PLOS ONE

RESEARCH ARTICLE

Bacterial contamination of chicken meat in

slaughterhouses and the associated risk
factors: A nationwide study in Thailand
Kunnanut Klaharn1, Duangporn Pichpol1,2,3, Tongkorn Meeyam ID1,2,3,
Thanida Harintharanon4, Patpong Lohaanukul4, Veerasak Punyapornwithaya ID2,3*
1 Faculty of Veterinary Medicine, Department of Veterinary Bioscience, Chiang Mai University, Chiang Mai,
Thailand, 2 Faculty of Veterinary Medicine, Veterinary Public Health Research Group, Chiang Mai University,
Chiang Mai, Thailand, 3 Faculty of Veterinary Medicine, Veterinary Public Health and Food Safety Centre for
Asia Pacific (VPHCAP), Chiang Mai University, Chiang Mai, Thailand, 4 Department of Livestock
a1111111111 Development, Bangkok, Thailand
a1111111111
a1111111111 * [email protected]
a1111111111
a1111111111
Abstract
Slaughterhouses are a key source of bacterial contamination in poultry meat and products,
which is a major health and economic concern for several public authorities. This study
OPEN ACCESS
aimed to quantify the non-compliance of bacterial contamination on chicken meat sampled
Citation: Klaharn K, Pichpol D, Meeyam T,
from slaughterhouses and identify risk factors associated with the contamination. A ques-
Harintharanon T, Lohaanukul P, Punyapornwithaya
V (2022) Bacterial contamination of chicken meat tionnaire survey of 569 chicken slaughterhouses was undertaken and 1,707 meat samples
in slaughterhouses and the associated risk factors: were collected to determine the level of bacterial contamination. The proportion of the non-
A nationwide study in Thailand. PLoS ONE 17(6):
compliance associated with aerobic plate count [APC] (24.6%), Staphylococcus aureus
e0269416. https://doi.org/10.1371/journal.
pone.0269416 (6.3%), Enterococcus spp. (24.7%), coliforms (13.5%), Escherichia coli (33.3%), and Sal-
monella spp. (33.4%) based on the livestock authorities’ criteria was determined. Our results
Editor: Frédérique Pasquali, University of Bologna,
ITALY highlighted that the scalding process without scalding water temperature control or improper
scalding increased the risk of APC (odds ratio, OR = 4.84, 95% CI: 2.72–8.61), S. aureus
Received: November 3, 2021
(OR = 2.68, 95% CI: 1.29–5.55), Enterococcus spp. (OR = 3.38, 95% CI: 2.01–5.69), coli-
Accepted: May 20, 2022
forms (OR = 3.01, 95% CI: 1.47–6.15), and E. coli (OR = 2.69, 95% CI: 1.58–4.56) contami-
Published: June 8, 2022 nation on meat samples. Meat from eviscerated carcasses was more likely to be non-
Copyright: © 2022 Klaharn et al. This is an open compliance due to contamination by E. coli (OR = 1.96, 95% CI: 1.14–3.38). Furthermore,
access article distributed under the terms of the open or semi-closed system slaughterhouses (OR = 1.79, 95% CI: 1.23–2.60) and lack of
Creative Commons Attribution License, which
equipment for specific slaughtering areas (OR = 1.65, 95% CI: 1.04–2.61) increased the
permits unrestricted use, distribution, and
reproduction in any medium, provided the original likelihood of Salmonella spp. occurrence. This is the first study of factors influencing the
author and source are credited. non-compliance of meat samples across Thailand. Authorities can use the study findings to
Data Availability Statement: The datasets enhance food safety strategies at the national level.
generated for this study will not be made publicly
available as the data has been provided by the
authority of the Department of Livestock
Development, Ministry of Agriculture and
Cooperatives, Thailand. Requests to access these
datasets should be directed to [email protected]. Introduction
Funding: This work was partially funded by Chiang Poultry meat production and consumption have substantially increased worldwide and are
Mai University. The funders had no role in study expected to rise in upcoming decades [1,2]. Interestingly, poultry meat consumption is the

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 1 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

design, data collection and analysis, decision to largest meat sector and has approximately doubled from 67 million tons in 2000 to 131 million
publish, or preparation of the manuscript. tons in 2020 [3]. The key factors that make poultry meat preferable are relative affordability
Competing interests: The authors have declared and economic costs in comparison to other meats, absence of religious or cultural restrictions,
that no competing interests exist. and dietary as well as nutritional properties [4].
Poultry meat is considered a potential vehicle for foodborne pathogens making it a major
public health concern worldwide [5,6]. This has a high global impact on human health and
socioeconomic burden [7–9]. Thailand reported 87,093 food poisoning cases with one death
in the year 2020 [10]. Besides foodborne diseases, spoilage bacteria may decrease the shelf life
leading to product losses in the poultry meat production industry causing substantial eco-
nomic repercussions [11].
The bacterial contamination has been demonstrated to occur along the production chain
from farm to fork including primary production at farm level along with live-poultry transpor-
tation, slaughtering processes, slaughterhouse environment, and in storage until it reaches
consumer [12,13]. Slaughtering processes in slaughterhouses play an important role in food-
borne microbial transmission. Contamination has been revealed to occur mostly during the
slaughtering processes [14,15], with plucking, evisceration, and chilling being the most crucial
processing steps [16–18]. Therefore, an improvement in hygienic practices across the food
chain is necessary to reduce the risk of the foodborne burden from poultry meat products.
In Thailand, the Department of Livestock Development (DLD) implements a monitoring
program to monitor levels of aerobic plate count (APC), Staphylococcus aureus, Enterococcus
spp., coliforms, Escherichia coli, and Salmonella spp. in meat at slaughterhouses [19]. Accord-
ing to the monitoring program, despite evidence of high levels of bacterial contamination in
meat samples [20], studies into potential causes of bacterial contamination during the slaugh-
tering process in Thailand are very limited. Furthermore, because none of the studies was con-
ducted on a national level, there is a lack of national baseline data, which is essential for
formulating a national strategic plan to improve chicken meat quality across the country.
Thus, this study aimed to determine the bacterial contamination status of the meat sampled
from slaughterhouses and to identify the potential risk factors associated with non-compliance
due to such contamination under the nationwide government-mandated quality control
program.

