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Applied and Environmental Microbiology, January 2004, p. 1-7, Vol. 70, No. 1
0099-2240/04/$08.00+0     DOI: 10.1128/AEM.70.1.1-7.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Characterization of Multiple-Antimicrobial-Resistant Salmonella Serovars Isolated from Retail Meats

Sheng Chen,1 Shaohua Zhao,2 David G. White,2 Carl M. Schroeder,1,{dagger} Ran Lu,3 Hanchun Yang,4 Patrick F. McDermott,2 Sherry Ayers,2 and Jianghong Meng1*

Department of Nutrition and Food Science, University of Maryland, College Park, Maryland,1 Division of Animal and Food Microbiology, Office of Research, Center for Veterinary Medicine, U.S. Food & Drug Administration, Laurel, Maryland,2 Institute for Food Safety & Inspection, Ministry of Health,3 China Agricultural University, Beijing, People's Republic of China4

Received 16 April 2003/ Accepted 10 September 2003


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ABSTRACT
 
A total of 133 Salmonella isolates recovered from retail meats purchased in the United States and the People's Republic of China were assayed for antimicrobial susceptibility, the presence of integrons and antimicrobial resistance genes, and horizontal transfer of characterized antimicrobial resistance determinants via conjugation. Seventy-three (82%) of these Salmonella isolates were resistant to at least one antimicrobial agent. Resistance to the following antibiotics was common among the United States isolates: tetracycline (68% of the isolates were resistant), streptomycin (61%), sulfamethoxazole (42%), and ampicillin (29%). Eight Salmonella isolates (6%) were resistant to ceftriaxone. Fourteen isolates (11%) from the People's Republic of China were resistant to nalidixic acid and displayed decreased susceptibility to ciprofloxacin. A total of 19 different antimicrobial resistance genes were identified in 30 multidrug-resistant Salmonella isolates. The blaCMY-2 gene, encoding a class A AmpC ß-lactamase, was detected in all 10 Salmonella isolates resistant to extended-spectrum ß-lactams. Resistance to ampicillin was most often associated with a TEM-1 family ß-lactamase gene. Six aminoglycoside resistance genes, aadA1, aadA2, aacC2, Kn, aph(3)-IIa, and aac(3)-IVa, were commonly present in the Salmonella isolates. Sixteen (54%) of 30 Salmonella isolates tested had integrons ranging in size from 0.75 to 2.7 kb. Conjugation studies demonstrated that there was plasmid-mediated transfer of genes encoding CMY-2 and TEM-1-like ß-lactamases. These data indicate that Salmonella isolates recovered from retail raw meats are commonly resistant to multiple antimicrobials, including those used for treating salmonellosis, such as ceftriaxone. Genes conferring antimicrobial resistance in Salmonella are often carried on integrons and plasmids and could be transmitted through conjugation. These mobile DNA elements have likely played an important role in transmission and dissemination of antimicrobial resistance determinants among Salmonella strains.


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INTRODUCTION
 
The emergence of antimicrobial-resistant bacterial pathogens has become a major public health concern. The use of antimicrobials in any venue, including disease treatment and growth promotion in domestic livestock, can potentially lead to widespread dissemination of antimicrobial-resistant bacteria (16, 29, 34). In recent years, testing of Salmonella isolates from the United States and other countries has shown that an increasing proportion are multidrug resistant (7, 15, 18, 27). Of particular concern is the isolation of ceftriaxone- and ciprofloxacin-resistant Salmonella, because of the importance of these two agents in treating Salmonella infections in children and adults (7, 11, 32), respectively.

