Article

Exposure assessment of Salmonella spp. in fresh pork

meat from two abattoirs in Colombia

M Fajardo-Guerrero1, C Rojas-Quintero1, I Chamorro-Tobar2,

C Zambrano2, F Sampedro3 and AK Carrascal-Camacho1

Abstract
Salmonella spp. prevails as the main cause of raw meat foodborne illnesses. Implementation of food safety
management systems such as Hazard Analysis and Critical Control Points in swine abattoirs can help to
mitigate pathogen exposure. The objective of the present study was to evaluate the impact of the HACCP
system in slaughterhouses in Colombia on reducing Salmonella spp. exposure due to the consumption of
fresh pork meat. Two slaughtering plants with a different degree of HACCP implementation were selected and
a quantitative microbiological mapping was built by collecting 820 samples of Salmonella spp. enumeration at
different processing stages. The overall Salmonella spp. mean concentration was 1.15  0.55 log MPN/g, with
no significant differences among plants (P > 0.05). Deficiencies during carcass disinfection and temperature
during distribution of meat cuts from the slaughterhouse lacking of HACCP resulted in a significant increase of
Salmonella spp. prevalence (20–40%) (P < 0.05). Processing stages with the highest pathogen prevalence
were transport (28–32%) and hanging (16–36%). The exposure assessment model estimated a higher degree
of pathogen contamination at the time of consumption in meat cuts from the slaughterhouse without HACCP
(3.36 versus 3.68 log MPN/g) and 10-fold increase in the probability a consumer would acquire a contami-
nated portion (0.011 versus 0.105). Implementation of the HACCP system in swine slaughterhouses repre-
sents tangible Salmonella spp. reduction control and public health protection measures.

Keywords
Microbial mapping, pork meat, Salmonella spp., exposure assessment, Colombia
Date received: 17 April 2019; accepted: 27 June 2019

