Prevalence, serovars, and risk factors associated with the presence of <i>Salmonella</i> in pork sold in public markets in Quito, Ecuador

Christian Vinueza-Burgos; Luis Hidalgo-Arellano; Carlos Gómez-Coronado; José Luis Medina-Santana; María Cevallos-Almeida

doi:10.12688/f1000research.138671.1

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Research Article

Prevalence, serovars, and risk factors associated with the presence of Salmonella in pork sold in public markets in Quito, Ecuador

[version 1; peer review: 1 approved, 1 approved with reservations]

Christian Vinueza-Burgos¹, Luis Hidalgo-Arellano², Carlos Gómez-Coronado², José Luis Medina-Santana¹, María Cevallos-Almeida ²

Christian Vinueza-Burgos¹, Luis Hidalgo-Arellano², [...] Carlos Gómez-Coronado², José Luis Medina-Santana¹, María Cevallos-Almeida ²

PUBLISHED 18 Oct 2023

Author details Author details

¹ Unidad de Investigación de Enfermedades Transmitidas por Alimentos y Resistencia a los Antimicrobianos (UNIETAR). Facultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador, Quito, Pichincha, Ecuador
² Laboratorio de Bacteriología y Micología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador, Quito, Pichincha, Ecuador

Christian Vinueza-Burgos
Roles: Formal Analysis, Writing – Review & Editing

Luis Hidalgo-Arellano
Roles: Conceptualization, Data Curation, Formal Analysis, Investigation, Methodology, Resources, Visualization, Writing – Original Draft Preparation

Carlos Gómez-Coronado
Roles: Data Curation, Formal Analysis, Investigation, Methodology, Project Administration, Resources, Supervision, Validation

José Luis Medina-Santana
Roles: Data Curation, Resources, Software, Writing – Original Draft Preparation, Writing – Review & Editing

María Cevallos-Almeida
Roles: Conceptualization, Data Curation, Formal Analysis, Funding Acquisition, Investigation, Project Administration, Resources, Supervision, Validation, Writing – Original Draft Preparation

OPEN PEER REVIEW

REVIEWER STATUS

This article is included in the Antimicrobial Resistance collection.

Abstract

Background: Salmonella enterica are bacteria that include more than 2,500 serovars. Most of these serovars have been linked to human foodborne illnesses, mainly related to poultry and pigs. Thus, these animals are considered the reservoirs of many Salmonella serovars and strains related to antibiotic resistance. This study aimed to determine the prevalence, serovars, β-lactam resistance genes, and the risk factors associated with Salmonella enterica in pork commercialized in open markets of Quito city.

Methods: For this, 165 pork meat samples were taken from municipal markets in three areas in the city. These samples were microbiologically processed following the ISO 6579-2014 standardized method. The polymerase chain reaction (PCR) test was used to identify Salmonella serotyping and resistance genes. Strains not identified by PCR were typed by the Kauffman White Le Minor scheme. A multivariate analysis was performed to identify risk factors associated with the presence of the microorganism.

Results: Salmonella prevalence in pork was 9.1%. Identified serovars were 4, [5], 12: i:- (53.3%), Infantis (33.3%), and Derby (13.4%). Furthermore, the β-lactam resistance genes bla CTX-M-65 could be identified in three S. infantis isolates. Multivariate analysis showed that temperature (above 8°C) and cutting surfaces (wood) presented significant association values.

Conclusions: This research represents the first report of several epidemiological aspects of Salmonella in pork in Ecuador.

Keywords

Salmonella, Infantis, monophasic S. Typhimurium, Derby, risk factors, pork, antibiotic resistance, Ecuador, Beta-lactamase

Corresponding author: María Cevallos-Almeida

Competing interests: No competing interests were disclosed.

Grant information: The author(s) declared that no grants were involved in supporting this work.

Copyright: © 2023 Vinueza-Burgos C et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: Vinueza-Burgos C, Hidalgo-Arellano L, Gómez-Coronado C et al. Prevalence, serovars, and risk factors associated with the presence of Salmonella in pork sold in public markets in Quito, Ecuador [version 1; peer review: 1 approved, 1 approved with reservations]. F1000Research 2023, 12:1367 (https://doi.org/10.12688/f1000research.138671.1) First published: 18 Oct 2023, 12:1367 (https://doi.org/10.12688/f1000research.138671.1) Latest published: 17 Apr 2024, 12:1367 (https://doi.org/10.12688/f1000research.138671.2)

Introduction

The consumption of undercooked food contaminated with non-typhoid Salmonella is one of the most important causes of human gastroenteritis worldwide. Foodborne diarrheal disease agents also caused 230,000 of the 420,000 deaths due to foodborne hazards in 2010. Of these, non-typhoidal S. enterica accounted for 59,000 deaths.¹

Contaminated food of animal origin is an important source of infection and spread of Salmonella.² This contamination can occur at any stage in the production chain.³^,⁴ Animals such as pigs can be infected or colonized by different Salmonella serovars, developing a disease or becoming a reservoir of this microorganism, excreting and spreading it.⁵ Contaminated pork plays an important role as one of the main sources of human infection with Salmonella in several countries.⁶^–⁸ It has to be considered that cross-contamination of food with Salmonella may occur by kitchen instruments, improper hygienic handling, etc.⁹

