Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 12, December 2005 1899
We compared antimicrobial resistance phenotypes
and pulsed-field gel electrophoresis (PFGE) subtypes of
1,028 human and 716 animal Salmonella enterica serotype
Typhimurium isolates from Minnesota from 1997 to 2003.
Overall, 29% of human isolates were multidrug resistant.
Predominant phenotypes included resistance to ampicillin,
chloramphenicol or kanamycin, streptomycin, sulfisoxa-
zole, and tetracycline (ACSSuT or AKSSuT). Most human
multidrug-resistant isolates belonged to PFGE clonal group
A, characterized by ACSSuT resistance (64%), or clonal
group B, characterized by AKSSuT resistance (19%). Most
animal isolates were from cattle (n = 358) or swine (n =
251). Eighty-one percent were multidrug resistant; of these,
54% were at least resistance phenotype ACSSuT, and 43%
were at least AKSSuT. More than 80% of multidrug-resist-
ant isolates had a clonal group A or B subtype. Resistance
to ceftriaxone and nalidixic acid increased, primarily among
clonal group A/ACSSuT isolates. Clonal group B/AKSSuT
isolates decreased over time. These data support the
hypothesis that food animals are the primary reservoir of
multidrug-resistant S. Typhimurium.
enterica serotype Typhimurium is the most common
serotype isolated from humans (2). In the 1990s, mul-
tidrug-resistant (MDR) S. Typhimurium definitive phage
type 104 (DT104) emerged in the United States; most iso-
lates were resistant to ampicillin, chloramphenicol, strep-
tomycin, sulfisoxazole, and tetracycline (resistance
phenotype [R-type] ACSSuT) (3). S. Typhimurium R-type
AKSSuT (with resistance to kanamycin) has also recently
ontyphoidal salmonellae are a leading cause of acute
gastroenteritis in the United States (1). Salmonella
emerged in the United States (4). Several studies have doc-
umented adverse health effects due to the increasing resist-
ance observed in S. Typhimurium (5–9). These effects
include an increased risk for infection with S.
Typhimurium (5), increased risk for bloodstream infection
(6), increased risk for hospitalization (6,7), treatment fail-
ures (8), and increased risk for death (9).
MDR S.Typhimurium strains have been well document-
ed in food animals, as have MDR S. Typhimurium out-
breaks in humans from animal contact or foods of animal
origin (8,10–17). However, contemporaneous parallel data
on resistance in human and animal S. Typhimurium isolates
in the United States are limited (18), and an advisory panel
has called for linking surveillance for bacterial resistance in
animals and humans to further evaluate the human health
effects of antimicrobial drug use in agriculture (19). The
objectives of our study were to evaluate antimicrobial
resistance and molecular subtyping data from all human
clinical S. Typhimurium isolates received through
statewide, population-based, active laboratory surveillance
in Minnesota and to compare the human isolates to isolates
from clinically ill animals in Minnesota identified by the
Minnesota Veterinary Diagnostic Laboratory (MVDL).
Human and Animal Isolates
The Minnesota Department of Health (MDH) requires
clinical laboratories to submit all Salmonella isolates to its
public health laboratory as part of active, laboratory-based
surveillance. MDH audits clinical laboratories to ensure
complete reporting. Human S. Typhimurium isolates sub-
mitted to MDH from 1997 to 2003 were eligible for this
study. Isolates that were part of an identified outbreak were
excluded, except for the index case-isolate. Isolates from
Antimic robial-drug S usc eptibility of
Human and Animal S almonella
Typhimurium, Minnesota, 1997–2003
Stephanie D. Wedel,* Jeffrey B. Bender,† Fe T. Leano,* David J. Boxrud,* Craig Hedberg,‡
and Kirk E. Smith*
*Minnesota Department of Health, Minneapolis, Minnesota, USA;
†University of Minnesota College of Veterinary Medicine, St. Paul,
Minnesota, USA; and ‡University of Minnesota School of Public
Health, Minneapolis, Minnesota, USA
secondary cases in household clusters and duplicate sub-
missions from the same case also were excluded.
