786

Journal of Food Protection, Vol. 76, No. 5, 2013, Pages 786795

doi:10.4315/0362-028X.JFP-12-079
Copyright G, International Association for Food Protection

Salmonella and Escherichia coli O157:H7 Prevalence in Cattle and

on Carcasses in a Vertically Integrated Feedlot and Harvest Plant
in Mexico
C. NARVAEZ-BRAVO,{ M. F. MILLER, T. JACKSON, S. JACKSON, A. RODAS-GONZALEZ,{ K. POND,{ A. ECHEVERRY,
AND M. M. BRASHEARS*
Department of Animal and Food Sciences, Texas Tech University, Box 42141, Lubbock, Texas 79409, USA
MS 12-079: Received 15 February 2012/Accepted 21 December 2012

ABSTRACT
To determine the prevalence of Salmonella and Escherichia coli O157:H7 in cattle feedlots and the impact of subsequent
contamination on carcasses in a Mexican Federal Inspection Type Standards harvest facility, 250 animals were tagged and
sampled in each step of the slaughter process. Samples were taken from hides and fecal grabs, and composite samples were taken
from three anatomical carcass sites (hindshank, foreshank, and inside round) during the slaughter process, at preevisceration (PE),
prior to entering the hot box (PHB), and after 24 h of dry chilling (DC). Additionally, 250 fecal samples were collected from the
feedlot (FL), holding pens (HP), and intestinal feces (IF), and water samples were taken from the HP area. E. coli O157:H7 and
Salmonella detection were carried out with the BAX System, immunomagnetic separation, and conventional methods. Overall
Salmonella prevalence was 52.5%. The highest prevalence (92.4%) was found on hides, followed by feces from the HP (91.0%),
FL (55.56%), PE (49.0%), IF (46.8%), and PHB (24.8%), for all sampling periods combined. The lowest prevalence of 6.0%
was found after DC. The overall prevalence of E. coli O157:H7 was as follows: 11.7% for hides, 5.2% for IF, 2.7% for FL, 2.0%
for HP, 0.8% for PE, 0.4% for PHB, and 0.4% for the cooler. High prevalence of Salmonella in IF and on hides present a
significant risk factor for contamination by Salmonella at the different processing steps. These results serve as a warning as to the
risks of contamination in meats for these pathogens and the importance of following good manufacturing practices during beef
production processes.

Salmonella and Escherichia coli O157:H7 are among

the most important foodborne pathogens worldwide and
continue to pose a major threat to human and public health
in both developed and developing countries. Salmonella and
E. coli O157:H7 are estimated to cause, respectively, 1.3
million and 62,000 cases of gastroenteritis each year in the
United States (43). Raw food of animal origin was linked
with foodborne outbreaks, and it was widely reported that
livestock animals are an important source of foodborne
pathogens (35, 69). Some investigations highlighted the
frequent detection of Salmonella and E. coli O157:H7 in
meat and meat products (e.g., (43)). Beef products can
become contaminated with these organisms through exposure to cattle feces or hides during processing, making
pathogen-reduction interventions during the harvest process
necessary in order to produce safer products (3). There are
numerous opportunities for cattle hides to become contaminated with pathogenic bacteria such as E. coli O157:H7 and
* Author for correspondence. Tel: 806-742-2805, Ext 235;
Fax: 806-742-4003; E-mail: mindy.brashears@ttu.edu.
{ Present address: Lacombe Research Center, 6000 C and E Trail,
Lacombe, Alberta, Canada T4L 1W1.
{ Present address: Colorado State University, Department of Animal
Sciences, Building 106C, Fort Collins, CO 80523-1171, USA.

Salmonella, including cross-contamination of cattle hides

from feedlot pen floors, packing plant holding pens, and/or
from restrainer floors, as well as during transportation (2, 5,
18, 60). It was also reported that carcass contamination can
be the result of pathogen transfer from the intestines during
the evisceration procedure, and from the hide onto the
carcass during skinning. However, the routes of contamination could have numerous other avenues, including
contaminated equipment and tools used during skinning,
contaminated operator hands, or contaminated dust particles
and water droplets spread by aerosols generated in the
production process (4). This information emphasizes the
importance of controls in the food chain to prevent
transmission of foodborne pathogens.
In Mexico, the harvest of beef is conducted under two
types of slaughter systems: (i) slaughter plants classified
as NonFederal Inspection Type Systems (non-TIF), also
known as rastros municipales (municipal slaughterhouses)
and (ii) slaughter plants that are Federal Inspection Type
Systems (TIF) certified, mostly under private management.
Rastros operate mostly under municipal or city direction.
Under Article 115 of the Mexican Constitution, the
slaughtering of animals is a service that local governments
must provide to the population. Municipalities have a duty