Resistance to antimicrobial agents in bacteria is mediated by several mechanisms, including (i) changes in bacterial cell wall permeability, (ii) energy-dependent removal of antimicrobials via membrane-bound efflux pumps, (iii) modification of the site of drug action, and (iv) destruction or inactivation of antimicrobials (3, 26). Acquired antimicrobial resistance phenotypes most often develop via conjugative transfer of plasmids (12, 14, 17). Plasmids may carry class I integrons, which are mobile DNA elements that are important in the proliferation of bacterial multidrug resistance (MDR), especially among the gram-negative enteric species (2, 10, 24, 30). Integrons primarily have been found located within transposons Tn402 and Tn21, which in turn reside on broad-host-range plasmids or the IncF plasmid (6, 31). By incorporating into transposons and plasmids, integrons participate in the capture of resistance genes and dissemination of these genes among bacteria.

Molecular genetic techniques have been used to characterize antimicrobial-resistant salmonellae, especially Salmonella enterica serovar Typhimurium DT104 (4, 5, 9, 23, 25). For instance, variant Salmonella genomic island 1 (SGI1) MDR regions, consisting of integrons encoding different resistance genes, have been found in the chromosomal DNA of Salmonella serovars Typhimurium DT104 and Agona (4). The formation of these MDR clusters is hypothesized to favor expression of a large number of resistance genes and to enhance their transfer to other bacteria. Also, because class I integrons have become integrated into the chromosome in Salmonella serovars Typhimurium DT104 and Agona, they are able to persist even in the absence of antimicrobial selection (4, 9) with no apparent fitness cost to the cell. This has led, in the case of Salmonella serovar Typhimurium DT104, to a stable and widely disseminated clone of multidrug-resistant Salmonella serovar Typhimurium.

The objectives of this study were to determine the antimicrobial susceptibility phenotypes of Salmonella strains isolated from retail meats purchased in the Washington, D.C., area in the United States and in the People's Republic of China and to characterize the genetic mechanisms underlying the antimicrobial-resistant phenotypes observed for the isolates. We also examined selected isolates for the ability to donate resistance genes via conjugative transfer of plasmids to Escherichia coli. Our goal was to increase our understanding of the molecular genetic mechanisms involved in the emergence and dissemination of antimicrobial-resistant Salmonella isolates.


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MATERIALS AND METHODS
 
Salmonella isolates.
A total of 133 Salmonella isolates were included in the study. Eighty-nine isolates were recovered from retail ground meat samples of chicken, turkey, pork, and beef purchased in the Washington, D.C., area; these isolates included 45 isolates from samples purchased between June and September 1998 and 44 isolates from samples purchased between August 1999 and August 2000. The other 44 Salmonella isolates were isolated from samples of pork, beef, chicken, and mutton purchased in 10 provinces in the People's Republic of China from October 1999 to December 2000.

All Salmonella isolates were recovered from meats by using methods described in the U.S. Food and Drug Administration Bacteriological Analytical Manual (13). The isolates were further identified with API identification kits (BioMerieux, Marcy, France) and were serotyped with commercial antiserum (Difco, Detroit, Mich.) used according to the manufacturer's instructions.

Antimicrobial susceptibility testing.
Antimicrobial MICs for the 133 Salmonella isolates were determined by using the Sensititre automated antimicrobial susceptibility system (Trek Diagnostic Systems, Westlake, Ohio) and were interpreted by using the National Committee for Clinical Laboratory Standards standards for microdilution broth methods (21, 22). The 17 antimicrobials used and their recommended resistance breakpoints are shown in Table 1. E. coli ATCC 25922 and ATCC 35218, Enterococcus faecalis ATCC 29212, Staphylococcus aureus ATCC 29213, and Pseudomonas aeruginosa ATCC 27853 were used as quality control organisms.


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  		TABLE 1. Antimicrobial resistance of Salmonella isolates from retail meats obtained in the United States and the People's Republic of China

