Next Article in Journal
Sonographic Characteristics of the Thymus in Healthy Canine Neonates
Next Article in Special Issue
Formulation-Level Tolerability of Repeated Drinking-Water Administration of a Commercial Multi-Component Bacteriophage Product in Ross 308 Broiler Chickens: A Pilot 27-Day Dose-Escalation Study
Previous Article in Journal
Effects of a Glycosylated Form of Active Vitamin D Combined with Natural Triterpenes on Sow Productive Performance, Mineral Homeostasis, Immune Biomarkers and Serum Proteome
Previous Article in Special Issue
Avian Candidiasis: A Comprehensive Review of Pathogenesis, Diagnosis, and Control
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Veterinary Sciences
Volume 13
Issue 3
10.3390/vetsci13030247
vetsci-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Quaternary Ammonium Biocide Resistance in Non-Typhoidal Salmonella from Pig Carcasses

by
Lorina Lourenço
1,
Vanessa Ferreira da Silva
2,3,
Madalena Vieira-Pinto
2,3,
Manuela Oliveira
1,3,4 and
João B. Cota
1,3,*
1
CIISA—Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, Avenida da Universidade Técnica, 1300-477 Lisbon, Portugal
2
Veterinary and Animal Research Centre (CECAV), University of Trás-os-Montes and Alto Douro (UTAD), 5000-801 Vila Real, Portugal
3
Associate Laboratory for Animal and Veterinary Science (Al4AnimalS), Av. da Universidade Técnica, 1300-477 Lisbon, Portugal
4
cE3c—Centre for Ecology, Evolution and Environmental Changes & CHANGE—Global Change and Sustainability Institute, Faculty of Sciences, University of Lisbon, Campo Grande, 1749-016 Lisbon, Portugal
*
Author to whom correspondence should be addressed.
Vet. Sci. 2026, 13(3), 247; https://doi.org/10.3390/vetsci13030247
Submission received: 29 January 2026 / Revised: 26 February 2026 / Accepted: 2 March 2026 / Published: 5 March 2026
(This article belongs to the Special Issue Exploring Antimicrobial Strategies in Veterinary Medicine: From In Vitro Research to In Vivo Applications)
Versions Notes

Simple Summary

In this study, we assessed the resistance ability of Salmonella isolated from pig carcasses to a commercial quaternary ammonium compound (QAC) disinfectant formulation and examined the prevalence of genes that are associated with such resistance and with possible persistence in the contaminated surfaces. Our results show that though the isolates carried resistance genes, they were susceptible to the disinfectant formulation, even at concentrations 10 times lower than the minimum recommended in-use concentration. These results show that the possible persistence of these bacteria in the environment of food processing facilities, such as slaughterhouses, should not be exclusively associated with disinfectant resistance, stressing the importance of correct cleaning and disinfection procedures and/or hygiene practices.

Abstract

Non-typhoidal Salmonella (NTS) are one of the most common foodborne pathogens worldwide, and pork is a major food vehicle together with eggs and poultry meat. Contamination of pork within food processing facilities, such as slaughterhouses, can be associated with persistence of Salmonella in the environment due to biocide resistance. In this study, we assessed the susceptibility of NTS isolates from pig carcasses to a QAC-based commercial formulation according to the EN 1656/2009 standard and the presence of QAC resistance genes through PCR. The qacEΔ1 and qacF genes were found in 31.8% and 29.5% of the isolates respectively, while qacE was absent. All isolates were found to be susceptible at a tested concentration 10 times lower (0.1%) than the minimum in-use recommended concentration, with MIC values below 0.1% (≈70 mg/L of Benzalkonium Chloride). Our findings point towards the importance of correct cleaning and disinfection protocols and the role of good hygiene practices as corrective and/or preventive measures to avoid cross-contamination.

1. Introduction

Non-typhoidal Salmonella (NTS) are still major foodborne pathogens despite the efforts to limit their impact on human health. It is estimated that between 1.2 and 1.35 million individuals fall ill with salmonellosis each year in the United States of America [1,2] and that NTS is responsible for 12,500 hospitalizations [3]. These numbers are only surpassed by Norovirus and Campylobacter spp., being estimated to cause 5.5 million and 1.9 million cases of disease/year, respectively [3]. In the European Union, during 2024, Salmonella was, alike the previous years, the second most commonly reported zoonotic pathogen, after Campylobacter spp., being responsible for 79,703 cases of illness, and the most frequently reported causative agent of multi-country foodborne outbreaks [4]. Though not exclusively, the major sources of human salmonellosis are animal-derived foods, namely eggs, poultry meat, pork and beef [5,6], especially in high-income countries where diarrheal NTS infections are classified as a foodborne disease [7]. Indeed, food-producing animals are the most relevant reservoirs of the multiple NTS serotypes responsible for human illness cases [8], and an association of some of the most relevant serotypes with specific animal species and/or animal-derived foods is frequently observed in foodborne outbreaks [9,10,11]. Regarding the isolation of Salmonella in pigs and along the pork production chain in Europe, the most frequently reported serotypes are Typhimurium, Derby, Rissen and the monophasic variant of Typhimurium [12].
Concerning meat and thereof products, contamination can take place along the multiple steps of the production chain, starting at abattoirs, mostly arising from the evisceration of Salmonella asymptomatic carriers and the contamination of the abattoir environment and equipment, up to processing and distribution, through cross-contamination and manipulation [13]. This scenario is also true for the pork production chain, with pork and pork products being among the food categories consistently implicated in salmonellosis foodborne outbreaks [14,15,16]. Besides the obvious consequences for human health of Salmonella-contaminated pork, the associated economic impacts should not be neglected, making it a multidimensional problem. It was previously estimated that the annual economic burden of foodborne illness of pork-associated Salmonella in the United States of America was 1.9 billion US dollars, ranking this food–pathogen pair as one of the most costly meat-related foodborne illnesses [17]. Additionally, the economic consequences of surveillance and control strategies at different levels are also relevant [18,19,20,21], as well as the economic costs of possible market recalls and limited market access [22].
One of the possible roots of cross-contamination of meat is the persistence of Salmonella in abattoirs and meat processing plants, where persistence of multiple Salmonella serotypes has been reported [23]. As reviewed previously [24], persistence refers to the ability of microorganisms to survive for extended periods of time in certain habitats; specifically in food processing environments, it means that the same bacterial strain is repeatedly isolated from the same location for months or years. It seems that the persistence of Salmonella in such environments results from a combination of different features, including the ability to form biofilms, presence and expression of virulence genes and ability to resist to antimicrobials and/or to disinfectants [23]. On the other hand, contamination arising from the environment and equipment can occur simply due to the inadequate application of cleaning and disinfection protocols, since it is generally believed that proper disinfection reduces the risk of Salmonella cross-contamination [25].
The correct use of biocides for disinfection purposes is essential to eliminate and/or prevent the growth of unwanted microorganisms in the surfaces and environments of diverse settings, namely those associated with food production, where such chemical substances are widely used [26]. Quaternary ammonium compounds (QACs) are frequently applied in these settings, belonging to the group of nonoxidizing antimicrobial biocides and being available in different formulations for domestic, industrial and healthcare usage. The antimicrobial activity of QACs is mainly associated with their ability to interact with the cytoplasmic membrane of microorganisms, leading to leakage of intracellular material, but they can also affect intracellular targets, degrading proteins and DNA [27,28]. There is an increasing concern regarding the loss of effectiveness of biocides through the development of bacterial resistance, and to the possibility of cross-resistance with other unrelated antimicrobial compounds [29]. Intrinsic resistance to QACs is mostly associated with membrane permeability barriers and with the activity of efflux pumps, while acquired resistance may result from either the overexpression of the chromosome-encoded efflux pumps, the reduction in membrane permeability, or the acquisition of efflux pump genes encoded in mobile genetic elements [30]. Among the genes associated with QAC resistance, the presence of qac genes have been studied in both Gram-positive and Gram-negative bacteria [31]. These genes, including qacE, qacF, qacH and qacI, among others, are carried in integrons, transposons, plasmids and other mobile genetic elements [32]. Additionally, qacEΔ1, considered to be a variant of qacE, is commonly found in Gram-negative bacteria, including in Enterobacteriaceae [31].
The aim of this study was to investigate the susceptibility of a collection of NTS isolated from pig carcasses to a commercial QAC formulation, under in vitro conditions, along with the presence of QAC resistance-associated genes.