other animals and surrounding environment in the

INTRODUCTION
Nontyphoidal Salmonella is one of the main causes of
foodborne diseases worldwide (WHO, 2015). In the
United States, Salmonellosis cases represent 9–15% of
the total foodborne illnesses where 7.5% have been
associated with pork meat and related products (Pires
et al., 2010). Salmonella spp. can be found throughout
the entire pork meat production chain. Swine can be
asymptomatic carriers during their productive stage
due to pathogen survival in mesenteric ganglia for up
to 28 weeks, becoming a contamination source for
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farm, transport, and slaughterhouse (Wales et al.,
2011). Swine infected with Salmonella spp. at the pre-
harvest level can disseminate the pathogen to fresh
meat due to cross-contamination at slaughtering and
deboning processes compromising public health as
1
Laboratorio de Microbiologı́a de Alimentos, Grupo de
Biotecnologı́a Ambiental e Industrial, Pontificia Universidad
Javeriana, Bogotá, Colombia
2
Asociación Porkcolombia, Fondo Nacional de la Porcicultura,
Centro de Investigación y Transferencia de Tecnologı́a del
sector Porcı́cola (Ceniporcino), Bogotá, Colombia
3
Environmental Health Sciences Department, School of Public
Health, University of Minnesota, Minneapolis, USA
Corresponding author:
F Sampedro, Environmental Health Sciences Department, School
of Public Health, University of Minnesota, Minneapolis, USA.
Email: fsampedr@umn.edu
Food Science and Technology International 0(0)
a result of poor handling practices and inadequate
cooking at home (O’Connor et al., 2012). Most coun-
tries use HACCP in the slaughterhouse and during
meat deboning as a measure to reduce pathogen preva-
lence and public health burden (Bolton et al., 2002).
Salmonella spp. studies conducted in the pork pro-
duction chain worldwide reveal the pathogen is fre-
quently found in pigs (asymptomatic carrier) or in
fresh meat. Studies conducted in large pork meat pro-
ducing countries, such as China and Vietnam, found
prevalence levels in fresh meat of 28.0 and 39.6%,
respectively (Thai et al., 2012; Yang et al., 2010). In
Latin America, studies conducted in Mexico and
Brazil reported prevalence levels of 17.3% in pork
meat (Miranda et al., 2009) and 93.3% in ground
meat (Borowsky et al., 2007), respectively. In
Colombia, studies performed by Arcos et al. (2013)
and Ayala et al. (2018) reported prevalence estimates
of 2.8% in pork carcasses, 2.2% in slaughterhouse
environmental samples, and 28.2% in mesenteric gang-
lia samples from swine. However, most studies only
report data on Salmonella spp. presence/absence, with
limited information on pathogen concentration levels
throughout the pork production chain. This fact
makes the identification of high-risk processing stages
and development of exposure assessment models extre-
mely difficult (Wheatley et al., 2014).
The objective of this study was to perform a quan-
titative microbiological mapping of Salmonella spp. in
two slaughtering plants with different production and
food safety management systems. The data were used
to identify the high-risk production stages for pathogen
contamination and to build a Salmonella spp. exposure
assessment model in fresh pork meat consumed in
Colombia.
MATERIALS AND METHODS
Abattoirs selection
Two slaughterhouses with a complete pork supply
chain, including farm, slaughterhouse, meat deboning,
Table 1. Productive system characteristics.
Characteristics
Good husbandry practices
Farm size
Transportation time
Slaughterhouse under same operation
HACCP system
Antimicrobial compound used
Transportation to meat deboning facility
HACCP: Hazard Analysis and Critical Control Points.
2
and retail market distribution were selected from the
central region of Colombia. Characteristics of the
productive system at both plants are summarized in
Table 1. Plant A was characterized by the implementa-
tion of HACCP in the slaughterhouse and meat debon-
ing stages and shorter farm to slaughter transportation
times (<2 h). Plant B was characterized by lack of
HACCP implementation in the slaughterhouse and
longer transportation times (up to 24 h).
Sampling design
The Salmonella spp. quantitative profile was conducted
in 17 sampling sites: preharvest (fecal samples), trans-
port (fecal samples from the truck during unloading),
slaughterhouse (carcass samples during hanging, scald-
ing, evisceration, carcass washing, chilling, cold room
storage), meat deboning (carcass and meat cuts), and
retail (meat cuts). Samples were collected on a monthly
basis during five months from April to August. For each
sampling event, five samples were collected from
each site (16 and 17 sites in plant A and B, respectively)
for a total of 820 samples. All the collected samples
were processed at the Food Microbiology Laboratory
of the Pontificia Universidad Javeriana in Bogotá,
Colombia.
Farm samples (50 fecal samples) were collected
by a previously trained veterinarian following the
World Organization for Animal Health (OIE, 2012)
biosecurity measures manual for terrestrial animals.
Five pigs per herd sharing the same farm management
practices were selected and marked for traceability pur-
poses. For each animal, a fecal sample containing 25 g
of feces was collected in sterile bags, properly identified
and kept refrigerated (4  C) until further laboratory
processing. A total of 425 samples were collected at
the slaughterhouse following a nondestructive method
described by Carrascal and Rodrı́guez (2014). A sterile
moistened swab (10 ml of buffered peptoned water) was
used to collect the carcass samples from the vertebral
column, gut, and leg area close to the rectus.
Plant A Plant B
Yes Incomplete
Small (5 farms) Large (1 farm)
2h >3 h
Yes No
Yes No
Citric acid (540–1080 ppm) Lactic acid (500 ppm)
No Yes