Material and methods

Study area
The study was conducted in 77 provinces across Thailand during 2019 and 2020 in chicken
slaughterhouses (n = 569) under the authority of the DLD. Slaughterhouses that produce meat
only for domestic consumption were included in this study. The number of chicken slaughter-
houses in each province is depicted in Fig 1.

Sample size calculation

The government program aimed to include all certified slaughterhouses in Thailand (n = 569),
thus the number of slaughterhouses was influenced by this objective. Therefore, the sample
size calculation was mainly considered on how many meat samples should be taken from each
slaughterhouse. To perform this calculation, we used the online Power Analysis application
designed to determine the sample size for a multilevel logistic regression analysis that corre-
sponds to the study with a multilevel structure [21].
We calculated the power of the test using the following parameters: the number of meat
samples taken from each slaughterhouse (the first level; n = 3), the number of slaughterhouses
(the second level, n = 569), and the number of fixed-effect factors (n = 3). Since our factors

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 2 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

Fig 1. Map of Thailand showing the number of certified chicken slaughterhouses in each province. The map
shown in Fig 1 was created using QGIS (version 2.18.28), QGIS Geographic Information System, and Open-Source
Geospatial Foundation Project, and all content is licensed under Creative Commons Attribution-Share Alike 3.0
license (CC BY-SA), available at (http://qgis.osgeo.org). In addition, geographical materials used for creating the map
(e.g., shape file) were supported by Chiang Mai University.
https://doi.org/10.1371/journal.pone.0269416.g001

were categorical variables, we specified the binomial distribution for them. Computer simula-
tions (n = 100 times) were performed to estimate the power of the test for multilevel logistic
regression. The results from the simulation showed that the statistical power was greater than
80%, which is generally accepted for statistical analysis [22].

Meat sampling, microbiological analysis, and questionnaire survey

Meat sampling. Trained livestock authorities obtained three meat samples from each
chicken slaughterhouse and submitted them (n = 1,707) to the DLD laboratory centers. Micro-
biological analysis was facilitated by the Bureau of Quality Control of Livestock Products
(BQCLP) and Regional Veterinary Research and Development Centers. Meat samples from
slaughterhouses were taken in accordance with the national monitoring program. The detail
of meat sampling was previously described [23,24]. Briefly, each meat sample was randomly
selected from an individual carcass by the authorities The samples were kept in an icebox to

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 3 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

keep the temperature below 4˚C. According to the DLD official guidelines, all samples were
transported to DLD laboratory centers for microbiological analysis [23].
Microbiological analysis and regulatory criteria. The meat samples were analyzed
according to the procedure given in FDA BAM Online, 2001 (Chapter 3) for aerobic plate
count (APC); ISO 6888–1: 1999 for Staphylococcus aureus; Nordic Committee on Food Analy-
sis, No. 68 5th Edition (2011) for Enterococcus spp.; FDA BAM Online, 2013 (Chapter 4) for
coliforms and Escherichia coli; and ISO 6579–1: 2017 for Salmonella spp. [25] (S1 Table).
Microbiological criteria and the procedure used in this study were derived from the manual of
Microbiological Standard for Livestock Products [26]. The criteria for determining whether
meat samples comply with the standard value [27] are provided in S1 Table.
Questionnaire survey. Provincial livestock authorities visited all slaughterhouses during
2019–2020 and interviewed the slaughterhouse managers using a structured questionnaire to
obtain data concerning slaughterhouse practices and facilities. Face-to-face interviews involv-
ing authorities and slaughterhouse supervisors have been used to collect data for the question-
naire. All data were reported to the Bureau of Livestock Standards and Certification (BLSC),
which is officially in charge of monitoring livestock products at slaughterhouses across
Thailand.

Statistical analyses
Data and descriptive statistics. The outcome variable was the compliant status of the
meat samples based on the DLD standard criteria (S1 Table) and was defined as a dichotomous
variable. Factors derived from the questionnaire used for further analysis are listed in S2 Table.
Based on the DLD standard criteria, the contamination status of the meat sample was classi-
fied as either compliance or non-compliance (0 = compliance and 1 = non-compliance). The
non-compliance of the meat samples for APC, S. aureus, Enterococcus spp., coliforms, E. coli,
and Salmonella spp. contamination levels was evaluated. The proportion of the non-compli-
ance and its 95% confidence interval (95% CI) was calculated based on Wald estimation [28].
Logistic regression analysis. Given the data structure, a multilevel mixed-effects logistic
regression model was used to determine the association between slaughterhouse process (fac-
tor) and non-compliance of meat samples for each contamination criteria using R statistical
software version 3.6.2 [29] with the “lme4” [30] and “dplyr” [31]. The analysis consisted of uni-
variable and multivariable mixed-effects logistic regression analysis. For the univariable analy-
sis, the association between each factor and the non-compliance was tested and factors with
p < 0.2 from the univariable analysis were selected for the multivariable analysis.
The mixed-effect logistic regression accounted for the multilevel structure [32] is written as
follow:
� �
Pi
ln ¼ b0 þ b1 X1 þ � � � þ bk Xk þ ujðiÞ
1 Pi

where Pi is the probability of non-compliant status of the ith meat sample, β0 is the model inter-
cept, Xk is the set of fixed-effects factors, and βk is the estimated coefficient according to the
factors, uj(i) is the random-effect of the jth slaughterhouse containing the ith meat sample and it
was assumed that ujðiÞ � NIDð0; s2u Þ.
Through model selection processes, a backward elimination technique was employed to
determine the final model. Also, multicollinearity among factors was evaluated during the
model selection process by examining variance inflation factors. Additionally, the logistic
regression assumption of a linear relationship between factors and the logit of the outcome
was evaluated by examining the scatter plot between each factor and the logit values.

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 4 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

Moreover, a goodness of fit for each final model was tested using the Hosmer-Lemeshow test
[33]. For each factor, the odds ratio and its 95% CI were calculated. The level of statistical sig-
nificance was set as α = 0.05.

