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Samper-Cativiela C, Torre-Fuentes L, Diéguez-Roda B, Maex M, Ugarte-Ruiz M, Carrizo P, Hernández M, Höfle Ú, Sáez JL, de Frutos C, Agüero M, Moreno MÁ, Domínguez L, Herrera-León S, Alvarez J. Molecular epidemiology of Salmonella Enteritidis in humans and animals in Spain. Antimicrob Agents Chemother 2025; 69:e0073824. [PMID: 40029002 PMCID: PMC11963599 DOI: 10.1128/aac.00738-24] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/10/2024] [Accepted: 01/11/2025] [Indexed: 03/05/2025] Open
Abstract
Salmonella Enteritidis, the most prevalent serovar-causing human gastroenteritis, has been traditionally linked to poultry sources. Although antimicrobial resistance (AMR) is not common in this serovar, increasing levels of resistance to fluoroquinolones and ampicillin have been reported in the last few years. Here, 298 isolates retrieved from different sources (human, livestock, wildlife, food, and environment) and years (2002-2021) in Spain were analyzed to evaluate their diversity, the distribution of AMR-conferring genes (ARGs), and mutations and reconstruct the epidemiology of infection due to this serovar. Isolates were clustered in two major clades (I and II), with strains in clade I (including 61.5% of all human isolates) displaying a pan-susceptible phenotype and not carrying AMR determinants. In contrast, clade II included 80.7% of isolates from animal/food/environmental sources, with the majority (69.8%) harboring mutations in the quinolone resistance determinant regions (QRDR). ARGs, although rare, were mostly found in clade II strains that also carried plasmid replicons, among which IncX1 was the most common. Although higher levels of phenotypic resistance were found in animal isolates, extended-spectrum beta-lactamase, plasmid-mediated AmpC, and carbapenemase-encoding genes were only found among human isolates. In summary, the majority of human and animal isolates from Spanish sources in our collection were classified in different phylogenetic branches, suggesting that additional sources are contributing to the occurrence of foodborne infections in Spain. Furthermore, the different distributions of virulence factors and ARGs in isolates from different sources and their association with specific plasmids suggest the presence of different dynamics contributing to the selection of resistant strains.
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Affiliation(s)
- Clara Samper-Cativiela
- VISAVET Health Surveillance Centre, Complutense University of Madrid, Madrid, Spain
- Department of Animal Health, Faculty of Veterinary Medicine, Complutense University of Madrid, Madrid, Spain
| | - Laura Torre-Fuentes
- VISAVET Health Surveillance Centre, Complutense University of Madrid, Madrid, Spain
| | | | - Margo Maex
- Division of Human Bacterial Diseases, Sciensano, Uccle, Belgium
| | - María Ugarte-Ruiz
- VISAVET Health Surveillance Centre, Complutense University of Madrid, Madrid, Spain
| | - Paula Carrizo
- VISAVET Health Surveillance Centre, Complutense University of Madrid, Madrid, Spain
- Department of Animal Health, Faculty of Veterinary Medicine, Complutense University of Madrid, Madrid, Spain
| | - Marta Hernández
- Departamento de Anatomía Patológica, Microbiología, Medicina Preventiva y Salud Pública, Medicina Legal y Forense. Facultad de Medicina, Universidad de Valladolid Facultad de Medicina, Valladolid, Spain
| | - Úrsula Höfle
- IREC, Instituto de Investigación en Recursos Cinegéticos, Ciudad Real, Spain
| | - José Luis Sáez
- Subdirección General de Sanidad e Higiene Animal y Trazabilidad, Dirección General de la Producción Agraria, Ministerio de Agricultura, Pesca y Alimentación, Madrid, Spain
| | - Cristina de Frutos
- Laboratorio Central de Veterinaria, Ministerio de Agricultura, Pesca y Alimentación, Algete, Spain
| | - Montserrat Agüero
- Laboratorio Central de Veterinaria, Ministerio de Agricultura, Pesca y Alimentación, Algete, Spain
| | - Miguel Ángel Moreno
- Department of Animal Health, Faculty of Veterinary Medicine, Complutense University of Madrid, Madrid, Spain
| | - Lucas Domínguez
- VISAVET Health Surveillance Centre, Complutense University of Madrid, Madrid, Spain
- Department of Animal Health, Faculty of Veterinary Medicine, Complutense University of Madrid, Madrid, Spain
| | - Silvia Herrera-León
- Laboratorio de Referencia e Investigación en Enfermedades Bacterianas Transmitidas por Alimentos, Instituto de Salud Carlos III, Madrid, Spain
| | - Julio Alvarez
- VISAVET Health Surveillance Centre, Complutense University of Madrid, Madrid, Spain
- Department of Animal Health, Faculty of Veterinary Medicine, Complutense University of Madrid, Madrid, Spain
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Keyvan E, Donmez S, Kahraman HA, Tutun H, Calişkan Z, Rugji J, Keyvan N, Şen E, Gumus H. Novel Photodynamic Inactivation Strategy for Salmonella Enteritidis PT4 on Eggshells: Exploiting the Antimicrobial Potential of Curcumin and Carvacrol. Vet Med Sci 2025; 11:e70135. [PMID: 39821598 PMCID: PMC11740504 DOI: 10.1002/vms3.70135] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/26/2024] [Revised: 10/15/2024] [Accepted: 11/11/2024] [Indexed: 01/19/2025] Open
Abstract