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SALMONELLA AND E. COLI O157:H7 PREVALENCE IN MEXICAN BEEF CARCASSES

to perform the services themselves or to outsource these

services by granting concessions to private individuals or
companies, and they cannot be penalized or closed even if
the establishments do not follow minimal good manufacturing practices (GMP) during processing.
On the other hand, TIF-certified slaughter plants
manufacture food products under official supervision and
they guarantee meeting quality control, sanitation, and
hygiene standards during processing. Rastros municipales
are not required to comply with the same food safety
regulations.
Research focused on the detection of E. coli O157:H7
is scarce in Mexico (11, 28, 65). Additionally, there is little
information available on Salmonella in beef and other food
products; therefore, more research is needed on the
prevalence of both pathogens in the different stages of
the Mexican beef production system. Data on the fecal
prevalence of Salmonella and E. coli O157:H7 in feed yards
is an important indication of the risks of contamination in
subsequent steps of the beef chain. This information can
facilitate the implementation of preharvest intervention
procedures at the feedlot level. Therefore, the objective of
this study was to determine the prevalence of Salmonella
and E. coli O157:H7 in a cattle feedlot in Mexico and the
subsequent contamination on carcasses in a TIF Mexican
harvest facility over time, and to determine if the relationship,
if any, between fecal and hide prevalence and carcass
contamination.
MATERIALS AND METHODS
Sample collection. Samples were collected at different
locations along the production and processing lines at a vertically
integrated feedlot (FL) and at a TIF-certified slaughter plant in
Mexico. For the purposes of this article, integrated means that the
Mexican company owns each link of the beef production chain,
specifically, facilities that raise animals, facilities that produce feed,
the facilities for slaughtering the animals, as well as the processing
and fabrication areas where the final products are packed.
In the FL, beef cattle, primarily zebu-type, crossbred young
bulls, were raised specifically for beef production; they were given
a diet of grain, hay, molasses, and spent distillers grain.
The slaughter plant primarily euthanizes animals from its own
FL; however, dairy cull bulls and cows are also slaughtered at the
plant, and these animals generally come from farms outside of the
vertical integration. All the animals were subject to antemortem
inspection by a veterinarian, and only the animals that passed the
screen (healthy) were slaughtered.
Sampling was conducted during July and December of 2009,
and April, August, and December of 2010. The months of June and
July are the hottest and most humid in Mexico. During the sample
time, the food safety team held workshops for the supervisory
personnel in charge of the quality and food safety programs at the
slaughter facility. The workshops addressed food safety topics such
as prerequisite programs (standard operational sanitary procedures,
GMP, and the hazard analysis and critical control points [HACCP]
system). Additionally, audits of their prerequisite and HACCP system
were conducted in order to improve food safety. As a result, some
changes were made over the sampling period at the slaughter facility.
Fecal samples. At the FL, different lots were examined. The
selection of the pen was based on the lots of animals the plant had

787

scheduled to be slaughtered on the sampling day. The purpose was

to collect fecal samples from the same lots of animals that would
be harvested at the slaughter plant. Approximately 40 g of sample
was taken from each fresh fecal pat by using plastic spoons (20)
and placed aseptically into a labeled, sterile plastic container. In the
holding pen area (HP) the same lots of animals previously sampled
in the FL were the target. Fecal samples were taken in the same
manner as described above in the FL. The HP consisted of any area
encountered by the animal from the time of unloading from the
truck to the stunning event.
Intestinal feces (IF) samples were collected after evisceration
from each tagged carcass. The entire gastrointestinal tract was
tagged and followed to the viscera table. On the viscera table, the
rectocolon portion of the intestines was cut, and approximately 40 g
of feces was taken and placed aseptically in a labeled, sterile plastic
container. All fecal samples were placed in a cooler.
Water samples. At the HP area, water samples were collected
directly from the dairy footbath through which animals walk, with
the purpose of cleansing the hooves before slaughter. The bath had
an approximate area of 11.7 m2, with a depth of approximately of
15 to 18 cm, and no antimicrobial or sanitizer was added to it. The
water was changed only onceat the end of the production day.
Hide samples. At the harvest facility, after each animal was
stunned, bled, and placed onto the rail system, a sample from each
hide was obtained, and the carcass was tagged after hide removal
so that the samples were matched from the hide through all the
other processing steps.
Composite samples were taken from inside rounds, hindshanks, and foreshanks, with a SpongeSicle (3M, Two Harbors,
MN) hydrated with 10 ml of buffered peptone water (Difco, BD,
Sparks, MD). A hide section of approximately 1 m2 was swabbed
in the perineal area, and another section approximately 250 cm2
was swabbed from each of the foreshanks and hindshanks. To
facilitate the sampling, two sponges were used for each carcass;
one sponge was used for the inside round and hindshanks, and the
other sponge was used for the foreshanks. Later, these two sponge
samples from the same carcass were combined into one sample bag
in the laboratory to obtain composite samples.
Carcass samples. Samples from the carcasses were collected
at each step of the slaughter process: after dehiding at
preevisceration (PE), pre-cooler (PC), just prior to entering the
hot box, and after 24 h of dry chilling (DC) in the coolers.
Composite samples were taken from inside rounds, hindshanks,
and foreshanks, with SpongeSicles hydrated with 10 ml of buffered
peptone water, following the same procedure describe above for
hide composite samples. The foreshank, hindshank, and inside
round areas were selected for sampling in this study, as those areas
were reported as heavily contaminated (53) in a previous study.
All samples were transported in coolers containing ice packs
to the microbiology laboratory in the Experimental Sciences
Building at Texas Tech University (Lubbock) by the sampling
team. The time the samples remained in the coolers on their way
from Mexico to the United States was approximately 24 to 48 h.
Salmonella detection. The fecal sample enrichment containing approximately 1.0 0.1 g of feces from the different sampling
locations (FL, HP, and IF) was placed into 9 ml of RappaportVassiliadis broth (EMD, Darmstadt, Germany) and 9 ml of
tetrathionate broth (Difco, BD) with novobiocin (20 mg/liter) and
0.1% brilliant green (10 ml/liter) (Sigma, St. Louis, MO). After
addition of the enrichment media, each tube was vortexed