2. Materials and Methods

2.1. Bacterial Isolates

A collection of 44 Salmonella spp. isolates originating from pigs slaughtered in a Portuguese abattoir located in the northern region of the country, previously characterized [33], was used in this study. Briefly, the isolation of Salmonella from skin after stunning and bleeding procedures, and from the external and internal carcass surfaces before cooling was achieved according to the ISO 6579:2002 standard [34]. All presumptive Salmonella isolates were serotyped according to the Kauffman-White scheme at the Instituto Nacional de Investigação Agrária e Veterinária (INIAV), the Portuguese National Reference Laboratory for Salmonella identification in animal and food samples. Additionally, the bacterial isolates were subjected to genomic fingerprinting by Pulse Field Gel Eletrophoresis (PFGE) using the PulseNet protocol [35], and the PFGE patterns were studied by computer-assisted cluster analysis using BioNumerics® version 6.6 software (Applied Maths, SintMartens-Lantem, Belgium).

2.2. Detection of Biocide Resistance Genes

PCR amplification was conducted to detect genes for QAC resistance genes. After bacterial DNA extraction performed according to the protocol of Moore et al. (2004) [36], the amplification of qacEΔ1, qacE and qacF gene was performed using previously reported primers [37]. Each PCR reaction was performed in a volume of 25 μL and consisting of 12.5 μL of NZYTaq II 2x Green Master Mix (NZYtech®, Lisbon, Portugal), 9.5 μL of nuclease-free water, 1 μL of forward primer (STAB VIDA, Lda., Caparica, Portugal) at a final concentration of 0.4 μM, 1 μL of reverse primer (STAB VIDA, Lda., Caparica, Portugal) at a final concentration of 0.4 μM and 1 μL of DNA from each isolate. The presence or absence of amplicons was confirmed by gel electrophoresis, in a 2% agarose gel stained with GreenSafe Premium® (NZYtech®, Lisbon, Portugal), and visualized using ChemiDoc XRS+ (BIO-RAD Laboratories, Inc., Algés, Portugal).

2.3. Determination of Minimum Inhibitory Concentration (MIC) and Minimum Bactericidal Concentration (MBC)

Twelve isolates harboring different biocide resistance gene combinations from the different Salmonella serotypes, from the different sampled regions (skin, and external and internal carcass surfaces) and from the different genomic clusters were selected for further characterization. Enterococcus hirae ATCC 10541, Staphylococcus aureus ATCC 6538, Escherichia coli ATCC 10536 and Pseudomonas aeruginosa ATCC 15442 were used as control strains.
The MIC and MBC of Suma Bac D10® (Diversey™), a QAC-based sanitizer formulation widely used in food handling and processing units, with Benzalkonium Chloride (BKC) as the biocide active substance at the concentration of 70 g/kg, was determined according to the EN 1656:2009 standard for the evaluation of bactericidal activity of chemical disinfectants and antiseptics used in the veterinary field [38]. Considering that the recommended manufacturer’s in-use concentrations vary between 1% (≈700 mg/L) and 4% (≈2800 mg/L), the commercial biocide formulation was diluted in sterile water to obtain the following eight concentrations to be tested—5% (≈3500 mg/L), 4% (≈2800 mg/L), 3% (≈2100 mg/L), 2% (≈1400 mg/L), 1% (≈700 mg/L), 0.5% (≈350 mg/L), 0.25% (≈125 mg/L), and 0.1% (≈70 mg/L). For neutralization of the biocide activity, a solution containing 30 g/L polysorbate 80 (Merck & Co., Inc., Rahway, NJ, USA), 30 g/L saponin (SigmaAldrich, St. Louis, MO, USA) and 3 g/L ovolecithin (The British Drug Houses Ltd., London, UK) was used [38]. Additionally, to simulate the presence of organic matter, the experiments were executed using low and high doses of interfering substances [38]. Thus, the MIC and MBC of the biocide were determined in three different conditions, namely with no interfering substances, and both with low and high levels of interfering substances. The solution of low-level interfering substance (LIS) was prepared by dissolving 3 g of bovine albumin fraction V (NZYTech®, Lisbon, Portugal) in 100 mL of water, followed by sterilization by membrane filtration with a 0.2 µm syringe filter (Nalgene®, New York, NY, USA). The high-level interfering substance (HIS) solution was prepared using two solutions. The first one was prepared by dissolving 50 g of yeast extract (Oxoid, Ltd., Hampshire, UK) in 250 mL of water, followed by sterilization by autoclave (120 °C, 20 min). The second one was prepared by dissolving 5 g of albumin in 25 mL of water, followed by sterilization with a 0.2 µm syringe filter (Nalgene®, New York, NY, USA). To obtain the final HIS solution, 25 mL of the yeast extract suspension were added to this last solution.
All experiments were carried out in 96-well plates (VWR International®, Leuven, Belgium). Briefly, using 24 h bacterial cultures grown on Brain Heart Infusion agar (VWR International®, Leuven, Belgium), bacterial suspensions of the selected isolates were prepared in sterile saline solution at a concentration corresponding to 0.5 McFarland (~1.5 × 108 CFU/mL). Then, the assay was performed using three microplates. In the first 96-well plate, 20 μL of the bacterial suspensions were added to pre-filled wells containing 160 μL of the biocide formulation at the different concentrations previously mentioned and either 20 μL of sterile water of LIS or of HIS. The mixture was incubated with agitation (700 rpm) for 5 min ± 10 s, as per the disinfectant manufacturer’s instructions. After, 20 μL of the mixture of each well of the first plate were transferred to the corresponding well of a second plate already containing 160 μL of the neutralizing solution and 20 μL of sterile water. The plates were incubated with agitation (700 rpm) for 5 min ± 10 s [38]. After neutralization, 20 μL of each well were added to the corresponding wells of a third plate, pre-filled with 180 μL of Tryptone Soya Broth (TSB) (Oxoid, Ltd., Hampshire, UK). Moreover, this third plate included both negative (wells with 200 μL of non-inoculated TSB) and positive controls (wells pre-filled with 180 μL of the bacterial suspensions in TSB). This last plate was incubated for 24 h at 37 °C, after which the MIC was visually determined as the minimum concentration of the biocide formulation able to inhibit bacterial multiplication.
To determine the MBC, 5 μL were taken from wells where no bacterial multiplication was observed, followed by inoculation on Tryptone Soya Agar (TSA) (Oxoid, Ltd., Hampshire, UK) and incubation for 24 h at 37 °C.
To evaluate the reproducibility of the experiments, the procedures were repeated for 10% of the 12 isolates tested, which were randomly selected.