Photodynamic inactivation (PDI) is a new and promising strategy for eliminating foodborne pathogenic bacteria in food preservation, reducing associated health risks for consumers. This study aimed to develop an innovative PDI-based system to inactivate Salmonella Enteritidis PT4 on eggshells. The system includes 405 nm light-emitting diodes (LEDs) and the application of curcumin or carvacrol as photosensitizers. The antibacterial activity of the system was investigated in eggshells inoculated with S. Enteritidis PT4 at different temperatures (4, 25, and 37°C) and exposure times (15, 30, and 45 min). Carvacrol + LEDs application was completely inhibited S. Enteritdis PT4 at 4 (after 30 min), 25, and 37°C at the 45th min. Curcumin + LED completely inhibited bacterial growth after 45 min at 4 and 25°C. The results showed that simultaneous use of carvacrol or curcumin with LEDs at various temperatures exhibited significant antibacterial activity against the bacteria depending on the exposure time. The application of curcumin or carvacrol sourced via PDI in the originally developed system resulted in any significant changes in egg quality parameters and sensory properties. This study demonstrated that PDI-based system using curcumin or carvacrol as photosensitizers could be a potential tool for decontamination of eggs contaminated with S. Enteritidis PT4.
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Affiliation(s)
- Erhan Keyvan
- Department of Food Hygiene and Technology, Faculty of Veterinary MedicineBurdur Mehmet Akif Ersoy UniversityBurdurTurkey
| | - Soner Donmez
- Bucak School of HealthBurdur Mehmet Akif Ersoy UniversityBurdurTurkey
| | - Hatice Ahu Kahraman
- Department of Food Hygiene and Technology, Faculty of Veterinary MedicineBurdur Mehmet Akif Ersoy UniversityBurdurTurkey
| | - Hidayet Tutun
- Department of Pharmacology and Toxicology, Faculty of Veterinary MedicineBurdur Mehmet Akif Ersoy UniversityBurdurTurkey
| | - Zuhal Calişkan
- Department of Food Hygiene and Technology, Faculty of Veterinary MedicineBurdur Mehmet Akif Ersoy UniversityBurdurTurkey
| | - Jerina Rugji
- Department of Food Hygiene and Technology, Faculty of Veterinary MedicineBurdur Mehmet Akif Ersoy UniversityBurdurTurkey
| | - Nilay Keyvan
- Department of Food Science and Technology, Institute of Health ScienceBurdur Mehmet Akif UniversityBurdurTurkey
| | - Erdi Şen
- Department of Food Hygiene and Technology, Faculty of Veterinary MedicineBurdur Mehmet Akif Ersoy UniversityBurdurTurkey
| | - Hidir Gumus
- Department of Animal Nutrition and Nutritional Disease, Faculty of Veterinary MedicineBurdur Mehmet Akif Ersoy UniversityBurdurTurkey
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Chen R, Yang L, Pajor MS, Wiedmann M, Orsi RH. Salmonella associated with agricultural animals exhibit diverse evolutionary rates and show evidence of recent clonal expansion. mBio 2024; 15:e0191324. [PMID: 39287448 PMCID: PMC11492988 DOI: 10.1128/mbio.01913-24] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/22/2024] [Accepted: 08/18/2024] [Indexed: 09/19/2024] Open
Abstract
Most foodborne salmonellosis outbreaks are linked to agricultural animal products with a few serovars accounting for most Salmonella isolated from specific animal products, suggesting an adaptation to the corresponding animal hosts and their respective environments. Here, we utilized whole-genome sequence (WGS) data to analyze the evolution and population genetics of seven serovars frequently isolated from ground beef (Montevideo, Cerro, and Dublin), chicken (Kentucky, Infantis, and Enteritidis), and turkey (Reading) in the United States. In addition, publicly available metadata were used to characterize major clades within each serovar with regard to public health significance. Except for Dublin, all serovars were polyphyletic, comprising 2-6 phylogenetic groups. Further partitioning of the phylogenies identified 25 major clades, including 12 associated with animal or environmental niches. These 12 clades differed in evolutionary parameters (e.g., substitution rates) as well as public health relevant characteristics (e.g., association with human illness, antimicrobial resistance). Overall, our results highlight several critical trends: (i) the Salmonella generation time appears to be more dependent on source than serovar and (ii) all serovars contain clades and sub-clades that are estimated to have emerged after the year 1940 and that are enriched for isolates associated with humans, agricultural animals, antimicrobial resistance (AMR), and/or specific geographical regions. These findings suggest that serotyping alone does not provide enough resolution to differentiate isolates that may have evolved independently, present distinct geographic distribution and host association, and possibly have distinct public health significance. IMPORTANCE Non-typhoidal Salmonella are major foodborne bacterial pathogens estimated to cause more than one million illnesses, thousands of hospitalizations, and hundreds of deaths annually in the United States. More than 70% of Salmonella outbreaks in the United States have been associated with agricultural animals. Certain serovars include persistent strains that have repeatedly contaminated beef, chicken, and turkey, causing outbreaks and sporadic cases over many years. These persistent strains represent a particular challenge to public health, as they are genetically clonal and widespread, making it difficult to differentiate distinct outbreak and contamination events using whole-genome sequence (WGS)-based subtyping methods (e.g., core genome allelic typing). Our results indicate that a phylogenetic approach is needed to investigate persistent strains and suggest that the association between a Salmonella serovar and an agricultural animal is driven by the expansion of clonal subtypes that likely became adapted to specific animals and associated environments.