Ethical statement
This study did not require ethical approval for animal research as live animals were not
involved. As authorized staff from government sectors were involved in meat sampling, micro-
biological analysis and interview as part of the national survey organized by DLD, Thailand;
no additional permission was required.

Results
Slaughterhouse characteristics
The characteristics of the slaughterhouses are shown in Table 1. In terms of slaughterhouse
structure, nearly half of all slaughterhouses were closed-system buildings. Approximately
91.4% of slaughterhouses had separated slaughtering lines for clean and unclean areas. About
80% of the slaughterhouses have dedicated workers for a specific area and these workers do
not have rotational duties at different areas within slaughterhouses. Likewise, the equipment is
also not mixed within the specific areas and is strictly kept designated to a particular area.
Before entering the slaughtering line, 77% of workers washed their hands and 76.5% wore pro-
tective clothing and boots. In less than half of the slaughterhouses, the slaughtering knife and
cutting knife were sanitized and scalding water temperature in the scalding process was con-
trolled. Only 20.9% of them had hanging equipment to prevent cross-contamination between
chicken carcasses and the slaughtering floor. Even though approximately 50% of slaughter-
houses did not use tap water, only 21.4% of slaughterhouses had water treatment systems in
place prior to using water for the slaughtering processes. According to product characteristics,
68% of chicken carcasses processed in slaughterhouses were eviscerated.

Table 1. The characteristics of the chicken slaughterhouses based on the questionnaire survey.
Characteristics n (N = 569) %
Slaughterhouse management practices
Water source; use of tap water in slaughterhouses 271 47.63
Slaughterhouses have the system to treat water used during 122 21.44
slaughtering process
Separating workers for clean and unclean area 428 75.22
Separating equipment for clean and unclean area 458 80.49
Hand cleaning practice before entering the slaughtering area 438 76.98
Changing protective clothes and boots before entering 435 76.45
the slaughtering area
Use of hanging equipment to prevent carcasses contamination 119 20.91
Slaughtering knives are sanitized before use 277 48.68
Cutting knives are sanitized before use 271 47.63
Having temperature control for scalding water 233 40.95
Slaughterhouse designated and facilities
Close-system building 250 43.94
Separating slaughtering line for clean and unclean area 520 91.39
Product characteristics
Eviscerated carcasses as the final products 387 68.01
https://doi.org/10.1371/journal.pone.0269416.t001

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 5 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

Fig 2. Proportion and 95% confidence interval (95% CI) of non-compliant meat samples according to the
Department of Livestock Development criteria.
https://doi.org/10.1371/journal.pone.0269416.g002

Bacterial contamination in chicken meat from slaughterhouses

The proportion of non-compliant meat samples according to DLD criteria for aerobic plate
count (APC), Staphylococcus aureus, Enterococcus spp., coliforms, Escherichia coli, and Salmo-
nella spp. are shown in Fig 2. The results indicated Salmonella spp. contamination was the
highest in the proportion of non-compliant meat samples (33.4%), followed by E. coli (33.3%)
and Enterococcus spp. (24.7%), whereas the lowest proportion of non-compliant meat samples
was S. aureus contamination (6.3%).

Risk factors
The results from the multivariable logistic regression highlighted that improper scalding pro-
cess increased the risk for APC (Table 2), S. aureus (Table 3), Enterococcus spp. (Table 4),

Table 2. Factors associated with the aerobic plate count non-compliance of meat samples based on the univariable and multivariable mixed-effects logistic
regression.
Factors Categories Univariable analysis Multivariable analysis
Odds ratio P-Value Adjusted OR� (95% CI) P-Value
(95% CI)
1 Use of hanging equipment to prevent carcasses contamination Yes -ref-
No 2.68 (1.31–5.48) 0.01 -
2 Slaughtering knives are sanitized before use Yes -ref-
No 1.91 (0.73–5.01) 0.18 -
3 Having temperature control for scalding water Yes -ref-
No 4.84 (2.72–8.61) <0.001 4.84 (2.72–8.61) <0.001
4 Eviscerated carcasses No -ref-
Yes 1.32 (1.04–1.69) 0.02 -
�
OR = odds ratio, -ref- = reference class.

https://doi.org/10.1371/journal.pone.0269416.t002

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 6 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

Table 3. Factors associated with the Staphylococcus aureus non-compliance of meat samples based on the univariable and multivariable mixed-effects logistic
regression.
Factors Categories Univariable analysis Multivariable analysis
Odds ratio P-Value Adjusted OR� P-Value
(95% CI) (95% CI)
1 Separating equipment for clean and unclean area Yes -ref-
No 1.57 (0.63–2.43) 0.06 -
2 Slaughtering knives are sanitized before use Yes -ref-
No 1.51 (1.01–2.25) 0.04 -
3 Cutting knives are sanitized before use Yes -ref-
No 1.56 (1.05–2.36) 0.03 -
4 Having temperature control for scalding water Yes -ref-
No 2.68 (1.29–5.55) 0.008 2.68 (1.29–5.55) 0.008
5 Separating slaughtering line for clean and unclean area Yes -ref-
No 2.48 (0.49–12.67) 0.15 -
�
OR = odds ratio, -ref- = reference class.

https://doi.org/10.1371/journal.pone.0269416.t003

coliforms (Table 5), and E. coli (Table 6) contamination in meat samples more than two-fold.
Additionally, eviscerated carcasses were also associated with non-compliant meat samples for
E. coli. Moreover, the factors associated with the non-compliant meat samples according to the
contamination of Salmonella spp. are shown in Table 7.