788

NARVAEZ-BRAVO ET AL.

thoroughly and then incubated at 42 2uC for 24 h. After

incubation, each tube was streaked for isolation onto xylose lysine
Tergitol 4 (XLT4) agar (BD, Franklin Lakes, NJ). Inoculated
XLT4 plates were incubated at 35 2uC for 24 h. Several
colonies were chosen from the same enrichment-plating combination to meet the goal of three isolates from each fecal sample.
Presumptive-positive colonies from XLT4 plates were tested with a
Salmonella latex agglutination kit (Oxoid, Ltd., Basingstoke, UK).
Positive colonies were stored at 280uC for further characterization.
For hides, each SpongeSicle bag was homogenized for 30 s
with a stomacher (Stomacher 400, Seward Medical, Ltd., West
Sussex, UK), and then 1 ml of sample from each bag was
aseptically transferred into a 9-ml tube of tetrathionate and
Rappaport-Vassiliadis broth. After addition of the enrichment
media, each tube was vortexed thoroughly, and then incubated at
42 2uC for 24 h. After incubation, each tube was streaked for
isolation onto XLT4. Incubation and identification followed the
same procedure detailed above for fecal samples.
E. coli O157:H7 detection. Immunomagnetic separation
(IMS) was used to isolate E. coli O157:H7 from the fecal and hide
samples. Approximately 1 g of fecal sample was diluted in 9 ml of
gram-negative broth supplemented with novobiocin (20 mg/liter,
10:1 dilution) (mGNB; Sigma). After addition of the selective
enrichment media, each tube was vortexed thoroughly, and then
incubated for 6 1 h at 37uC. After the incubation period, IMS
was performed with Dynabeads by using the BeadRetriever
instrument (Dynal, Lake Success, NY), following the manufacturers recommendations. Samples were subjected to IMS by mixing
1 ml of the culture with 20 ml of anti-O157 beads (Dynal). Beads
were washed three times in phosphate-buffered salineTween 20
and 50 ml of the bead-bacteria mixture of E. coli O157; the beads
were then spread onto CHROMagar O157 (BBL, BD, Sparks,
MD) plates. Plates were incubated at 37uC overnight. From each
CHROMagar O157 plate, typical colonies (mauve) were tested
against O157 serogroup-specific antisera by a slide agglutination
test (DrySpot, Oxoid, Ltd.). Final confirmation was performed by
PCR analysis for E. coli O157:H7 serotype by using the BAX
System (DuPont Qualicon, Wilmington, DE).
For hides, each SpongeSicle bag was homogenized with the
Stomacher 400 for 30 s, and then a 1-ml sample from each bag was
aseptically transferred into 9 ml of mGNB. After addition of the
selective enrichment media, each tube was vortexed thoroughly,
and then incubated for 6 1 h at 37uC. Incubation and
identification followed the same procedure explained above for
the fecal samples.
Salmonella and E. coli O157:H7 detection on carcasses by
using the BAX System. The carcass samples were enriched in
modified tryptic soy broth (mTSB; Difco, BD) to detect for E. coli
O157 and in TSB (Difco, BD) for Salmonella detection. Each
SpongeSicle bag was homogenized for 30 s with the Stomacher
400, and then 1 ml of sample from each bag was aseptically
transferred into 9 ml of mTSB (20 mg/liter; Sigma) or TSB. Each
tube was vortexed thoroughly and incubated for 14 h at 37uC and
24 h at 37uC, for E. coli and Salmonella, respectively. After
enrichment, E. coli O157:H7 and Salmonella were detected with
the AOAC Internationalapproved BAX System (PCR) detection
unit, according to the manufacturers instructions. IMS was also
used to recover the isolates (Salmonella and E. coli O157 strains)
from carcass samples that were BAX System positive. Final
confirmation was performed by latex agglutination and PCR
analysis for the E. coli O157:H7 serotype and generic Salmonella
by using the BAX System.

J. Food Prot., Vol. 76, No. 5

FIGURE 1. Overall Salmonella prevalence in FL, IF, HP, hide,

and carcasses at PE, PC, and cooler. Chi-square analysis
indicates that the distribution differed between different locations
along production and processing (P . 0.0001).
It is important to mention that the utilization of different
detection methods in this research was based on the results
obtained in a previous pilot study performed in this same location
by our research team. These results showed low Salmonella and E.
coli O157:H7 loads on samples obtained from carcasses, and it was
then decided to use the BAX System in order to improve the
likelihood of detection of these two pathogens on carcasses.
Although the method used for carcasses differs from the previous
one used for Salmonella and E. coli detection on hide and fecal
samples, all the results from conventional BAX System and IMS
methods were comparable for prevalence, based on the fact that
these methods have similar sensitivity and indicate the presence or
absence of the pathogens in question.
Serotyping. A small fraction (7.6%) of Salmonella isolates
recovered during the first sampling date (July 2009) from different
samples (hides, FL, PE, PC, cooler, and water from dairy footbath
samples) were serotyped by the Salmonella Reference Center at the
University of Pennsylvania (New Bolton).
Statistical analyses. Data were imported into a commercially
available software package for exploration and analyses (SAS,
version 9.2, SAS Institute Inc., Cary, NC). Frequency tables were
generated to provide an initial exploration of unadjusted point
estimates. Generalized linear models were constructed to explore
relationships between the response variable and various independent variables. Where evidence of over-dispersion existed, the data
were scaled with an over-dispersion parameter. Risk factors were
analyzed with SAS logistic regression models (PROC LOGISTIC)
(56).