DNA isolation, PCR, and gene sequence analysis.
Based on serotypes and antimicrobial resistance profiles, 30 multidrug-resistant Salmonella isolates were selected for further characterization of antimicrobial resistance genes and class 1 integrons. Chromosomal and plasmid DNA of these bacterial isolates were isolated by using a Wizard genomic DNA purification kit (Promega, Madison, Wis.) and a High plasmid purification kit (Roche, Indianapolis, Ind.), respectively. The quantity of the DNA was determined by using a Smartspect 3000 spectrophotometer (Bio-Rad, Hercules, Calif.). Sixty-one pairs of oligonucleotide primers (Table 2) were designed to target 61 antimicrobial resistance genes that confer resistance to six categories of antimicrobial agents, including ß-lactams, aminoglycosides, phenicols, tetracycline, trimethoprim, and sulfonamides. Most primers were designed to differentiate the specific gene sequence of interest; the only exceptions were the blaTEM-1 primers, which amplified the entire family of blaTEM genes. The primers were designed by using the OLIGO 5.0 software program (National Biosciences, Inc., Plymouth, Minn.) and were synthesized commercially (Invitrogen, Carlsbad, Calif.). PCR was performed in 50 µl (total volume) of distilled H2O containing each deoxyribonucleotide at a concentration of 0.25 mM, 1.5 mM MgCl2, 0.2 U of Gold Taq DNA polymerase, and 50 pmol of each primer. The temperature profile included an initial template denaturation step consisting of 95°C for 10 min, followed by 30 cycles of 95°C for 30 s, 55°C for 1 min, and 72°C for 1 min and a final step consisting of 72°C for 7 min (8). The presence of class I integrons among the 30 Salmonella isolates was determined by PCR by using primers 5'CS (5'-GGCATCCAAGCACAAGC-3') and 3'-CS (5'-AAGCAGACTTGACTGAT-3') as previously described (35).


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  		TABLE 2. Sequences of oligonucleotide primers used in PCR assays for identification of antimicrobial resistance genes in Salmonella isolates from retail meats

All PCR products were purified with High PCR purification kits (Roche) and were sequenced at the University of Maryland Center of Agriculture Biotechnology, College Park, Md. The resulting DNA sequence data were compared to data in the GenBank database by using the BLAST algorithm (1) available at the National Center for Biotechnology Information web site (www.ncbi.nlm.nih.gov).

Conjugation experiments.
Multidrug-resistant Salmonella isolates recovered from retail meats (10 isolates from the Washington, D.C., area and 4 isolates from the People's Republic of China) were used as donor strains in conjugation experiments to study antimicrobial resistance gene transfer. Two nalidixic acid-resistant E. coli strains (1003 and 1016) were used as recipient strains. Conjugation was performed by the filter mating method as described previously (8). Briefly, donor and recipient cells (ratio, 1:10) were mixed in Luria-Bertani broth (Difco). The mixture was then collected on a 0.45-µm-pore-size filter and incubated on blood agar plates (BAP) at 37°C overnight. The mating mixture was washed from the filter and spread onto BAP containing a combination of nalidixic acid (60 µg/ml) and streptomycin (50 µg/ml) or a combination of nalidixic acid (100 µg/ml) and kanamycin (50 µg/ml). Bacterial colonies on BAP containing appropriate antibiotics were transferred onto MacConkey agar (Difco) plates and incubated overnight at 37°C. Presumptive E. coli transconjugants were confirmed to be E. coli by the API test and were assayed for susceptibility to 17 antimicrobial agents. Transfer of antimicrobial resistance genes was confirmed by PCR by using primers shown in Table 2.


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RESULTS
 
Antimicrobial resistance of Salmonella isolates.
Seventy-three (82%) of the Salmonella strains isolated from retail meats purchased in the Washington, D.C., area exhibited resistance to at least one antimicrobial. Resistance to tetracycline (68% of the isolates were resistant), resistance to streptomycin (61%), and resistance to sulfamethoxazole (42%) were observed most often, whereas resistance to ß-lactams was observed less frequently (Table 1). Among the ß-lactams, resistance was greatest to ampicillin (29% of the isolates were resistant), followed by cephalothin (24%), amoxicillin-clavulanate (21%), ceftiofur (19%), cefoxitin (18%), and ceftriaxone (9%). In addition to eight isolates resistant to ceftriaxone, nine isolates (10%) exhibited intermediate susceptibility to ceftriaxone. All the Salmonella isolates that exhibited intermediate susceptibility to ceftriaxone were resistant to the other ß-lactams tested. The Salmonella isolates also exhibited resistance to chloramphenicol (11% of the isolates were resistant), kanamycin (6%), and gentamicin (2%). All Salmonella isolates recovered from retail foods in the Washington, D.C., area were susceptible to amikacin, apramycin, ciprofloxacin, and nalidixic acid (Table 1).

