases (also known as imported, transmissible, foreign, or mobile AmpC ß-lactamases). Like ESBLs, plasmid-mediated AmpC ß-lactamases have a broad substrate profile that includes penicillins, cephalosporins (apart from zwitterionic cephalosporins), and monobactams. In contrast to ESBLs, they hydrolyze cephamycins and are not inhibited by commercially available ß-lactamase inhibitors. These enzymes are typically associated with multiple antibiotic resistance, leaving few therapeutic options (7, 24, 26). Bacteria, mostly Klebsiella pneumoniae and E. coli, producing plasmid-mediated AmpC ß-lactamases have been responsible for nosocomial outbreaks of infection and colonization (16, 17, 20, 21).

According to the report of Pai et al. (20), plasmid-mediated AmpCs are associated with potentially fatal errors of false susceptibility in routine susceptibility tests. These authors reported therapeutic failures with cefotaxime and ceftazidime among 28 bacteremia cases caused by AmpC-producing K. pneumoniae, some of which involved isolates that did not respond to "definitive treatment," i.e., were susceptible to these agents in vitro. The failures included deaths and failures until therapy was switched to a carbapenem. This report raised concerns similar to those associated with ESBLs (8, 22). It also indicated that some plasmid-mediated AmpC ß-lactamases may be clinically more harmful than others. In this study the inducible DHA-1 enzyme was associated with a crude mortality rate of 46%, whereas the constitutively produced CMY-1-like enzyme was associated with only a 14.3% mortality rate. Given the relatively small number of cases, it is unclear how much significance should be attributed to the findings, but it is clear that they should be taken seriously and that further investigations are warranted. For this to happen, it is essential that clinical laboratories accurately detect isolates producing a plasmid-mediated AmpC ß-lactamase.

Testing for plasmid-mediated AmpC ß-lactamases is not widely attempted by clinical laboratories because the available phenotypic tests are either inconvenient, subjective, lack sensitivity and/or specificity, or require reagents that are not readily available (2, 4, 10, 12, 29, 31, 18). For this reason, a study was designed to evaluate the potential of a novel disk test to detect production of plasmid-mediated AmpC ß-lactamases in isolates that lack a chromosomally encoded AmpC ß-lactamase.


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MATERIALS AND METHODS
 
Bacterial strains. (i) Clinical isolates: 140 nonduplicate recent U.S. hospital isolates of Klebsiella species, Proteus mirabilis, and Salmonella species with cefoxitin MICs of ≥16 µg/ml were used. The isolates were obtained from a 2000-2001 study involving 63 United States clinical sites. The sites providing the isolates are listed in Acknowledgments.

(ii) Control strains. Plasmid-mediated AmpC-producing strains, K. pneumoniae HVAMC 39 (high level ACT-1) and K. pneumoniae UMJMH14 (low level DHA-1); three South African strains of K. pneumoniae with reduced outer membrane permeability (one of which produced SHV-2); and phenotypically ß-lactamase-negative E. coli ATCC 25922 (actually possesses ampC gene but only produces an insignificant amount of AmpC ß-lactamase) were used.

ß-Lactamase investigations. The types of ß-lactamase production of the clinical isolates were investigated by phenotypic inhibitor-based microdilution tests using cefpodoxime, cefepime, cefotaxime, or ceftazidime tested alone and in combination with clavulanate; tests for inducibility with cefoxitin and/or imipenem by the disk approximation method (27) and/or by a broth induction method in which spectrophotometric assays using crude cell sonicates were used to compare the level of ß-lactamase production that had occurred in log-phase growth in the presence and absence of 1/4 the MIC of the inducing agent (28); previously described isoelectric focusing overlay procedures to determine the pIs of ß-lactamases, the capabilities of clavulanate and cloxacillin to inhibit the ß-lactamases, and the capabilities of the ß-lactamases to hydrolyze cefotaxime (15); microbiological and spectrophotometric assays to investigate carbapenem hydrolysis (13, 28); molecular identification tests utilizing multiplex PCR for plasmid-mediated AmpC ß-lactamases (23); PCR primers specific for TEM-, SHV-, OXA-, CTX-M-, PSE-, and OXY-derived ß-lactamases; and DNA sequencing (some enzymes only) (15) were used.