RESULTS AND DISCUSSION

Salmonella prevalence. A total of 1,695 samples were
collected from different locations, including the FL and the
slaughter plant. Salmonella was isolated from 52.5% of
these samples. Overall, the highest prevalence was found on
the hides (92.4%), followed by feces at the HP (91.0%), FL
(55.6%), PE (49%), IF (46.8%), PC (24.8%), and cooler
(6%) (P . 0.0001) (Fig. 1). The lowest prevalence (6.0%)
was found in the carcasses after 24 h of DC in the cooler
(Fig. 1).
The results obtained from IF show that almost half
(46.8%) the animals were Salmonella carriers, which

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SALMONELLA AND E. COLI O157:H7 PREVALENCE IN MEXICAN BEEF CARCASSES

indicates that Salmonella was widespread in the FL. It is

possible that some problems such as animal feed or water
contamination with Salmonella could have been present.
Cattle typically acquire Salmonella enterica from other
infected livestock, which spread the pathogen throughout
the herd via contaminated cattle feces, feed, and water (23,
69). Previous studies reported that one of the important
factors that could have a major impact on animal infection is
the ubiquity and persistence of S. enterica at concentrated
animal feeding operations and dairy herds, where livestock
feed is susceptible to contamination from wildlife excreta
during on-farm storage (19, 32, 34). Animal feed, spent
distillers grain, and water samples at the feeding operation
were not collected in this study, and because of this, we
cannot ascertain with certainty the real source of Salmonella
infection; however, we recommended for future investigations that animal feed and environmental samples be
obtained at animal feeding operations in order to determine
sources of animal infection and the extent of contamination,
as well as to better understand the epidemiology of this
pathogen in Mexican beef production systems.
Fresh fecal pats collected from FLs and abattoir HP
showed prevalences of 55.6 and 91.0% respectively. As
these prevalence values are considered high, we hypothesize
that one of the factors that explains this high prevalence is
the fact that a high number of animals were Salmonella
carriers; in fact, the prevalence (55.6%) in FL was very
similar to the prevalence (46.8%) in IF. The 91% prevalence
at abattoir HP shows high contamination, which could be
attributable to multiple cattle in multiple lots passing through
and being held in the same FLs and HP. Additionally, the
slaughter plant received animals from a diverse group of
farms, and although these animals were kept separate in the
abattoir HP, eventually the same HP was used for other
animal lots over time, making possible the contamination
from one processing day to another. Small et al. (61) reported
that pathogens survived for more than 1 week in a lairage
environment, and it was also reported that contamination of
lairages with pathogens could be carried over from one batch
of animals to another and/or from one day to the next (59, 61),
likely the occurrence of cross-contamination with lots of
animals originating from external and internal farms. It is
also possible that external animals/species or vehicles
adjacent to the farms share the same or higher Salmonella
prevalence than the prevalence found in internal farms, which
would have an impact on abattoir HP contamination (23). The
abattoir had in place some HP cleaning procedures, which
basically consisted of mechanical removal of the fecal
material from the HP floor (roughened concrete), followed
by application of water to remove visual fecal material
remains. This cleaning was usually performed once a day, at
the end of the harvest day. During the course of the day, only
mechanical removal of the fecal material from the floor was
performed on an as-needed basis, and no attention was given
to corridors for cleaning purposes, and no sanitizer was
applied. Likely, this cleaning procedure was not enough to
effectively eliminate bacterial pathogens, for which an
evaluation of these procedures is needed in order to assess

789

FIGURE 2. Average Salmonella prevalence before and after

removal of the abattoir dairy footbath, in hide, PE, PC, and
cooler samples. Preintervention samples included the samplings of
July 2009, December 2009, and April 2010, while postintervention
samples included August and December 2010. Chi-square analysis
indicates that the distribution differed before and after intervention
for all variables (P , 0.0001).