2.4. Efflux Pump Activity Assay

Efflux pump activity was assessed using the ethidium bromide (EtBr) agar cartwheel method [39]. Briefly, the agar plates were prepared using Luria Broth agar (NZYTech®, Lisbon, Portugal) and EtBr. EtBr was prepared from a stock solution diluted to obtain the desired final concentration and added to the LB agar after sterilization. Assays were performed using five different EtBr concentrations, namely 0.50, 1.00, 1.50, 2.00 and 2.50. The plates were inoculated by swabbing, with freshly prepared 0.5 McFarland bacterial suspensions of the 12 selected isolates. The plates were then incubated for 18 h at 37 °C, protected from light. After incubation, the presence or absence of fluorescence was assessed by UV transillumination using ChemiDoc XRS+ (BIO-RAD Laboratories, Inc., Algés, Portugal). In each assay, Enterococcus faecium CCUG 36804, with high efflux pump activity, and Enterococcus faecalis ATCC 29212, with no efflux pump activity, were also tested.

2.5. Statistical Analysis

The possible statistical associations between the presence of QAC resistance gene and isolate characteristics were evaluated using Fisher’s exact test performed on IBM SPSS Statistics version 28 (SPSS Inc. Chicago, IL, USA). Statistically significant differences corresponded to p values lower than 0.05.

3. Results

3.1. Detection of QAC Resistance Genes

None of the isolates harbored the qacE gene (Table 1). The presence of qacEΔ1 was observed in 31.8% (14/44) of isolates and qacF was found in 29.5% (13/44) of isolates. Thus, regarding QAC resistance genotypes, the most frequent were qacEΔ1 present in 15.9% (7/44), qacEΔ1/qacF in 15.9% (7/44) followed by qacF in 13.6% (6/44).
In the collection under study, the frequency of qacEΔ1 was diverse between serotypes, being present in 23.8% (5/21) of the Salmonella 4,[5],12:i:- isolates, in 22.2% (4/18) of the Rissen isolates and in all five Derby isolates (p < 0.05). On the other hand, qacF was mostly found in Rissen isolates, with a frequency of 55.6% (10/18), being less frequent in Salmonella 4,[5],12:i:- isolates (14.3%; 3/21) and absent in the Derby isolates (p < 0.05).
Focusing on the genomic clusters, the presence of those resistance genes was more common in some clusters when compared to others, as observed for qacF in cluster IB (90%) and for qacEΔ1 in clusters III (100%) and IB (40%) (p < 0.05).

3.2. Minimum Inhibitory Concentration and Minimum Bactericidal Concentration

The mean Suma Bac D10® MIC and MBC values found for the 12 selected isolates is presented in Table 2.
In all assays, including those performed without interfering substance (NIS), with low interfering substance (LIS) or with high interfering substance (HIS), the MIC values obtained were below the lowest recommended concentration for the biocide formulation studied (0.1%), since in all three conditions (NIS, LIS and HIS), the lowest concentration tested (0.1%) had a bactericidal effect (MBC) for all the isolates studied. No differences between MIC or MBC values and the diverse QAC resistance genotypes, genomic clusters or serotypes were observed.

3.3. Efflux Pump Activity

The level of efflux activity of the previously 12 selected isolates was evaluated using the EtBr cartwheel method. After incubation, none of the isolates showed any efflux activity at any of the EtBr concentrations tested, showing a similar level of fluorescence as Enterococcus faecalis ATCC 29212 (negative for efflux activity included in each test).