AmpC disk test. The test is based on use of Tris-EDTA to permeabilize a bacterial cell and release ß-lactamases into the external environment. AmpC disks (i.e., filter paper disks containing Tris-EDTA, available from BD Diagnostic Systems, Sparks, MD) were prepared in-house by applying 20 µl of a 1:1 mixture of saline and 100x Tris-EDTA (catalog code T-9285; Sigma-Aldrich Corp., St. Louis, MO) to sterile filter paper disks, allowing the disks to dry, and storing them at 2 to 8°C. The surface of a Mueller-Hinton agar plate (Oxoid Ltd., Basingstoke, Hampshire, England) was inoculated with a lawn of cefoxitin-susceptible E. coli ATCC 25922 according to the standard disk diffusion method (19). Immediately prior to use, AmpC disks were rehydrated with 20 µl of saline and several colonies of each test organism were applied to a disk. A 30-µg cefoxitin disk (Becton Dickinson, Sparks, MD) was placed on the inoculated surface of the Mueller-Hinton agar. The inoculated AmpC disk was then placed almost touching the antibiotic disk with the inoculated disk face in contact with the agar surface. The plate was then inverted and incubated overnight at 35°C in ambient air. After incubation, plates were examined for either an indentation or a flattening of the zone of inhibition, indicating enzymatic inactivation of cefoxitin (positive result), or the absence of a distortion, indicating no significant inactivation of cefoxitin (negative result) (Fig. 1).



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  		FIG. 1. Representative results obtained with the AmpC disk test with six isolates being tested on a 90-mm plate, with one isolate inoculated onto disks placed on either side of three cefoxitin (FOX) disks.


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RESULTS
 
Forty-four of the 140 cefoxitin-insusceptible clinical isolates yielded positive AmpC disk tests (31%), and the remaining 96 were negative (69%) (Table 1). The negative isolates were confirmed as negative for AmpC production with the three-dimensional test (29). Forty-two of the 44 positive isolates were confirmed as being plasmid-mediated AmpC ß-lactamase producers by the isoelectric focusing overlay technique and multiplex PCR. Most ß-lactamases were identified only to the family level (e.g., FOX-like), but a few enzymes were identified definitively by sequencing. The two test-positive isolates that were not confirmed as producing a plasmid-mediated AmpC ß-lactamase were an imipenem-resistant isolate of K. pneumoniae (strain 01BH79; MIC, 64 µg/ml), which produced the class A carbapenem-hydrolyzing ß-lactamase, KPC-2, and also an SHV-derived ESBL; and K. pneumoniae 01JMH4, which produced an as-yet-unidentified, clavulanate-sensitive, cloxacillin-resistant ß-lactamase with a pI of 8.0. Based on these findings, the disk test exhibited 100% sensitivity and 98% specificity for detection of plasmid-mediated AmpC ß-lactamases in these isolates. The two AmpC-producing control strains yielded positive test results, and the negative controls strains, including the three porin mutants, yielded negative test results.


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  		TABLE 1. AmpC disk test results with clinical strains


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DISCUSSION
 
There is a paucity of data about the prevalence and clinical significance of plasmid-mediated AmpC ß-lactamases. It is now well over a decade since the first confirmed reports of these enzymes (3, 21). Where accurate testing has been done, isolates producing plasmid-mediated AmpC ß-lactamases have been shown to be now widespread (24). For example, during the period 1992 to 2000, Alvarez et al. reported plasmid-mediated AmpC-producing K. pneumoniae isolates in the United States to have a prevalence of 8.5% among clinical isolates of this species and to occur at 20 of 70 centers (29%) (1). Plasmid-mediated AmpC-producing Salmonella and E. coli isolates are also a veterinary problem, affecting livestock, pets, and their human contacts (6, 11, 25, 30). In view of the apparently uncontained spread and the concern of false-susceptible in vitro test results with cephalosporins (20), there is good justification for clinical and veterinary microbiology laboratories to test for plasmid-mediated AmpC ß-lactamases.

In this study the AmpC disk test provided a simple, convenient, and accurate means of detection of plasmid-mediated AmpC ß-lactamases in organisms lacking a chromosomally mediated AmpC ß-lactamase, i.e., K. pneumoniae, Klebsiella oxytoca, Salmonella spp., and P. mirabilis. These organisms were chosen for the study because they are convenient indicator organisms for this resistance mechanism in that a positive test can unequivocally indicate the presence of a foreign, or plasmid-mediated, AmpC ß-lactamase. The test accurately distinguished between cefoxitin insusceptibility caused by AmpC production and non-ß-lactamase mechanisms, such as reduced outer membrane permeability (porin mutations). Distinguishing between these types of mechanisms is a current diagnostic problem for laboratories wanting to detect AmpC ß-lactamases. Coproduction of ESBLs did not interfere with the detection of the AmpC ß-lactamases.