if Salmonella and E. coli O157:H7 are effectively eliminated

from HP.
The highest (92.0%) prevalence on hides was consistent with other research that reported cattle hides as an
important source of Salmonella contamination (8, 10). Other
researchers also reported Salmonella prevalence on hides in
the range of 20.0 to 100% (25). One factor that might have
contributed to this high level of contamination on the hides
was the high Salmonella prevalence in the IF, FL, and
abattoir HP, where the bacteria could be picked up on the
hides and be easily spread onto the environment in times of
heavy rain and humidity. Another factor that might have
contributed to Salmonella contamination of the hides in this
particular abattoir was the dairy footbath. The animals were
passed through the dairy footbath immediately before
harvest, and usually more than one animal went through it
at the same time; consequently, animal movement in this
bath caused dirty water to splash and droplets contaminated
with Salmonella and other bacteria to spread over the
animals, even reaching the dorsal midline, thus contaminating the hides. This water was changed at the end of the day,
no disinfectant was added, and results of Salmonella testing
were 100% positive. These results were expected because
of the high contamination of the FL and abattoir HP with
Salmonella, where animals carry the bacteria on the hooves
and legs (mud and fecal material), which then accumulates
in the bath. Once the dairy footbath was removed (after the
first visit), the prevalence of Salmonella was reduced
significantly, from 99.3 to 82% (P , 0.001) (Fig. 2). This
type of cross-contamination was documented by Arthur et
al. (3), with pulsed-field gel electrophoresis tracking, and
the results indicated that an important part of bacteria
transfer onto cattle hides occurs in the abattoir HP.
An additional important factor that could have an effect
on Salmonella prevalence was the weather. The month of
July 2009 showed higher prevalence (74.5%); July also had

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NARVAEZ-BRAVO ET AL.

J. Food Prot., Vol. 76, No. 5

TABLE 1. Risk factors associating hide, IF, FL, HP, and carcass at different steps of the slaughter process: PE, PC, and cooler with
Salmonella-positive carcasses
Sample area

Hide

PE

PC
Cooler

Stage

Odds ratio

95% confidence interval

P value

IF
FL
HP
Water
IF
Hide
Lairage
Water
Feedlot
IF
PE
IF
FL
PE
PC

8.23
1.22
1.28
,0.001
2.80
2.71
0.78
,0.001
0.96
2.28
5.95
4.23
2.17
2.36
8.19

1.8237.22
0.433.49
1.2811.56
,0.001.999.9
1.644.77
0.858.67
0.282.19
,0.001.999.9
0.61.65
1.154.32
2.8512.42
0.8820.38
0.657.16
0.4612.23
2.0532.79

0.006
0.7
0.8
0.9
0.0001
0.09
0.6
0.9
0.8
0.01
,0.0001
0.07
0.2
0.3
0.003

the most rain and humidity. It was also observed during this
sampling that the slaughtered animals were particularly
dirty, which reinforced our belief that environmental factors
could have contributed to the spread and cross-contamination
of the hides with Salmonella.
In this particular abattoir, there were no hide wash
cabinets; instead, they washed the hides by using regular
hose water pressure.
With regard to fecal samples, the percentages of
positive samples (HP, IF, FL) obtained in this study were
considerably higher than those in other studies48.0% for
HP and 16.0% for IF (25)while other authors reported a
smaller prevalence in IF, ranging from 0.0 to 5.5% (3, 24,
64) and fecal samples in the FL (33.9%) (27). The overall
prevalence of Salmonella at PE (49%), and cooler (6%),
was similar to those reported in the United States at PE
(44.0 to 55.0%), but with higher reduction after interventions at the cooler carcasses (0.1 to 1%) (10). In the United
Kingdom, Small et al. (59) reported a Salmonella
occurrence from 0 to 20% in beef carcasses sampled before
chilling; the prevalence found in this research was slightly
higher (24.8%). A Belgian surveillance report showed a
lower prevalence (2.5%) on meat carcasses sampled in the
chilling room between 2 and 4 h after slaughtering (29).
When comparing the prevalence before chilling (after
washing) obtained in this study (24.8% at PC) with the
prevalence (15.5% [78 of 505]) reported in non-TIF small
abattoirs before chilling (after washing) in Mexico (49), our
prevalence was higher. This is likely because of differing
sampling and detection methods, as well as different animal
populations and geographic location.
Carcass contamination was likely a result of transfer
of the pathogen from intestines during the evisceration
procedure and from hides onto the carcasses during
skinning. It is also possible that cross-contamination from
previous days could have occurred because of improper
cleaning and disinfection of tools and equipment, although
the plant under study complied with international food
safety regulations such as implementation of standard

operation procedures, GMP, and HACCP, and the installations always appeared clean; however, environmental
samples were not collected, and conclusions cannot be
drawn regarding these circumstances. The routes for
pathogen transfer during the harvest process could have
numerous avenues, and it was suggested that contaminated
equipment and tools used during skinning, contaminated
operator hands, or contaminated dust particles and/or water
droplets spread by aerosols, generated in the process could
play an important role (4). It is important to mention that
animal hides were washed with water by using a hose after
the shackling of the animal, which could increase the water
droplets spread during the process, leading to contamination
of the carcasses.
When the samples were analyzed for overall prevalence
by date of sampling, variations in prevalence were observed:
74.5% in July 2009, 33% in August 2009, 48% in
December 2009, 60% in April 2010, and 41% in December
2010 (P , 0.0001), which showed a tendency to decrease
over time. On the first sampling date, the proportion of
positive samples for Salmonella was 74.5%, while on the
last day of sampling, the prevalence was 41.0%. The
smallest prevalence was observed on the fourth sampling
day, at 33.0%. It is possible that this reduction was the result
of the HACCP training performed during the second
sampling date, and audits of the HACCP system, performed
over the 3-year duration of the project, which included
modifications and consequent improvement of food safety
programs. These modifications could have played a role
in the overall reduction of Salmonella prevalence (P ,
0.0001). One of these changes was the removal of the dairy
footbath at the abattoir HP (Fig. 2), and the application of
lactic acid to the carcass surfaces as an intervention for
pathogen reduction.
Salmonella risk factors. A positive correlation in the
presence of Salmonella in IF and on hides, and contamination of the carcasses was observed. A risk analysis
showing the likelihood of contamination of the carcasses