4. Discussion

In this study, the susceptibility of a collection of Salmonella isolates collected from pig carcasses to a QAC commercial biocide formulation was assessed in in vitro conditions, in addition to the presence of QAC resistance genes (qacE, qacEΔ1 and qacF). This research was designed to better understand the possible persistence ability of Salmonella isolates of the pork production chain in food processing environments and the association with their resistance ability to a biocidal active substance commonly used in the agri-food industry.
Firstly, all 44 isolates were screened for the presence of QAC resistance genes through conventional PCR. The presence of specific genes coding for efflux pumps has been pointed out as one of the possible mechanisms for QAC resistance. Such genes, namely qacE, qacF, qacG, qacH and qacI, have been associated with reduced susceptibility to QACs in Gram-negative bacteria [30]. Additionally, qacEΔ1 gene, a variation of the qacE gene, has been found to be present in Gram-negative bacteria [40], including in different Salmonella serotypes [41]. Furthermore, these genes can be carried together in mobile genetic elements, along with other antimicrobial resistant determinants [42]. Our results show that almost a third (31.8%) of all isolates harbored the qacEΔ1 gene, isolated or in combination with qacF, while qacE was not detected. The prevalence of such biocide resistance genes in Salmonella isolated from pigs in Portugal is still a knowledge gap, with limited information available. Nevertheless, our results are in accordance with a previous report focusing on Salmonella isolates from pig and poultry, obtained from feces, rectal swabs, drinking water and feed samples, which described a qacEΔ1 prevalence of 27% and the absence of qacE [43]. The qacEΔ1 gene is typically associated with class 1 integrons resulting from a deletion of qacE gene, found fused with the sulfonamide resistance gene sul1 [44]. Previously, these integrons have been found in 14 Salmonella Rissen and 15 Salmonella Typhimurium isolates belonging to a collection of 40 antibiotic resistant Salmonella isolates from fecal samples of domestic pigs and wild boars in Portugal [45]. Our results revealed that the presence of qacEΔ1 was associated with the Derby serotype, with all of the isolates belonging to that serotype harboring the QAC resistance gene.
Besides qacEΔ1, qacF was also found in 29.5% of the isolates, alone or in combination with qacEΔ1 gene, mostly among Salmonella Rissen isolates. Both qacE and qacF show a high degree of similarity, being found in class 1 integrons [46], though the prevalence of the latter has not been a subject of extensive research, being considered to occur sporadically [31]. The presence of qacEΔ1 and qacF simultaneously was observed in 15.9% of the isolates, from both the Rissen and 4,[5],12:i:- serotypes. These biocide resistance genes have been found in Salmonella from other settings, namely from poultry and egg production chains [47,48] and retail food of animal origin [49], but similar data focusing on pig and/or pork is scarce. Further studies are needed to achieve a clearer assessment of the actual dissemination of these and other QAC resistance genes, along with the sequence of class 1 integrons among Salmonella from the pork production chain.
From the 44 isolates studied, 12 were selected for biocide susceptibility testing according to the EN 1656:2009 protocol. In total, eight concentrations of QAC commercial formulation were tested, considering the manufacturer’s recommendations. After validation of the protocol, all isolates were found to be susceptible to every biocide concentration tested, since the MBC obtained was the lowest concentration tested (0.1% ≈ 70 mg/L of BKC), regardless of the absence or presence of organic matter. This concentration should be interpreted as the lowest attaining a bactericidal effect in our experimental conditions and not as the actual MBC of the QAC formulation towards the tested Salmonella isolates. In fact, the MBC of BKC for Salmonella can be as low as 0.003 mg/L [50], which is about 20,000-fold lower than the lowest concentration tested in our study. As previously reviewed [51], the MIC of BKC for Salmonella isolates is quite variable, ranging from concentrations as low as 0.003 mg/L to 256 mg/L. In the present work, under the conditions tested, it was not possible to calculate the actual MIC for any of the isolates and the presented result, <0.1%, should be carefully interpreted.
Though the presence of qacEΔ1 gene was not previously associated with increased BKC MIC values in Salmonella isolates from poultry and swine [43], a more recent study has found that class 1 integrons carrying that gene conferred resistance to both antibiotics and disinfectants in Salmonella, namely to BKC [52]. The influence of the presence of qacEΔ1 and qacF genes on the MIC and MBC values could not be attained in our study, as this could only be achieved after the determining the actual MIC and MBC values towards isolates with and without these genes. This approach could also be improved by expanding the number of isolates tested in order to grasp the possible variability that was not detected in the present experimental design. Determining the actual influence of disinfectant resistance genes on the Salmonella isolates, in light of the findings of the present study, is important for a better understanding of their impact on phenotypic biocide susceptibility and should therefore be addressed in future research. Nevertheless, all results should also be interpreted through the practical perspective, considering the discrepancy between the BKC concentrations tested in vitro and those in-use.
The QAC resistance genes studied encode for transmembrane efflux pumps, whose expression, in theory, should provide bacteria with increased resistance to QAC biocides. Thus, the level of efflux pump activity was assessed through a semi-quantitative method, exposing the isolates to different concentrations of EtBr. A similar approach was previously pursued to study the level of efflux pump activity of multi-drug resistant NTS from food-producing animals and handlers [53]. It was not possible to observe any increase in efflux pump activity when comparing isolates harboring or not harboring the QAC resistance genes and the negative control. Whether these genes are in fact silent or being expressed at low levels should be assessed through finer molecular methodologies in future studies.
Above all, even when increased MIC and MBC values of BKC were reported, the bacterial strains tested were still susceptible to the in-use concentrations [51]. In our study, and despite the presence of QAC resistance genes, the studied isolates were susceptible to the QAC formulation, even at a 10-fold dilution of the lowest in-use concentration. This result is in line with the fact that commercial biocide formulations are established so that the in-use concentration is more than 1000-fold higher than the biocides’ MIC [51]. The concentration of the biocide is one of the factors that can contribute to the development of resistance or reduced susceptibility in bacteria, namely through the application of incorrect dilutions of active substances or formulations [54]. Though such improper dilutions are not likely to be applied in animal husbandry and/or food processing environments, bacteria in natural environments can be exposed to sub-inhibitory concentrations of biocides, as the substances used in the cleaning and disinfection procedures can be washed away and reach waste waters [55]. For Salmonella, it has been shown that exposure to sub-inhibitory concentrations of BKC can lead to increased MIC and MBC values [50,56,57].
Overall, our results highlight the importance of the correct and judicious use of antimicrobial biocides, and the implementation of proper cleaning and disinfection protocols and good hygiene practices in food processing environments, especially in abattoirs, to effectively control Salmonella cross-contamination.

5. Conclusions

The present study reports the susceptibility of NTS isolates from pig carcasses to a QAC-based commercial formulation. The QAC resistance genes qacEΔ1 and qacF were identified among the isolates studied; however, their impact on the susceptibility to the biocide formulation was not fully evaluated under the experimental conditions used, thus further studies should be undertaken to better understand their role. All isolates tested were susceptible to the QAC formulation at concentrations 10 times lower (≈70 mg/L of BKC) than the minimum recommended in-use concentration. The present work brings new insights within the framework of Salmonella control in the pork production chain.