Different Salmonella serovars can be implicated in a large number of human infections. Therefore, serovar identification is essential in the epidemiological surveillance of this pathogen.¹⁰ Several serovars have been reported in pork and pig production, associated with different geographical localization. Thus, S. Derby and S. Typhimurium were the most prevalent serovars in Europe, Oceania, Asia, and North America,¹¹ while S. Derby has been reported as the most pervasive serovar in pork in Latin America.¹²

Besides, antimicrobial resistance has posed a critical problem for human and animal health in the last 20 years.¹³ The overuse of antibiotics in these two areas has contributed to the emergence of antibiotic resistance in foodborne bacteria.¹⁴ Thus, several studies have reported multi-resistant Salmonella strains (MDR) in which Salmonella isolates producing extended-spectrum beta-lactamase enzymes (ESBL) are common findings.¹⁵^–¹⁷ Although the importance of non-typhoid Salmonella and its antimicrobial resistance is evident in food production, epidemiological information about the presence of this bacteria in pork is still limited in Ecuador. Therefore, this research aimed to estimate the prevalence of Salmonella serovars, antimicrobial resistance, and risk factors associated with Salmonella enterica in pork meat sold in markets in Quito-Ecuador.

Methods

Sample collection

A total of 165 pork samples were collected in 11 traditional markets in three areas of Quito. Samples of 100 g of meat from 25 butcheries were collected between March and May 2021. Each sample was collected in sterile plastic flasks and transported to the laboratory in an icebox at 2–8°C.

Survey information

An epidemiological questionnaire to estimate the risk factors for pork contamination was developed and applied to the butchery employees (Table 1).

Table 1. Variables included in the epidemiological survey.

Variables	Description
Location	North
	Center
	South
Owner's education level	None
	Elemental
	High school
	University
Number of people at the sales stand	One person
	Two people
	>2 people
Functionally age of butchery	<1 year to 5 years
Functionally age of butchery	>5 years
Types of commercialized meats	Only pork
	Two meat products
	>3 meat products
Meat preservation temperature	Temperature < 8°C
Meat preservation temperature	Temperature > 8°C
Meat preservation time	Unknown
Meat preservation time	1–2 days
Meat location at the seller’s shop	Metal Hanger/Refrigerator
	Refrigerator/Cold room (CR)
	Refrigerator/CR/freezer
	Metal hangers & trays
Meat cutting surface	Metallic & acrylic
Meat cutting surface	Wood
Origin of pork	Metropolitan slaughterhouse
Origin of pork	Other origin
Type of water used	Potable Drinking water
Type of water used	Without water at the butchery
Type of cleaning material	Wipe
Type of cleaning material	Disposable paper & wipe
Cleaning products used for disinfection	Detergent & degreaser
Cleaning products used for disinfection	>3 Cleaning products

Isolation and identification of Salmonella

Salmonella was isolated and identified according to the ISO 6579: 2017 standardized method.¹⁸ Briefly, 25 g of pork and 225 ml of Buffered Peptone Water – BPW (BD Difco 218105 – USA) were placed in a sterile zip bag and homogenized to obtain a 1:10 suspension. The combination was incubated at 37°C ± 1°C for 18 h ± 2 h. After incubation, 0.1 ml of the pre-enriched culture as 1–3 equally spaced spots on the surface of Modified Semisolid Rappaport Vassidialis - MSRV plates (BD Difco 218681 – USA) and incubated at 41.5°C for 24 h ± 3 h. A loop of 1 μl was taken inside the edge of the opaque growth in MSRV and plated in the Xylose Lysine, Deoxycholate – XLD agar (BD Difco 278850 – USA) and incubated at 37°C for 24 ± 3 h. Typical colonies of Salmonella spp. in XLD (black center with a slightly transparent reddish area) were then identified by biochemical tests. These tests included Triple Sugar Agar – TSI (BD Difco 226540 – USA), Lysine Iron Agar – LIA (BD Difco 284920 – USA), Simmons Citrate BD (Difco 211620 – USA), and Urea broth (BD Difco 227210 – USA). All the positive isolates were conserved at -70°C in a Brain Head Infusion medium (BD Difco 241830 – USA) with glycerol (Fisher Chemical G33500 – USA).

DNA extraction

DNA extraction was performed using the boiling method. Briefly, Salmonella isolates were plated in XLD agar and incubated at 37±1°C for 24 hours. A typical Salmonella colony was transferred to a sterile Eppendorf tube containing 300 μl of 1X TE buffer (Tris base Promega H5131 – USA + EDTA Promega V4231 – USA) and lysed at 95°C for 20 minutes. The supernatant was collected and stored at -20°C.