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SALMONELLA AND E. COLI O157:H7 PREVALENCE IN MEXICAN BEEF CARCASSES

when the animals were asymptomatic carriers and when

they were shedding the pathogen (P , 0.005) is presented in
Table 1. The analysis yielded the following results: positive
animals for Salmonella in IF had an 8-times-higher
likelihood of testing positive on hides (P ~ 0.006), were
almost 3 times more likely to test positive on carcasses at PE
(P ~ 0.0001), and were 2 times more likely to test positive
on carcasses prior to entering the hot box (P ~ 0.01).
Moreover, positive carcasses at PE had an increased chance
of testing positive for Salmonella at the PC by 5.95 times
(P , 0.0001), and positive carcasses at the PC had an 8-fold
increased chance of a positive carcass after 24 h of DC (P ~
0.003). Regarding comparison between results obtained
by different pathogen detection methods applied in this
research, we considered the results obtained comparable for
an appropriated statistical analysis. The reasons are as
follow.
Conventional culture methods remain the most reliable
and accurate technique for foodborne pathogen detection,
with effectiveness based on stepwise cultural enrichment
to enhance the detection of specific pathogens (39, 66).
Salmonella culturebased techniques that include stepwise
culture enrichment are considered the gold standard, and
when new rapid methods are developed, conventional
culture techniques are used as a reference method and to
calculate accuracy. Additionally, many nonconventional
detection systems need an enrichment, and positive results
must be confirmed by the appropriate official method, which
involves culturing (26). Comparisons between Salmonella
conventional culture methods and molecular detection
methods such as real-time PCR and the BAX System have
demonstrated similar sensitivity (6, 51, 58, 73). PCR is a
rapid technique in which a few copies of target DNA can be
amplified to a level detectable by gel electrophoresis.
However, PCR can be inhibited by several factors such as
food components, humic acid, urine, and bile salts, among
others (38, 54, 57), for which the removal of inhibitory
substances is a major step in the preparation of samples for
PCR-based detection of food pathogens (36). Conventional
PCR is superior to culture for detecting the main pathogens
in food samples when the prevalence is low (1). Regarding
real-time PCR sensitivity, the limit of quantification with
food samples is around 103 to 104 CFU/g. This limit is
considered high, since most samples at the food supply chain
are usually contaminated with fewer pathogen cells (normally
,100 CFU/g). Consequently, this requires some enrichment
of the microorganisms to be done prior to analysis (39).
The BAX System is a real-time PCRbased technique
in which the testing sample consists of an aliquot of
enrichment broth after incubation with the sample in
question. The disadvantage of this is that the bacteria
isolated (if needed for further characterization or confirmation) need to be isolated with conventional culture
techniques. It is also important to consider that PCR
techniques cannot distinguish between live and dead cells
and hence provide more false-positive results, and confirmation is usually a requirement when positives results are
obtained.

791

One of the problems that can arise with conventional

methods is that only a small amount of the enrichment
culture is used to strike the sample onto the selective agar
plates; consequently, when the amount of bacteria cells is
low in the enrichment broth, it is difficult to recover the
isolate. One approach toward solving this problem is to
use a specific IMS of the target organism directly from the
sample or preenrichment medium. Additionally, when
background flora is abundant, such as in fecal samples,
IMS is a powerful tool to extract bacteria from the matrix of
the sample, facilitating detection on the agar plate (16).
Based on the above information and the previous pilot
research conducted in Mexico by our team, we chose to
use conventional methods for Salmonella detection in what
we call dirty samples (feces, hides, and water from the
dairy footbath). The decision was based on the fact that
prevalences found in the pilot studys results for these
particular samples were high, for which Salmonella
recovery was not considered as a problem. In the case of
E. coli O157:H7, IMS was chosen to recover E. coli
O157:H7 from dirty samples because of the low occurrence
of O157:H7 in fecal samples and the high background flora,
and compared with culture standard methods, IMS showed
a better sensitivity (100-fold) than direct culture (16). Some
research has indicated that IMS and PCR methods compare
well (14, 17), while other research suggests that PCR could
be more sensitive than IMS (13). The BAX System was not
used in this research to detect E. coli O157:H7 in fecal
samples, because in our previous experience, we determined
the BAX System does not perform well with fecal samples
because of the inhibitors present in the fecal matrix. In this
case, the use of a stool DNA kit to clean the DNA is
recommended, which is expensive and time-consuming
because of the amount of samples. It is also important to
mention that the BAX System is only intended for analysis
of food samples. Additionally IMS was used to recover
Salmonella and E. coli O157:H7 isolates when culture
methods failed, e.g., a positive BAX System sample was
normally struck onto a selective agar plate, but when
recovery was unsuccessful, IMS was performed on the
sample in order to recover the pathogen and perform further
confirmation.
In the case of clean samples (carcasses) we chose
to use the BAX System because low Salmonella and E. coli
O157:H7 prevalence rates were expected. This assumption
was made on the premise that the abattoir was federally
certified and on previous studies on E. coli O157:H7
prevalence in Mexico where the IMS technique was used as
the detection method (11). The BAX System is an accurate,
rapid method, and it performs well when an enrichment step
is included, saving time and effort. After a sample showed
positive results for the specific pathogen, IMS was used in
order to recover the isolates for further characterization.
Detection methods utilized for Salmonella vary in their
sensitivity; however, other researchers that compared
Salmonella conventional culture methods and the BAX
System for Salmonella showed similarities in sensitivity (6,
58), as well as other real-time PCR platforms (51, 73).