Twenty-eight (64%) Salmonella isolates from the People's Republic of China exhibited resistance to at least one antimicrobial. The highest frequencies of resistance were the frequencies of resistance to tetracycline (43% of the isolates were resistant), ampicillin (39%), and streptomycin (32%). Resistance was also observed, but to a lesser extent, for chloramphenicol (20%), sulfamethoxazole (16%), kanamycin (11%), and trimethoprim (9%) (Table 1). None of the isolates exhibited resistance to ß-lactams other than ampicillin, except for one isolate that was resistant to cephalothin. In contrast to the United States isolates, approximately one-third of the isolates from the People's Republic of China were quinolone resistant. Fourteen (32%) of the isolates were resistant to nalidixic acid and also had increased MICs of ciprofloxacin. The MIC at which 90% of the isolates tested were inhibited by ciprofloxacin for the isolates from the People's Republic of China was more than 30 times higher (0.5 µg/ml) than the corresponding value for the isolates from the United States (<0.015 µg/ml) (data not shown).

Antimicrobial resistance genes and class 1 integrons.
Among the 30 multiple-antimicrobial-resistant Salmonella isolates (defined as isolates that were resistant to two or more antimicrobials), 19 resistance genes conferring resistance to six categories of antimicrobials, including ß-lactams, aminoglycosides, phenicols, tetracycline, trimethoprim, and sulfonamides, were identified. The PCR results were consistent with the antimicrobial susceptibility phenotypes (Table 3). For example, the sulI and/or sulII genes were detected in each of the sulfonamide-resistant Salmonella isolates; the tetA and/or tetB genes were detected in each of the tetracycline-resistant isolates; and the dihydrofolate reductase genes, dhfr1, dhfr12, and dhfr13, were detected in each of the trimethoprim-resistant isolates. Either or both of the chloramphenicol acetyltransferase genes, cat1 and cat2, were detected in the chloramphenicol-resistant Salmonella isolates from the People's Republic of China, while the flo gene was detected in each of the chloramphenicol-resistant Salmonella isolates from the United States.


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  		TABLE 3. Antimicrobial resistance and resistance gene profiles and class I integrons of Salmonella isolates from retail meats obtained in the United States and the People's Republic of China

The distribution of aminoglycoside resistance genes in the Salmonella isolates was diverse. Six different resistance genes, aadA1, aadA2, aacC2, Kn, aph(3)-IIa, and aac(3)-IVa, were detected. The aadA1 gene was detected most frequently and was present in 17 of the isolates. Three isolates contained aadA1 and aadA2. Isolate CHS31 contained four types of aminoglycoside resistance genes, aadA1, aadA2, aacC2, and aac(3)-Iva. A total of 12 antimicrobial resistance genes were amplified from the DNA of this isolate. The aac(3)-IVa and aacC2 genes (conferring resistance to gentamicin) and the aph(3)-IIa gene (conferring resistance to kanamycin) were detected in Salmonlella isolates from the People's Republic of China.

Three kinds of ß-lactamase genes were detected in the Salmonella isolates. The blaCMY-2 gene was detected in 10 extended-spectrum ß-lactamase-resistant Salmonella isolates, 5 of which also contained a blaTEM-1-like gene. Each of the nine ampicillin-resistant isolates from the People's Republic of China contained a blaTEM-1-like gene. Consistent with previous findings (19), the blaPSE-1gene, which was located in a 1.0-kb class 1 integron, was amplified in each of two Salmonella serovar Typhimurium DT104 isolates with an ACSSuT antibiogram (Table 3).