MVDL is a regional laboratory for veterinarians; perti-
nent diagnostic samples are cultured for Salmonella spp.
Isolates are sent to the National Veterinary Services
Laboratories (Ames, Iowa) for serotyping. Confirmed S.
Typhimurium isolates are forwarded to MDH. S.
Typhimurium isolates obtained from diagnostic specimens
from sick animals cultured at MVDL from 1997 to 2003
were eligible for this study. Isolates from the same farm
with the same pulsed-field gel electrophoresis (PFGE)
subtype discovered within 1 year of the initial isolate col-
lection date were excluded. Research animal submission,
environmental sample, and non-Minnesota animal isolates
From 1997 to 2003, a total of 4,333 culture-confirmed
cases of human salmonellosis were reported in Minnesota.
S. Typhimurium was the most common serotype; it
accounted for 1,193 (28%) cases overall (median 172
cases/year, range 124–201). Of the 1,193 human S.
Typhimurium case-isolates, 1,028 (86%) were included in
this study (Table 1).
A total of 716 animal isolates were included in this
study (median 91/year, range, 67–150) (Table 1). Isolates
represented 644 farms and animal owners and 72 of 87
Minnesota counties. Most isolates were of bovine (n = 358,
50%) or porcine (n = 251, 35%) origin. Cattle isolates
decreased markedly over time: 106 isolates in 1997, 100
isolates in 1998, 49 isolates in 1999, 31 isolates in 2000,
29 isolates in 2001, 18 isolates in 2002, and 25 isolates in
2003. Conversely, swine isolates increased over time: 32
isolates in 1997, 27 isolates in 1998, 33 isolates in 1999,
22 isolates in 2000, 44 isolates in 2001, 39 isolates in 2002,
and 54 isolates in 2003. The remaining isolates included 38
(5%) avian (5 turkey, 1 chicken, 7 unknown, and 25 mis-
cellaneous species), 29 (4%) equine, 21 (3%) feline, 7
(1%) canine, and 12 (2%) other species.
All S. Typhimurium isolates (including variant
Copenhagen) submitted to MDH were confirmed as S.
Typhimurium and subtyped by PFGE. PFGE patterns were
compared by using BioNumerics software (Applied
Maths, Sint-Martens-Latem, Belgium) with the Dice coef-
ficient and a 1% band matching criterion (20). Patterns
with no visible differences were considered indistinguish-
able. Subtypes for S. Typhimurium at MDH are designated
with the prefix “TM” followed by a number (e.g., TM123).
PFGE patterns are also submitted to the PulseNet national
database. Antimicrobial susceptibility testing was per-
formed with the disc diffusion method and interpretive
standards of the National Committee for Clinical and
Laboratory Standards (NCCLS) (21). Antimicrobial sus-
ceptibility was determined for ampicillin (A), chloram-
phenicol (C), kanamycin (K), streptomycin (S),
sulfisoxazole (Su), tetracycline (T), cephalothin (Ct), cef-
triaxone (Cr), ciprofloxacin (Cp), gentamicin (G), nalidix-
ic acid (Na), and trimethoprim/sulfamethoxazole (Sxt).
The Etest for MIC was performed on isolates with interme-
diate susceptibility to ceftriaxone by disc diffusion; MICs
1900 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 12, December 2005
were interpreted according to NCCLS criteria (21). An
MIC of 48 µg/mL was considered resistant. Multidrug
resistance was defined as resistance to >5 antimicrobial
PFGE data were analyzed by the first 3 tiers of criteria
described by Tenover et al. (0, 1- to 3-, and 4- to 6-band
differences) (22). Two primary PFGE subtype clusters that
accounted for a large proportion of MDR isolates were
identified on the basis of a <3-band difference: 1) clonal
group A (CGA), composed of subtypes <3 bands different
from PFGE subtype TM5b, and 2) clonal group B (CGB),
composed of subtypes <3 bands different from PFGE sub-
Resistance was analyzed in terms of R-types ACSSuT,
AKSSuT, and ACKSSuT. R-type ACKSSuT isolates were
included in analyses of “at least R-type ACSSuT” isolates,
but not “at least R-type AKSSuT” isolates. Where indicat-
ed, ACKSSuT isolates were evaluated independently of
ACSSuT. R-types were analyzed in terms of clonal group.
