Multidrug-Resistant Salmonella Isolates from Retail Chicken Meat Compared with Human Clinical Isolates

Abstract

Aim:

To examine the prevalence of antimicrobial-resistant Salmonella in chicken meat and correlate with isolates from ill humans.

Methods:

We isolated Salmonella from raw chicken purchased from a randomly selected sample of retail outlets in central Pennsylvania during 2006–2007. Salmonella isolates from meat were compared, using pulsed-field gel electrophoresis, to isolates in the PulseNet database of Salmonella recovered from humans.

Results:

Of 378 chicken meat samples, 84 (22%) contained Salmonella. Twenty-six (31%) of the Salmonella isolates were resistant to ≥3 antimicrobials and 18 (21%) were resistant to ceftiofur. All ceftiofur-resistant isolates exhibited reduced susceptibility (minimum inhibitory concentration >2 μg/mL) to ceftriaxone and carried a bla _CMY gene, as detected by polymerase chain reaction. Among the 28 Salmonella serovar Typhimurium isolates, 20 (71.4%) were resistant to ≥3 antimicrobials and 12 (42.9%) were resistant to ceftiofur. One ceftiofur-resistant Salmonella serovar Typhimurium poultry isolate exhibited a rare pulsed-field gel electrophoresis pattern indistinguishable from a human isolate in PulseNet; both isolates carried the bla _CMY-2 gene.

Conclusions:

These data demonstrate the presence of multidrug-resistant Salmonella in poultry meat, including bla _CMY plasmid-mediated genes that confer resistance to both ceftiofur, used in poultry, and ceftriaxone, used for treating salmonellosis in humans. This study illustrates the potential for molecular subtyping databases to identify related Salmonella isolates from meat and ill humans, and suggests that chicken could be a source for multidrug-resistant salmonellosis in humans.

Introduction

S almonella enterica causes an estimated 1.4 million foodborne illnesses annually in the United States, resulting in over 168,000 physician visits and 15,000 hospitalizations (Voetsch et al., 2004). S. enterica is widely distributed in the environment and in intestinal tracts of animals; most human infections are acquired through consumption of contaminated food of animal origin (Lynch et al., 2006). The overall incidence of salmonellosis was 16.2 cases per 100,000 in 2008, well above the 2010 national health objective of 6.80 cases per 100,000 population (CDC, 2009). The persistently high number of Salmonella infections suggests gaps in the food safety system and a need for better ways to enhance food safety.

Fluoroquinolones and extended-spectrum cephalosporins (ESC) are the preferred antimicrobial agents for the treatment of complicated Salmonella infections in adults and children, respectively (Hohmann, 2001). Resistance to ceftiofur, an ESC used to treat bacterial infections in food animals, including poultry (FDA, 2008), is highly correlated with reduced susceptibility to ceftriaxone (minimum inhibitory concentration, MIC, >2 μg/mL), an ESC used to treat salmonellosis in humans (Hohmann, 2001; CDC, 2006). Among human Salmonella isolates tested by the National Antimicrobial Resistance Monitoring System (NARMS) in 2006, 3.6% (79/2184) demonstrated resistance to ceftiofur compared to 0.2% (2/1324) of isolates tested in 1996 (CDC, 2006). Ceftiofur resistance among Salmonella isolates from retail chicken increased from 10.0% (6/10) in 2002 to 16.2% (16/99) in 2007 (FDA, 2007).

Here we sought to determine the prevalence of multidrug-resistant (MDR) Salmonella in retail chicken purchased in Pennsylvania. We aimed to determine whether the type of retail outlet, packaging type, or claims of “organic” or “antibiotic-free” had an impact on prevalence of antimicrobial resistance. We also compared retail chicken isolates with isolates from human sources and those from other retail meat surveys.

Materials and Methods

Collection of retail chicken meat samples, Salmonella isolation, and serotyping

Monthly, from February 2006 to January 2007, we purchased raw chicken meat samples in three categories based on packing label (prepackaged boneless breast “cutlets,” open-display cutlets, and organic or antibiotic-free cutlets) from randomly selected grocery stores (n = 10) and farmers' markets (n = 8) in central Pennsylvania. Packaging claims about the poultry production environment were used to categorize a sample as “organic” or “antibiotic-free.” When present on the package label, the U.S. Department of Agriculture (USDA) establishment number was also recorded for correlation with a corporate address in a USDA directory of regulated poultry plants (FSIS, 2006). Standard methods were used for Salmonella isolation, confirmation, and serotyping (FDA, 2003; Popoff et al., 2001).