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Affiliation(s)
- Ruixi Chen
- Department of Food
Science, Cornell University,
Ithaca, New York, USA
| | - Linghuan Yang
- Department of Food
Science, Cornell University,
Ithaca, New York, USA
| | | | - Martin Wiedmann
- Department of Food
Science, Cornell University,
Ithaca, New York, USA
| | - Renato H. Orsi
- Department of Food
Science, Cornell University,
Ithaca, New York, USA
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Liao YS, Lauderdale TL, Chang JH, Liang SY, Tsao CS, Wei HL, Wang YW, Teng RH, Hong YP, Chen BH, Chiou CS. Epidemiological trends in serotypes distribution and antimicrobial resistance in Salmonella from humans in Taiwan, 2004-2022. IJID REGIONS 2024; 11:100372. [PMID: 38799797 PMCID: PMC11126859 DOI: 10.1016/j.ijregi.2024.100372] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 03/27/2024] [Revised: 04/23/2024] [Accepted: 04/25/2024] [Indexed: 05/29/2024]
Abstract
Objectives Salmonella, a zoonotic pathogen, significantly impacts global human health. Understanding its serotype distribution and antimicrobial resistance is crucial for effective control measures and medical interventions. Methods We collected Salmonella isolates and demographic data from Taiwanese hospitals between 2004 and 2022, analyzing their serotypes and antimicrobial susceptibility. Results Among 40,595 isolates, salmonellosis predominated in children aged 0-4 (61.2%) years and among males (55.2%). Males also showed higher rates of extraintestinal infections (18.1% vs 16.0%, P <0.001), particularly, in the ≥65 years age group (52.4%). The top five serovars were S. Enteritidis (32.8%), S. Typhimurium (21.7%), S. Newport (6.2%), S. Stanley (4.7%), and S. Anatum (4.0%). Notably, S. Enteritidis prevalence increased from 23.9% (2004-2005) to 43.6% (2021-2022). Antimicrobial resistance was high, with a 51.6% multidrug resistance (MDR) rate. Disturbingly, MDR rates exceeded 90% in serovars Albany, Schwarzengrund, Choleraesuis, and Goldcoast. Resistance to key therapeutic agents, azithromycin, cefotaxime, and ciprofloxacin, exhibited concerning upward trends, and the surge in cefotaxime and ciprofloxacin resistance was closely linked to the emergence and spread of MDR S. Anatum and S. Goldcoast clones. Conclusions Prioritizing control measures against S. Enteritidis and closely monitoring the prevalence and spread of MDR clones are imperative to mitigate Salmonella infections in Taiwan.