Swabs were stored in plastic bags with 15 ml of buffered
peptoned water and kept refrigerated (4  C) until fur-
ther laboratory processing.
Fresh meat samples (200 g) were collected during
meat deboning (45 samples) and retail market (300
samples) with a sterile scalpel for each selected cut
(chop, shoulder, and loin cuts).
Salmonella spp. most probable number (MPN)
quantification method
The quantification of Salmonella spp. was performed
using the MPN method described by Pavic et al.
(2010). Briefly, Salmonella spp. was isolated in chromo-
genic agar (ChromagarTM Salmonella Plus base) and
Hektoen agar (DifcoTM). Colonies showing typical
Salmonella spp. phenotype characteristics (purple colo-
nies in chromogenic agar and black colonies with trans-
lucent halo in Hektoen agar) were cultured in trypticase
soy agar (Scharlau, Spain) and confirmed using
MALDI-TOF (Bruker, Daltonics Inc.) mass spectrom-
etry. MPN values were calculated by a three tube series
table (Pavic et al., 2010). The limit of quantification for
the method used was set at 3 MPN/g.
A unit correction was performed in the swab samples
(ml to cm2) to account for the sample area (400 cm2) by
using equation (1) and in the fecal (25 g) and meat cut
(200 g) samples (ml to g) by using equation (2) (Mion
et al., 2016)
MPN MPN of the suspension  sampled area
2
¼ ml
cm diluent volume
ð1Þ
MPN
MPN ml of the suspension  sample weight
¼
g diluent volume
ð2Þ
where MPN is the most probable number obtained
by the method, area is the surface analyzed
(400 cm2), sample weight is the amount analyzed
(25 and 200 g), and diluent volume is the sponge
volume (25 ml).
Statistical analysis
Salmonella spp. levels reported for each sample with a
value of <3 MPN/g or <5 MPN/cm2 were expressed as
a categorical ‘‘negative’’ variable. In contrast, when the
value was >3 MPN/g or cm2 results were reported as
‘‘positive.’’ To determine significant differences between
plant A and B pathogen counts, a Tukey’s test was
performed with an a ¼ 0.05 value and a confidence
interval of 95%.
Fajardo-Guerrero et al.
Probabilistic exposure assessment model
Enumeration data (log MPN/g) and Salmonella spp.
prevalence (percentage of positive samples) from the
microbiological profile at the slaughterhouses were
used to build a probabilistic exposure assessment
model to estimate the Salmonella spp. concentration
in fresh meat at the time of consumption and the prob-
ability that a consumer in Colombia would acquire a
contaminated cut. The model was built in @Risk 7.5.2
(Palisade, Inc.) software characterizing each of the
model input variables with probability distributions to
account for the associated variability and uncertainty
(Table 2).
A Monte Carlo simulation with Latin hypercube
sampling method (10,000 iterations) was used to gener-
ate pseudo random numbers from all input probability
distributions defined in the model (i.e. one iteration).
The final probability density function of the output
(mean, 95% confidence interval) accurately accounted
for all possible scenarios for the given set of parameters
defined in the exposure model.
RESULTS AND DISCUSSION
Salmonella spp. cross-contamination can occur at dif-
ferent processing stages during slaughtering or meat
deboning. Conducting a microbiological mapping
throughout the entire production chain is crucial to
identify stages with the highest probability of contam-
ination (De Busser et al., 2013). Salmonella spp. enu-
meration levels during the five sampling events in plant
A and B are shown in Figure 1. Progressive reduction in
the mean pathogen prevalence and enumeration levels
was observed for plant A for intermediate stages (dis-
infection) and latter processing stages (below the detec-
tion limit of Salmonella spp. during deboning and retail
sale). Such behavior was not observed for plant B
(without HACCP) where there was an increase on the
mean Salmonella spp. prevalence and enumeration
levels throughout the production chain, including dis-
tribution and retail sale.
A significant correlation has been observed between
Salmonella spp. prevalence at the farm level by the pres-
ence of infected pigs and contamination of fresh meat
(Andres and Davies, 2015). No infected animals were
observed in plant A (30 sampled pigs), whereas 28% of
sampled animals from plant B (25 sampled pigs)
showed Salmonella spp. infection with mean levels of
1.16  0.56 log MPN/g. Final prevalence levels in fresh
meat cuts from plant B (4–40%) were significantly
higher than levels found in plant A (pathogen below
the detection limit in all meat cuts) (P < 0.05), suggest-
ing a significant correlation. Andres and Davies (2015)
observed that farm biosecurity measures (animal
replacement, cleaning and disinfection, feed and water
3
Food Science and Technology International 0(0)

Table 2. Exposure assessment model inputs of Salmonella spp. in pork meat.

Input Value Reference

Overall prevalence (%) Plant A: Beta (2þ1,1752þ1) Present study

Plant B: Beta (27þ1,17527þ1)
Final concentration (log CFU/g)a Plant A: Normal (1.07, 0.28) Present study
Plant B: Normal (1.23, 0.47)
pffiffiffiffi
Salmonella growth during  ¼ 0:0243  T  0:0825 Data from Velugoti et al. (2011)
shelf-life (log CFU/g) Shelf-life: 4–10 C, 3 days using COMBASE
Uniform (0, 1.28)
Annual per capita consumption 46 portions Data provided by Porkcolombia
(Economic Division)
Percentage of pork meat 67% Data provided by Porkcolombia
consumers in Colombia (Economic Division)
Portion size (g) Triangular (90,100,125) Data provided by Porkcolombia
(Economic Division)
Percent surface with respect 20–30% Present study
to the total cut volumea
CFU: Colony Forming Units.
a
All cuts combined.

below the detection limit level after the disinfection

120 stage. Prevalence was maintained between 4% and
100
below the detection limit in the rest of the processing
stages and the pathogen was only detected in two out of
80
seven meat cuts evaluated. Pathogen prevalence levels
60 in plant B were also reduced after scalding (12% reduc-
MPN/g – cm2

tion). However, an increase was observed after eviscer-

40
ation and carcass washing stages (8% increase each)
20 and no reduction effect was measured after disinfection.
0
A complete pathogen reduction was observed during
chilling; however, at latter stages (unloading and cold
–20
room) prevalence increased and was maintained at
–40 20%. All samples obtained from meat cuts in plant B
rm ing ing ing ion ng on ing ion m at op ., oin let. m. in. showed Salmonella spp. presence with prevalence
Fa load ang cald erat ashi fecti Chill ortat d roout me Ch Arm L Cut Ar Lo
Un H S isc W isin p ol c
Ev D ns C ace
Tra
Su
rf values between 4 and 40%.
Company A
Company B
Stool and meat cut samples: g Lack of HACCP implementation in plant B could
Carcass samples: cm2
have caused an increase in prevalence levels during
slaughterhouse processing stages, suggesting cross-con-
Figure 1. Mean Salmonella spp. enumeration level from tamination between carcasses or utensils, lack of ade-
five sampling events in plants A and B.
quate cleaning and disinfection of transportation
vehicles (live animals and carcasses), and inadequate
supplements, among others) aimed at reducing carcass disinfection process (antimicrobial concentra-
Salmonella spp. prevalence in animal carriers show a tion and contact time). Likewise, abuse temperatures
reduction effect on the pathogen levels in the final prod- (average of 10  C, data not shown) were observed
uct. Lack of good husbandry practices and a greater during storage and distribution of meat cuts. All the
farm size could explain the higher pathogen prevalence processing failures observed in plant B would explain
observed in plant B (Table 1). the pathogen increase measured throughout the study.
Salmonella spp. prevalence during transportation Data observed in the present study are in agreement
and unloading was 28–36 and 16–32% for plants A with systematic reviews on Salmonella spp. mapping in
and B, respectively. Pathogen prevalence levels in the pork meat chain described by O’Connor et al.
plant A decreased steadily throughout the process (2012) and Wheatley et al. (2014), where they found
with a 28% decrease after scalding and 4% after each scalding had a significant reduction effect on
stage of evisceration and carcass washing, reaching Salmonella spp. prevalence due to the temperatures

4

employed (60–65  C). Additionally, the chilling process
could result in an additional Salmonella spp. reduction
given the effect low temperatures have on stressed cells
(Ferrasso et al., 2017).
Salmonella spp. mean concentration level at the
slaughterhouse was maintained near to 1.0 log MPN/
cm2 or g (1.07  0.28 in plant A and 1.23  0.47 in plant
B) and no significant differences were observed between
plants (P > 0.05). Disinfection process in plant A was
able to reduce below the detection limit of the initial
microbial load (1.04 log MPN/cm2 reduction), whereas
for plant B an increase in concentration was detected
after the carcass washing reaching a concentration of
1.19  0.20 log MPN/g and no effect was observed after
disinfection. Evisceration is frequently reported as the
highest source of contamination in pig carcasses
during slaughter (Young et al., 2016). Present study
observed low Salmonella spp. levels after evisceration
(1.04  0.27 and 1.10  0.22 log MPN/cm2 in plant A
and B, respectively), suggesting adequate management
(bunging, double knife use, personnel training) avoid-
ing fecal contamination from intestine rupture.
Cold chain breakdown during transport in plant B
resulted in 1.70  0.57 and 1.50  0.74 log MPN/g
counts for shoulder and loin cuts, respectively. Data
from microbiological mapping reports in Brazil
describe higher counts in comparison with the present
study in ground meat (2.38 log MPN/g) and meat prod-
ucts (1.96 log MPN/g) (Borowsky et al., 2007; Ristori
et al., 2017). In contrast, reports by Prendergast et al.
(2009) in meat cuts from the Irish retail market showed
lower counts (0.23 log MPN/g). Differences in storage
temperatures among countries could explain these
differences.
The high-risk stages for Salmonella spp. contamin-
ation were identified during transportation (36% preva-
lence in both plants) and hanging (28%) in plant A.
Hernández et al. (2013) also identified transportation
(23% prevalence in samples collected from trucks)
and hanging (36% prevalence) as the stages with the
highest prevalence. An increase in Salmonella spp.
levels during transportation could be due to dissemin-
ation of bacteria in the animal feces and inadequate
truck washing (Ayala et al., 2018; Wales et al., 2011).
Increased bacteria excretion during transport is asso-
ciated with elevated stress levels in swine due to inad-
equate animal handling during loading and unloading,
high dense population, long transportation times from
the farm to the abattoir, and adverse climate conditions
(Hurd et al., 2002). These authors observed an increase
in Salmonella spp. prevalence greater than 7-fold
(5.3–39.9%) between the levels observed at the farm
and after transport. In the present study, a 4% increase
in prevalence was observed between the farm and
slaughterhouse in plant B, possibly caused by the long
Fajardo-Guerrero et al.
transportation time and other plausible causes previ-
ously mentioned. Increase in prevalence between
transport and animal hanging stages could be due to
fecal–oral contamination or skin contamination as a
consequence of high animal density during lairage
(company A has small holding pens) that can facilitate
pathogen dissemination (Boughton et al., 2007).
Probabilistic exposure assessment model
Table 2 shows the Salmonella spp. exposure assessment
model input variables in fresh pork meat produced in
two abattoirs in Colombia. The mean Salmonella spp.
prevalence of meat cuts was characterized by a beta
distribution. Salmonella spp. growth rate values
(m, log CFU/g/h) at 4–10  C were obtained from
COMBASE tool (www.combase.cc) (Baranyi and
Tamplin, 2004) and a study by Velugoti et al. (2011)
on Salmonella spp. growth in ground pork meat.
Salmonella spp. growth during the shelf-life (4–10  C
for three days) was estimated through a linear regres-
sion of the growth rate values at different temperatures
(Table 2). It was assumed that microbial contamination
in meat occurred on the surface, accounting for
20–30% of the total cut volume (2 mm by experimental
estimation in the present study).
Table 3 presents the model outputs after the Monte
Carlo simulation. No significant differences were
observed in the mean contamination level estimated
by the model (3.68 versus 3.36 log MPN/g) at the
time of consumption (P > 0.05). Giovannini et al.
(2004) reported low Salmonella spp. levels (1.39 to
0.52 log MPN/g) in half of the samples and higher
levels in the other half (0.44 to 2.04 log MPN/g) in
fresh pork sausages sampled in Italy. In the present
study, the probability of acquiring a contaminated por-
tion from plant B was 10 times higher (10.5%) in com-
parison with plant A (1.1%) due to the higher mean
prevalence of meat cuts from plant B. The average
number of contaminated portions acquired by an aver-
age consumer in a year was estimated to be greater than
seven portions if the meat would come from plant B
and less than a portion if processed in plant A
(Table 3). Various authors have estimated the risk of
becoming ill from the consumption of contaminated
pork meat with Salmonella spp. Dang et al. (2017)
showed in a given year a Salmonella spp. prevalence
of 44.4% in fresh pork meat from wet markets in
Vietnam and a probability of illness from consumption
of boiled pork of 17.7% (0.89–45.96%, 95% CI).
Another study in pork meat from Hanoi’s urban
areas found a probability of illness of 9.5%
(0.4–30%, 95% CI) (Toan et al., 2013). The risk of
illness from the consumption of fresh pork meat will
greatly depend on the food handling practices at home
5
Food Science and Technology International 0(0)
Table 3. Exposure assessment model outputs of Salmonella spp. in pork meat.
Output Formula
Salmonella spp. final 10^final concentration  portion
concentration (log MPN) size  % cut surface
Probability of acquiring a Prevalence  consumer proportion
contaminated portion
Number of contaminated portions Total contaminated portions/
acquired by an average consumer Number of consumers
MPN: most probable number.
a
mean and 95% CI.
to avoid cross-contamination or inadequate cooking.
Inadequate use and disinfection of cutting boards and
utensils, and transfer of contamination to other fresh
products, such as fruits and vegetables have been
observed as the main contamination routes. Gonzales-
Barron et al. (2012) found that reducing the cold stor-
age by approximately 8 h and cooking for an additional
half minute could reduce the current risk level by
50% in fresh pork sausages. For the present study,
the effect of cooking practices on the risk of illness
would be insignificant, since it was assumed that pork
meat cuts would be sterile in the inside.
CONCLUSIONS
Data obtained from this study reflect the impact of
HACCP implementation on Salmonella spp. prevalence
and enumeration levels along the pork meat production
chain in two abattoirs in Colombia. Deficiencies were
observed in the carcass washing and disinfection pro-
cesses and cold chain distribution of meat cuts for the
plant lacking of HACCP, resulting in a significant
increase in Salmonella spp. presence. The higher
Salmonella prevalence in the meat cuts significantly
increased the probability a consumer would acquire a
contaminated portion and the risk of illness. A hurdle
approach combining farm interventions to reduce the
number of infected animals with HACCP at the slaugh-
terhouse, adequate cold chain during distribution, and
educating the consumer in adequate food handling at
the home are the most efficient ways of controlling the
pathogen in fresh pork meat.
ACKNOWLEDGEMENTS
The authors manifest their gratitude to the two companies for
granting access to sample collection. Additionally, they thank
Jessed Gutiérrez and Jackeline Martı́n (Porkcolombia,
DVMs) for helping with the sample collection.
DECLARATION OF CONFLICTING INTERESTS
The authors declared no potential conflicts of interest with
respect to the research, authorship, and/or publication of this
article.
6
Valuea
Plant A: 3.36 (2.25–4.00)
Plant B: 3.68 (2.11–4.44)
Plant A: 0.011 (0.0024–0.0271)
Plant B: 0.105 (0.0726–0.144)
Plant A: 0.77 (0.16–1.84)
Plant B: 7.21 (4.94–9.82)
FUNDING
The author(s) disclosed receipt of the following financial sup-
port for the research, authorship and/or publication of this
article: The authors thank Porkcolombia (National pig indus-
try fund) for financing this project No. 002-17 and for finan-
cing the English translation.
ORCID ID
F Sampedro https://orcid.org/0000-0003-1155-2751
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