Susceptibility testing and detection of bla _CMY genes

All Salmonella isolates from retail chicken were tested by the broth microdilution method (Sensititre^®; Trek Diagnostics, Westlake, OH). The MICs for 15 antimicrobial agents used by NARMS (CDC, 2006)—amoxicillin/clavulanic acid, ampicillin, chloramphenicol, ceftiofur, ceftriaxone, ciprofloxacin, gentamicin, kanamycin, nalidixic acid, streptomycin, sulfisoxazole, trimethoprim-sulfamethoxazole, and tetracycline—were determined and interpreted according to Clinical and Laboratory Standards Institute guidelines (NCCLS, 2001, 2002). Ceftiofur-resistant isolates were tested for the presence of bla _CMY genes by polymerase chain reaction using previously described primers (M'Zali et al., 1997).

Comparison of antimicrobial-resistant Salmonella strains from human and nonhuman sources by pulsed-field gel electrophoresis

We used pulsed-field gel electrophoresis (PFGE) to compare Salmonella isolates resistant to ≥1 antibiotic from retail chicken in this study with PFGE patterns of human and other isolates in the PulseNet database (CDC, 2008). PFGE analysis was performed according to the PulseNet standardized protocol for subtyping Salmonella (Ribot et al., 2001; Hunter et al., 2005) using XbaI restriction endonuclease digestion. Gel images were stained with ethidium bromide, photographed with a ChemiDoc XRS documentation system (Bio-Rad Laboratories, Hercules, CA), and analyzed with BioNumerics software version 4.0 (Applied Maths, Sint-Martens-Latem, Belgium). Retail chicken isolates in this study that appeared indistinguishable by XbaI digestion from isolates in PulseNet were also assayed with a second enzyme, BlnI. For isolates from chicken meat that were indistinguishable from human isolates, PCR was performed to amplify the entire CMY gene for DNA sequencing analysis, using previously described procedures (Winokur et al., 2001).

Statistical analyses

Sample and laboratory data were entered into a Microsoft Access database (Microsoft Corp., Redmond, WA) and later transferred to a Stata database. Analyses were performed using Stata version 10 (Stata Corp., College Station, TX). Each type of retail outlet, grocery story or farmers' market, was treated as a primary sampling unit for purposes of variance estimation. This study was approved by the Pennsylvania Department of Health Institutional Review Board.

Results

Recovery of Salmonella from raw chicken meat

Salmonella was isolated from 84 (22.2%) of 378 retail fresh chicken meat samples. The prevalence of Salmonella isolated from raw chicken samples varied slightly by source (Table 1). The prevalence of Salmonella in chicken meat purchased from open displays was 54 (23.9%) of 226 compared to 30 (19.7%) of 152 in prepackaged samples (p = 0.64). Six serovars were identified among the 84 isolates. The three most common serovars accounted for 88% of the isolates: 28 (33.3%) of the 84 isolates were serovar Typhimurium, 24 (28.5%) serovar Kentucky, and 22 (26.2%) serovar Enteritidis. The remaining 10 isolates were 3 (3.6%) serovar Mbandaka, 2 (2.4%) serovar Heidelberg, 2 (2.4%) serovar Braenderup, and 3 (3.6%) untypeable strains.

Table 1.

Prevalence of Antimicrobial-Resistant Salmonella in Raw Chicken Samples from Retail Outlets by Source and Sample Type, Pennsylvania 2006–2007

					No. (%) of isolates resistant to multiple antimicrobials
Source and sample type		No. of samples tested	No. of samples positive	% Positive for Salmonella^a	≥1	≥3	≥5
Source	Grocery store	183	38	20.8^c	17 (44.7)	11 (29)	7 (18)
	Farmers' market	195	46	23.6^c	29 (63)	15 (33)	11 (24)
Sample type^b	Open display	226	54	23.9^d	32 (59.2)	17 (31)	11 (20)
	Prepackaged	152	30	19.7	14 (46.7)	9 (30)	7 (23)
	Organic	56	13	23.2^d	5 (38.4)	5 (38.4)	4 (30.7)
	Antibiotic-free	25	6	24.0^d	3 (50)	1 (16.7)	1 (16.7)
	Cutlet pack^e	71	11	15.5^d	6 (54.5)	3 (27.2)	2 (18.1)
Total (all sample types)		378	84	22.2	46 (54.8)	26 (30.9)	18 (21.4)

Because of rounding, percentages do not add to 100.