The χ2test for trend was used to evaluate resistance trends
(EpiInfo 6.04d, Centers for Disease Control and
Prevention, Atlanta, GA, USA). Proportions were com-
pared by using the χ2test. Uncorrected p value and exact
95% mid-p limits for the maximum likelihood estimate of
the odds ratio (OR) were used. A p value <0.05 was con-
Of the 1,028 S. Typhimurium isolates, 455 (44%) were
resistant to >1 antimicrobial drug, and 296 (29%) were
MDR (Table 1). Among MDR isolates, 217 (73%) were at
least R-type ACSSuT, and 64 (22%) were at least AKSSuT
(Table 2). The proportion of MDR isolates decreased from
32% in 1997 to 25% in 2003 (χ2for linear trend 6.3, p =
0.01) (Figure 1). The proportion that were at least AKSSuT
also decreased, from 10% in 1997 to 3% in 2003 (χ2for
linear trend 17.7, p<0.001).
Eighteen (1.8%) isolates were resistant to ceftriaxone;
all were MDR (Table 1). Ceftriaxone resistance was more
prevalent from 2000 to 2003 (2.8%) than from 1997 to
1999 (0.6%) (OR 4.6, 95% confidence interval [CI]
1.4–20.0, p = 0.008). Eleven (1.2%) isolates were resistant
to nalidixic acid; all were MDR. Nalidixic acid resistance
was more prevalent from 2000 to 2003 (1.8%) than from
1997 to 1999 (0.2%) (OR 9.2, 95% CI 1.5–200.8, p =
0.011). Fifty-one (5%) isolates were resistant to trimetho-
prim-sulfamethoxazole. Of these, 34 (67%) were MDR,
including 20 (39%) that were at least R-type ACSSuT and
6 (12%) that were at least AKSSuT. Forty-three (4%) iso-
lates were resistant to gentamicin; of these, 23 (53%) were
We identified 271 unique PFGE subtypes among the
1,028 human S. Typhimurium isolates (median 63 sub-
types/year, range 52–72). The 10 most common subtypes
accounted for 509 (50%) isolates. CGA was composed of
31 PFGE subtypes. These subtypes accounted for 217
(21%) of all 1,028 human isolates, 188 (64%) of 296 MDR
isolates, and 181 (83%) of 217 isolates that were at least R-
type ACSSuT, including 12 isolates that were at least R-
type ACKSSuT (Table 2, Figures 2 and 3).
CGB was composed of 20 subtypes and accounted for
81 (8%) of all 1,028 human isolates, 55 (19%) of 296
MDR isolates, and 51 (80%) of 64 isolates that were at
least R-type AKSSuT (Table 2, Figures 2 and 3). The num-
ber of isolates with CGB subtypes decreased substantially
from 2001 to 2003 (Figure 2).
Overall, 640 (89%) of the 716 animal S. Typhimurium
isolates were resistant to >1 antimicrobial drug, and 580
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 12, December 20051901
Salmonella Typhimurium, Minnesota, 1997–2003
(81%) were MDR (Table 1). Of the 580 MDR isolates, 315
(54%) were at least ACSSuT, and 250 (43%) were at least
AKSSuT (Table 2). The proportion of isolates that were at
least ACSSuT increased over time (χ2for linear trend 39.5,
p<0.001). Conversely, the proportion that were at least
AKSSuT decreased (χ2for linear trend 71.7, p<0.001)
Of the 358 cattle isolates, 205 (57%) were at least R-
type AKSSuT, and 101 (28%) were at least ACSSuT. The
decrease in cattle isolates over time reflected a decrease in
the number that were at least AKSSuT (Figure 2). In addi-
tion, the proportion of cattle isolates that were at least
AKSSuT decreased significantly over time (χ2for linear
trend 8.9, p = 0.003).
