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Salmonella and Salmonellosis: Implications in Public Health

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A special issue of Animals (ISSN 2076-2615). This special issue belongs to the section "Animal System and Management".

Deadline for manuscript submissions: closed (31 December 2024) | Viewed by 32370

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Special Issue Editors

Prof. Dr. Rafael Jesús Astorga

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Guest Editor

Animal Health Department, Veterinary Faculty, University of Cordoba, Cordoba, Spain
Interests: Salmonella and salmonellosis; food-borne pathogens; antimicrobial resistance; zoonoses; emergence diseases

Dr. Angela Galán Relaño

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Guest Editor

Department of Nursing, Pharmacology and Physiotherapy, Pharmacology Area, University of Córdoba, Córdoba, Spain
Interests: domestic and wild animal infectious diseases; antimicrobial resistance; genetic analysis; food-borne pathogens; zoonoses

Prof. Dr. Antonio Valero Díaz

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Guest Editor

Food Science and Technology Department, Veterinary Faculty, University of Cordoba, Cordoba, Spain
Interests: predictive microbiology models; quantitative microbial risk assessment; antimicrobial resistance; food shelf-life; biopreservation
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Salmonella is one of the most important zoonotic pathogen agents causing an estimated number of 93.8 million cases of gastroenteritis worldwide annually, with 155,000 deaths. Efforts to reduce transmission of Salmonella by food and other routes must be implemented on a global scale.

Salmonellosis control strategies are based on two fundamental aspects: (a) the reduction of prevalence levels in animals, and (b) the protection of infection in humans. For that reason, this Special Issue will be focused on Salmonella and its relationship between Animal and Public Health. The Issue scope must be Salmonella and salmonellosis along the food-borne chain, from farm to fork. And the aim is to update the status of Salmonella in the world with special reference to its implications on Public Health.

We strongly believe that this Issue can be an opportunity to collect significant and relevant information with an integral approach on Animal Health, on Public Health and the relationship between both.

The topics of this Special Issue include, but are not limited to:

1) Interactions between Salmonella, hosts, and microbiota.
2) New tools for Salmonella detection, characterization and typing.
3) Whole genome sequencing and comparative genomics.
4) Ecology and epidemiology along the food chain.
5) Risk assessment and control strategies.
6) Epidemiology and Public Health.
7) Control and prevention of Salmonella; feeding and non-feeding strategies.
8) Salmonella and biosecurity.
9) New vaccine candidates.

Prof. Dr. Rafael Jesús Astorga
Dr. Angela Galán Relaño
Prof. Dr. Antonio Valero Díaz
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Animals is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2400 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

Salmonella and salmonellosis
characterization and typing
epidemiology and public health
food chain
antimicrobial resistance
risk assessment
control strategies
one health

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Published Papers (11 papers)

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Research

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10 pages, 613 KiB

Open AccessArticle

Phenotypic and Genomic Assessment of Antimicrobial Resistance and Virulence Factors Determinants in Salmonella Heidelberg Isolated from Broiler Chickens

by Arthur de Almeida Figueira, Thomas Salles Dias, Gisllany Alves Costa, Dayse Lima da Costa Abreu, Luciana dos Santos Medeiros and Virginia Léo de Almeida Pereira

Animals 2025, 15(7), 1003; https://doi.org/10.3390/ani15071003 - 30 Mar 2025

Viewed by 426

Abstract

Salmonella Heidelberg is frequently found in poultry and poultry products and is associated with antimicrobial resistance strains and infections and mortality in humans. Whole-genome sequencing is used to monitor and understand epidemiological factors related to antimicrobial resistance. This study aimed to characterize the phenotypic resistance and sequence the whole genome of Salmonella Heidelberg strains isolated from poultry products in Brazil. Fourteen Salmonella Heidelberg strains isolated from whole broiler chicken carcasses and portions in Brazil between 2013 and 2019 were used in this study. Genus confirmation was performed by polymerase chain reaction. The disk diffusion test was conducted to assess the phenotypical antimicrobial susceptibility of the strains. Whole-genome sequencing was carried out to investigate the presence of antimicrobial resistance genes, plasmids, multilocus sequence typing, and virulence-associated genes. A high frequency of phenotypic resistance to cephalosporins, tetracyclines, and sulfonamides was detected. All strains had mutations in gyrA and parC and contained the genes tet(A), fosA7, and sul. The presence of genes originating from Yersinia pathogenicity islands was also detected. This study identified a high frequency of antimicrobial resistance in Salmonella Heidelberg strains from broilers slaughtered in different regions of Brazil, all belonging to the same sequence type (ST15) and associated with multiple resistance and virulence genes. The presence of the Yersinia high-pathogenicity island was detected, indicating potential virulence. These findings highlight the importance of continuously monitoring antimicrobial resistance to control and prevent foodborne infections and maintain the efficacy of treatments for human salmonellosis. Full article