Sample type was based on packaged label.

F-test comparison, p = 0.64.

F-test comparison, p = 0.72.

Cutlet pack samples in this category had no claim for organic or antibiotic-free and were assumed to be from conventional sources.

Information regarding production environment (e.g., antibiotic-free) or USDA establishment-specific identification numbers was not available for samples from open-display counters. Eighty-one (53.3%) of prepackaged samples had claims of “organic” or “antibiotic-free”; Salmonella prevalence was similar across all types of samples (Table 1). Of the 152 prepackaged chicken samples, 130 (85.5%) had a label with a USDA establishment-specific identification number; the labeled samples originated from 16 different plants.

Antimicrobial resistance

Forty-six (54.8%) of the 84 Salmonella isolates were resistant to one or more drugs and 26 (30.9%) exhibited resistance to three or more drugs (Table 2). Eighteen (21.4%) of the isolates were resistant to ceftiofur and also had reduced susceptibility (MIC >2 μg/mL) to ceftriaxone. Polymerase chain reaction analysis showed that all 18 of the ceftiofur-resistant isolates carried the bla_CMY gene. Among the Salmonella serovar Typhimurium isolates, 26 (92.9%) exhibited resistance to tetracycline, 20 (71.4%) were resistant to at least three drugs, and 12 (42.9%) were resistant to ceftiofur. Five (20.8%) Salmonella serovar Kentucky isolates were resistant to at least three antibiotics (Table 2). None of the isolates from the other serovars (Salmonella serovar Enteritidis [n = 22], Salmonella serovar Braenderup [n = 2], or the untypeable strains [n = 3]) were resistant to any of the 15 drugs tested. All Salmonella isolates were susceptible to amikacin, ciprofloxacin, chloramphenicol, nalidixic acid, and trimethoprim/sulfamethoxazole.

Table 2.

Antimicrobial Resistance in Salmonella Serovars from Raw Chicken Meat, Pennsylvania, 2006–2007 ^a

Serovar		No. of isolates resistant to each antibiotic ^b								No. (%) of isolates showing resistance to multiple antibiotics
Name	No. of isolates	Amc	Amp	Tio	Fox	Kan	Str	Sul	Tet	≥1	≥3	≥5
Typhimurium	28	14	14	12	13	9	3	25	26	26 (92.9)	20 (71.4)	14 (50)
Kentucky	24	5	5	5	5	0	12	1	15	18 (75)	5 (20.8)	4 (16.7)
Mbandaka	3	1	1	1	1	0	1	0	0	1 (33.3)	1 (33.3)	0
Heidelberg	2	0	0	0	0	0	1	0	0	1 (50)	0	0
All serovars	84	20	20	18^c	19	9	16	26	41	46 (54.8)	26 (30.9)	18 (21.4)

All Salmonella isolates were susceptible to amikacin, ciprofloxacin, chloramphenicol, nalidixic acid, and trimethoprim/sulfamethoxazole; none of the isolates from the other serovars (Salmonella serovar Enteritidis [n = 22], Salmonella serovar Braenderup [n = 2], and the untypeable Salmonella [n = 3]) were resistant to any of the 15 antibiotics tested.

Percentages for all serovars (n = 84) included the three untypeable Salmonella isolates recovered from chicken meat samples.

These 18 isolates were resistant to ceftiofur and they exhibited reduced susceptibility to ceftriaxone.

Amc, amoxicillin/clavulanic acid; Amp, ampicillin; Tio, ceftiofur; Fox, Cefoxitin; Kan, kanamycin; Str, streptomycin; Sul, sulfamethoxazole; Tet, tetracycline.

Contamination with antimicrobial-resistant Salmonella did not significantly differ by type of retail outlet (farmers' market vs. grocery market) or among samples from open-display counters compared with prepackaged samples (Table 1). There was also no significant difference in contamination with antimicrobial-resistant Salmonella among chicken samples with any claim (e.g., “organic” or “antibiotic-free”) versus samples without claims. One of the six samples with an antibiotic-free claim was resistant to at least three antibiotics (Table 1).