Discussion
This study provided nationwide data on bacterial contamination of chicken meat from all
approved slaughterhouses in Thailand. The major findings were the high non-compliance for
Salmonella spp. and Escherichia coli contamination in meat samples. Furthermore, this study
showed that the non-compliance of meat samples due to bacterial contamination based on reg-
ulatory standard criteria was related to slaughterhouse structure, hygienic practices, and prod-
uct characteristics.
The proportion of non-compliant status due to aerobic plate count (APC), S. aureus,
Enterococcus spp., coliforms, E. coli, and Salmonella spp. determined in this study present a
national baseline. The 95% CI of the proportion calculated herein also provides the lower and
upper bound for statistical estimation that accounts for sampling variation offering a border of
interpretation. Overall, compared to other reports in Thailand, our bacterial contamination

Table 4. Factors associated with the Enterococcus spp. non-compliance of meat samples based on the univariable and multivariable mixed-effects logistic
regression.
Factors Categories Univariable analysis Multivariable analysis
Odds ratio P-Value Adjusted OR� P-Value
(95% CI) (95% CI)
1 Separating workers for clean and unclean area Yes -ref-
No 1.58 (0.90–2.78) 0.11 -
2 Use of hanging equipment to prevent carcasses contamination Yes -ref-
No 2.10 (1.10–4.02) 0.03 -
3 Having temperature control for scalding water Yes -ref-
No 3.38 (2.01–5.69) < 0.001 3.38 (2.01–5.69) < 0.001
4 Eviscerated carcasses No -ref-
Yes 1.39(1.09–1.79) 0.01 -
�
OR = odds ratio, -ref- = reference class.

https://doi.org/10.1371/journal.pone.0269416.t004

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 7 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

Table 5. Factors associated with the coliforms non-compliance of meat samples based on the univariable and multivariable mixed-effects logistic regression.
Factors Categories Univariable analysis Multivariable analysis
Odds ratio P-Value Adjusted OR� P-Value
(95% CI) (95% CI)
1 Slaughterhouses have the system to treat water used during slaughtering process Yes -ref-
No 1.73 (1.19–2.61) 0.01 -
2 Separating workers for clean and unclean area Yes -ref-
No 2.36 (1.11–5.05) 0.02 -
3 Separating equipment for clean and unclean area Yes -ref-
No 1.72 (1.26–2.36) 0.01 -
4 Use of hanging equipment to prevent carcasses contamination Yes -ref-
No 1.91 (0.75–4.85) 0.17 -
5 Slaughtering knives are sanitized before use Yes -ref-
No 1.98 (1.48–2.65) 0.01 -
6 Having temperature control for scalding water Yes -ref-
No 3.01 (1.47–6.15) 0.003 3.01 (1.47–6.15) 0.003
7 Eviscerated carcasses No -ref-
Yes 1.89 (0.89–4.00) 0.09 -
�
OR = odds ratio, -ref- = reference class.

https://doi.org/10.1371/journal.pone.0269416.t005

results are in agreement with the previous study conducted at the provincial and regional levels
that focused on meat contamination in slaughterhouses [34] but differed from other studies
[20,35,36]. The variability may be a result of differences in study designs, year of the study con-
ducted, and sampling variations.
In comparison with reports from other countries, diverse findings were found according to
their safety limitations. For APC as a hygienic indicator [37], the proportion of non-compliant
meat samples in this study was lower than the finding reported in Moroccan slaughterhouses
(29.2%) but higher than those of Indian slaughterhouses (14%) [38,39]. Generally, S. aureus
contamination usually reflects as a consequence of inadequate control measures and poor

Table 6. Factors associated with the Escherichia coli non-compliance of meat samples based on the univariable and multivariable mixed-effects logistic regression.
Factors Categories Univariable analysis Multivariable analysis
Odds ratio P-Value Adjusted OR� P-Value
(95% CI) (95% CI)
1 Slaughterhouses have the system to treat water used during slaughtering process Yes -ref-
No 1.76 (0.93–3.35) 0.08 -
2 Separating workers for clean and unclean area Yes -ref-
No 2.36 (1.32–4.22) 0.01 -
3 Use of hanging equipment to prevent carcasses contamination Yes -ref-
No 2.29 (1.21–4.35) 0.02 -
4 Slaughtering knives are sanitized before use Yes -ref-
No 1.67 (0.97–2.90) 0.06 -
5 Cutting knives are sanitized before use Yes -ref-
No 1.62 (0.93–2.82) 0.09 -
6 Having temperature control for scalding water Yes -ref-
No 2.58 (1.52–4.38) <0.001 2.69 (1.58–4.56) <0.001
7 Building system Close -ref-
Open or semi-close 1.99 (1.20–3.29) 0.01 -
8 Eviscerated carcasses No -ref-
Yes 1.85 (1.07–3.20) 0.01 1.96 (1.14–3.38) 0.02
�
OR = odds ratio, -ref- = reference class.

https://doi.org/10.1371/journal.pone.0269416.t006

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 8 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

Table 7. Factors associated with the Salmonella spp. non-compliance of meat samples based on the univariable and multivariable mixed-effects logistic regression.
Factors Categories Univariable analysis Multivariable analysis
Odds ratio P-Value Adjusted OR� P-Value
(95% CI) (95% CI)
1 Slaughterhouses have the system to treat water used during slaughtering process Yes -ref-
No 1.52 (0.94–2.48) 0.09 -
2 Separating workers for clean and unclean area Yes -ref-
No 1.59 (1.18–2.19) 0.02 -
3 Separating equipment for clean and unclean area Yes -ref-
No 1.74 (1.10–2.76) 0.01 1.65 (1.04–2.61) 0.02
4 Use of hanging equipment to prevent carcasses contamination Yes -ref-
No 1.67 (1.03–2.69) 0.04 -
5 Cutting knives are sanitized before use Yes -ref-
No 1.23 (0.98–1.47) 0.08 -
6 Building system Close -ref-
Open or semi-close 1.84 (1.27–2.69) 0.001 1.79 (1.23–2.60) 0.002
�
OR = odds ratio, -ref- = reference class.