Six integron amplicons, which were 0.75, 1, 1.2, 1.5, 2.0, and 2.7 kb long, were detected in 16 (54%) of the 30 Salmonella isolates (Table 3). The most common antimicrobial resistance genes carried by these integrons were aadA1 and aadA2 conferring resistance to streptomycin and dhfrXII conferring resistance to trimethoprim. A 2.7-kb integron in two Salmonella serovar Typhimurium DT208 isolates contained an aadA gene, as well as a 1.2-kb gene having an unknown function (GenBank accession no. AY204504). A protein BLAST search revealed that the 1.2-kb open reading frame exhibited 56% amino acid homology with a reverse transcriptase from Serratia marcescens. No change in antimicrobial susceptibility was observed when this open reading frame was overexpressed as a cloned copy in E. coli (data not shown).

Conjugative transfer of resistance genes.
The 10 Salmonella isolates from retail meats purchased in the Washington, D.C., area transferred their plasmids to E. coli at rates ranging from 6.0 x 10-8 to 2.4 x 10-4 transconjugant per recipient cell. Examples of the conjugation study results are shown in Table 4. Transconjugants 1083/1003 and 1290/1003 acquired resistance to 9 and 11 of the antimicrobial agents tested, respectively. Transfer of blaCMY-2 and blaTEM-1-like genes to the recipient E. coli strain was confirmed by a PCR assay. Because antimicrobial resistance genes specifying the ACSSuT resistance phenotype have integrated into the Salmonella chromosome (4, 5), the two Salmonella serovar Typhimurium DT104 isolates did not transfer this phenotype to the E. coli recipient strain (Table 4). One of four Salmonella isolates from the People's Republic of China transferred the ampicillin resistance phenotype to E. coli 1016. The transfer of other resistance phenotypes could not be measured because E. coli 1016 had these phenotypes prior to the conjugation experiment (Table 4).


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  		TABLE 4. Antimicrobial susceptibility profiles of donors, recipients, and transconjugants in the conjugation experiments


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DISCUSSION
 
In this study, we examined Salmonella isolates recovered from retail meats purchased in the United States and the People's Republic of China to determine their antimicrobial susceptibility phenotypes and genotypes. In general, our findings are similar to those described in previous studies showing that Salmonella isolates in retail meats are commonly resistant to multiple antimicrobials, including tetracycline, sulfamethoxazole, and streptomycin (20, 32). Our findings also showed that the frequencies of antimicrobial resistance among Salmonella strains isolated from retail meats purchased in the People's Republic of China were lower than the frequencies of antimicrobial resistance among Salmonella strains isolated from retail meats purchased in the United States. Further studies involving larger sample sizes are necessary to more precisely determine if there are differences in antimicrobial resistance between Salmonella isolates from the two countries.

Resistance to ceftriaxone is a concern because of the importance of this agent for treatment of salmonellosis in children. Ceftriaxone resistance in Salmonella is largely due to the AmpC ß-lactamase (blaCMY-2) gene, and reports of this resistance have been increasing in the United States (11, 32, 33). Strains of Salmonella carrying blaCMY-2 were first isolated from human, animal, and food samples in the United States in 1996 (11, 36). In this study, 19% of Salmonella isolates from retail meats purchased in the United States were resistant or exhibited intermediate susceptibility to ceftriaxone and harbored the blaCMY-2 gene. Conversely, all of the Salmonella isolates from the People's Republic of China were susceptible to ceftriaxone (and other cephalosporins), and none harbored blaCMY-2. A possible explanation for these observations is that ceftriaxone-resistant Salmonella strains in meats have arisen due to cross-resistance between ceftriaxone and ceftiofur, a cephalosporin used in food animals (29, 33). Ceftiofur, the only cephalosporin approved for therapeutic use in cattle, has been approved for use in the United States since 1988, whereas it was approved for use in the People's Republic of China in 2002 (www.agri.gov.cn/blgg/t20021219_36976.htm).