Salmonella from retail chicken indistinguishable by PFGE with Salmonella in PulseNet database

PFGE analysis of the 26 Salmonella serovar Typhimurium isolates resistant to ≥1 antibiotic revealed 19 different XbaI patterns. One of these was indistinguishable by both XbaI and BlnI patterns from a human isolate (designated pattern combination JPXX01.1273/JPXA16.0328) in the PulseNet national database (Fig. 1). The sequence of the bla _CMY-2 gene of the study isolate was identical to the gene of the isolate from the human source. The Salmonella serovar Typhimurium isolated from the chicken sample, collected on February 7, 2006, was resistant to amoxicillin/clavulanic acid, ampicillin, cefoxitin, ceftiofur, sulfisoxazole, and tetracycline in addition to reduced susceptibility to ceftriaxone (MIC 16 μg/mL). The Salmonella serovar Typhimurium isolated from the human source exhibited resistance to these antibiotics and to kanamycin. This isolate was collected on June 13, 2006, from a 17-year-old female Philadelphia resident who had salmonellosis; consumption of chicken was noted as a possible risk factor. In addition to the human isolate, the pattern combination JPXX01.1273/JPXA16.0328 was also observed in 14 NARMS isolates recovered from chicken meat beginning in 2004.

FIG. 1.

Salmonella Typhimurium from chicken compared with Salmonella Typhimurium from a human source by PFGE using two enzymes, XbaI and BlnI. PFGE was performed as described in the Materials and Methods section. The PulseNet-USA pattern names of human isolate # 768 are JPXX01.1273 (XbaI) and JPXA26.0328 (BlnI). PFGE, pulsed-field gel electrophoresis.

Analysis of the serovar Kentucky isolates resistant to ≥1 antibiotic recovered from chicken meat in this study revealed one that was indistinguishable by both XbaI and BlnI patterns (JGPX01.0027 for XbaI and JGPA26.0011 for BlnI) from three other NARMS serovar Kentucky (n = 708) isolates collected from poultry beginning in 2005. The indistinguishable isolate from our study was resistant to amoxicillin/clavulanic acid, ampicillin, cefoxitin, ceftiofur, streptomycin, and tetracycline, and had reduced susceptibility to ceftriaxone (MIC 16 μg/mL).

Discussion

In this study, approximately 22% of raw chicken meat samples purchased during 2006–2007 from retail outlets in central Pennsylvania contained Salmonella. This prevalence is higher than the 11.5% prevalence reported by the FDA NARMS retail chicken meat survey conducted in FoodNet sites in 2007 (FDA, 2007). Although regional variation has been observed in previous FoodNet surveys, the prevalence in the Pennsylvania samples is among the highest observed. Salmonella was found in retail chicken purchased from both farmers' markets and grocery stores and at a similar isolation rate in packaged and unpackaged poultry. Prepackaged chicken meat with claims of “organic” or “antibiotic-free” also had similar rates of contamination.

Among Salmonella isolates from chicken meat tested in this study, 54.8% were resistant to one or more antimicrobial agents and 21% were resistant to ceftiofur. Among the most common serovar, Typhimurium, over 70% of the isolates were MDR, defined here as resistant to ≥3 drugs, and 43% were resistant to ceftiofur. Our results are consistent with findings from chicken meat surveys reported by FoodNet sites in 2007 (FDA, 2007). In the United States, Ceftiofur is approved for use in food animals, including day-old chicks; its use in these settings potentially leads to selection of resistant strains (Carattoli et al., 2002; FDA, 2008; FDA, 2009). Resistance to ceftiofur in Salmonella correlates with decreased susceptibility to other ESC, including ceftriaxone, a drug of choice for treatment of severe salmonellosis in humans (Hohmann, 2001; Pegues et al., 2009), particularly in children where therapeutic options are limited (WHO, 2005). All ceftiofur-resistant isolates in our chicken meat study carried a bla _CMY gene, identified as the major mechanism for resistance to ESC in Salmonella in other studies of food animals and in isolates from ill humans (Zaidi et al., 2006).

It remains highly debated whether or not development of antibiotic-resistant Salmonella in poultry, a common source of food consumed in the United States, translates into increasing rates of resistance among Salmonella that cause disease in humans (FDA; Sarwari et al., 2001; Carattoli et al., 2002; CDC, 2006). CDC NARMS data on Salmonella isolates from human sources show a 17-fold increase in resistance to ESC/ceftiofur from 1996 to 2006 (CDC, 2006). Among the isolates of Salmonella serovar Typhimurium, the second most frequently reported serovar among human clinical isolates, CDC NARMS testing identified ESC/ceftiofur resistance in 4.2% of cases (CDC, 2006, 2009). One of the serovar Typhimurium isolates from chicken meat in this study was indistinguishable (by both XbaI and BlnI analyses) from a human isolate in the PulseNet database. Both isolates were resistant to multiple antimicrobial agents and harbored the bla _CMY-2 gene. The human isolate originated from the geographical region where retail meat samples were collected and consumption of chicken was reported by the patient during the epidemiologic investigation.

The PFGE pattern found both in the study and among human isolates was observed in only 14 other isolates (all from poultry sources) in the PulseNet collection of more than 45,000 serovar Typhimurium isolates. One explanation for the low representation of this strain in PulseNet is that MDR Salmonella infections are not often transmitted from poultry to humans. It is also possible that the strain has caused more human illnesses that have not been detected because of low rates of submission and incomplete testing of Salmonella isolates in the current surveillance system (CDC, 2009); even so, it is likely that this strain has, to date, only caused a small proportion of human illnesses. The primary concern is whether these MDR strains will emerge as more predominant causes of human illness. A review of the PulseNet database on January 25, 2010, found five additional Salmonella isolates from humans that had a PFGE pattern indistinguishable from the one found in our study; these isolates originated from five different states.

Although the prevalence of the unique PFGE pattern found in this study is currently low in human and poultry isolates, previous studies have documented the emergence of MDR bla _CMY-2 Salmonella in food-producing animal populations before they emerge in the human population (Angulo et al., 2000). During the last two decades, emergence of Salmonella Newport MDR-AmpC infections in the United States coincided with an increase in Salmonella Newport MDR-AmpC infections in cattle (Gupta et al., 2003). A recent study conducted in Yucatan, Mexico, also documented emergence and widespread dissemination of MDR bla _CMY-2 Salmonella in food animals and in human clinical isolates (Zaidi et al., 2007). Investigators reported that this highly resistant MDR Salmonella serovar Typhimurium accounted for 75% of clinical isolates tested and had caused severe pediatric infections. In addition to serving as a source for MDR Salmonella human infections, there is another concern that food-producing animals may facilitate dissemination of mobile genetic elements with resistance genes to other enteropathogens (Aarestrup et al., 2008; Ajiboye et al., 2009).

The primary limitation of this study was small sample sizes of certain subsets, which limited our ability to stratify samples. Further, lack of a commercial standard definition for “antibiotic-free” products allows a variety of advertising claims by chicken producers, thus limiting accurate sub-analyses of these items.

This study documented significant contamination of poultry meat with MDR Salmonella, including strains that had plasmid-borne resistance genes (bla _CMY), which confers resistance to both ceftiofur, used in poultry, and ceftriaxone, used for treating salmonellosis in humans. We also found an MDR Salmonella strain from a retail chicken sample that was indistinguishable by PFGE pattern from an isolate that had been associated with human illness; the two isolates also had nearly identical phenotypes. Conducted in collaboration with three state institutions and two federal agencies, this study illustrates how existing resources can be used to enhance current molecular-subtyping-based surveillance for foodborne pathogens. Programs that compare molecular characteristics of isolates from food animals and ill humans could provide local and national data to inform policies and guidelines aimed at preserving critical antibiotics used in treatment of enteropathogens in humans.

Footnotes

Acknowledgments

We acknowledge with gratitude David G. White, U.S. Food and Drug Administration Center for Veterinary Medicine (FDA CVM), for assistance with the study design. We also acknowledge Kevin Joyce, CDC NARMS FoodNet Laboratory, and Jason Abbot, FDA CVM NARMS Laboratory, for their help with molecular characterization of Salmonella isolates. We are also indebted to Kathleen G. Julian, from Penn State College of Medicine, for her assistance and valuable comments in preparation of this article. This study was presented in part at the 24th International Conference on Pharmacoepidemiology and Drug Safety in Copenhagen, Denmark, in August 2008.

This study was supported in part by the Agency for Healthcare Research and Quality Centers for Education and Research on Therapeutics cooperative agreement (U18-HS10399) and by the Pennsylvania Department of Health through Centers for Disease Control and Prevention grant (ELC-04040) for National Antimicrobial Resistance Monitoring.

Disclosure Statement

No competing financial interests exist.

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