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Affiliation(s)
- Ying-Shu Liao
- Center for Diagnostics and Vaccine Development, Centres for Disease Control, Taichung, Taiwan
| | - Tsai-Ling Lauderdale
- National Institute of Infectious Diseases and Vaccinology, National Health Research Institutes, Miaoli, Taiwan
| | - Jui-Hsien Chang
- Center for Diagnostics and Vaccine Development, Centres for Disease Control, Taichung, Taiwan
| | - Shiu-Yun Liang
- Center for Diagnostics and Vaccine Development, Centres for Disease Control, Taichung, Taiwan
| | - Chi-Sen Tsao
- Center for Diagnostics and Vaccine Development, Centres for Disease Control, Taichung, Taiwan
| | - Hsiao Lun Wei
- Center for Diagnostics and Vaccine Development, Centres for Disease Control, Taichung, Taiwan
| | - You-Wun Wang
- Center for Diagnostics and Vaccine Development, Centres for Disease Control, Taichung, Taiwan
| | - Ru-Hsiou Teng
- Center for Diagnostics and Vaccine Development, Centres for Disease Control, Taichung, Taiwan
| | - Yu-Ping Hong
- Center for Diagnostics and Vaccine Development, Centres for Disease Control, Taichung, Taiwan
| | - Bo-Han Chen
- Center for Diagnostics and Vaccine Development, Centres for Disease Control, Taichung, Taiwan
| | - Chien-Shun Chiou
- Center for Diagnostics and Vaccine Development, Centres for Disease Control, Taichung, Taiwan
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Huang L, Ahmad NH, Juneja V, Stapp-Kamotani E, Gabiola J, Minocha U, Phillips R, Hooker M, Walls I, Cook K, Lindsay J. Growth kinetics of Bacillus cytotoxicus in liquid Egg yolk during treatment with phospholipase A 2 - A one-step global dynamic analysis. Food Microbiol 2024; 118:104420. [PMID: 38049265 DOI: 10.1016/j.fm.2023.104420] [Citation(s) in RCA: 2] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/12/2023] [Revised: 10/17/2023] [Accepted: 10/30/2023] [Indexed: 12/06/2023]
Abstract
During commercial production of liquid egg yolk (LEY), phospholipase A2 (PLA2) is used to improve its emulsification capacity and thermal stability. The enzymatic treatment may occur at elevated temperatures such as 50 °C, potentially allowing foodborne pathogens, such as Bacillus cereus, to grow. Little knowledge is available concerning growth of B. cereus in LEY during PLA2 treatment. Therefore, the objective of this study was to investigate the growth kinetics of B. cereus during PLA2 treatment using pathogenic B. cytotoxicus NVH391-98, the most thermotolerant member in the B. cereus group, as a surrogate. Inoculated LEY samples were placed in precision programmable incubators to observe the growth of B. cytotoxicus NVH391-98 under multiple isothermal and dynamic temperature conditions between 20 and 53 °C. The bacterial growth was described using the differential Baranyi model coupled with two different secondary models. The kinetic parameters were determined using one-step dynamic inverse analysis of multiple growth curves. The least square method was used in combination with the 4th order Runge-Kutta method to solve the differential Baranyi model using multiple growth curves to determine the cardinal kinetic parameters. The results showed that B. cytotoxicus NVH391-98 can grow prolifically at 50 °C. The estimated minimum, optimum and maximum temperatures were 16.7 or 18.5, 47.8 or 48.1, and 52.1 or 52.4 °C, respectively, depending on the secondary models, with an optimum growth rate of 2.1 log colony-forming-unit (CFU)/g per hour. The dynamic model is validated using isothermal curves with reasonable accuracy. B. cytotoxicus died off slowly at 15 °C. At 55 °C, thermal inactivation was observed, with a D value of approximately 2.7 h. Holding at 55 °C or below 15 °C can effectively prevent the growth of B. cytotoxicus in egg yolk.
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Affiliation(s)
- Lihan Huang
- USDA-Agriculture Research Service, Wyndmoor, PA, USA.
| | - Nurul Hawa Ahmad
- ORISE Postdoctoral Research Fellow, Universiti Putra Malaysia, Malaysia
| | - Vijay Juneja
- USDA-Agriculture Research Service, Wyndmoor, PA, USA
| | | | - Jose Gabiola
- USDA-Food Safety and Inspection Service, Washington, DC, USA
| | - Udit Minocha
- USDA-Food Safety and Inspection Service, Washington, DC, USA
| | | | - Marie Hooker
- USDA-Food Safety and Inspection Service, Athens, GA, USA
| | - Isabel Walls
- USDA-Food Safety and Inspection Service, Washington, DC, USA
| | - Kim Cook
- USDA-Agriculture Research Service, Beltsville, MD, USA
| | - James Lindsay
- USDA-Agriculture Research Service, Beltsville, MD, USA
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Lamichhane B, Mawad AMM, Saleh M, Kelley WG, Harrington PJ, Lovestad CW, Amezcua J, Sarhan MM, El Zowalaty ME, Ramadan H, Morgan M, Helmy YA. Salmonellosis: An Overview of Epidemiology, Pathogenesis, and Innovative Approaches to Mitigate the Antimicrobial Resistant Infections. Antibiotics (Basel) 2024; 13:76. [PMID: 38247636 PMCID: PMC10812683 DOI: 10.3390/antibiotics13010076] [Citation(s) in RCA: 25] [Impact Index Per Article: 25.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/21/2023] [Revised: 12/24/2023] [Accepted: 01/10/2024] [Indexed: 01/23/2024] Open
Abstract
Salmonella is a major foodborne pathogen and a leading cause of gastroenteritis in humans and animals. Salmonella is highly pathogenic and encompasses more than 2600 characterized serovars. The transmission of Salmonella to humans occurs through the farm-to-fork continuum and is commonly linked to the consumption of animal-derived food products. Among these sources, poultry and poultry products are primary contributors, followed by beef, pork, fish, and non-animal-derived food such as fruits and vegetables. While antibiotics constitute the primary treatment for salmonellosis, the emergence of antibiotic resistance and the rise of multidrug-resistant (MDR) Salmonella strains have highlighted the urgency of developing antibiotic alternatives. Effective infection management necessitates a comprehensive understanding of the pathogen's epidemiology and transmission dynamics. Therefore, this comprehensive review focuses on the epidemiology, sources of infection, risk factors, transmission dynamics, and the host range of Salmonella serotypes. This review also investigates the disease characteristics observed in both humans and animals, antibiotic resistance, pathogenesis, and potential strategies for treatment and control of salmonellosis, emphasizing the most recent antibiotic-alternative approaches for infection control.