Of the 251 swine isolates, 180 (72%) were at least R-
type ACSSuT, and 30 (12%) were at least AKSSuT. The
increase in swine isolates over time reflected an increase in
the number that were at least ACSSuT (Figure 2). In addi-
tion, the proportion of swine isolates that were at least
ACSSuT increased significantly over time (χ2for linear
trend 25.4, p<0.001). Nine (24%) of 38 avian isolates, 19
(66%) of 29 equine isolates, and 15 (71%) of 21 feline iso-
lates were MDR.
Twenty-five (3.5%) animal isolates were resistant to
ceftriaxone. Ceftriaxone resistance was more prevalent
from 2000 to 2003 (5.1%) than from 1997 to 1999 (2.2%)
(OR 2.4, 95% CI 1.0–5.7, p = 0.035). Twelve ceftriaxone-
resistant isolates were from cattle, and 10 were from
swine. Four (0.6%) animal isolates were resistant to
nalidixic acid, including 1 bovine isolate in 1997 and 3
turkey isolates in 2003. Eighty-one (11%) animal isolates
were resistant to trimethoprim-sulfamethoxazole. Of these,
79 (98%) were MDR, and 62 (77%) were at least ACSSuT.
Seventy-one (10%) animal isolates were resistant to gen-
tamicin. Of these, 69 (97%) were MDR, and 44 (62%)
were at least ACSSuT.
A total of 190 unique PFGE subtypes were identified
among the 716 animal isolates (median 36 subtypes/year,
range 31–47). Among animal isolates, CGAwas composed
of 48 PFGE subtypes. CGAaccounted for 264 (37%) of all
716 animal isolates, 256 (44%) of 580 MDR isolates, and
249 (79%) of 315 isolates that were at least R-type
ACSSuT, including 67 at least ACKSSuT isolates (Table 2,
Figures 2 and 3). CGB was composed of 35 subtypes.
CGB accounted for 278 (39%) of all 716 animal isolates,
250 (43%) of 580 MDR isolates, and 227 (91%) of 250
isolates that were at least R-type AKSSuT.
Distribution of PFGE subtypes differed by species and
year (Figures 2 and 4). CGB subtypes occurred predomi-
nantly in cattle and accounted for 67% of cattle isolates. As
with AKSSuT isolates, CGB subtype isolates were numer-
ous in cattle from 1997 to 1998, but the number dropped
markedly in 2002 and 2003 (Figure 2). CGA subtype iso-
lates increased in swine from 2000 to 2003 and substantial-
ly outnumbered CGA cattle isolates during those years.
CGA isolates in cattle were most common from 1997 to
1998 and then declined to a relatively stable, low level
Of 9 MDR avian isolates, 5 were in CGA and 1 was in
CGB. Of 19 MDR equine isolates, 4 were in CGA and 5
were in CGB. Of 15 MDR feline isolates, 8 were in CGA
and 6 were in CGB.
Animal-Human Isolate Comparison
Combining the 1,028 human and 716 animal S.
Typhimurium study isolates, 395 PFGE subtypes were
identified. Sixty-six subtypes occurred both in animals and
humans. These 66 subtypes represented 673 (65%) of
human and 537 (75%) of animal isolates. Eighteen (27%)
of shared subtypes were in CGA, and 12 (18%) were in
Combining the 296 MDR human isolates and the 580
MDR animal isolates, 183 PFGE subtypes were identified.
1902 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 12, December 2005
Figure 1. Percentage of Salmonella enterica serovar Typhimurium
isolates from Minnesota humans (A) and animals (B) with mul-
tidrug resistance (i.e., resistance to >5 antimicrobial drugs), includ-
ing resistance phenotypes (R-types) ACSSuT and AKSSuT,
1997–2003. A, ampicillin; C, chloramphenicol; K, kanamycin; S,
streptomycin; Su, sulfisoxazole; T, tetracycline. R-type ACKSSuT
is included as R-type ACSSuT but not AKSSuT.
Of these subtypes, 31 occurred both among human and
animal MDR isolates. These 31 subtypes represented 237
(80%) human MDR isolates and 442 (76%) animal MDR
isolates. Eighteen of the 31 shared MDR subtypes were in
CGA, and 7 were in CGB. Of the 296 MDR human iso-
lates, 177 (60%) had a CGA subtype that also occurred
among MDR animal isolates, and 51 (17%) had a CGB
subtype that also occurred among MDR animal isolates.