792

NARVAEZ-BRAVO ET AL.

FIGURE 3. Overall Escherichia coli O157:H7 prevalence in FL,

IF, HP, hide, and carcasses at PE, PC, and cooler. Chi-square
analysis indicates that the distribution differed between different
locations along production and processing (P . 0.0001).

Salmonella serotypes. A total of 1,620 Salmonella

isolates were recovered from the different samples. A small
portion (7.6%) was sent for serotyping. In total, 10
S. enterica serotypes were found in different points (hides,
FL, PE, PC, cooler, and water from the dairy footbath):
Anatum, Montevideo, Tennessee, Kentucky, Muenster,
Give, Reading, Mbandaka, Meleagridis, and Fresno. In
Mexico, Anatum, Meleagridis, Agona, and Typhimurium
were the serotypes most commonly found in retail beef from
2000 to 2005 (71, 72). More recent research conducted in
Jalisco, Mexico, reported the following serotypes: Give,
Typhimurium, Infantis, Anatum, Bovismorbificans, Montevideo, Havana, Muenster, Enteritidis, Livingstone, Oranienburg, Panama, and Sinstorf (49).
A report that compiled results corresponding to the
period of 1972 to 1999 of Salmonella isolates from private
and public laboratories across Mexico investigated a total of
24,394 Salmonella isolates, of which 15,843 isolates came
from human sources and 8,551 from non-human sources.
One hundred ninety-nine Salmonella serotypes were
identified (30). When compared with these data, all the
serotypes found in this research were listed by the Mexican
report, with exception of serotype Fresno. No updated
information was found; however, it could be ascertained that
these serotypes have been circulating in Mexico for a long
time, and have been found in humans and non-human
samples. More research in this area needs to be conducted
in Mexico, in order to compare the relationship of specific
strains throughout cattle production systems and their
relation to human isolates.
Escherichia coli O157:H7 prevalence. The prevalence of E. coli O157:H7 on hides and carcasses was lower
than the prevalence of Salmonella. The overall prevalence
of E. coli O157:H7 was as follows (in order of magnitude):
11.7% for hides, 5.2% for IF, 2.7% for FL, 2% for HP,
0.8% for PE, 0.4% for PC, and 0.4% for cooler (P .
0.0001) (Fig. 3).
Hides had the highest occurrence of E. coli O157:H7 in
this slaughter plant (Fig. 3) when compared with the other

J. Food Prot., Vol. 76, No. 5

FIGURE 4. Average Escherichia coli O157:H7 prevalence before

and after the removal of the dairy footbath in hide, PE, PC, and
cooler samples. Preintervention samples included the samplings of
July 2009, December 2009, and April 2010, while postintervention
samples included August and December 2010. Chi-square analysis
indicates that the distribution differed before and after intervention
for hides (P ~ 0.02), but not for PE, PC, and cooler (P , 0.05).

samples. Researchers have reported hides as the major

source for pathogen contamination of beef carcasses during
the harvest process (7, 10, 42) and the main source of E. coli
O157:H7 (15, 22), with prevalences of 11.0 to 85.0% (9, 10,
21, 63, 68, 70). As with Salmonella, a reduction of E. coli
O157:H7 prevalence (P , 0.0001) over time was observed
(Fig. 3), presumably as a result of the modifications and
implementation of food safety procedures at the abattoir. One
of these changes was the removal of the dairy footbath at the
HP area (Fig. 4) and the application of lactic acid to the carcass
surfaces as an intervention for pathogen reduction. When
E. coli O157:H7 fecal shedding results in this study were
compared with other reports, there was a high degree of
variation in prevalence. This variation could be attributed to
different epidemiological factors such as geographical location, seasonality, temperature, humidity, vectors, diet, and
breed on the populations of study at the different locations, as
well as to differences in experimental design and detection
methods (sensitivity, specificity) among other variables.
In the United States, Sargeant et al. (55) showed a
prevalence of E. coli O157:H7 of 52.0% in the HP and 95.9%
in the FL; however, the typical prevalence in cattle was
reported to be between 1.0 and 27.8% (15, 22, 31, 44, 62, 67).
In Argentina, Padola et al. (48) reported a prevalence of E.
coli O157:H7 of 6.8% in cattle. In an Irish abattoir, E. coli
O157:H7 was isolated from 2.4% of fecal samples (41). In
Venezuela, the prevalence in dual purpose cattle (beef and
milk) was 1.94% (46). Similarly, in Mexico, the reported
prevalence of E. coli O157:H7 was lower, 1.25% on cattle
farms (11). These last results were obtained with detection
techniques similar to those used in this study, such as IMS,
which has an increased specificity, and as a consequence,
shows an increase in the reported incidence in cattle (15, 22).
However, no further reports were found with regard to E. coli
O157:H7 prevalence in cattle in Mexico or any Central and/or
South American countries.

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SALMONELLA AND E. COLI O157:H7 PREVALENCE IN MEXICAN BEEF CARCASSES

Despite the E. coli O157:H7 burden, mostly on hides,

a low proportion of contamination occurred during the
slaughter process (0.8% for PE, 0.4% for PC, and 0.4%
after DC). Elder et al. (22) reported a prevalence of 43.0% at
PE, 18% at postevisceration, and 18.0 and 2.0% after 2 h in
the chiller. McEvoy et al. (42) reported an E. coli O157:H7
occurrence of 3.2% on carcass in an Irish abattoir. In
another beef slaughter plant in Ireland, E. coli O157 was
recovered from 3.0% (4 of 132) of carcasses (12). In
Argentina, a survey of 1,622 fecal and carcass samples,
conducted in nine beef exporting abattoirs, reported an
average prevalence of 4.1% in fecal content and 2.6% in
carcasses (40). In Mexico, two studies conducted in beef
slaughter plants found an E. coli O157:H7 prevalence of
66.6% on hot carcass samples collected during inspection
and grading (28) and 2.7% on chilled carcasses in a non-TIF
slaughter plant (65), similar to the results reported in this
research (2.0%). A study in the United States reported a
prevalence that ranged from 46.9% on hides to 16.7% at PE
(10). Other research carried out in Mexico to determine the
prevalence of E. coli O157:H7 in whole beef, whole pork,
ground beef, and ground pork products, collected at four
types of retail channels (supermarkets, city markets, street
vendors, and butcher shops) in different cities of Mexico
(Mexico City, Guadalajara, and Monterrey), and using the
BAX System as a detection method for E. coli O157:H7 did
not detect any positive samples for E. coli O157:H7 (50).
The reduction effect observed in our research might be
because of refrigeration and implementation of microbiological interventions such as lactic acid wash and steam
vacuum after our first sampling period. Regarding E. coli
O157:H7 risk analysis, it was not conducted because of the
low prevalence.
The low E. coli O157:H7 prevalence in cattle found in
this study is consistent with the low incidence of E. coli
O157:H7 human infections in Mexico (47). In addition, to
date, no cases of hemorrhagic colitis and/or hemolytic uremic
syndrome associated with E. coli O157:H7 infection were
reported (47). The reason for the lack of clinical cases in
Mexico is not clear; however, our hypothesis is that the low
prevalence in humans is because of an ineffective surveillance
system or immunity in the population to these pathogens, as
proposed by Navarro et al. (47), but the definitive answer is
uncertain. Because of the lack of scientific information,
researchers cannot state that E. coli O157:H7 is not prevalent
in Mexico, because epidemiological data are unavailable.
When analyzing the overall prevalence by date of
sampling, a variation was observed: 8.6% in July 2009,
1.3% in December 2009, 0.0% in April 2010, 5.0% in
August 2010, and 2.3% in December 2010 (P , 0.0001),
which tended to decrease. At the first sampling date (July
2009), the proportion of samples that tested positive for E.
coli O157:H7 was 8.6%, while on the last day of sampling
(December 2010), the prevalence was 2.3%. The lowest
prevalence was observed at sampling day 3, at 0% (April
2010). To know whether this variation was because of
seasonal effect, the overall prevalence data at the different
locations (FL, IF, HP, PE, PC, and cooler) was compared by
season (spring includes April 2010, summer includes July

793

2009 and August 2010, and winter includes December 2009

and December 2010), with results showing significant
differences (P , 0.05), suggesting that E. coli O157:H7
prevalence could be influenced by season. These results are
similar to previous research carried out in Mexico by
Varela-Hernandez et al. (65) and other researchers, who
reported that E. coli O157:H7 prevalence increased during
the summer and early fall months (15, 22, 42, 64). At other
times of the year, it was present in low levels, with the
potential to drop to zero during the winter months (22, 52).
The overall objective of this study was to determine
the prevalence of Salmonella and E. coli O157:H7 in
a vertically integrated beef production system in Mexico
and to determine any relationship between fecal and hide
prevalence with carcass contamination. The results showed
the presence of E. coli O157:H7 and Salmonella was widely
distributed in all steps of the harvest process, and with high
prevalence in fecal samples, showed that Mexican cattle can
act as a reservoir for these pathogens. Risk analyses showed
the importance of knowing pathogen prevalence at the
preharvest level, and how it could impact the safety of the
final product in a Mexican slaughter plant.
This research can be used to create a pathogen baseline;
however, more research is needed in different regions of
the country to determine seasonality prevalence and other
possible risk factors. This information is important for the
Mexican industry and the government, and can be used to
develop additional criteria and standards in the future
(national and international regulations regarding Salmonella
and E. coli O157:H7) to consider the development and
implementation of pre- and postharvest interventions, and to
evaluate trends in bacterial prevalence, providing safer food
to domestic and international consumers.
ACKNOWLEDGMENT
The authors thank the processing facility in Mexico for their
invaluable help and assistance in conducting this project.

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