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Affiliation(s)
- Bibek Lamichhane
- Department of Veterinary Science, Martin-Gatton College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY 40546, USA
| | - Asmaa M. M. Mawad
- Botany and Microbiology Department, Faculty of Science, Assiut University, Assiut 71516, Egypt
| | - Mohamed Saleh
- Department of Veterinary Science, Martin-Gatton College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY 40546, USA
| | - William G. Kelley
- Department of Veterinary Science, Martin-Gatton College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY 40546, USA
| | - Patrick J. Harrington
- Department of Veterinary Science, Martin-Gatton College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY 40546, USA
| | - Cayenne W. Lovestad
- Department of Veterinary Science, Martin-Gatton College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY 40546, USA
| | - Jessica Amezcua
- Department of Veterinary Science, Martin-Gatton College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY 40546, USA
| | - Mohamed M. Sarhan
- Faculty of Pharmacy, King Salman International University (KSIU), Ras Sudr 8744304, Egypt
| | - Mohamed E. El Zowalaty
- Veterinary Medicine and Food Security Research Group, Medical Laboratory Sciences Program, Faculty of Health Sciences, Abu Dhabi Women’s Campus, Higher Colleges of Technology, Abu Dhabi 41012, United Arab Emirates
| | - Hazem Ramadan
- Hygiene and Zoonoses Department, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt
| | - Melissa Morgan
- Department of Animal and Food Sciences, Martin-Gatton College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY 40546, USA
| | - Yosra A. Helmy
- Department of Veterinary Science, Martin-Gatton College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY 40546, USA
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Abramov VM, Kosarev IV, Machulin AV, Deryusheva EI, Priputnevich TV, Panin AN, Chikileva IO, Abashina TN, Manoyan AM, Akhmetzyanova AA, Blumenkrants DA, Ivanova OE, Papazyan TT, Nikonov IN, Suzina NE, Melnikov VG, Khlebnikov VS, Sakulin VK, Samoilenko VA, Gordeev AB, Sukhikh GT, Uversky VN, Karlyshev AV. Anti- Salmonella Defence and Intestinal Homeostatic Maintenance In Vitro of a Consortium Containing Limosilactobacillus fermentum 3872 and Ligilactobacillus salivarius 7247 Strains in Human, Porcine, and Chicken Enterocytes. Antibiotics (Basel) 2023; 13:30. [PMID: 38247590 PMCID: PMC10812507 DOI: 10.3390/antibiotics13010030] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/07/2023] [Revised: 12/18/2023] [Accepted: 12/22/2023] [Indexed: 01/23/2024] Open
Abstract
Limosilactobacillus fermentum strain 3872 (LF3872) was originally isolated from the breast milk of a healthy woman during lactation and the breastfeeding of a child. Ligilactobacillus salivarius strain 7247 (LS7247) was isolated at the same time from the intestines and reproductive system of a healthy woman. The genomes of these strains contain genes responsible for the production of peptidoglycan-degrading enzymes and factors that increase the permeability of the outer membrane of Gram-negative pathogens. In this work, the anti-Salmonella and intestinal homeostatic features of the LF3872 and LS7247 consortium were studied. A multi-drug resistant (MDR) strain of Salmonella enteritidis (SE) was used in the experiments. The consortium effectively inhibited the adhesion of SE to intact and activated human, porcine, and chicken enterocytes and reduced invasion. The consortium had a bactericidal effect on SE in 6 h of co-culturing. A gene expression analysis of SE showed that the cell-free supernatant (CFS) of the consortium inhibited the expression of virulence genes critical for the colonization of human and animal enterocytes. The CFS stimulated the production of an intestinal homeostatic factor-intestinal alkaline phosphatase (IAP)-in Caco-2 and HT-29 enterocytes. The consortium decreased the production of pro-inflammatory cytokines IL-8, TNF-α, and IL-1β, and TLR4 mRNA expression in human and animal enterocytes. It stimulated the expression of TLR9 in human and porcine enterocytes and stimulated the expression of TLR21 in chicken enterocytes. The consortium also protected the intestinal barrier functions through the increase of transepithelial electrical resistance (TEER) and the inhibition of paracellular permeability in the monolayers of human and animal enterocytes. The results obtained suggest that a LF3872 and LS7247 consortium can be used as an innovative feed additive to reduce the spread of MDR SE among the population and farm animals.
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Affiliation(s)
- Vyacheslav M. Abramov
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia
- Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health, 117997 Moscow, Russia (A.B.G.)
| | - Igor V. Kosarev
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia
- Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health, 117997 Moscow, Russia (A.B.G.)
| | - Andrey V. Machulin
- Skryabin Institute of Biochemistry and Physiology of Microorganisms, Federal Research Center “Pushchino Scientific Center for Biological Research of Russian Academy of Science”, Russian Academy of Science, 142290 Pushchino, Russia
| | - Evgenia I. Deryusheva
- Institute for Biological Instrumentation, Federal Research Center “Pushchino Scientific Center for Biological Research of Russian Academy of Science”, Russian Academy of Science, 142290 Pushchino, Russia
| | - Tatiana V. Priputnevich
- Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health, 117997 Moscow, Russia (A.B.G.)
| | - Alexander N. Panin
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia
| | - Irina O. Chikileva
- Blokhin National Research Center of Oncology, Ministry of Health RF, 115478 Moscow, Russia
| | - Tatiana N. Abashina
- Skryabin Institute of Biochemistry and Physiology of Microorganisms, Federal Research Center “Pushchino Scientific Center for Biological Research of Russian Academy of Science”, Russian Academy of Science, 142290 Pushchino, Russia
| | - Ashot M. Manoyan
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia
| | - Anna A. Akhmetzyanova
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia
| | - Dmitriy A. Blumenkrants
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia
| | - Olga E. Ivanova
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia
| | | | - Ilia N. Nikonov
- Federal State Educational Institution of Higher Professional Education, Moscow State Academy of Veterinary Medicine and Biotechnology Named after K.I. Skryabin, 109472 Moscow, Russia;
| | - Nataliya E. Suzina
- Skryabin Institute of Biochemistry and Physiology of Microorganisms, Federal Research Center “Pushchino Scientific Center for Biological Research of Russian Academy of Science”, Russian Academy of Science, 142290 Pushchino, Russia
| | - Vyacheslav G. Melnikov
- Gabrichevsky Research Institute for Epidemiology and Microbiology, 125212 Moscow, Russia
| | | | - Vadim K. Sakulin
- Institute of Immunological Engineering, 142380 Lyubuchany, Russia; (V.S.K.); (V.K.S.)
| | - Vladimir A. Samoilenko
- Skryabin Institute of Biochemistry and Physiology of Microorganisms, Federal Research Center “Pushchino Scientific Center for Biological Research of Russian Academy of Science”, Russian Academy of Science, 142290 Pushchino, Russia
| | - Alexey B. Gordeev
- Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health, 117997 Moscow, Russia (A.B.G.)
| | - Gennady T. Sukhikh
- Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health, 117997 Moscow, Russia (A.B.G.)
| | - Vladimir N. Uversky
- Department of Molecular Medicine, Morsani College of Medicine, University of South Florida, Tampa, FL 33612, USA;
| | - Andrey V. Karlyshev
- Department of Biomolecular Sciences, School of Life Sciences, Chemistry and Pharmacy, Faculty of Health, Science, Social Care and Education, Kingston University London, Kingston upon Thames KT1 2EE, UK
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Ju Z, Cui L, Lei C, Song M, Chen X, Liao Z, Zhang T, Wang H. Whole-Genome Sequencing Analysis of Non-Typhoidal Salmonella Isolated from Breeder Poultry Farm Sources in China, 2020-2021. Antibiotics (Basel) 2023; 12:1642. [PMID: 37998844 PMCID: PMC10669045 DOI: 10.3390/antibiotics12111642] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/19/2023] [Revised: 11/12/2023] [Accepted: 11/13/2023] [Indexed: 11/25/2023] Open
Abstract
Non-typhoidal salmonellosis is a dangerous foodborne disease that causes enormous economic loss and threatens public health worldwide. The consumption of food, especially poultry or poultry products, contaminated with non-typhoidal Salmonella (NTS) is the main cause of human salmonellosis. To date, no research has identified the molecular epidemiological characteristics of NTS strains isolated from breeder chicken farms in different provinces of China. In our study, we investigated the antimicrobial resistance, phylogenetic relationships, presence of antimicrobial resistance and virulence genes, and plasmids of NTS isolates recovered from breeder chicken farms in five provinces of China between 2020 and 2021 by using a whole-genome sequencing (WGS) approach and phenotypic methods. All sequenced isolates belonged to six serovars with seven sequence types. Nearly half of the isolates (44.87%) showed phenotypic resistance to at least three classes of antimicrobials. Salmonella enterica serotype Kentucky harbored more antimicrobial resistance genes than the others, which was highly consistent with phenotypic resistance. Furthermore, the carried rate of 104 out of 135 detected virulence genes was 100%. Overall, our WGS results highlight the need for the continuous monitoring of, and additional studies on, the antimicrobial resistance of NTS.
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Affiliation(s)
- Zijing Ju
- Laboratory of Bio-Resource and Eco-Environment, Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610017, China; (Z.J.); (C.L.); (X.C.); (Z.L.); (T.Z.)