Author Contributions

Conceptualization, M.O. and J.B.C.; methodology, L.L. and V.F.d.S.; software, L.L. and J.B.C.; validation, M.O. and J.B.C.; formal analysis, L.L. and J.B.C.; investigation, L.L. and J.B.C.; resources, V.F.d.S., M.V.-P., M.O. and J.B.C.; data curation, L.L.; writing—original draft preparation, L.L. and J.B.C.; writing—review and editing, M.V.-P., M.O. and J.B.C.; visualization, L.L. and J.B.C.; supervision, J.B.C.; project administration, J.B.C.; funding acquisition, J.B.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by CIISA/FMV Project UID/00276/2025 (https://doi.org/10.54499/UID/00276/2025, accessed on 1 March 2026) and LA/P/0059/2020—AL4AnimalS (both funded by the Portuguese Foundation for Science and Technology-FCT). Participation of Madalena Vieira-Pinto was funded by CECAV Project UID/00772/2025, (https://doi.org/10.54499/UID/00772/2025, accessed on 1 March 2026) funded by FCT.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
PCRPolymerase Chain Reaction

References

  1. Scallan, E.; Hoekstra, R.M.; Angulo, F.J.; Tauxe, R.V.; Widdowson, M.A.; Roy, S.L.; Jones, J.L.; Griffin, P.M. Foodborne Illness Acquired in the United States—Major Pathogens. Emerg. Infect. Dis. 2011, 17, 7–15. [Google Scholar] [CrossRef]
  2. Get the Facts About Salmonella|FDA. Available online: https://www.fda.gov/animal-veterinary/animal-health-literacy/get-facts-about-salmonella (accessed on 16 January 2026).
  3. Scallan Walter, E.J.; Cui, Z.; Tierney, R.; Griffin, P.M.; Hoekstra, R.M.; Payne, D.C.; Rose, E.B.; Devine, C.; Namwase, A.S.; Mirza, S.A.; et al. Foodborne Illness Acquired in the United States—Major Pathogens, 2019. Emerg. Infect. Dis. 2025, 31, 669–677. [Google Scholar] [CrossRef]
  4. European Food Safety Authority (EFSA); European Centre for Disease Prevention and Control (ECDC). The European Union One Health 2024 Zoonoses Report. EFSA J. 2025, 23, e9759. [Google Scholar] [CrossRef]
  5. Kumar, G.; Kumar, S.; Jangid, H.; Dutta, J.; Shidiki, A. The Rise of Non-Typhoidal Salmonella: An Emerging Global Public Health Concern. Front. Microbiol. 2025, 16, 1524287. [Google Scholar] [CrossRef]
  6. Teklemariam, A.D.; Al-Hindi, R.R.; Albiheyri, R.S.; Alharbi, M.G.; Alghamdi, M.A.; Filimban, A.A.R.; Al Mutiri, A.S.; Al-Alyani, A.M.; Alseghayer, M.S.; Almaneea, A.M.; et al. Human Salmonellosis: A Continuous Global Threat in the Farm-to-Fork Food Safety Continuum. Foods 2023, 12, 1756. [Google Scholar] [CrossRef]
  7. Chirwa, E.B.; Dale, H.; Gordon, M.A.; Ashton, P.M. What Is the Source of Infections Causing Invasive Nontyphoidal Salmonella Disease? Open Forum Infect. Dis. 2023, 10, ofad086. [Google Scholar] [CrossRef]
  8. Arya, G.; Holtslander, R.; Robertson, J.; Yoshida, C.; Harris, J.; Parmley, J.; Nichani, A.; Johnson, R.; Poppe, C. Epidemiology, Pathogenesis, Genoserotyping, Antimicrobial Resistance, and Prevention and Control of Non-Typhoidal Salmonella Serovars. Curr. Clin. Microbiol. Rep. 2017, 4, 43–53. [Google Scholar] [CrossRef]
  9. Snyder, T.R.; Boktor, S.W.; M’ikanatha, N.M. Salmonellosis Outbreaks by Food Vehicle, Serotype, Season, and Geographical Location, United States, 1998 to 2015. J. Food Prot. 2019, 82, 1191–1199. [Google Scholar] [CrossRef] [PubMed]
  10. Chanamé Pinedo, L.; Mughini-Gras, L.; Franz, E.; Hald, T.; Pires, S.M. Sources and Trends of Human Salmonellosis in Europe, 2015–2019: An Analysis of Outbreak Data. Int. J. Food Microbiol. 2022, 379, 109850. [Google Scholar] [CrossRef] [PubMed]
  11. Marshall, K.E.; Cui, Z.; Gleason, B.L.; Hartley, C.; Wise, M.E.; Bruce, B.B.; Griffin, P.M. An Approach to Describe Salmonella Serotypes of Concern for Outbreaks: Using Burden and Trajectory of Outbreak-Related Illnesses Associated with Meat and Poultry. J. Food Prot. 2024, 87, 100331. [Google Scholar] [CrossRef]
  12. Roasto, M.; Bonardi, S.; Mäesaar, M.; Alban, L.; Gomes-Neves, E.; Vieira-Pinto, M.; Vågsholm, I.; Elias, T.; Lindegaard, L.L.; Blagojevic, B. Salmonella Enterica Prevalence, Serotype Diversity, Antimicrobial Resistance and Control in the European Pork Production Chain. Trends Food Sci. Technol. 2023, 131, 210–219. [Google Scholar] [CrossRef]
  13. Rincón-Gamboa, S.M.; Poutou-Piñales, R.A.; Carrascal-Camacho, A.K. Antimicrobial Resistance of Non-Typhoid Salmonella in Meat and Meat Products. Foods 2021, 10, 1731. [Google Scholar] [CrossRef]
  14. Bonardi, S. Salmonella in the Pork Production Chain and Its Impact on Human Health in the European Union. Epidemiol. Infect. 2017, 145, 1513–1526. [Google Scholar] [CrossRef] [PubMed]
  15. Buyrukoğlu, G.; Moreira, J.; Topalcengiz, Z. Causal Mediation Analysis of Foodborne Salmonella Outbreaks in the United States: Serotypes and Food Vehicles. Pathogens 2024, 13, 1134. [Google Scholar] [CrossRef]
  16. Abrego, A.; Wiseman, B.; Gragg, S.E. Summarizing the Current Knowledge and Existing Knowledge Gaps for Preharvest and Postharvest Salmonella Contamination in Pork. J. Food Prot. 2025, 88, 100609. [Google Scholar] [CrossRef]