(This article belongs to the Special Issue Salmonella and Salmonellosis: Implications in Public Health)

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17 pages, 2331 KiB

Open AccessArticle

miR-215 Modulates Ubiquitination to Impair Inflammasome Activation and Autophagy During Salmonella Typhimurium Infection in Porcine Intestinal Cells

by Carmen Entrenas-García, José M. Suárez-Cárdenas, Raúl Fernández-Rodríguez, Rocío Bautista, M. Gonzalo Claros, Juan J. Garrido and Sara Zaldívar-López

Animals 2025, 15(3), 431; https://doi.org/10.3390/ani15030431 - 4 Feb 2025

Viewed by 1022

Abstract

The host response to S. Typhimurium infection can be post-transcriptionally regulated by miRNAs. In this study, we investigated the role of miR-215 using both in vivo porcine infection models and in vitro intestinal epithelial cell lines. Several miRNAs were found to be dysregulated in the porcine ileum during infection with wild-type and SPI2-defective mutant strains of S. Typhimurium, with some changes being SPI2-dependent. Notably, miR-215 was significantly downregulated during infection. To explore its functional role, gain-of-function experiments were performed by transfecting porcine intestinal epithelial cells (IPEC-J2) with a miR-215-5p mimic, followed by label-free quantitative (LFQ) proteomic analysis. This analysis identified 157 proteins, of which 35 were downregulated in response to miR-215 overexpression, suggesting they are potential targets of this miRNA. Among these, E2 small ubiquitin-like modifier (SUMO)-conjugating enzyme UBC9 and E3 ubiquitin-ligase HUWE1 were identified as key targets, both of which are upregulated during S. Typhimurium infection. The miR-215-mediated downregulation of these proteins resulted in a significant decrease in overall ubiquitination, a process crucial for regulating inflammasome activation and autophagy. Consistently, inflammasome markers caspase 1 (CASP1) and apoptosis-associated speck-like protein containing a CARD (ASC), as well as autophagy markers microtubule-associated protein 1A/1B-light chain 3 (LC3B) and Ras-related protein Rab-11 (RAB11A), showed decreased expression in miR-215 mimic-transfected and infected IPEC-J2 cells. To further validate these findings, human intestinal epithelial cells (HT29) were used as a complementary model, providing additional insights into conserved immune pathways and extending the observations made in the porcine system. Overall, our findings demonstrate that miR-215 plays a significant role in modulating host inflammasome activation and autophagy by targeting proteins involved in ubiquitination during S. Typhimurium infection. Full article

(This article belongs to the Special Issue Salmonella and Salmonellosis: Implications in Public Health)

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12 pages, 5150 KiB

Open AccessFeature PaperArticle

Integron-Mediated Antimicrobial Resistance and Virulence Factors in Salmonella Typhimurium Isolated from Poultry

by Elizabeth Kim, Nora Jean Nealon, Katherine A. Murray, Cydney Jardine, Roberta Magnuson and Sangeeta Rao

Animals 2024, 14(23), 3483; https://doi.org/10.3390/ani14233483 - 2 Dec 2024

Viewed by 1680

Abstract

This study investigates antimicrobial-resistant (AMR) Salmonella Typhimurium in poultry, focusing on how class I integrons contribute to AMR and virulence. Using whole genome sequencing, researchers analyzed 26 S. Typhimurium isolates from U.S. poultry, finding that three isolates contained integrons (1000 base pairs each). These integron-positive isolates exhibited significantly higher resistance to beta-lactams, phenicols, and tetracyclines compared to integron-free isolates (p = 0.004, 0.009, and 0.02, respectively) and harbored genes like ges, imp, and oxa, which are linked to extended-spectrum beta-lactamase resistance. Most AMR gene classes (64%) were chromosome-based, with integron-positive isolates showing a broader array of resistance genes, including catB and tetA. Integron-bearing isolates had higher occurrences of bacteriocin genes and specific AMR genes like aminoglycoside and beta-lactam resistance genes, while integron-free isolates had more fimbrial and pilus genes. The presence of integrons may trend with increased AMR genes and virulence factors, highlighting the role of integron screening in enhancing AMR surveillance and reducing the need for high-priority antimicrobial treatments in poultry. These findings could support better AMR stewardship practices in poultry production, potentially lowering infection risks in humans and livestock. Full article

(This article belongs to the Special Issue Salmonella and Salmonellosis: Implications in Public Health)

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11 pages, 1784 KiB

Open AccessFeature PaperArticle

Post-Antibiotic and Post-Antibiotic Sub-Minimum Inhibitory Concentration Effects of Carvacrol against Salmonella Typhimurium

by Eva Boyer, Ángela Galán-Relaño, Antonio Romero-Salmoral, Paula Barraza, Lidia Gómez-Gascón, Carmen Tarradas, Inmaculada Luque, Fabiana Carolina de Aguiar and Belén Huerta Lorenzo

Animals 2024, 14(18), 2631; https://doi.org/10.3390/ani14182631 - 11 Sep 2024

Viewed by 1166

Abstract

Carvacrol is a compound present in essential oils with proven antimicrobial activity against numerous pathogens. We firstly determine the post-antibiotic effect (PAE) of carvacrol (1×, 2×, 4× MIC) and post-antibiotic sub-minimum inhibitory concentration (MIC) effect (1× + 0.25× MIC and 2× + 0.25× MIC) for two concentrations of Salmonella Typhimurium ATCC14028 (10⁶ and 10⁸ CFU/mL). Prior to testing, the minimum concentration and exposure time to achieve the bacterial inhibition (MIC 0.6 mg/mL and 10 min) were determined by broth microdilution and time–kill curve methods, respectively. At the MIC, carvacrol did not generate any PAE. At twice the MIC, the PAE was 2 h with the standard inoculum (10⁶ CFU/mL) and 1 h with the high-density inoculum (10⁸ CFU/mL). At 4× MIC concentrations, the PAE was higher in both cases > 43.5 h. Continuous exposure of post-antibiotic phase bacteria (1× and 2× MIC) to carvacrol at 0.25× MIC (0.15 mg/mL) resulted in an increase in PAE (PA-SME) above 43.5 h with both inocula. These results suggest that the PA-SME of carvacrol for S. Typhimurium can be significantly prolonged by increasing the sub-MICs, which would allow dose spacing, reduce adverse effects and improve its efficacy in the treatment of infected animals and as a disinfectant in agri-food facilities. Full article

(This article belongs to the Special Issue Salmonella and Salmonellosis: Implications in Public Health)

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12 pages, 956 KiB

Open AccessArticle

Limited Emergence of Salmonella enterica Serovar Infantis Variants with Reduced Phage Susceptibility in PhagoVet-Treated Broilers

by Sandra Sevilla-Navarro, Jennifer Otero, Júlia López-Pérez, Jan Torres-Boncompte, Tiago Prucha, Maarten De Gussem, Daniela Silva, Julia Burgan, Pablo Catalá-Gregori, Pilar Cortés and Montserrat Llagostera

Animals 2024, 14(16), 2352; https://doi.org/10.3390/ani14162352 - 14 Aug 2024

Cited by 1 | Viewed by 1129

Abstract

Salmonella enterica serovar Infantis (S. Infantis) poses a growing issue in the poultry sector, with phage-based products emerging as a safe and effective control measure. This study investigated the emergence of reduced-phage-susceptibility variants (RPSV) of S. Infantis in PhagoVet-treated broilers, given that RPSV could undermine phage treatment efficacy. The bacteriophages in the PhagoVet product were characterized using transmission electron microscopy (TEM), genome sequencing, and infection profiling. Furthermore, two broiler trials were conducted: a challenge group (T1) and a challenge-and-treated group (T2). The S. Infantis infective dose was set at 10⁴ and 10⁶ colony-forming units (CFUs) per animal, with PhagoVet administration at 10⁶ and 10⁸ plaque-forming units (PFUs) per animal, in Trials 1 and 2, respectively. The results revealed that the four PhagoVet bacteriophages belonged to different genera. PhagoVet evidenced broad-spectrum efficacy against 271 strains representing 18 Salmonella serovars. In Trial 1, PhagoVet reduced bacterial counts in feces to nearly undetectable levels by day 42, with no RPSV detected. However, in Trial 2, three and five RPSVs were detected in feces and ceca, respectively. Consequently, PhagoVet demonstrated efficacy against S. Infantis in broilers, and the potential impact of RPSV is deemed unlikely to compromise its efficacy. Full article

(This article belongs to the Special Issue Salmonella and Salmonellosis: Implications in Public Health)

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17 pages, 2485 KiB

Open AccessArticle

Risk Factors for Salmonella Detection in Commercial Layer Flocks in Spain

by Clara Samper-Cativiela, Maria Esther Prieto, Soledad Collado, Cristina De Frutos, Adam J. Branscum, Jose Luis Saez and Julio Alvarez

Animals 2023, 13(20), 3181; https://doi.org/10.3390/ani13203181 - 12 Oct 2023

Cited by 3 | Viewed by 1829

Abstract

Trends in Salmonella human infections are assumed to be related to the distribution of the pathogen in the animal reservoir/food products, and cases in humans are most often linked to poultry and poultry products (eggs, meat). Therefore, ongoing Salmonella national control programs (NCPs) in European Union Member States have the objective of monitoring and reducing its prevalence in commercial poultry flocks. Results from NCPs have shown certain factors (housing systems, season of sampling and if sampling is conducted by food business operators (FBOps) or competent authorities (CAs), among others) can influence detection rates, but associations are often not consistent. Here, we analyzed data from the Spanish NCP on 7216 laying hen flocks subjected to 36,193 sampling events over a six-year period to characterize its performance and identify variables influencing detection rates. Overall, 1205 sampling events were positive for Salmonella spp. (any serovar) and 132 for S. Enteritidis-S. Typhimurium/monophasic. Bayesian multivariable models adjusting for multiple covariates concluded that sampling events later in the year, in caged flocks with older animals and conducted by CAs had increased odds of positivity for Salmonella spp., revealing aspects linked with a differential estimation of Salmonella levels in laying hen flocks. Full article

(This article belongs to the Special Issue Salmonella and Salmonellosis: Implications in Public Health)

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Review

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27 pages, 920 KiB

Open AccessReview

Pre-Harvest Non-Typhoidal Salmonella Control Strategies in Commercial Layer Chickens

by Roshen N. Neelawala, Lekshmi K. Edison and Subhashinie Kariyawasam

Animals 2024, 14(24), 3578; https://doi.org/10.3390/ani14243578 - 11 Dec 2024

Cited by 2 | Viewed by 2098

Abstract

Non-typhoidal Salmonella (NTS) infections in poultry, particularly in commercial-layer chickens, pose a critical risk to food safety and public health worldwide. NTS bacteria can remain undetected in poultry flocks, contaminating products and potentially leading to gastroenteritis in humans. This review examines pre-harvest control strategies for NTS in layer chickens, including biosecurity protocols, vaccinations, feed additives, genetic selection, and environmental management. These strategies have substantially reduced Salmonella colonization and product contamination rates in the commercial layer industry. By evaluating these strategies, this review highlights the importance of integrated control measures to limit NTS colonization, reduce antimicrobial resistance, and improve poultry health. This review aims to provide producers, researchers, and policymakers with insights into effective practices to minimize Salmonella contamination and enhance both animal and human health outcomes. Full article

(This article belongs to the Special Issue Salmonella and Salmonellosis: Implications in Public Health)

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13 pages, 1557 KiB

Open AccessReview

Scoping Review About Salmonella spp. in Colombian Pig Farms from 2009 to Mid-2024

by Adriana Pulido-Villamarín, Iliana Chamorro-Tobar, Ana K. Carrascal-Camacho, Fernando Sampedro, Marcela Rodríguez-Moreno, Fernando Rojas-Bermúdez, Mónica Pérez-Vargas, Ivonne Hernández-Toro, Alejandra Camacho-Carrillo and Raúl A. Poutou-Piñales

Animals 2024, 14(23), 3542; https://doi.org/10.3390/ani14233542 - 8 Dec 2024

Viewed by 1041

Abstract

In Colombia, research on Salmonella concerning animal health, veterinary diagnostics, and epidemiology within the primary production chain is limited. This study aimed to analyze the published data about Salmonella in the Colombian primary pig production chain from 2009 to mid-2024. This involved an exploratory literature review using systematic search strategies, including articles, graduate studies, conference presentations, and technical reports from the selected period. Of the 35 studies reviewed, 30 met the inclusion criteria, with eleven being from the grey literature. The pooled prevalence of Salmonella spp. on Colombian farms was 8.9%, while the seroprevalence ranged from 27 to 40%. Risk factors associated with the presence of this bacterium on farms included aspects such as water sources, pest control, the farm type, and management practices. Few scientific publications address the presence of this pathogen in primary pig production in Colombia, underscoring the need to raise awareness within the academic and production communities about the importance of conducting and reporting new studies and cases. Full article

(This article belongs to the Special Issue Salmonella and Salmonellosis: Implications in Public Health)

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15 pages, 747 KiB

Open AccessFeature PaperReview

Salmonella Control in Swine: A Thoughtful Discussion of the Pre- and Post-Harvest Control Approaches in Industrialized Countries

by Ana Carvajal, Melvin Kramer and Héctor Argüello

Animals 2024, 14(7), 1035; https://doi.org/10.3390/ani14071035 - 28 Mar 2024

Cited by 3 | Viewed by 2574

Abstract

Pork is among the major sources of human salmonellosis in developed countries. Since the 1990s, different surveys and cross-sectional studies, both national and international (i.e., the baseline studies performed in the European Union), have revealed and confirmed the widespread non-typhoidal Salmonella serotypes in pigs. A number of countries have implemented control programs with different approaches and degrees of success. The efforts could be implemented either at farms, in post-harvest stages, or both. The current review revises the current state of the art in Salmonella in swine, the control programs ongoing or conducted in the past, and their strengths and failures, with particular attention to the weight of pre- and post-harvest control and the implications that both have for the success of interventions or mitigation after outbreaks. This review provides a novel perspective on Salmonella control in swine, a matter that still includes uncertainties and room for improvement as a question of public health and One Health. Full article

(This article belongs to the Special Issue Salmonella and Salmonellosis: Implications in Public Health)

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22 pages, 1153 KiB

Open AccessReview

Phage-Based Biosanitation Strategies for Minimizing Persistent Salmonella and Campylobacter Bacteria in Poultry

by Jaume Jordá, Laura Lorenzo-Rebenaque, Laura Montoro-Dasi, Ana Marco-Fuertes, Santiago Vega and Clara Marin

Animals 2023, 13(24), 3826; https://doi.org/10.3390/ani13243826 - 12 Dec 2023

Cited by 5 | Viewed by 3869

Abstract

Control strategies to minimize pathogenic bacteria in food animal production are one of the key components in ensuring safer food for consumers. The most significant challenges confronting the food industry, particularly in the major poultry and swine sectors, are antibiotic resistance and resistance to cleaning and disinfection in zoonotic bacteria. In this context, bacteriophages have emerged as a promising tool for zoonotic bacteria control in the food industry, from animals and farm facilities to the final product. Phages are viruses that infect bacteria, with several advantages as a biocontrol agent such as high specificity, self-replication, self-limitation, continuous adaptation, low inherent toxicity and easy isolation. Their development as a biocontrol agent is of particular interest, as it would allow the application of a promising and even necessary “green” technology to combat pathogenic bacteria in the environment. However, bacteriophage applications have limitations, including selecting appropriate phages, legal restrictions, purification, dosage determination and bacterial resistance. Overcoming these limitations is crucial to enhance phage therapy’s effectiveness against zoonotic bacteria in poultry. Thus, this review aims to provide a comprehensive view of the phage-biosanitation strategies for minimizing persistent Salmonella and Campylobacter bacteria in poultry. Full article

(This article belongs to the Special Issue Salmonella and Salmonellosis: Implications in Public Health)

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22 pages, 1071 KiB

Open AccessReview

Salmonella and Salmonellosis: An Update on Public Health Implications and Control Strategies

by Ángela Galán-Relaño, Antonio Valero Díaz, Belén Huerta Lorenzo, Lidia Gómez-Gascón, M.ª Ángeles Mena Rodríguez, Elena Carrasco Jiménez, Fernando Pérez Rodríguez and Rafael J. Astorga Márquez

Animals 2023, 13(23), 3666; https://doi.org/10.3390/ani13233666 - 27 Nov 2023

Cited by 59 | Viewed by 13706

Abstract

Salmonellosis is globally recognized as one of the leading causes of acute human bacterial gastroenteritis resulting from the consumption of animal-derived products, particularly those derived from the poultry and pig industry. Salmonella spp. is generally associated with self-limiting gastrointestinal symptoms, lasting between 2 and 7 days, which can vary from mild to severe. The bacteria can also spread in the bloodstream, causing sepsis and requiring effective antimicrobial therapy; however, sepsis rarely occurs. Salmonellosis control strategies are based on two fundamental aspects: (a) the reduction of prevalence levels in animals by means of health, biosecurity, or food strategies and (b) protection against infection in humans. At the food chain level, the prevention of salmonellosis requires a comprehensive approach at farm, manufacturing, distribution, and consumer levels. Proper handling of food, avoiding cross-contamination, and thorough cooking can reduce the risk and ensure the safety of food. Efforts to reduce transmission of Salmonella by food and other routes must be implemented using a One Health approach. Therefore, in this review we provide an update on Salmonella, one of the main zoonotic pathogens, emphasizing its relationship with animal and public health. We carry out a review on different topics about Salmonella and salmonellosis, with a special emphasis on epidemiology and public health, microbial behavior along the food chain, predictive microbiology principles, antimicrobial resistance, and control strategies. Full article

(This article belongs to the Special Issue Salmonella and Salmonellosis: Implications in Public Health)

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