Care is required in interpreting the test with isolates exhibiting reduced carbapenem susceptibility, since this may be due to other, currently rare ß-lactamases capable of hydrolyzing cefoxitin, e.g., carbapenemases.

E. coli isolates that produce plasmid-mediated AmpC ß-lactamases were not included in this study, because the test does not discriminate between positive results due to upregulated chromosomally mediated AmpC ß-lactamases and those due to plasmid-mediated AmpC ß-lactamases. Additional studies showed that the AmpC disk test also reliably detected plasmid-mediated AmpC ß-lactamases in E. coli and also high-level production of chromosomally mediated AmpC ß-lactamases in E. coli, Enterobacter cloacae, Pseudomonas aeruginosa, and Acinetobacter spp. (unpublished results). The follow-up of positive disk tests with E. coli isolates should, ideally, be done by genetic testing, e.g., AmpC multiplex PCR testing (23). However, if this is not feasible, an experienced microbiologist may sometimes be able to presumptively distinguish between chromosomal and plasmid-mediated AmpC ß-lactamases by comparing the E. coli susceptibility pattern with that of a Klebsiella sp. (or other organism) from the same patient population that is already known to produce a plasmid-mediated AmpC ß-lactamase.

Optimal screening agents for plasmid-mediated AmpC ß-lactamases have yet to be defined. Currently used screens include that for cefoxitin insusceptibility in Klebsiella, E. coli, P. mirabilis, or Salmonella and positive ESBL screens that are not confirmed by ESBL confirmatory tests.

Given the need for a test for AmpC ß-lactamases and the fact that many clinical laboratories are often short staffed and overworked, the AmpC disk test could fill a current gap in diagnostic microbiology. Adoption of this test would make it possible to learn more about the clinical implications of plasmid-mediated AmpC ß-lactamases and to contain the spread of organisms possessing this resistance mechanism. The potential benefits would include better patient outcomes in terms of avoiding inappropriate therapy and a reduction in the escalation of antibiotic resistance through better infection control.


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ACKNOWLEDGMENTS
 
The laboratory investigations were funded by the Center for Research in Antiinfectives and Biotechnology at Creighton University. The patent costs (U.S. patent application serial no. 10/387,788) were funded by the Department of Technology Transfer at Creighton University.

We thank Nancy D. Hanson for providing molecular testing and for her helpful advice and Thomas J. Lockhart and Lloyd Olsen for excellent technical assistance. We also thank the microbiologists at the following institutions for providing the isolates used in this study: University of Florida, Gainesville, FL; Tampa General Hospital, Tampa, FL; Jackson Memorial Hospital, Miami, FL; Wishard Memorial Hospital, Indianapolis, IN; Clarian Health Methodist Hospital, Indianapolis, IN; University of California, San Francisco, CA; Bellevue Hospital, New York, NY; Columbia Presbyterian Medical Center, New York, NY; Inova Fairfax Hospital, Falls Church, VA; The Cleveland Clinic, Cleveland, OH; Acadiana Medical Laboratory, Lafayette, LA; Children's Memorial Hospital, Chicago, IL; Cook County Hospital, Chicago, IL; Crawford Long Hospital, Atlanta, GA; VA North Texas Health Care System, Dallas, TX; Baltimore Veterans Administration Medical Center, Baltimore, MD; Christus Schumpert Health System, Shreveport, LA; Vencor of Arizona, Tempe, AZ; Sunrise Regional Medical Center, Las Vegas, NV; Kindred Hospital, Denver, CO; Massachusetts General Hospital, Boston, MA; Temple University Hospital, Philadelphia, PA; and Tygerberg Hospital, Cape Town, South Africa.


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FOOTNOTES
 
* Corresponding author. Mailing address: Center for Research in Antiinfectives and Biotechnology, Department of Medical Microbiology and Immunology, Creighton University School of Medicine, 2500 California Plaza, Omaha, NE 68178. Phone: (402) 280-2921. Fax: (402) 280-1875. E-mail: kstaac{at}creighton.edu. Back


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Journal of Clinical Microbiology, July 2005, p. 3110-3113, Vol. 43, No. 7
0095-1137/05/$08.00+0     doi:10.1128/JCM.43.7.3110-3113.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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