  17. Scharff, R.L. Food Attribution and Economic Cost Estimates for Meat- and Poultry-Related Illnesses. J. Food Prot. 2020, 83, 959–967. [Google Scholar] [CrossRef]
  18. Baptista, F.M.; Halasa, T.; Alban, L.; Nielsen, L.R. Modelling Food Safety and Economic Consequences of Surveillance and Control Strategies for Salmonella in Pigs and Pork. Epidemiol. Infect. 2011, 139, 754–764. [Google Scholar] [CrossRef]
  19. Soliani, L.; Rugna, G.; Prosperi, A.; Chiapponi, C.; Luppi, A. Salmonella Infection in Pigs: Disease, Prevalence, and a Link between Swine and Human Health. Pathogens 2023, 12, 1267. [Google Scholar] [CrossRef]
  20. Carvajal, A.; Kramer, M.; Argüello, H. Salmonella Control in Swine: A Thoughtful Discussion of the Pre- and Post-Harvest Control Approaches in Industrialized Countries. Animals 2024, 14, 1035. [Google Scholar] [CrossRef]
  21. Papoula-Pereira, R.; Alvseike, O.; Cenci-Goga, B.T.; Grispoldi, L.; Nagel-Alne, G.E.; Ros-Lis, J.V.; Thomas, L.F. Economic Evidence for the Control of Salmonella in Animal-Derived Food Systems: A Scoping Review. Food Control 2025, 175, 111275. [Google Scholar] [CrossRef]
  22. FAO; WHO. Interventions for the Control of Non-Typhoidal Salmonella spp. in Beef and Pork: Meeting Report and Systematic Review; Microbiological Risk Assessment Series No. 30; WHO: Rome, Italy, 2016; 276p. [Google Scholar]
  23. Koutsoumanis, K.; Allende, A.; Bolton, D.; Bover-Cid, S.; Chemaly, M.; De Cesare, A.; Herman, L.; Hilbert, F.; Lindqvist, R.; Nauta, M.; et al. Persistence of Microbiological Hazards in Food and Feed Production and Processing Environments. EFSA J. 2024, 22, e8521. [Google Scholar] [CrossRef] [PubMed]
  24. Larsen, M.H.; Dalmasso, M.; Ingmer, H.; Langsrud, S.; Malakauskas, M.; Mader, A.; Møretrø, T.; Smole Možina, S.; Rychli, K.; Wagner, M.; et al. Persistence of Foodborne Pathogens and Their Control in Primary and Secondary Food Production Chains. Food Control 2014, 44, 92–109. [Google Scholar] [CrossRef]
  25. Møretrø, T.; Heir, E.; Nesse, L.L.; Vestby, L.K.; Langsrud, S. Control of Salmonella in Food Related Environments by Chemical Disinfection. Food Res. Int. 2012, 45, 532–544. [Google Scholar] [CrossRef]
  26. Donaghy, J.A.; Jagadeesan, B.; Goodburn, K.; Grunwald, L.; Jensen, O.N.; Jespers, A.; Kanagachandran, K.; Lafforgue, H.; Seefelder, W.; Quentin, M.C. Relationship of Sanitizers, Disinfectants, and Cleaning Agents with Antimicrobial Resistance. J. Food Prot. 2019, 82, 889–902. [Google Scholar] [CrossRef]
  27. Gerba, C.P. Quaternary Ammonium Biocides: Efficacy in Application. Appl. Environ. Microbiol. 2015, 81, 464–469. [Google Scholar] [CrossRef] [PubMed]
  28. Lu, Z.; Mahony, A.K.; Arnold, W.A.; Marshall, C.W.; McNamara, P.J. Quaternary Ammonia Compounds in Disinfectant Products: Evaluating the Potential for Promoting Antibiotic Resistance and Disrupting Wastewater Treatment Plant Performance. Environ. Sci. Adv. 2024, 3, 208–226. [Google Scholar] [CrossRef]
  29. Maillard, J.-Y. Resistance of Bacteria to Biocides. Microbiol. Spectr. 2018, 6, 10-1128. [Google Scholar] [CrossRef]
  30. Hegstad, K.; Langsrud, S.; Lunestad, B.T.; Scheie, A.A.; Sunde, M.; Yazdankhah, S.P. Does the Wide Use of Quaternary Ammonium Compounds Enhance the Selection and Spread of Antimicrobial Resistance and Thus Threaten Our Health? Microb. Drug Resist. 2010, 16, 91–104. [Google Scholar] [CrossRef]
  31. Jaglic, Z.; Cervinkova, D. Genetic Basis of Resistance to Quaternary Ammonium Compounds—The Qac Genes and Their Role: A Review. Veterinární Medicína 2012, 57, 275–281. [Google Scholar] [CrossRef]
  32. McCarlie, S.M.; Staats, G.; Belter, B.; Van Der Walt, B.; Bragg, R. Molecular Tools for the Study of Resistance to Disinfectants. In Global Antimicrobial Resistance Epidemic—Innovative. Approaches and Cutting-Edge Solutions; Téllez-Isaías, G., Ed.; IntechOpen: London, UK, 2022. [Google Scholar] [CrossRef]
  33. Cota, J.B.; da Silva, V.F.; Chambel, L.; Veloso, M.G.; Vieira-Pinto, M.; Oliveira, M. Pheno and Genotyping of Salmonella from Slaughtered Pigs in a Portuguese Abattoir Reveal Differential Persistence Ability. Vet. Microbiol. 2019, 239, 108457. [Google Scholar] [CrossRef] [PubMed]
  34. ISO 6579:2002; Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for the Detection of Salmonella spp. International Organization for Standardization (ISO): Geneva, Switzerland, 2002.
  35. CDC (Centers for Disease Control and Prevention). Standard Operating Procedure for PulseNet PFGE of Escherichia coli O157:H7, Escherichia coli Non-O157 (STEC), Salmonella Serotypes, Shigella sonnei and Shigella flexneri. 2013. Available online: https://www.pulsenetinternational.org/protocols/pfge (accessed on 2 September 2018).
  36. Moore, E.; Arnscheidt, A.; Krüger, A.; Strömpl, C.; Mau, M. Section 1 Update: Simplified Protocols for the Preparation of Genomic DNA from Bacterial Cultures. Mol. Microb. Ecol. Man. 2004, 1, 1905–1919. [Google Scholar] [CrossRef]