Serovars identification

Serovars Infantis, Enteritidis, Typhimurium, and its monophasic variant (1,4, [5], 12: i:-) were identified by polymerase chain reaction (PCR), using the invA gene as housekeeping control. Primers and annealing temperature for these PCR protocols are described in Table 2. GoTaq^® Flexi DNA Polymerase (Promega M8291 – USA), nuclease-Free Water (Promega P1197 – USA), and dNTP Mix (Promega U1515 – USA) were used as PCR reagents on a SimpliAmp™ Thermal Cycler (Thermo Fisher A24811 – USA) to perform all reactions. According to the Kauffmann-White scheme, Salmonella isolates not typed by PCR were serotyped using the agglutination method.¹⁹ Briefly, each strain was recovered in Nutrient Agar (BD Difco 213000 – USA) and incubated for 16 to 20 h at 37°C ± 2. Then, the agglutination test was performed, confronting the bacterial suspension to specific antisera in a multi-cup plate. Positive agglutination is visualized by aggregate formation (more or less cottony appearance) exerting a moderate circular agitation of the plaque. Determination of somatic antigen (O antigen) requires the primary test of polyvalent sera (OMA, OMB, OMC, OMD, OME, OMF, and OMG) followed by monovalent ones (Remel™ Agglutinating Sera – UK). To determine flagellar antigen (H antigen), agglutination with one of the mixing sera for orientation (HMA, HMB, HMC) or the versatile serum H1 was observed (Remel™ Agglutinating Sera – UK). The determination of the flagellar antigen is obtained by successive elimination until detection of agglutination with one of the specific sera included in the mixing serum (search for major H then minor H). The combination of somatic antigen and flagellar antigen defines the serotype of the strain under study. The Kauffmann–White scheme gathers the groups and the corresponding sera.

Table 2. Primers used for Salmonella serovars identification.

Target gene	Primers	Sequence	Amplicons size (pb)	Annealing Tem.	Ref.
Salmonella spp.	InvAF	5′-AAACCTAAAACCAGCAAAGG-3′	605	58	²⁰
Salmonella spp.	InvAR	5′-TGTACCGTGGCATGTCTGAG-3′	605	58	²⁰
S. Infantis	IMP1-F	5′-GGTCATTGTCGGAAACCTGC-3′	95	60	²⁰
	IMP1-R	5′-ACATTCCCCCTTCCACTGCC-3′	95	60
	IMP2-F	5′-CGCGAAGAAGTGCATAAACC-3′	198	60
	IMP2-R	5′-CGCCACTTTCGTTATCTGAG-3′	198	60
	IMP3-F	5′-ACCTACTACTATCCCTGATG-3′	304	60
	IMP3-R	5′-GCGAATTTTGCTACTTGAAG-3′	304	60
S. Enteritidis	EMP1-F	5′-AATACAGCCTCAACCAGCTA-3′	101	60	²⁰
	EMP1-R	5′-ATTGGTTCACCCGTTGCAAT-3′	101	60
	EMP2-F	5′-AGATAAGCCCTCCCTGCTTA-3	203	60
	EMP2-R	5′-CCCTCCTTTCACTGCAAGTC-3′	203	60
	EMP3-F	5′-CAAAAGCGACAAATAATCTG-3′	299	60
	EMP3-R	5′-TTTCTCCGCCTGTTTTCGTT-3′	299	60
S. Typhimurium	TMP1-F	5′-ATGCGGGTATGACAAACCCT-3′	94	60	²⁰
	TMP1-R	5′-TTAGCCCCATTTGGACCTTT-3′	94	60
	TMP2-F	5′-CAGACCAGGTAAGTTTCTGG-3′	196	60
	TMP2-R	5′-CGCATATTTGGTGCAGAAAT-3′	196	60
	TMP3-F	5′-TTTACCTCAATGGCGGAACC-3′	303	60
	TMP3-R	5′-CCCAAAAGCTGGGTTAGCAA-3′	303	60
S. Typhimurium Monophasic	MDH F	5′-TGCCAACGGAAGTTGAAGTG-3′	260	58	²¹
	MDH R	5′-CGCATTCCACCACGCCCTTC-3′	550	58
	fliC F	5′-ATAGCCATCTTTACCAGTTCC-3′	1389	58
	fliC R	5′-ACTCAGGCTTCCCGTAACGC-3′	1389	58
	fljB F	5′-CAACAACAACCTGCAGCGTGTGCG-3′	964	64
	fljB R	5′-GCCATATTTCAGCCTCTCGCCCG-3′	964	64
	FFLiB	5′-CTGGCGACGATCTGTCGATG-3′	964	64
	RFLIA	5′-GCGGTATACAGTGAATTCAC-3′	964	64

Antimicrobial susceptibility test

Identification of antimicrobial resistance Salmonella isolates was carried out using the Kirby-Bauer disk diffusion method according to the Clinical and Laboratory Standards Institute guidelines.²² Briefly, from a culture of 18 to 24 hours on Nutrient Agar (BD Difco 213000 – USA), several colonies were taken with a handle and inoculated in physiological serum to reach a turbidity equivalent to 0.5 of the McFarland scale. The previous suspension was seeded into the Müller-Hinton plates (BD Difco 275730 – USA) using a swab without leaving any free area. After, antibiotic discs were placed equidistantly using sterile tweezers. The plates were incubated at 37°C for 16–18 hours and the diameter of the inhibition halos was measured. The clinical cut-offs of M100 CLSI standards (CLSI, 2022) were used as references integrating intermedia values as resistant. The antibiotics used were: Ampicillin (Oxoid, USA; 10 μg), Cefoxitin (Oxoid CT0003B – USA; 30 μg), Cefotaxime (BD 231606 – USA; 30 μg), Ceftazidime (BD 231632 – USA; 30 μg), Amoxicillin + clavulanic acid (Oxoid CT0223B – USA; 30 μg), Ertapenem (BD 232175 – USA 10 μg), Tetracycline (Oxoid CT0054B – USA; 30 μg), Tigecycline (Oxoid CT1841B – USA; 15 μg), Chloramphenicol (Oxoid CT0013B – USA; 30 μg), Ciprofloxacin (Oxoid CT0425B – USA; 5 μg), Sulfamethoxazole + Trimethoprim (Oxoid CT0052B – USA; 30 μg), Gentamicin (Oxoid CT0024B – USA; 10 μg), Amikacin (Oxoid CT0107B – USA; 30 μg), Nitrofurantoin (Oxoid CT0036B – USA; 300 μg), Fosfomycin (Oxoid CT0758B – USA; 200 μg).

PCR further studied isolates with phenotypic resistance to beta-lactams to detect bla_CTX-M, bla_TEM, bla_CMY, and bla_SHV genes. Additionally, the bla_CTX-M subgroups were identified for later sequencing. Primers and annealing temperature for these PCR protocols are described in Table 3. PCR reagents and equipment used for serotyping by PCR were used in this step.

Table 3. Primers used for Beta-lactams identification.

Target gene	Primers	Sequence	Amplicon size (pb)	Annealing Tem.	Ref.
bla_{CTX-M General}	CTX-MU1	5′-ATG TGC AGY ACC AGT AAR GTK ATG GC	592	60	²³^,²⁴
bla_{CTX-M General}	CTX-MU2	5′-TGG GTR AAR TAR GTS ACC AGA AYS AGC GG	592	60	²³^,²⁴
bla_SHV	SHVOS5	5′-TTA TCT CCC TGT TAG CCA CC	795	60	²⁴^,²⁵
bla_SHV	SHVOS6	5′-GAT TTG CTG ATT TCG CTC GG	795	60	²⁴^,²⁵
bla_TEM	TEM front P1	5′-GCG GAA CCC CTA TTT G	964	55	²⁴^,²⁶
bla_TEM	TEM-C-R-ny	5′-ACC AAT GCT TAA TCA GTG AG	964	55	²⁴^,²⁶
bla_CMY	Queprev cmy-2 sart	5′-ATG ATG AAA AAA TCG TTA TGC TGC	1117	60	²³^,²⁴
bla_CMY	cmy-group2-R	5′-GCT TTT CAA GAA TGC GCC AGG	1117	60	²³^,²⁴
bla_{CTX-M1 Group}	CTX-1-SEQ-F	5′-CCC ATG GTT AAA AAA TCA CTG C	1000	60	²⁷^,²⁸
bla_{CTX-M1 Group}	CTX-1-SEQ-R	5′-CAG CGC TTT TGC CGT CTA AG	1000	60	²⁷^,²⁸
bla_{CTX-M2 Group}	CTX-M-2F	5′-ATG ATG ACT CAG AGC ATT CG	1179	60	²⁹^,³⁰
bla_{CTX-M2 Group}	CTX-M-2R	5′-TGG GTT ACG ATT TTC GCC GC	1179	60	²⁹^,³⁰
bla_{CTX-M8 Group}	CTX-Mgp8-F	5′-TGA TGA GAC ATC GCG TTA AG	871	55	³¹^,³²
bla_{CTX-M8 Group}	CTX-Mgp8-R	5′-TAA CCG TCG GTG ACG ATT TT	871	55	³¹^,³²
bla_{CTX-M9 Group}	CTX-M-9-1F	5′-TGG TGA CAA AGA GAG TGC AAC G	874	60	³³^,³⁴
	CTX-M-9-R	5′-TCA CAG CCC TTC GGC GAT	874	60
	CTX-M-9_792_F	5′-CTA TTT TAC CCA GCC GCA AC	238	60
	CTX-M-9_1029_r	5′-GTT ATG GAG CCA CGG TTG AT	238	60

All amplified PCR products were exanimated by electrophoresis in a 1% Agarose, LE, Analytical Grade (Promega V3125 – USA) on 0.5X TAE Buffer (Promega V4281 – USA) and stained with SYBR™ Safe DNA Gel Stain (Invitrogen S33102 – USA). Amplicons’ size was estimated by 100 bp Plus DNA Ladder (Bioneer D-1035 – Korea). Gel casting and electrophoresis were performed in a horizontal electrophoresis system (CBS Scientific HSU-014, EPS-300X – USA). Specific bands were visualized on ENDURO™ UV Transilluminator (Labnet U1001 – USA). Raw and edited images of all PCR products are available in the Underlying data.³⁵ All betalactamese PCR products were sent for sequencing to Macrogen Inc. (Seul-South Korea), and obtained sequences were aligned against reference sequences by the web tool ResFinder 4.0.³⁶

Statistical analysis

The free software R Studio (Version 1.4.1717) was used for statistical analysis. Descriptive statistics were used to facilitate the calculation of frequencies observed for each variable that would be used in the univariate analysis. For the bivariate analysis, we included variables of interest regarding the prevalence of Salmonella and then performed the chi-squared test and Fisher’s exact test. A univariate and multivariate logistic regression study was used to obtain odds ratios and 95% confidence intervals (CI). The level of significance was determined as p < 0.05.