Quinolones and fluoroquinolones have been used in veterinary medicine in the People's Republic of China since the 1980s. In contrast, they were not approved for therapeutic use in animals in the United States until 1995. The differences in fluoroquinolone susceptibility between isolates from the United States and isolates from the People's Republic of China likely reflect the different approval dates in the two countries. Thirty-two of the Salmonella isolates from the People's Republic of China were resistant to nalidixic acid and had increased MICs of ciprofloxacin, while all of the isolates from the United States were susceptible to these drugs. Nevertheless, the relatively high frequency of increased MICs of ciprofloxacin among the isolates from the People's Republic of China warrants continued surveillance to detect emerging ciprofloxacin-resistant phenotypes.

Two Salmonella serovar Typhimurium DT104 strains (1275 and S21) isolated from pork within a 1-year span in the Washington, D.C., area displayed very similar antimicrobial resistance phenotypes, genotypes, and pulsed-field gel electrophoresis patterns. Both of these isolates had the classical ACSSuT resistance phenotype and, accordingly, were found to contain the bla PSE-1, flo-1, aadA2, sulI, and tetA genes. These genes are known constituents of the SGI1 MDR region (4, 23). In addition, three more resistance genes, sulII, aadA1, and tetB, were detected in these isolates, suggesting that Salmonella may contain multiple genes that specify resistance to similar drugs (5, 9). In Salmonella serovar Typhimurium DT104, the resistance genes known to be constituents of SGI1 were not transferred to E. coli, whereas the aadA1 gene specifying the streptomycin-resistant determinant is encoded in a conjugal plasmid, which can be transferred to E. coli by conjugation. In contrast to the antimicrobial resistance determinants in Salmonella serovar Typhimurium DT104, most of the antimicrobial resistance determinants in other Salmonella isolates were encoded in a transferable plasmid and could be transferred to E. coli by conjugation. Furthermore, the molecular mechanisms of antimicrobial resistance in these isolates were also different from SGI1 MDR in Salmonella serovar Typhimurium DT104. The reason for the widespread dissemination of SGI1 MDR among Salmonella serovar Typhimurium DT104 isolates is not clear.

Most of the resistance genes, including blaCMY-2 and the genes contained in integrons, were located on plasmids in the Salmonella isolates in this study. Plasmids carrying blaCMY-2 resistance were readily transferred under the selective pressure of ß-lactam antibiotics; they were also cotransferred by selection with other antibiotics on the same plasmid (e.g., streptomycin). The E. coli recipient cells acquired 9 to 11 antimicrobial resistance phenotypes by receiving the plasmid from Salmonella serovar Agona and Salmonella serovar Typhimurium DT208 via conjugation. These findings indicated that conjugal plasmids play a significant role in the dissemination of multiple-antimicrobial-resistant bacteria.

A better understanding of the molecular mechanisms by which antimicrobial resistance emerges and spreads should enable us in the future to design intervention strategies to reduce its progression. Because antimicrobial-resistant bacteria may be transferred to humans through the food chain (28, 34), selection of novel antimicrobial resistance mechanisms in Salmonella in animals (28), which specify resistance to antibiotics used in humans, is troubling. Efforts that include further implementation of hazard analysis of critical control point programs in food production are needed to reduce the incidence of Salmonella in food. The judicious use of antibiotics, including cephalosporins and fluoroquinolones in food animals, is also critical to control the rapid spread of antimicrobial-resistant bacteria.


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FOOTNOTES
 
* Corresponding author. Mailing address: Department of Nutrition and Food Science, 0112 Skinner Building, University of Maryland, College Park, MD 20742. Phone: (301) 405-1399. Fax: (301) 314-3313. E-mail: jm332{at}umail.umd.edu. Back

{dagger} Present address: Food Safety and Inspection Service, United States Department of Agriculture, Washington, DC 20250-3700. Back


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Applied and Environmental Microbiology, January 2004, p. 1-7, Vol. 70, No. 1
0099-2240/04/$08.00+0     DOI: 10.1128/AEM.70.1.1-7.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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