https://doi.org/10.1371/journal.pone.0269416.t007

personal hygiene [6,16]. Studies conducted in Algeria and European countries revealed a
higher S. aureus non-compliance ranging between 38.5 and 46.7% compared to the findings in
this study [6,40]. Meat samples contaminated with Enterococcus spp. found in this study were
consistent with those observed in Slovakia and Brazil which ranged from 1.8 to 50.9% [41,42].
Those might be indicated contamination from slaughtering equipment, wastewater, and
slaughterhouse environment [43–45]. Our findings showed the proportion of coliforms and E.
coli non-compliant meat samples to be lower than the 22% of coliforms and 43% of E. coli con-
tamination recorded in a previous study [38]. These occurrences might result from unsatisfac-
tory sanitary conditions of slaughtering as well as fecal contamination [46,47]. Given that the
majority of Salmonella spp., a well-known foodborne pathogen, was slightly lower than the
findings in previous studies in other countries, with isolation rates ranging from 36 to 56%
[48–50]. On the contrary, other reports had indicated lower amounts of the Salmonella-posi-
tive samples at 7.1% and 9.5% in European countries and South Korea, respectively [6,14].
The present study also determined the factors associated with the non-compliance of the
meat samples in the slaughterhouses. According to the multivariable mixed-effect logistic
regression analysis, the results highlighted that the scalding process without scalding water
temperature control or improper scalding had a significant impact on the non-compliant meat
samples for APC, S. aureus, Enterococcus spp., coliforms, and E. coli contamination. Our find-
ings were in agreement with other studies that revealed an increase in bacterial contamination
on chicken carcasses following the scalding process due to the differences in the scalding tem-
perature, the amount of freshwater added during the scalding process, and the immersion
time [51,52]. The findings in this study are also supported by results from several studies [53–
58] that indicate the role of proper scalding process in significantly reduced bacterial contami-
nation. The scalding temperature had a great impact; in particular, when the scalding tempera-
ture reached 60˚C, bacteria on chicken carcasses reduced approximately by 2 log CFU/cm2
[57]. In this study, based on livestock authorities’ inspection, the scalding water temperature
ranged between 55–65˚C. This finding clearly showed that temperature control during the
scalding process significantly reduced bacterial contamination in chicken carcasses. The tem-
perature observed in this study was in agreement with a previous report in Thailand that
revealed the temperature of scalding water with the range of 62–66˚C [59], while reports from
other countries showed the temperature range between 50–70˚C [51,52,56].

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 9 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

In addition to the improper scalding, product characteristic was associated with E. coli non-com-
pliant meat samples. Our result indicated that eviscerated carcasses were more likely than non-evis-
cerated carcasses to be contaminated with E. coli. This finding was in concordance with other studies
showing similar results, which found a significant increase in E. coli after evisceration process [60]. It
is probable that bacterial cross-contamination from leaking intestinal content, giblets, and equipment
to carcasses occurred during the evisceration process [61]. Similar observations were noted for
increasing the level of E. coli on chicken carcasses during the evisceration process [16,54,60]. Given
that more than 60% of chicken carcasses processed in slaughterhouses were eviscerated in this study,
it is important to raise slaughterhouse workers’ awareness of E. coli contamination.
Salmonella spp. could be found as early as the chicken farms, transport vehicles, live bird
crates, and equipment along the slaughtering area [14,15,62]. In this study, the cross-contami-
nation from equipment in slaughtering lines was identified as the factor associated with the
Salmonella spp. contamination in meat. This finding was in a line with results from other stud-
ies demonstrating slaughter equipment including tables, gloves, baskets as well as the slaugh-
terhouse environment as the sources of cross-contamination for carcasses [15,52,63–66].
Additionally, we found an association between open or semi-closed slaughterhouses and a
higher risk of Salmonella spp. contamination in chicken meat. In contrast to closed slaughter-
houses, these facilities allow for more unfettered contact between flies and carcasses, thereby
increasing the possibility of cross-contamination since some flies presented in slaughterhouses
(approximately 15%) could carry viable Salmonella spp. [67].
To the best of our knowledge, this was the first study in Thailand to identify the risk factors
associated with non-compliant meat samples owing to bacterial contamination in slaughter-
houses through the official nationwide survey conducted by the livestock authorities. Based on
the findings from the present study, we recommend that the authorities should supervise
slaughterhouse personnel to enhance the slaughtering processes and facilities including proper
scalding, evisceration, slaughtering equipment, and slaughterhouse structure. Also, imple-
menting training or education programs for stakeholders or slaughterhouse staff for safe meat
production would be prudent. Moreover, the public should be made well-aware of the high
prevalence of foodborne pathogens such as Salmonella spp. on the meat. This study offers
information on bacterial contamination and associated risk factors for the bacterial contami-
nations based on nationwide data, and thereby contributes to the national need for informa-
tion on this subject. The data provided in this study could be used as a basic information that
can be gathered for future use by international organizations. We hope that our results could
be also useful to other chicken slaughterhouses with similar conditions outside Thailand.

Conclusions
In spite of dedicated efforts from the government authorities to implement control over bacte-
rial contamination in slaughterhouses, especially by foodborne pathogens such as Salmonella
spp., the challenge to achieve compliance to the regulations persists. In this study, we identified
several risk factors for bacterial contamination of chicken meat from slaughterhouses across
Thailand. Our results indicated that the scalding process, evisceration, equipment, and slaugh-
terhouse structure were the critical issues that warrant improvement. Therefore, a specific stra-
tegic plan based on these issues needs to be formulated.

Supporting information
S1 Table. Department of Livestock Development microbiological criteria and laboratory
method for livestock products.
(DOCX)

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 10 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

S2 Table. Factors used for the mixed-effects logistic regression analysis.

(DOCX)

Acknowledgments
The authors would like to acknowledge all of their colleagues, as well as the authorities of the
Department of Livestock Development (DLD) and the slaughterhouse supervisors, for their
willingness to participate in and contribute to this research.

Author Contributions
Conceptualization: Duangporn Pichpol, Tongkorn Meeyam, Thanida Harintharanon, Veera-
sak Punyapornwithaya.
Data curation: Kunnanut Klaharn, Veerasak Punyapornwithaya.
Formal analysis: Kunnanut Klaharn, Veerasak Punyapornwithaya.
Funding acquisition: Veerasak Punyapornwithaya.
Investigation: Thanida Harintharanon, Patpong Lohaanukul.
Methodology: Thanida Harintharanon, Patpong Lohaanukul, Veerasak Punyapornwithaya.
Project administration: Veerasak Punyapornwithaya.
Resources: Thanida Harintharanon, Patpong Lohaanukul.
Software: Veerasak Punyapornwithaya.
Supervision: Veerasak Punyapornwithaya.
Validation: Veerasak Punyapornwithaya.
Visualization: Kunnanut Klaharn, Veerasak Punyapornwithaya.
Writing – original draft: Kunnanut Klaharn.
Writing – review & editing: Duangporn Pichpol, Tongkorn Meeyam, Thanida Harinthara-
non, Patpong Lohaanukul, Veerasak Punyapornwithaya.

References
1. Cavani C, Petracci M, Trocino A, Xiccato G. Advances in research on poultry and rabbit meat quality.
Italian Journal of Animal Science. 2009; 8: 741–50.
2. Windhorst H-W. Changes in poultry production and trade worldwide. World’s Poultry Science Journal.
2006; 62(4): 585–602.
3. OECD. Meat consumption. 2021 [cited 14 May 2021]. Available: https://data.oecd.org/agroutput/meat-
consumption.htm.
4. Valceschini E, editor. Poultry meat trends and consumer attitudes. Proceedings of the XII European
Poultry Conference; 2006.
5. Antunes P, Mourão J, Campos J, Peixe L. Salmonellosis: the role of poultry meat. Clinical Microbiology
and Infection. 2016; 22(2): 110–21. https://doi.org/10.1016/j.cmi.2015.12.004 PMID: 26708671
6. Gonçalves-Tenório A, Silva BN, Rodrigues V, Cadavez V, Gonzales-Barron U. Prevalence of patho-
gens in poultry meat: a meta-analysis of European published surveys. Foods. 2018; 7(5): 69. https://
doi.org/10.3390/foods7050069 PMID: 29751496
7. Parisi A, Stanaway J, Sarkar K, Crump J. The global burden of non-typhoidal Salmonella invasive dis-
ease: a systematic analysis for the Global Burden of Disease Study 2017. International Journal of Infec-
tious Diseases. 2020; 101: 341–359.

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 11 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

8. WHO. WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemi-
ology reference group 2007–2015. 2015 [cited 14 May 2021]. Available: https://www.who.int/
foodsafety/publications/foodborne_disease/fergreport/en/.
9. Buzby JC, Roberts T. The economics of enteric infections: human foodborne disease costs. Gastroen-
terology. 2009; 136(6): 1851–62. https://doi.org/10.1053/j.gastro.2009.01.074 PMID: 19457414
10. Department of Disease Control. Food Poisoning Situation in Thailand. 2021 [cited 14 May 2021]. Avail-
able: https://ddc.moph.go.th/brc/news.php?news=17033&deptcode=brc.
11. Rouger A, Tresse O, Zagorec M. Bacterial contaminants of poultry meat: sources, species, and dynam-
ics. Microorganisms. 2017; 5(3):50–63.
12. Heyndrickx M, Vandekerchove D, Herman L, Rollier I, Grijspeerdt K, De Zutter L. Routes for Salmonella
contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiology &
Infection. 2002; 129(2):253–65. https://doi.org/10.1017/s0950268802007380 PMID: 12403101
13. Ananchaipattana C, Hosotani Y, Kawasaki S, Pongsawat S, Md. Latiful B, Isobe S, et al. Prevalence of
foodborne pathogens in retailed foods in Thailand. Foodborne pathogens and disease. 2012; 9(9):
835–40. https://doi.org/10.1089/fpd.2012.1169 PMID: 22953752
14. Shang K, Wei B, Jang H-K, Kang M. Phenotypic characteristics and genotypic correlation of antimicro-
bial resistant (AMR) Salmonella isolates from a poultry slaughterhouse and its downstream retail mar-
kets. Food Control. 2019; 100: 35–45.
15. Rasschaert G, Houf K, Godard C, Wildemauwe C, Pastuszczak-Frak M, De Zutter L. Contamination of
carcasses with Salmonella during poultry slaughter. Journal of Food Protection. 2008; 71(1):146–52.
https://doi.org/10.4315/0362-028x-71.1.146 PMID: 18236675
16. Maharjan S, Rayamajhee B, Chhetri VS, Sherchan SP, Panta OP, Karki TB. Microbial quality of poultry
meat in an ISO 22000: 2005 certified poultry processing plant of Kathmandu valley. International Jour-
nal of Food Contamination. 2019; 6(1):1–9.
17. Pacholewicz E, Sura Barus SA, Swart A, Havelaar AH, Lipman LJA, Luning PA. Influence of food han-
dlers’ compliance with procedures of poultry carcasses contamination: A case study concerning evis-
ceration in broiler slaughterhouses. Food Control. 2016; 68: 367–78.
18. Perez-Arnedo I, Cantalejo MJ, Martı́nez-Laorden A, Gonzalez-Fandos E. Effect of processing on the
microbiological quality and safety of chicken carcasses at slaughterhouse. International Journal of Food
Science & Technology. 2020.
19. The Department of Livestock Development. Microbiological Standard for Livestock Products. 2008
[cited 15 May 2021]. Available: http://qcontrol.dld.go.th/index.php/2013-12-11-03-23-37/127-2013-12-
09-03-56-19.
20. Butkool W, Saccavadit S. Contamination of pathogenic bacteria in meat samples from slaughterhouses
in the Lower Northern Region of Thailand during 2009–2013. 2014 [cited 22 June 2021]. Available from:
http://vrd-sn.dld.go.th/webnew/images/stories/service/Brochure/year57/Y11special.pdf.
21. Astivia OLO, Gadermann A, Guhn M. The relationship between statistical power and predictor distribu-
tion in multilevel logistic regression: a simulation-based approach. BMC medical research methodology.
2019; 19(1): 97. https://doi.org/10.1186/s12874-019-0742-8 PMID: 31072299
22. Lane SP, Hennes EP. Power struggles: Estimating sample size for multilevel relationships research.
Journal of Social and Personal Relationships. 2018; 35(1): 7–31.
23. The Department of Livestock Development. The National Monitoring Program for Slaughterhouse
Inspection and Certification. 2019 [cited 15 May 2021]. Available: http://certify.dld.go.th/certify/index.
php/th/2016-05-01-14-53-29/2562.
24. Klaharn K, Pichpol D, Meeyam T, Pfeiffer D, Moomon A, Lohaanukul P, et al. Analysis of nationwide
survey data to determine bacterial contamination levels in meat from pig slaughterhouses in Thailand.
Food Control. 2021; 126: 108005.
25. The Department of Livestock Development. The Laboratory of Bureau of Quality Control of Livestock
Products. 2017 [cited 22 May 2021]. Available: http://qcontrol.dld.go.th/index.php/84-2013-11-18-02-
58-45.
26. Department of Livestock Development. Manual of Slaughterhouse Standard Development and Meat
Distribution. Thailand: Ministry of Agriculture and Cooperatives; 2008.
27. Department of Livestock Development. Microbiological Standard for Livestock Products. 2008 [cited 22
May 2021]. Available: http://qcontrol.dld.go.th/index.php/2013-12-11-03-23-37/127-2013-12-09-03-56-
19.
28. Brown LD, Cai TT, DasGupta A. Interval estimation for a binomial proportion. Statistical science. 2001:
101–17.
29. R Core Team. R: A Language and Environment for Statistical Computing. 2020 [cited 14 May 2021].
Available: https://www.R-project.org/.

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 12 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

30. Bates D, Maechler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. Journal of
Statistical Software. 2015; 67(1): 1–48.
31. Wickham H, François R, Henry L, Müller K. dplyr: A Grammar of Data Manipulation. 2020 [cited 14 June
2021]. Available: https://CRAN.R-project.org/package=dplyr.
32. Larsen K, Petersen JH, Budtz-Jørgensen E, Endahl L. Interpreting parameters in the logistic regression
model with random effects. Biometrics. 2000; 56(3): 909–14. https://doi.org/10.1111/j.0006-341x.2000.
00909.x PMID: 10985236
33. Bewick V, Cheek L, Ball J. Statistics review 14: Logistic regression. Critical care. 2005; 9(1): 1–7.
https://doi.org/10.1186/cc3045 PMID: 15693993
34. Boonkerd T, Areekul V. Prevalence of Salmonella spp. contamination in fresh chicken meat from
slaughterhouses. International Congress of Meat Science and Technology; Bangkok, Thailand. 2016.
35. Teeyasuksaet N, Immak N. Bacterial contamination in meat from slaughterhouses in the Upper North-
ern Region of Thailand during 2015–2017. 2018 [cited 14 May 2021]. Available: http://region5.dld.go.th/
webnew/images/stories/2562/paper/paper207082562.pdf.
36. Vidayanti IN, Sukon P, Khaengair S, Pulsrikarn C, Angkittitrakul S. Prevalence and antimicrobial resis-
tance of Salmonella spp. isolated from chicken meat in upper northeastern Thailand. Veterinary Integra-
tive Sciences. 2021; 19(2).
37. Li Y, Pei X, Zhang X, Wu L, Liu Y, Zhou H, et al. A surveillance of microbiological contamination on raw
poultry meat at retail markets in China. Food Control. 2019; 104: 99–104.
38. Cohen N, Ennaji H, Bouchrif B, Hassar M, Karib H. Comparative study of microbiological quality of raw
poultry meat at various seasons and for different slaughtering processes in Casablanca (Morocco).
Journal of Applied Poultry Research. 2007; 16(4): 502–8.
39. Kumar P, Rao J, Haribabu Y. Microbiological quality of meat collected from municipal slaughter houses
and retail meat shops from Hyderabad Karnataka region, India. APCBEE procedia. 2014; 8: 364–9.
40. Guergueb N, Alloui N, Ayachi A, Bennoune O. Effect of slaughterhouse hygienic practices on the bacte-
rial contamination of chicken meat. Scientific Journal of Veterinary Advances. 2014; 3: 71–6.
41. DUCKOVÁ MKMČV. Occurrence, isolation and antibiotic resistance of Enterococcus species isolated
from raw pork, beef and poultry. Journal of Food and Nutrition Research. 2007; 46(2): 91–5.
42. Fracalanzza SAP, Scheidegger EMD, Santos PFd, Leite PC, Teixeira LM. Antimicrobial resistance pro-
files of enterococci isolated from poultry meat and pasteurized milk in Rio de Janeiro, Brazil. Memórias
do Instituto Oswaldo Cruz. 2007; 102(7): 853–9. https://doi.org/10.1590/s0074-02762007005000120
PMID: 18060316
43. Wambui J, Tasara T, Njage PMK, Stephan R. Species distribution and antimicrobial profiles of Entero-
coccus spp. isolates from Kenyan small and medium enterprise slaughterhouses. Journal of food pro-
tection. 2018; 81(9):1445–9. https://doi.org/10.4315/0362-028X.JFP-18-130 PMID: 30080119
44. Bakhtiary F, Sayevand HR, Remely M, Hippe B, Hosseini H, Haslberger AG. Evaluation of bacterial
contamination sources in meat production line. Journal of food quality. 2016; 39(6):750–6.
45. Igbinosa I, Raje O. Characterization of Enterococcus species isolated from abattoir environment in
Benin city, Nigeria. Ife Journal of Science. 2019; 21(3): 81–95.
46. Kim JH, Hur SJ, Yim DG. Monitoring of microbial contaminants of beef, pork, and chicken in HACCP
implemented meat processing plants of Korea. Korean journal for food science of animal resources.
2018; 38(2): 282. https://doi.org/10.5851/kosfa.2018.38.2.282 PMID: 29805278
47. McEvoy J, Sheridan J, Blair I, McDowell D. Microbial contamination on beef in relation to hygiene
assessment based on criteria used in EU Decision 2001/471/EC. International Journal of Food Microbi-
ology. 2004; 92(2):217–25. https://doi.org/10.1016/j.ijfoodmicro.2003.09.010 PMID: 15109799
48. Bai L, Lan R, Zhang X, Cui S, Xu J, Guo Y, et al. Prevalence of Salmonella isolates from chicken and
pig slaughterhouses and emergence of ciprofloxacin and cefotaxime co-resistant S. enterica serovar
Indiana in Henan, China. PLoS One. 2015; 10(12): e0144532. https://doi.org/10.1371/journal.pone.
0144532 PMID: 26650239
49. Sakaridis I, Soultos N, Iossifidou E, Koidis P, Ambrosiadis I. Prevalence and antimicrobial resistance of
Salmonella serovars from chicken carcasses in northern Greece. Journal of Food Safety. 2011; 31(2):
203–10.
50. Vinueza-Burgos C, Baquero M, Medina J, De Zutter L. Occurrence, genotypes and antimicrobial sus-
ceptibility of Salmonella collected from the broiler production chain within an integrated poultry com-
pany. International Journal of Food Microbiology. 2019; 299: 1–7. https://doi.org/10.1016/j.ijfoodmicro.
2019.03.014 PMID: 30933685
51. Cardinale E, Tall F, Cissé M, Guèye E, Salvat G, Mead G. Risk factors associated with Salmonella
enterica subsp. enterica contamination of chicken carcases in Senegal. British poultry science. 2005;
46(3): 293–9. https://doi.org/10.1080/00071660500098467 PMID: 16050182

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 13 / 14

PLOS ONE Risk factors for bacterial contamination of chicken meat in slaughterhouses in Thailand

52. Chaiba A, Filali FR. Risk Factors Associated with Salmonella Contamination of Chicken Carcases in
Traditional Slaughterhouses in Morocco. Microbiology Research Journal International. 2017: 1–7.
53. Göksoy EO, Kirkan S, Kok F. Microbiological quality of broiler carcasses during processing in two
slaughterhouses in Turkey. Poultry science. 2004; 83(8): 1427–32. https://doi.org/10.1093/ps/83.8.
1427 PMID: 15339020
54. Vaidya V, Paturkar A, Waskar V, Zende R, Rawool D. Detection of indicator organisms on poultry car-
cass sites in an organized slaughterhouse. Journal of Muscle Foods. 2005; 16(4): 289–97.
55. Ho C, Huang N, Chen B. A survey of microbial contamination of food contact surfaces at broiler slaugh-
ter plants in Taiwan. Journal of food protection. 2004; 67(12): 2809–11. https://doi.org/10.4315/0362-
028x-67.12.2809 PMID: 15633692
56. Xiao X, Wang W, Zhang X, Zhang J, Liao M, Yang H, et al. Modeling the reduction of Salmonella spp.
on chicken breasts and wingettes during scalding for QMRA of the poultry supply chain in China. Micro-
organisms. 2019; 7(6): 165. https://doi.org/10.3390/microorganisms7060165 PMID: 31174317
57. Yang H, Li Y, Johnson MG. Survival and death of Salmonella Typhimurium and Campylobacter jejuni in
processing water and on chicken skin during poultry scalding and chilling. Journal of food protection.
2001; 64(6): 770–6. https://doi.org/10.4315/0362-028x-64.6.770 PMID: 11403124
58. Osiriphun S, Tuitemwong P, Koetsinchai W, Tuitemwong K, Erickson LE. Model of inactivation of Cam-
pylobacter jejuni in poultry scalding. Journal of food engineering. 2012; 110(1): 38–43.
59. Parntong V. Comparison standard and microbiological quality change of chicken meat from small
slaughterhouses. 2011 [cited 9 March 2021]. Available: http://ebook.lib.kmitl.ac.th/library/book_detail/
09000872.
60. Pacholewicz E, Swart A, Schipper M, Gortemaker BG, Wagenaar JA, Havelaar AH, et al. A comparison
of fluctuations of Campylobacter and Escherichia coli concentrations on broiler chicken carcasses dur-
ing processing in two slaughterhouses. International Journal of Food Microbiology. 2015; 205: 119–27.
https://doi.org/10.1016/j.ijfoodmicro.2015.04.006 PMID: 25950748
61. Rodrigo S, Adesiyun A, Asgarali Z, Swanston W. Occurrence of selected foodborne pathogens on poul-
try and poultry giblets from small retail processing operations in Trinidad. Journal of food protection.
2006; 69(5): 1096–105. https://doi.org/10.4315/0362-028x-69.5.1096 PMID: 16715810
62. Corry JE, Allen V, Hudson W, Breslin M, Davies R. Sources of Salmonella on broiler carcasses during
transportation and processing: modes of contamination and methods of control. Journal of Applied
Microbiology. 2002; 92(3): 424–32. https://doi.org/10.1046/j.1365-2672.2002.01543.x PMID:
11872117
63. Lin C-H, Huang J-F, Sun Y-F, Adams PJ, Lin J-H, Robertson ID. Detection of chicken carcasses con-
taminated with Salmonella enterica serovar in the abattoir environment of Taiwan. International Journal
of Food Microbiology. 2020; 325: 108640. https://doi.org/10.1016/j.ijfoodmicro.2020.108640 PMID:
32344254
64. Reiter M, Fiorese M, Moretto G, López M, Jordano R. Prevalence of Salmonella in a poultry slaughter-
house. Journal of food protection. 2007; 70(7): 1723–5. https://doi.org/10.4315/0362-028x-70.7.1723
PMID: 17685349
65. Zeng H, De Reu K, Gabriël S, Mattheus W, De Zutter L, Rasschaert G. Salmonella prevalence and per-
sistence in industrialized poultry slaughterhouses. Poultry Science. 2021; 100(4): 100991. https://doi.
org/10.1016/j.psj.2021.01.014 PMID: 33610890
66. Van Hoek AH, De Jonge R, Van Overbeek WM, Bouw E, Pielaat A, Smid JH, et al. A quantitative
approach towards a better understanding of the dynamics of Salmonella spp. in a pork slaughter-line.
International Journal of Food Microbiology. 2012; 153(1–2): 45–52. https://doi.org/10.1016/j.
ijfoodmicro.2011.10.013 PMID: 22119458
67. Ly TL-K, Tran TTD, Nguyen VH, Tran TP, Toan HT. Isolation of Salmonella from flies in the Mekong
Delta, Vietnam. Journal of Veterinary Epidemiology. 2010; 14(1): 41–6.

PLOS ONE | https://doi.org/10.1371/journal.pone.0269416 June 8, 2022 14 / 14