Results

The prevalence of Salmonella was 9.1% (15/165; CI_95% = 5.6-14.5).

Serovar identification of Salmonella

The PCR technique allowed the identification of five S. Infantis and eight monophasic variants of S. Typhimurium (1,4,[5],12:i:-) isolates. Additionally, two S. Derby isolates were characterized by the Kauffman White scheme.

Antimicrobial resistance analysis

Four antimicrobial resistance profiles were found in 11 isolates (Table 4). Three and seven isolates of S. Infantis and S. 1,4,[5],12:i:- presented multi-resistant patterns, respectively. The two S. Derby and two S. Infantis isolates showed to be susceptible to all tested antibiotics.

Table 4. Antibiotic resistance patterns of Salmonella isolates*.

N° of antibiotic families	Resistance patterns	S. Infantis	S. 4,[5],12:i:-	Total
7	SAQBTFN	3	-	3
4	QBTF	-	1	1
3	QTF	-	6	6
2	TF	-	1	1
Total		3	8	11

* Four Salmonella isolates were susceptible to all tested antibiotics.

The highest resistance levels were present in three S. Infantis isolates with resistance phenotypes for 11 antibiotics. Additionally, all S. 4,[5],12:i:- isolates showed resistance to tetracycline and chloramphenicol (Table 5). The bla_CTX-M-65 gene was identified in all the S. Infantis isolates resistant to cefotaxime. On the other hand, none of the studied β-lactamase genes were identified in S. 4,[5],12:i:- isolates resistant to β-lactams.

Table 5. Resistance rates for tested antibiotics.

Antibiotic family	Antibiotic	Serotype
Antibiotic family	Antibiotic	S. Infantis	S. 4,[5],12:i:-
Tetracycline	Tetracycline	60% (3)	100% (8)
Tetracycline	Tigecycline	0%	0%
Phenicol	Chloramphenicol	60% (3)	100% (8)
Quinolones	Ciprofloxacin	60% (3)	87.5% (7)
Beta-lactams	Ampicillin	60% (3)	12.5% (1)
	Cefotaxime	60% (3)	12.5% (1)
	Amoxicillin + Clavulanic acid	60% (3)	12.5% (1)
	Ceftazidime	40% (2)	0%
	Cefoxitin	40% (2)	0%
Folate pathway inhibitor	Sulfamethoxazole + Trimethoprim	60% (3)	0%
Aminoglycosides	Gentamicin	60% (3)	0%
Aminoglycosides	Amikacin	0%	0%
Nitrofurans	Nitrofurantoin	60% (3)	0%
Fosfomycin	Fosfomycin	0%	0%
Carbapenems	Ertapenem	0%	0%

Risk factors for pork contamination

In bivariate analysis, the variable “Meat cutting surface wood” showed a significant association with Salmonella in pork (p = 0.0349). Multiple logistic regression analysis determined that the variable “Meat preservation temperature” (higher than 8°C) also showed significant values (p = 0.031) (Table 6).

Table 6. Logistic regression model analysis of variables with significant values.

Variables	Standard error (SE)	P value	Odds Ratio	I.C. 95%
Meat preservation temperature (>8°C)	0.1	0.03171 *	1.15	1.02	1.33
Meat cutting surface (wood)	1.6	0.01107 *	59.31	3.15	2 829.14

Full responses for the survey, metadata, and susceptibility test reports are available in the Underlying data.⁷⁷

Discussion

This research aimed to determine the prevalence of Salmonella enterica in pork meat in public markets of Quito, Ecuador. Identification of Salmonella serovars, antimicrobial resistance profiles, and risk factors associated with the presence of the microorganism were included in this work.

In the present study, the prevalence of Salmonella in pork was 9.1% (95% CI = 5.6 – 14.5). Another study in Quito reported a higher Salmonella occurrence in pork in 2016.³⁷ This decrease in Salmonella occurrence could indicate that some interventions for improving market sanitary conditions could have been implemented. Several studies around the world have reported different levels of Salmonella in pork. In Europe, the prevalence of Salmonella in pork was 0.64% in 2019 (n=20 613),³⁸ while in Asian countries, the prevalence of Salmonella varies from 14.1% to 57.74%.³^,³⁹^,⁴⁰ Overall, variations of Salmonella prevalence within countries or among regions of the world could be associated with the implementation of specific technologies in meat treatment or the existence of specific regulations that could be put in place in Ecuadorian markets.⁴¹

Salmonella Typhimurium monophasic variant (S. 1,4,[5],12:i:-) was the predominant serovar in this study (53.4%), becoming the first report of this serovar in pig meat in Ecuador.

It has been mentioned that isolation of S. 1,4,[5],12:i:- has increased worldwide during the last 20 years.⁴² Pigs are ranked as the main reservoir of this serovar in the European Union.⁴³ Furthermore, S. 1,4,[5],12:i:- has become one of the most common variants of Salmonella in pork production,⁴⁴^,⁴⁵ being considered an emerging serovar in many countries.⁴⁵ The present study demonstrates that this serovar may be relevant in the epidemiology of Salmonella linked to food contamination in Ecuador.