  37. Zou, L.; Meng, J.; McDermott, P.F.; Wang, F.; Yang, Q.; Cao, G.; Hoffmann, M.; Zhao, S. Presence of Disinfectant Resistance Genes in Escherichia coli Isolated from Retail Meats in the USA. J. Antimicrob. Chemother. 2014, 69, 2644–2649. [Google Scholar] [CrossRef] [PubMed]
  38. EN 1656:2009; Chemical Disinfectants and Antiseptics—Quantitative Suspension Test for the Evaluation of Bactericidal Activity of Chemical Disinfectants and Antiseptics Used in the Veterinary Area—Test Method and Requirements (Phase 2, Step 1). CEN-CENELEC Management Centre: Brussels, Belgium, 2009.
  39. Martins, M.; McCusker, M.P.; Viveiros, M.; Couto, I.; Fanning, S.; Pagès, J.-M.; Amaral, L. A Simple Method for Assessment of MDR Bacteria for Over-Expressed Efflux Pumps. Open Microbiol. J. 2013, 7, 72. [Google Scholar] [CrossRef]
  40. Kazama, H.; Hamashima, H.; Sasatsu, M.; Arai, T. Distribution of the Antiseptic-Resistance Genes QacE and QacE Delta 1 in Gram-Negative Bacteria. FEMS Microbiol. Lett. 1998, 159, 173–178. [Google Scholar] [CrossRef] [PubMed]
  41. Vilela, F.P.; Falcão, J.P.; Campioni, F. Analysis of Resistance Gene Prevalence in Whole-Genome Sequenced Enterobacteriales from Brazil. Microb. Drug Resist. 2020, 26, 594–604. [Google Scholar] [CrossRef]
  42. Buffet-Bataillon, S.; Tattevin, P.; Bonnaure-Mallet, M.; Jolivet-Gougeon, A. Emergence of Resistance to Antibacterial Agents: The Role of Quaternary Ammonium Compounds—A Critical Review. Int. J. Antimicrob. Agents 2012, 39, 381–389. [Google Scholar] [CrossRef]
  43. Chuanchuen, R.; Khemtong, S.; Padungtod, P. Occurrence of qacE/qacEDelta1 Genes and Their Correlation with Class 1 Integrons in Salmonella enterica Isolates from Poultry and Swine. Southeast Asian J. Trop. Med. Public Health 2007, 38, 855–862. [Google Scholar]
  44. Gillings, M.; Boucher, Y.; Labbate, M.; Holmes, A.; Krishnan, S.; Holley, M.; Stokes, H.W. The Evolution of Class 1 Integrons and the Rise of Antibiotic Resistance. J. Bacteriol. 2008, 190, 5095–5100. [Google Scholar] [CrossRef]
  45. Caleja, C.; de Toro, M.; Gonçalves, A.; Themudo, P.; Vieira-Pinto, M.; Monteiro, D.; Rodrigues, J.; Sáenz, Y.; Carvalho, C.; Igrejas, G.; et al. Antimicrobial Resistance and Class I Integrons in Salmonella enterica Isolates from Wild Boars and Bísaro Pigs. Int. Microbiol. 2011, 14, 19–24. [Google Scholar] [CrossRef]
  46. Ploy, M.C.; Courvalin, P.; Lambert, T. Characterization of In40 of Enterobacter aerogenes BM2688, a Class 1 Integron with Two New Gene Cassettes, cmlA2 and qacF. Antimicrob. Agents Chemother. 1998, 42, 2557–2563. [Google Scholar] [CrossRef]
  47. Chen, Y.; Liu, L.; Guo, Y.; Chu, J.; Wang, B.; Sui, Y.; Wei, H.; Hao, H.; Huang, L.; Cheng, G. Distribution and Genetic Characterization of Fluoroquinolone Resistance Gene qnr among Salmonella Strains from Chicken in China. Microbiol. Spectr. 2024, 12, e0300023. [Google Scholar] [CrossRef]
  48. Long, M.; Lai, H.; Deng, W.; Zhou, K.; Li, B.; Liu, S.; Fan, L.; Wang, H.; Zou, L. Disinfectant Susceptibility of Different Salmonella Serotypes Isolated from Chicken and Egg Production Chains. J. Appl. Microbiol. 2016, 121, 672–681. [Google Scholar] [CrossRef]
  49. Deng, W.; Quan, Y.; Yang, S.; Guo, L.; Zhang, X.; Liu, S.; Chen, S.; Zhou, K.; He, L.; Li, B.; et al. Antibiotic Resistance in Salmonella from Retail Foods of Animal Origin and Its Association with Disinfectant and Heavy Metal Resistance. Microb. Drug Resist. 2018, 24, 782–791. [Google Scholar] [CrossRef]
  50. Knapp, L.; Amézquita, A.; McClure, P.; Stewart, S.; Maillard, J.Y. Development of a Protocol for Predicting Bacterial Resistance to Microbicides. Appl. Environ. Microbiol. 2015, 81, 2652–2659. [Google Scholar] [CrossRef] [PubMed]
  51. Maillard, J.Y. Impact of Benzalkonium Chloride, Benzethonium Chloride and Chloroxylenol on Bacterial Antimicrobial Resistance. J. Appl. Microbiol. 2022, 133, 3322–3346. [Google Scholar] [CrossRef] [PubMed]
  52. Chen, S.; Fu, J.; Zhao, K.; Yang, S.; Li, C.; Penttinen, P.; Ao, X.; Liu, A.; Hu, K.; Li, J.; et al. Class 1 Integron Carrying qacEΔ1 Gene Confers Resistance to Disinfectant and Antibiotics in Salmonella. Int. J. Food Microbiol. 2023, 404, 110319. [Google Scholar] [CrossRef]
  53. Olubisose, E.T.; Ajayi, A.; Adeleye, A.I.; Smith, S.I. Molecular and Phenotypic Characterization of Efflux Pump and Biofilm in Multi-Drug Resistant Non-Typhoidal Salmonella Serovars Isolated from Food Animals and Handlers in Lagos Nigeria. One Heal. Outlook 2021, 3, 2. [Google Scholar] [CrossRef]
  54. Maillard, J.Y.; Bloomfield, S.; Coelho, J.R.; Collier, P.; Cookson, B.; Fanning, S.; Hill, A.; Hartemann, P.; McBain, A.J.; Oggioni, M.; et al. Does Microbicide Use in Consumer Products Promote Antimicrobial Resistance? A Critical Review and Recommendations for a Cohesive Approach to Risk Assessment. Microb. Drug Resist. 2013, 19, 344–354. [Google Scholar] [CrossRef] [PubMed]
  55. Sousa, M.; Machado, I.; Simões, L.C.; Simões, M. Biocides as Drivers of Antibiotic Resistance: A Critical Review of Environmental Implications and Public Health Risks. Environ. Sci. Ecotechnology 2025, 25, 100557. [Google Scholar] [CrossRef]