Of the 296 MDR human isolates, 243 (82%) belonged to
CGA (64%) or CGB (19%). Of the 580 MDR animal iso-
lates, 506 (87%) belonged to CGA (44%) or CGB (43%).
The 6 most common individual subtypes in animals, all
of which were in CGAor CGB (Figure 3), were represent-
ed among human isolates (Figure 4). TM5b, the second
most common animal subtype, was the most common
human subtype. TM54, the most common animal subtype,
was sixth in humans. TM123 was the third most common
animal subtype and fifth in humans (Figure 4).
This study provides a comprehensive comparison of
clinical human and animal S. Typhimurium isolates from
the same area. Overall, 29% of human S. Typhimurium
isolates in Minnesota were MDR. Isolates with at least R-
types ACSSuT or AKSSuT made up almost all (95%) of
MDR S. Typhimurium in humans. Resistance phenotypes
that were at least ACSSuTpredominated. The level of mul-
tidrug resistance in human isolates decreased from 1997 to
2003, corresponding to a decrease in R-type AKSSuT iso-
lates. Resistance to at least ACSSuT was stable over time.
The level of multidrug resistance observed in human iso-
lates in Minnesota was slightly lower than that observed
through the National Antimicrobial Resistance Monitoring
System (NARMS) through 2002; however, multidrug
resistance trends for S. Typhimurium generally paralleled
NARMS findings (4,23).
Increasing resistance to ceftriaxone documented in
human isolates in Minnesota indicated that ceftriaxone
resistance continues to emerge in S. Typhimurium in the
United States (13,24). The 1.8% resistance to nalidixic
acid observed in human isolates from 2000 to 2003 was
not substantially higher than the 1% resistance among
NARMS isolates from 2000 to 2002 (23) but was signifi-
cantly higher than that seen in our isolates from 1997 to
1999. Most of the isolates that were resistant to both cef-
triaxone and nalidixic acid were from 2000 or later.
Resistance to these antimicrobial agents, as well as gen-
tamicin and trimethoprim-sulfamethoxazole, frequently
occurred in isolates that were also resistant to >5 other
antimicrobial drugs; this finding was true for all isolates
that were resistant to ceftriaxone or nalidixic acid.
Resistance to these clinically important antimicrobial
drugs was associated most frequently with ACSSuT resist-
ance rather than AKSSuT resistance.
The increasing resistance to ceftriaxone and nalidixic
acid (an elementary quinolone) is of concern because
extended-spectrum cephalosporins and fluoroquinolones
are needed to treat serious Salmonella infections. Recent
experiences in Denmark have shown treatment failures
and excess deaths associated with quinolone-resistant S.
Typhimurium (8,9). The addition of resistance to clinical-
ly useful antimicrobial drugs to already-pentaresistant R-
types is added cause for concern because pentaresistant S.
Typhimurium strains are more likely to cause infection (5)
and adverse health outcomes (6,7) than drug-susceptible
Despite the overall diversity observed among S.
Typhimurium isolates by PFGE, human MDR isolates
were highly clonal. Even when a relatively stringent defi-
nition of a clonal group (<3-band difference) was used,
>80% of human MDR isolates composed 2 clonal groups.
CGA isolates were characterized by ACSSuT resistance
and represented most human MDR isolates. Of isolates
from this study that were previously phage typed, those in
CGA have all been in the DT104 complex (12,25,26). The
clonal nature of ACSSuT/DT104 S. Typhimurium in the
United States has been well documented (20,27).
CGB isolates were characterized by AKSSuT resist-
ance. This group accounted for 19% of human MDR iso-
lates overall but was more prevalent early in the study,
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 12, December 20051903
Figure 2. Distribution of Salmonella enterica serovar Typhimurium
clonal group A pulsed-field gel electrophoresis (PFGE) subtypes
and clonal group B PFGE subtypes among clinical isolates from
humans and animals by species, Minnesota, 1997–2003. Clonal
group A subtypes were <3 bands different from subtype TM5b by
PFGE and were associated with resistance to ampicillin, chloram-
phenicol, streptomycin, sulfisoxazole, and tetracycline. Clonal
group B PFGE subtypes were <3 bands different from subtype
TM54 and were associated with resistance to ampicillin,
kanamycin, streptomycin, sulfisoxazole, and tetracycline. H, C,
and S indicate human, cattle, and swine isolates, respectively.
Salmonella Typhimurium, Minnesota, 1997–2003
after which a marked decline occurred. As with the
ACSSuT/DT104 complex, AKSSuT isolates appear to be
largely clonal in nature.
Most S.Typhimurium isolates from clinically ill animals
in Minnesota were MDR, which emphasizes that MDR
strains are prevalent animal pathogens (10). High resistance
levels occurred in all species, throughout the state, and dur-
ing the entire study period. As with humans, most MDR
animal isolates were in either the CGA/ACSSuT (DT104)
or CGB/AKSSuT clonal groups. PFGE subtypes found
among human and animal MDR isolates were remarkably
similar. This similarity is striking considering that
Minnesota residents may be exposed to S. Typhimurium
during travel or from food produced outside Minnesota.
Among animals, the CGB/AKSSuT clonal group was
most common in cattle. The sharp decrease in CGB iso-
lates in cattle was mirrored by a similar decrease in
humans. The cause of this decrease in cattle is not known.
The CGA/ACSSuT clonal group was distributed more
evenly among all animal species but became more com-
mon in swine over time. The cause for the increase in
swine CGA/ACSSuT isolates is not known.
MDR S. Typhimurium strains similar to those from our
study have been recovered from food animals and retail
meat products by other investigators, and multiple MDR S.
Typhimurium outbreaks caused by foods of animal origin
or animal contact have been documented (8,10,11,13–
16,28,29). Our data provide additional evidence that food
animals are the primary reservoir of MDR S. Typhimurium
for humans; MDR S. Typhimurium that belong to CGA or
CGB were documented in cattle or swine herds on hun-
dreds of farms throughout Minnesota. Testing isolates with
additional genetic subtyping methods and identifying
resistance determinants would help further characterize the
relationship between animal and human isolates (22,30).
In addition, data on use of antimicrobial drugs in animal
production (which are currently unavailable in the United
States because requirements are lacking) would be helpful
in assessing this issue.
Although the number of isolates was relatively small,
the level of multidrug resistance was high in both cat and
horse isolates. CGA/ACSSuT and CGB/AKSSuT isolates
were observed in both species. The importance of these
infections in companion animals has been demonstrated by
recent MDR S. Typhimurium outbreaks in humans associ-
ated with small animal veterinary facilities, including a
Minnesota outbreak of CGA/ACSSuT DT104 infections in
persons who adopted infected kittens from a humane
The source of animal isolates for our study is a limita-
tion in that Salmonella isolates from clinically ill animals
overstate the level of antimicrobial resistance observed in
isolates from healthy animals; therefore, strains from ill
animals are not representative of strains carried by animals
at slaughter (31,32). However, when we have evaluated S.
Typhimurium isolates from other studies, the most promi-
nent CGA and CGB subtypes from our study also have
been found in healthy food animals or their environments.
For example, TM5b and TM123 isolates were recovered
1904 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 12, December 2005
Figure 3. Pulsed-field gel electrophoresis
(PFGE) patterns of common Salmonella
enterica serovar Typhimurium subtypes
observed among clinical isolates from
humans and animals in Minnesota. The 3
clonal group B (CGB) PFGE subtypes rep-
resent the 3 most common CGB subtypes
in animals and humans. The 3 clonal
group A (CGA) PFGE subtypes represent
the most common CGA subtypes in ani-
mals and humans. PulseNet designations
are those used in the PulseNet national
database of the Centers for Disease
Control and Prevention (CDC).
Figure 4. Frequency of pulsed-field gel electrophoresis (PFGE)
subtypes that occurred >15 times among clinical human or animal
Salmonella enterica serovar Typhimurium isolates in Minnesota,
1997–2003. Subtypes TM5b, TM123, and TM218 are part of clon-
al group A (subtypes <3 bands different from subtype TM5b).
Subtypes TM54, TM54a, and TM97 are part of clonal group B
(subtypes <3 bands different from subtype TM54).
from healthy, market-ready pigs at slaughter (J.B. Bender,
unpub. data). Subtypes TM5b, TM123, and TM54 were
represented among poultry isolates evaluated by
Rajashekara et al. (28). In a study of Salmonella isolates on
dairy farms in 4 states, including Minnesota, subtypes
TM5b and TM54 were recovered from healthy dairy cows
or environmental samples (33). Finally, MDR S.
Typhimurium is present in the retail meat supply; in a
recent study, almost all strains of S. Typhimurium recov-
ered from ground meat (pork and chicken) were MDR
phage types DT104 or DT208 (29).
Another limitation of our study was the underrepresen-
tation of poultry isolates. Minnesota is a leading poultry
producer; however, most poultry diagnostics are conduct-
ed by the Minnesota Poultry Testing Laboratory. This lab-
oratory has documented DT104 in Minnesota poultry (28).
In our study, 3 of 4 nalidixic acid–resistant animal isolates
were from turkeys, even though very few turkey isolates
were tested. The role of poultry as a potential reservoir for
MDR S. Typhimurium, including nalidixic acid–resistant
strains, should be more thoroughly evaluated.
We agree with other investigators that the emergence of
multidrug resistance in S. Typhimurium is associated with
the widespread dissemination of clonal groups (27,34).
The changing trends of MDR S. Typhimurium in cattle
versus swine observed in our study and the presence of
MDR strains in poultry indicate that more study of individ-
ual subtypes and resistance determinants (including specif-
ic mobile genetic elements) is required to understand the
movement of these strains within and between animal
species. Improved biosecurity practices to interrupt dis-
semination are undoubtedly the key in controlling these
The potential role of the selection pressure of antimi-
crobial drugs used in animal agriculture in the dissemina-
tion of MDR S. Typhimurium clonal groups must be
considered. The ability of MDR S. Typhimurium strains to
accumulate additional resistances allows them to survive
under a wide range of conditions when antimicrobial
agents are used. Use of antimicrobial drugs to which MDR
S. Typhimurium strains are already resistant may increase
the number of animals infected with these strains and the
number of animals that manifest clinical illness. This use
is inherently likely to contribute to increased dissemina-
tion, both within and between farms. Thus, we encourage
the judicious use of all antimicrobial drugs in animals as
well as in humans. In particular, the recommendation (19)
that nonessential uses of specific antimicrobial drugs in
food animals should be eliminated (e.g., the use of tetracy-
clines and penicillins for growth promotion and feed effi-
ciency) has merit. MDR S. Typhimurium strains are
serious pathogens in food animals and humans. Restricting
conditions that favor their dissemination should return the
benefits of reduced incidence and severity of S.
Typhimurium infections in both animals and humans.
We thank laboratory staff at the University of Minnesota
Veterinary Diagnostic Laboratory, John Besser and staff at the
Minnesota Department of Health Public Health Laboratory for
their work with Salmonella isolates for this project, and staff
from the Minnesota Department of Health Acute Disease
Investigation and Control Section, who participated in data col-
lection for this project or reviewed this manuscript.
This work was supported in part through cooperative agree-
ments with the Centers for Disease Control and Prevention
(CDC) Emerging Infections Program, Foodborne Diseases
Active Surveillance Network (FoodNet) (U50/CCU511190-10)
and the CDC Epidemiology and Laboratory Capacity for
Infectious Diseases Program (U50/CCU519683-04-4).
Ms Wedel is an epidemiologist in the Minnesota Department
of Health, Foodborne, Vectorborne, and Zoonotic Diseases Unit.
Her professional interests include foodborne diseases, zoonotic
diseases, molecular epidemiology, and antimicrobial resistance
of foodborne bacterial pathogens.
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Address for correspondence: Stephanie D. Wedel, Acute Disease
Investigation and Control Section, Minnesota Department of Health, 625
Robert St N, PO Box 64975, St. Paul, MN 55164-0975, USA; fax: 651-
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