Concerning S. Infantis, our results differ from those reported by Mejia et al.,³⁷ who showed this serovar as the most isolated one in pig meat samples in retail markets in Ecuador. Since the later study samples were taken from supermarkets, this difference could be determined by the pig meat supply chain. In this regard, pork in traditional markets comes from many small pig production farms. On the other hand, pork from supermarkets comes from a few companies with intensive industrial production. These facts could explain the differences between studies. Moreover, S. Infantis has been reported as one of the most frequent serovars in industrial poultry production in many countries,⁴⁶^–⁴⁸ indicating that this serovar is well adapted to industrial conditions.⁴⁹^,⁵⁰ Since S. Infantis has been reported to cause human diseases,⁵¹ the epidemiology of this serotype in pork and its relationship with other meat products (e.g., poultry) should be further investigated. Similar considerations must be made for other serovars like S. Derby because the surveillance of Salmonella serovars shapes the epidemiology of these pathogens in foodstuffs.

Antimicrobial resistance (AMR) of Salmonella isolates from pork and pig production has been reported in other countries at regional and global levels showing multi-resistant phenotypes.⁵²^,⁵³ However, AMR varies according to Salmonella serotypes. In this study, S. Infantis was the least susceptible serotype with resistance patterns of up to seven antimicrobial families. In the same way, S. Infantis isolates with high rates of AMR have been reported in the poultry industry of Ecuador,⁵⁰^,⁵⁴ which has been linked to the overuse of antimicrobials in this sector.⁵⁵ However, multi-resistant S. Infantis has been reported worldwide, demonstrating that multi-resistance is an important feature of this serovar, possibly linked to specific plasmids. Thus, the capacity of S. Infantis to acquire genetic determinants of resistance has been associated with the “plasmid of emerging S. enterica Infantis” (pESI) and related plasmids (pESI-like plasmids).⁵⁶ The bla_CTX-M-65 gene identified in three S. Infantis isolates has been closely related to this megaplasmid in local studies⁵⁰^,⁵⁴^,⁵⁷^,⁵⁸ and globally.⁵⁹^–⁶¹

The same can be said for S. 4, [5],12:i:- whose majority of isolates showed multi-resistant patterns. Moreover, this serotype has been reported in several countries, showing that S. 4,[5],12:i:- is specially adapted to the pig production sector and could represent a public health concern.⁶²^–⁶⁴

High levels of AMR Salmonella have been related to the incorrect use of antibiotics in animal production. The administration of cephalosporins and other beta-lactams in pig production has seen to increase in many countries, like France,⁶⁵ India,⁶⁶ and Brazil.⁶⁷ Moreover, in Ecuador, the misuse of antibiotics in animal production systems has been reported.⁶⁸^,⁶⁹ This aspect has particular relevance since beta-lactams are widely used in animal husbandry.⁷⁰^,⁷¹ It must also be considered that ESBL genes could determine failure in treating diseased people with complicated infections caused by Salmonella and other bacteria to which horizontal transference of genes may occur.⁷² In the present work, we found that meat preservation above 8°C (OR = 1.15) and wooden surfaces for meat cutting (OR = 59.31) were risk factors for Salmonella in pork meat. This is unsurprising since the lack of an appropriate cool chain allows the growth of contaminating microorganisms and pathogens in food products.⁷³ Besides, the porosity of wood in cutting tables will enable bacteria to grow in the presence of humidity, promoting cross-contamination of foodstuffs with Salmonella.⁷⁴^–⁷⁶ Whether Salmonella isolates recuperated in our study originated in the primary sector or are the result of such cross-contamination events should be further studied, targeting samples from pig production farms and conducting analysis of genomic clonality.

In conclusion, pork expended in traditional markets of Quito showed contamination of Salmonella enterica, whose main serovars are of public health concern. Beta-lactam-resistance in Salmonella isolates is also remarkable, which could become a risk for pork consumers.

Data availability

Underlying data

Figshare: PCR images of Prevalence, serovars, and risk factors associated with the presence of Salmonella in pork sold in public markets in Quito, Ecuador. https://doi.org/10.6084/m9.figshare.24195030.v1.³⁵

This project contains the following underlying data:

• CTX-M-9 Edited.jpg
• CTX-M-9 RAW.jpeg
• fljA-B-C edited.jpg
• fljA-B-C raw.jpeg
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Figshare: Pork_database_risk_factors.xlsx. https://doi.org/10.6084/m9.figshare.23699505.v1.⁷⁷

Data are available under the terms of the Creative Commons Attribution 4.0 International license (CC-BY 4.0).

Acknowledgment

We acknowledge to Health Services of Quito Municipality for the assistance and collaboration provided in the markets for the collection of samples. We also are grateful for the help provided by Laboratorio de Resistencia Antimicrobiana del Instituto Nacional de Investigación en Salud Pública - INSPI “Dr. Leopoldo Izquieta Perez” for their collaboration in the identification of the Salmonella Derby serovar. We also acknowledge Dr. Pamela Martinez for her help in the statistical analysis.

References

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¹ Unidad de Investigación de Enfermedades Transmitidas por Alimentos y Resistencia a los Antimicrobianos (UNIETAR). Facultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador, Quito, Pichincha, Ecuador
² Laboratorio de Bacteriología y Micología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador, Quito, Pichincha, Ecuador

Christian Vinueza-Burgos
Roles: Formal Analysis, Writing – Review & Editing

Luis Hidalgo-Arellano
Roles: Conceptualization, Data Curation, Formal Analysis, Investigation, Methodology, Resources, Visualization, Writing – Original Draft Preparation

Carlos Gómez-Coronado
Roles: Data Curation, Formal Analysis, Investigation, Methodology, Project Administration, Resources, Supervision, Validation

José Luis Medina-Santana
Roles: Data Curation, Resources, Software, Writing – Original Draft Preparation, Writing – Review & Editing

María Cevallos-Almeida
Roles: Conceptualization, Data Curation, Formal Analysis, Funding Acquisition, Investigation, Project Administration, Resources, Supervision, Validation, Writing – Original Draft Preparation

Competing interests

No competing interests were disclosed.

Grant information

The author(s) declared that no grants were involved in supporting this work.

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Vinueza-Burgos C, Hidalgo-Arellano L, Gómez-Coronado C et al. Prevalence, serovars, and risk factors associated with the presence of Salmonella in pork sold in public markets in Quito, Ecuador [version 1; peer review: 1 approved, 1 approved with reservations] F1000Research 2023, 12:1367 (https://doi.org/10.12688/f1000research.138671.1)

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ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested

Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.

Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions

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Reviewer Report 15 Feb 2024

Ma Soledad Vázquez-Garcidueñas, Facultad de Ciencias Médicas y Biológicas, Universidad Michoacana de San Nicolas de Hidalgo, Morelia, Michoacán, Mexico

Approved

https://doi.org/10.5256/f1000research.151889.r240450

This work is very relevant since it aimed to determine the prevalence, serovars, β-lactam resistance genes, and the risk factors associated with Salmonella enterica in pork since these animals are considered the reservoirs of many Salmonella serovars and strains related ... Continue reading

This work is very relevant since it aimed to determine the prevalence, serovars, β-lactam resistance genes, and the risk factors associated with Salmonella enterica in pork since these animals are considered the reservoirs of many Salmonella serovars and strains related to antibiotic resistance, and this information is still limited in Ecuador. Identification of Salmonella serovars, antimicrobial resistance profiles, and risk factors associated with the presence of the microorganism were included in this work.

It is recommended to make the following modifications:
The conclusion of the summary is obvious and uninformative, it is recommended to write one that better describes the results.
In the introduction, if the information in pork is limited in Ecuador, put a reference to how little is known or in any case change it to non-existent information.
Since they amplified beta-lactamase, it is necessary to justify in the introduction why these were specifically sought.
In materials and methods, change minutes and hours by min and h respectively.
In PCR amplifications, include the amount of DNA contained in the assay.
If possible, update the bibliography since there are some references that are too old.

Is the work clearly and accurately presented and does it cite the current literature?

Partly
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Molecular epidemiology of Salmonella, Acinetobacter and Mycobacterium tuberculosis

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

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Reviewer Report 15 Feb 2024

Patricio Retamal, Departamento de Medicina Preventiva Animal, Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Santiago, Chile

Approved with Reservations

https://doi.org/10.5256/f1000research.151889.r234636

This article describes the detection of Salmonella serovars in pork meat from several markets in Quito, Ecuador. It's an interesting work that depicts contamination rates of this food commodity and raises concerns about public health risks for people involved in ... Continue reading

This article describes the detection of Salmonella serovars in pork meat from several markets in Quito, Ecuador. It's an interesting work that depicts contamination rates of this food commodity and raises concerns about public health risks for people involved in processing or consuming this product due to the presence of multidrug-resistant pathogenic bacteria.

However, there are some major comments about the text that should be addressed by the authors before indexing.

A major issue is related to the serotyping methodology. The PCR reaction for serotyping should be backed up with the traditional Kauffmann-White scheme or with whole-genome sequencing. Because PCR may have some false positive results (as indicated in the cited reference), all isolates should have been confirmed with KW. Why did the authors do it partially?

Conclusions, both in the abstract and within the main text, should address the main findings of this work.

Cited references need an update. Just one of them is from 2023, and some data is definitely old. For instance, the first paragraph of the introduction indicates cases from 2010.

The text should be revised by a native English speaker. There are several mistakes throughout the manuscript.

What was the criterion for the selection of markets? Clarification is required.

What was the criterion for the selection of butcheries and interviewed employees?

Normally, variables included in epidemiological surveys are selected from previous reports or locally identified during in situ observations. What were the sources for the included variables?

Other minor comments:

The Kauffmann-White serotyping is a standard procedure that does not require a detailed description. A reference is enough. The same occurs with the Kirby-Bauer method.

What was the control strain in the Kirby-Bauer procedure? It is required to validate results.

Tables 4 and 5 should be merged, and optimally, all isolates should be described (antimicrobial phenotypes and genotypes) in this new table.

In the discussion, the second paragraph, the potential causes of differences between Salmonella prevalence values between countries or continents are multifactorial, but authors identify "technologies for meat treatment or specific regulations." I think a broader analysis should be made for observed differences.

In the discussion, paragraphs 3 and 4 should be merged.

In the discussion, the fifth paragraph, I don't understand the statement "because the surveillance of Salmonella serovars shapes the epidemiology of these pathogens in foodstuffs." Please give some clarification.

Please verify references 6 and 8. I think they are incompletely written.

Is the work clearly and accurately presented and does it cite the current literature?

Partly
Is the study design appropriate and is the work technically sound?

Partly
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Partly

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Microbiology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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Patricio Retamal, Departamento de Medicina Preventiva Animal, Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Santiago, Chile
Ma Soledad Vázquez-Garcidueñas, Universidad Michoacana de San Nicolas de Hidalgo, Morelia, Mexico

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Reviewer Report

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15 Feb 2024 | for Version 1

Ma Soledad Vázquez-Garcidueñas, Facultad de Ciencias Médicas y Biológicas, Universidad Michoacana de San Nicolas de Hidalgo, Morelia, Michoacán, Mexico

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Approved

This work is very relevant since it aimed to determine the prevalence, serovars, β-lactam resistance genes, and the risk factors associated with Salmonella enterica in pork since these animals are considered the reservoirs of many Salmonella serovars and strains related to antibiotic resistance, and this information is still limited in Ecuador. Identification of Salmonella serovars, antimicrobial resistance profiles, and risk factors associated with the presence of the microorganism were included in this work.

It is recommended to make the following modifications:
The conclusion of the summary is obvious and uninformative, it is recommended to write one that better describes the results.
In the introduction, if the information in pork is limited in Ecuador, put a reference to how little is known or in any case change it to non-existent information.
Since they amplified beta-lactamase, it is necessary to justify in the introduction why these were specifically sought.
In materials and methods, change minutes and hours by min and h respectively.
In PCR amplifications, include the amount of DNA contained in the assay.
If possible, update the bibliography since there are some references that are too old.

Is the work clearly and accurately presented and does it cite the current literature?

Partly
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Molecular epidemiology of Salmonella, Acinetobacter and Mycobacterium tuberculosis

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

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Reviewer Report

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15 Feb 2024 | for Version 1

Patricio Retamal, Departamento de Medicina Preventiva Animal, Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Santiago, Chile

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Approved With Reservations

This article describes the detection of Salmonella serovars in pork meat from several markets in Quito, Ecuador. It's an interesting work that depicts contamination rates of this food commodity and raises concerns about public health risks for people involved in processing or consuming this product due to the presence of multidrug-resistant pathogenic bacteria.

However, there are some major comments about the text that should be addressed by the authors before indexing.

A major issue is related to the serotyping methodology. The PCR reaction for serotyping should be backed up with the traditional Kauffmann-White scheme or with whole-genome sequencing. Because PCR may have some false positive results (as indicated in the cited reference), all isolates should have been confirmed with KW. Why did the authors do it partially?

Conclusions, both in the abstract and within the main text, should address the main findings of this work.

Cited references need an update. Just one of them is from 2023, and some data is definitely old. For instance, the first paragraph of the introduction indicates cases from 2010.

The text should be revised by a native English speaker. There are several mistakes throughout the manuscript.

What was the criterion for the selection of markets? Clarification is required.

What was the criterion for the selection of butcheries and interviewed employees?

Normally, variables included in epidemiological surveys are selected from previous reports or locally identified during in situ observations. What were the sources for the included variables?

Other minor comments:

The Kauffmann-White serotyping is a standard procedure that does not require a detailed description. A reference is enough. The same occurs with the Kirby-Bauer method.

What was the control strain in the Kirby-Bauer procedure? It is required to validate results.

Tables 4 and 5 should be merged, and optimally, all isolates should be described (antimicrobial phenotypes and genotypes) in this new table.

In the discussion, the second paragraph, the potential causes of differences between Salmonella prevalence values between countries or continents are multifactorial, but authors identify "technologies for meat treatment or specific regulations." I think a broader analysis should be made for observed differences.

In the discussion, paragraphs 3 and 4 should be merged.

In the discussion, the fifth paragraph, I don't understand the statement "because the surveillance of Salmonella serovars shapes the epidemiology of these pathogens in foodstuffs." Please give some clarification.

Please verify references 6 and 8. I think they are incompletely written.

Is the work clearly and accurately presented and does it cite the current literature?

Partly
Is the study design appropriate and is the work technically sound?

Partly
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Partly

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Microbiology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

Respond to this report

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Prevalence, serovars, and risk factors associated with the presence of Salmonella in pork sold in public markets in Quito, Ecuador

Abstract

Keywords

Introduction

Methods

Sample collection

Survey information

Table 1. Variables included in the epidemiological survey.

Isolation and identification of Salmonella

DNA extraction

Serovars identification

Table 2. Primers used for Salmonella serovars identification.

Antimicrobial susceptibility test

Table 3. Primers used for Beta-lactams identification.

Statistical analysis

Results

Serovar identification of Salmonella

Antimicrobial resistance analysis

Table 4. Antibiotic resistance patterns of Salmonella isolates*.

Table 5. Resistance rates for tested antibiotics.

Risk factors for pork contamination

Table 6. Logistic regression model analysis of variables with significant values.

Discussion

Data availability

Underlying data

Acknowledgment

References

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