  56. Chuanchuen, R.; Pathanasophon, P.; Khemtong, S.; Wannaprasat, W.; Padungtod, P. Susceptibilities to Antimicrobials and Disinfectants in Salmonella Isolates Obtained from Poultry and Swine in Thailand. J. Vet. Med. Sci. 2008, 70, 595–601. [Google Scholar] [CrossRef]
  57. Nhung, N.T.; Thuy, C.T.; Trung, N.V.; Campbell, J.; Baker, S.; Thwaites, G.; Hoa, N.T.; Carrique-Mas, J. Induction of Antimicrobial Resistance in Escherichia coli and Non-Typhoidal Salmonella Strains after Adaptation to Disinfectant Commonly Used on Farms in Vietnam. Antibiotics 2015, 4, 480–494. [Google Scholar] [CrossRef] [PubMed]
Table 1. Detection of the QAC resistance genes qacEΔ1, qacE and qacF by PCR amplification in the Salmonella isolates under study and corresponding resistance genotype.
Table 1. Detection of the QAC resistance genes qacEΔ1, qacE and qacF by PCR amplification in the Salmonella isolates under study and corresponding resistance genotype.
Isolate qacEΔ1qacEqacFGenotypeCluster Serotype
p1 −−−−IA Rissen
p3 −−−−IA
p4 −−−−IA
p5 −−−−IA
p58 −−−−IA
p116−−−−IA
ci57 −−−−IA
p25 −−+qacFIB Rissen
p31 −−+qacFIB
p61−−+qacFIB
p62 −−+qacFIB
p64+−+qacEΔ1/qacFIB
ce21+−+qacEΔ1/qacFIB
ce37+−+qacEΔ1/qacFIB
ce44 −−+qacFIB
ci21 +−+qacEΔ1/qacFIB
ci55−−−−IB
p55 +−-qacEΔ1IIA 4,[5],12:i:-
p56 −−−−IIA
p96 −−−−IIB 4,[5],12:i:-
p104 −−−−IIB
p106 +−+qacEΔ1/qacFIIB
p107 −−−−IIB
p109 +−+qacEΔ1/qacFIIB
p110 −−−−IIB
p112 −−−−IIB
p114 −−−−IIB
p115 −−−−IIB
p118−−−−IIB
ci104+−+qacEΔ1/qacFIIB
ci105−−−−IIB
ci108−−−−IIB
ci109−−−−IIB
ci110−−−−IIB
ci111−−−−IIB
ci115−−−−IIB
ci116−−−−IIB
ci117+−−qacEΔ1IIB
p66 +−−qacEΔ1III Derby
p67 +−−qacEΔ1III
p68 +−−qacEΔ1III
ce70 +−−qacEΔ1III
ci68 +−−qacEΔ1III
ci38 −−+qacFind Rissen
“p”—isolates from pig skin before scalding; “ci”—isolates from the internal surface of the carcass; “ce”—isolates that came from the external surface of the carcass; “+”—positive; “−”—negative; IA and IB—genomic clusters associated with Rissen serotype; IIA and IIB—genomic clusters associated with Typhimurium from monophasic variant (4,[5],12:i:-); III—genomic cluster associated with Derby serotype; ind—independent genomic cluster [33].
Table 2. Suma Bac D10® MIC and MBC medium values for the selected isolates under different testing conditions—no interfering substance (NIS), low interfering substance (LIS) and high interfering substance (HIS).
Table 2. Suma Bac D10® MIC and MBC medium values for the selected isolates under different testing conditions—no interfering substance (NIS), low interfering substance (LIS) and high interfering substance (HIS).
IsolateSerotypeQAC Resistance GenotypeCluster MIC (%) MBC (%)
NISLISHISNISLISHIS
p1 Rissen−IA<0.100<0.100<0.1000.1000.1000.100
ce21 RissenqacEΔ1/qacFIB<0.100<0.100<0.1000.1000.1000.100
ce37 RissenqacEΔ1/qacFIB<0.100<0.100<0.1000.1000.1000.100
ci21 RissenqacEΔ1/qacFIB<0.100<0.100<0.1000.1000.1000.100
p64 RissenqacEΔ1/qacFIB<0.100<0.100<0.1000.1000.1000.100
p55 4,[5],12:i:-qacEΔ1IIA<0.100<0.100<0.1000.1000.1000.100
p56 4,[5],12:i:-−IIA<0.100<0.100<0.1000.1000.1000.100
ci104 4,[5],12:i:-qacEΔ1/qacFIIB<0.100<0.100<0.1000.1000.1000.100
ci117 4,[5],12:i:-qacEΔ1IIB<0.100<0.100<0.1000.1000.1000.100
p109 4,[5],12:i:-qacEΔ1/qacFIIB<0.100<0.100<0.1000.1000.1000.100
ce70 DerbyqacEΔ1III<0.100<0.100<0.1000.1000.1000.100
ci38 RissenqacFind<0.100<0.100<0.1000.1000.1000.100
x−−−−0.1000.1000.1000.1000.1000.100
σ−−−0.0000.0000.0000.0000.0000.000
NIS—no interfering substance; LIS—low interfering substance; HIS—high interfering substance; x−—mean; σ—standard deviation. “p”—isolates from pig skin before scalding; “ci”—isolates from the internal surface of the carcass; “ce”—isolates that came from the external surface of the carcass; “−”—negative; IA and IB—genomic clusters associated with Rissen serotype; IIA and IIB—genomic clusters associated with Typhimurium from monophasic variant (4,[5],12:i:-); III—genomic cluster associated Derby serotype; ind—independent genomic cluster [33].
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Lourenço, L.; Silva, V.F.d.; Vieira-Pinto, M.; Oliveira, M.; Cota, J.B. Quaternary Ammonium Biocide Resistance in Non-Typhoidal Salmonella from Pig Carcasses. Vet. Sci. 2026, 13, 247. https://doi.org/10.3390/vetsci13030247

AMA Style

Lourenço L, Silva VFd, Vieira-Pinto M, Oliveira M, Cota JB. Quaternary Ammonium Biocide Resistance in Non-Typhoidal Salmonella from Pig Carcasses. Veterinary Sciences. 2026; 13(3):247. https://doi.org/10.3390/vetsci13030247

Chicago/Turabian Style

Lourenço, Lorina, Vanessa Ferreira da Silva, Madalena Vieira-Pinto, Manuela Oliveira, and João B. Cota. 2026. "Quaternary Ammonium Biocide Resistance in Non-Typhoidal Salmonella from Pig Carcasses" Veterinary Sciences 13, no. 3: 247. https://doi.org/10.3390/vetsci13030247

APA Style

Lourenço, L., Silva, V. F. d., Vieira-Pinto, M., Oliveira, M., & Cota, J. B. (2026). Quaternary Ammonium Biocide Resistance in Non-Typhoidal Salmonella from Pig Carcasses. Veterinary Sciences, 13(3), 247. https://doi.org/10.3390/vetsci13030247

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop