Multidrug-Resistant Salmonella Isolates from Retail Chicken
Meat Compared with Human Clinical Isolates
Nkuchia M. M’ikanatha,1,2Carol H. Sandt,3A. Russell Localio,2Deepanker Tewari,4Shelley C. Rankin,2
Jean M. Whichard,5Sean F. Altekruse,6Ebbing Lautenbach,2Jason P. Folster,5,7Anthony Russo,4
Tom M. Chiller,5Stanley M. Reynolds,3and Patrick F. McDermott8
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 >2mg=mL) to ceftriaxone and carried a
blaCMYgene, 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 indis-
tinguishable from a human isolate in PulseNet; both isolates carried the blaCMY-2gene.
Conclusions: These data demonstrate the presence of multidrug-resistant Salmonella in poultry meat, including
blaCMYplasmid-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.
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
the 2010 national health objective of 6.80 cases per 100,000
almonella enterica causes an estimated 1.4 million
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 sus-
ceptibility to ceftriaxone (minimum inhibitory concentration,
MIC, >2mg=mL), an ESC used to treat salmonellosis in humans
1Division of Infectious Disease Epidemiology, Pennsylvania Department of Health, Harrisburg, Pennsylvania.
2Center for Clinical Epidemiology and Biostatistics, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania.
3Pennsylvania Department of Health Bureau of Laboratories, Exton, Pennsylvania.
4Pennsylvania Department of Agriculture, Harrisburg, Pennsylvania.
5Centers for Disease Control and Prevention, Atlanta, Georgia.
6National Institutes of Health, Bethesda, Maryland.
7Atlanta Research and Education Foundation, Atlanta, Georgia.
8U.S. Food and Drug Administration, Center for Veterinary Medicine, Laurel, Maryland.
FOODBORNE PATHOGENS AND DISEASE
Volume 00, Number 00, 2010
ª Mary Ann Liebert, Inc.
(Hohmann, 2001; CDC, 2006). Among human Salmonella iso-
lates tested by the National Antimicrobial Resistance Monitor-
ing 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 Salmo-
nella 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
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 pur-
chased raw chicken meatsamples in three categories basedon
packing label (prepackaged boneless breast ‘‘cutlets,’’ open-
display cutlets, and organic or antibiotic-free cutlets) from
randomly selected grocery stores (n¼10) and farmers’ mar-
kets (n¼8) in central Pennsylvania. Packaging claims about
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 Salmo-
nella isolation, confirmation, and serotyping (FDA, 2003;
Popoff et al., 2001).
Susceptibility testing and detection of blaCMYgenes
broth microdilution method (Sensititre?; Trek Diagnostics,
Westlake, OH). The MICs for 15 antimicrobial agents used by
NARMS (CDC, 2006)—amoxicillin=clavulanic acid, ampicil-
lin, chloramphenicol, ceftiofur, ceftriaxone, ciprofloxacin,
gentamicin, kanamycin, nalidixic acid, streptomycin, sulfi-
soxazole, 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 blaCMYgenes by polymerase chain reaction using previ-
ously 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 com-
pare 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 stan-
dardized 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 sys-
tem (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 indistinguish-
able from human isolates, PCR was performed to amplify the
entire CMY gene for DNA sequencing analysis, using previ-
ously described procedures (Winokur et al., 2001).
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.
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 displayswas54(23.9%) of226compared to30(19.7%)of
152 in prepackaged samples (p¼0.64). 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%) un-
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 la-
beled samples originated from 16 different plants.
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 >2mg=mL) to ceftriaxone. Polymerase chain reaction
analysis showed that all 18 of the ceftiofur-resistant isolates
carried the blaCMYgene. Among the Salmonella serovar Ty-
phimurium isolates, 26 (92.9%) exhibited resistance to tetra-
cycline, 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 anti-
biotics (Table 2). None of the isolates from the other serovars
(Salmonella serovar Enteritidis [n¼22], Salmonella serovar
Braenderup [n¼2], or the untypeable strains [n¼3]) were re-
2M’IKANATHA ET AL.
susceptible to amikacin, ciprofloxacin, chloramphenicol, nali-
dixic acid, and trimethoprim=sulfamethoxazole.
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
counterscompared with prepackaged samples(Table 1).There
was also no significant difference in contamination with
antimicrobial-resistant Salmonella amongchicken 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 com-
bination JPXX01.1273=JPXA16.0328) in the PulseNet national
database (Fig. 1). The sequence of the blaCMY-2gene 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 re-
duced susceptibility to ceftriaxone (MIC 16mg=mL). The Sal-
monella serovar Typhimurium isolated from the human
source exhibited resistance to these antibiotics and to kana-
mycin. This isolate was collected on June 13, 2006, from a
17-year-old female Philadelphia resident who had salmonel-
losis; consumption of chicken was noted as a possible risk
factor. In addition to the human isolate, the pattern combi-
nation JPXX01.1273=JPXA16.0328 was also observed in 14
NARMS isolates recovered from chicken meat beginning in
Analysis of the serovar Kentucky isolates resistant to ?1
antibiotic recovered from chicken meat in this study revealed
Table 1. Prevalence of Antimicrobial-Resistant Salmonella in Raw Chicken Samples
from Retail Outlets by Source and Sample Type, Pennsylvania 2006–2007
Source and sample type
No. (%) of isolates resistant
to multiple antimicrobials
Total (all sample types)
aBecause of rounding, percentages do not add to 100.
bSample type was based on packaged label.
cF-test comparison, p¼0.64.
dF-test comparison, p¼0.72.
eCutlet pack samples in this category had no claim for organic or antibiotic-free and were assumed to be from conventional sources.
Table 2. Antimicrobial Resistance in Salmonella Serovars from Raw Chicken Meat, Pennsylvania, 2006–2007a
SerovarNo. of isolates resistant to each antibioticb
No. (%) of isolates showing
resistance to multiple antibiotics
isolates AmcAmp TioFox Kan StrSul Tet
aAll Salmonella isolates were susceptible to amikacin, ciprofloxacin, chloramphenicol, nalidixic acid, and trimethoprim=sulfamethoxazole;
none of the isolates from the other serovars (Salmonella serovar Enteritidis [n¼22], Salmonella serovar Braenderup [n¼2], and the untypeable
Salmonella [n¼3]) were resistant to any of the 15 antibiotics tested.
bPercentages for all serovars (n¼84) included the three untypeable Salmonella isolates recovered from chicken meat samples.
cThese 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;
MDR SALMONELLA IN MEAT AND HUMAN SOURCES3
one that was indistinguishable by both XbaI and BlnI pat-
terns (JGPX01.0027 for XbaI and JGPA26.0011 for BlnI) from
three other NARMS serovar Kentucky (n¼708) isolates col-
lected from poultry beginning in 2005. The indistinguishable
isolate from our study was resistant to amoxicillin=clavulanic
acid, ampicillin, cefoxitin, ceftiofur, streptomycin, and tetra-
cycline, and had reduced susceptibility to ceftriaxone (MIC
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
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
and 21% were resistant to ceftiofur. Among the most common
serovar, Typhimurium, over 70% of the isolates were MDR,
ceftiofur. Our results are consistent with findings from chicken
the United States, Ceftiofur is approved for use in food ani-
mals, including day-old chicks; its use in these settings po-
tentially leads to selection of resistant strains (Carattoli et al.,
2002; FDA, 2008; FDA, 2009). Resistance to ceftiofur in Salmo-
nella correlates with decreased susceptibility to other ESC, in-
cluding 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 blaCMY 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.,
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 Sal-
monella 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 fromchicken meatinthis study wasindistinguishable
(by both XbaI and BlnI analyses) from a human isolate in
antimicrobial agents and harbored the blaCMY-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
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 whe-
ther these MDR strains will emerge as more predominant
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
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
blaCMY-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 coin-
cided with an increase in Salmonella Newport MDR-AmpC
infections in cattle (Gupta et al., 2003). A recent study con-
ducted in Yucatan, Mexico, also documented emergence and
widespread dissemination ofMDR blaCMY-2Salmonellainfood
animals and in human clinical isolates (Zaidi et al., 2007). In-
vestigators 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 re-
sistance genes to other enteropathogens (Aarestrup et al.,
2008; Ajiboye et al., 2009).
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.
Salmonella Typhimurium from chicken compared with Salmonella Typhimurium from a human source by PFGE using
4M’IKANATHA ET AL.
The primary limitation of this study was small sample sizes
of certain subsets, which limited our ability to stratify sam-
ples. Further, lack of a commercial standard definition for
by chicken producers, thus limiting accurate sub-analyses of
This study documented significant contamination of
poultry meat with MDR Salmonella, including strains that had
plasmid-borne resistance genes (blaCMY), which confers re-
sistance 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 food-
borne pathogens. Programs that compare molecular charac-
teristics 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.
We acknowledgewithgratitude DavidG.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 Labora-
tory, and Jason Abbot, FDA CVM NARMS Laboratory, for
their help with molecular characterization of Salmonella iso-
lates. 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 pre-
sented in part at the 24th International Conference on Phar-
Denmark, in August 2008.
This study was supported in part by the Agency for Health-
care Research and Quality Centers for Education and Research
on Therapeutics cooperative agreement (U18-HS10399) and by
the Pennsylvania Department of Health through Centers for
Antimicrobial Resistance Monitoring.
No competing financial interests exist.
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Address correspondence to:
Nkuchia M. M’ikanatha, Dr.P.H., M.P.H.
Division of Infectious Disease Epidemiology
Pennsylvania Department of Health
Harrisburg, PA 17120
6M’IKANATHA ET AL.
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