- Animal Disease Prevention and Food Safety Key Laboratory of Sichuan Province, Chengdu 610064, China
| | - Lulu Cui
- Shandong Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an 271018, China; (L.C.); (M.S.)
| | - Changwei Lei
- Laboratory of Bio-Resource and Eco-Environment, Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610017, China; (Z.J.); (C.L.); (X.C.); (Z.L.); (T.Z.)
- Animal Disease Prevention and Food Safety Key Laboratory of Sichuan Province, Chengdu 610064, China
| | - Mengze Song
- Shandong Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an 271018, China; (L.C.); (M.S.)
| | - Xuan Chen
- Laboratory of Bio-Resource and Eco-Environment, Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610017, China; (Z.J.); (C.L.); (X.C.); (Z.L.); (T.Z.)
- Animal Disease Prevention and Food Safety Key Laboratory of Sichuan Province, Chengdu 610064, China
| | - Ziwei Liao
- Laboratory of Bio-Resource and Eco-Environment, Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610017, China; (Z.J.); (C.L.); (X.C.); (Z.L.); (T.Z.)
- Animal Disease Prevention and Food Safety Key Laboratory of Sichuan Province, Chengdu 610064, China
| | - Tiejun Zhang
- Laboratory of Bio-Resource and Eco-Environment, Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610017, China; (Z.J.); (C.L.); (X.C.); (Z.L.); (T.Z.)
- Animal Disease Prevention and Food Safety Key Laboratory of Sichuan Province, Chengdu 610064, China
| | - Hongning Wang
- Laboratory of Bio-Resource and Eco-Environment, Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610017, China; (Z.J.); (C.L.); (X.C.); (Z.L.); (T.Z.)
- Animal Disease Prevention and Food Safety Key Laboratory of Sichuan Province, Chengdu 610064, China
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Abramov VM, Kosarev IV, Machulin AV, Deryusheva EI, Priputnevich TV, Panin AN, Chikileva IO, Abashina TN, Manoyan AM, Ahmetzyanova AA, Ivanova OE, Papazyan TT, Nikonov IN, Suzina NE, Melnikov VG, Khlebnikov VS, Sakulin VK, Samoilenko VA, Gordeev AB, Sukhikh GT, Uversky VN. Ligilactobacillus salivarius 7247 Strain: Probiotic Properties and Anti- Salmonella Effect with Prebiotics. Antibiotics (Basel) 2023; 12:1535. [PMID: 37887236 PMCID: PMC10604316 DOI: 10.3390/antibiotics12101535] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/12/2023] [Revised: 09/28/2023] [Accepted: 10/02/2023] [Indexed: 10/28/2023] Open
Abstract
The Ligilactobacillus salivarius 7247 (LS7247) strain, originally isolated from a healthy woman's intestines and reproductive system, has been studied for its probiotic potential, particularly against Salmonella Enteritidis (SE) and Salmonella Typhimurium (ST) as well as its potential use in synbiotics. LS7247 showed high tolerance to gastric and intestinal stress and effectively adhered to human and animal enterocyte monolayers, essential for realizing its probiotic properties. LS7247 showed high anti-Salmonella activity. Additionally, the cell-free culture supernatant (CFS) of LS7247 exhibited anti-Salmonella activity, with a partial reduction upon neutralization with NaOH (p < 0.05), suggesting the presence of anti-Salmonella factors such as lactic acid (LA) and bacteriocins. LS7247 produced a high concentration of LA, reaching 124.0 ± 2.5 mM after 48 h of cultivation. Unique gene clusters in the genome of LS7247 contribute to the production of Enterolysin A and metalloendopeptidase. Notably, LS7247 carries a plasmid with a gene cluster identical to human intestinal strain L. salivarius UCC118, responsible for class IIb bacteriocin synthesis, and a gene cluster identical to porcine strain L. salivarius P1ACE3, responsible for nisin S synthesis. Co-cultivation of LS7247 with SE and ST pathogens reduced their viability by 1.0-1.5 log, attributed to cell wall damage and ATP leakage caused by the CFS. For the first time, the CFS of LS7247 has been shown to inhibit adhesion of SE and ST to human and animal enterocytes (p < 0.01). The combination of Actigen prebiotic and the CFS of LS7247 demonstrated a significant combined effect in inhibiting the adhesion of SE and ST to human and animal enterocytes (p < 0.001). These findings highlight the potential of using the LS7247 as a preventive strategy and employing probiotics and synbiotics to combat the prevalence of salmonellosis in animals and humans caused by multidrug resistant (MDR) strains of SE and ST pathogens.
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Affiliation(s)
- Vyacheslav M. Abramov
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia; (I.V.K.)
- Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health, 117997 Moscow, Russia
| | - Igor V. Kosarev
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia; (I.V.K.)
- Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health, 117997 Moscow, Russia
| | - Andrey V. Machulin
- Skryabin Institute of Biochemistry and Physiology of Microorganisms, Federal Research Center “Pushchino Scientific Center for Biological Research of Russian Academy of Science”, Russian Academy of Science, 142290 Pushchino, Russia
| | - Evgenia I. Deryusheva
- Institute for Biological Instrumentation, Federal Research Center “Pushchino Scientific Center for Biological Research of Russian Academy of Science”, Russian Academy of Science, 142290 Pushchino, Russia
| | - Tatiana V. Priputnevich
- Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health, 117997 Moscow, Russia
| | - Alexander N. Panin
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia; (I.V.K.)
| | - Irina O. Chikileva
- Laboratory of Cell Immunity, Blokhin National Research Center of Oncology, Ministry of Health RF, 115478 Moscow, Russia;
| | - Tatiana N. Abashina
- Skryabin Institute of Biochemistry and Physiology of Microorganisms, Federal Research Center “Pushchino Scientific Center for Biological Research of Russian Academy of Science”, Russian Academy of Science, 142290 Pushchino, Russia
| | - Ashot M. Manoyan
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia; (I.V.K.)
| | - Anna A. Ahmetzyanova
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia; (I.V.K.)
| | - Olga E. Ivanova
- Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) Federal State Budgetary Institution “The Russian State Center for Animal Feed and Drug Standardization and Quality” (FGBU VGNKI), 123022 Moscow, Russia; (I.V.K.)
| | | | - Ilia N. Nikonov
- Federal State Educational Institution of Higher Professional Education Moscow State Academy of Veterinary Medicine and Biotechnology Named after K.I. Skryabin, 109472 Moscow, Russia
| | - Nataliya E. Suzina
- Skryabin Institute of Biochemistry and Physiology of Microorganisms, Federal Research Center “Pushchino Scientific Center for Biological Research of Russian Academy of Science”, Russian Academy of Science, 142290 Pushchino, Russia
| | - Vyacheslav G. Melnikov
- Gabrichevsky Research Institute for Epidemiology and Microbiology, 125212 Moscow, Russia
| | | | - Vadim K. Sakulin
- Institute of Immunological Engineering, 142380 Lyubuchany, Russia
| | - Vladimir A. Samoilenko
- Skryabin Institute of Biochemistry and Physiology of Microorganisms, Federal Research Center “Pushchino Scientific Center for Biological Research of Russian Academy of Science”, Russian Academy of Science, 142290 Pushchino, Russia
| | - Alexey B. Gordeev
- Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health, 117997 Moscow, Russia
| | - Gennady T. Sukhikh
- Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health, 117997 Moscow, Russia
| | - Vladimir N. Uversky
- Department of Molecular Medicine, Morsani College of Medicine, University of South Florida, Tampa, FL 33612, USA;
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Narasimhan SL, Salvi D, Schaffner DW, Karwe MV, Tan J. Efficacy of cold plasma-activated water as an environmentally friendly sanitizer in egg washing. Poult Sci 2023; 102:102893. [PMID: 37473520 PMCID: PMC10371827 DOI: 10.1016/j.psj.2023.102893] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/13/2023] [Revised: 06/16/2023] [Accepted: 06/24/2023] [Indexed: 07/22/2023] Open
Abstract
Eggs in the United States are typically washed using chemical sanitizers such as quaternary ammonia (QA) or chlorine. Such treatments generate wash water, which could be potentially hazardous to the environment. A novel, nonthermal sanitization technique for washing shell eggs using cold plasma-activated water (PAW) was investigated in this study. The inactivation efficacy of PAW on Klebsiella michiganensis and the impact of PAW on the cuticle of the eggshell and shell strength were tested in comparison to QA. Washing inoculated eggs with PAW and QA achieved a similar microbial reduction (>5.28 log CFU/egg). Colorimetric analysis showed that ∆E-value for PAW-treated eggs was significantly lower than QA-treated eggs, suggesting higher cuticle coverage in eggs treated with PAW. The texture analysis to test for shell egg strength indicated that washing eggs with PAW did not affect the structural integrity of the eggshell when compared to eggs washed with QA. According to this study, PAW has the potential as an alternative to commercial sanitizers like QA in the egg-washing industry. PAW does not detrimentally impact shell strength or cuticle coverage and provides similar microbial reduction efficacy.
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Affiliation(s)
- Shruthi L Narasimhan
- Department of Food Science, Rutgers The State University of New Jersey, New Brunswick, NJ 08901, USA
| | - Deepti Salvi
- Department of Food, Bioprocessing and Nutrition Sciences, North Carolina State University, Raleigh, NC 27607, USA
| | - Donald W Schaffner
- Department of Food Science, Rutgers The State University of New Jersey, New Brunswick, NJ 08901, USA
| | - Mukund V Karwe
- Department of Food Science, Rutgers The State University of New Jersey, New Brunswick, NJ 08901, USA
| | - Juzhong Tan
- College of Agriculture and Food Science, Florida A&M University, Tallahassee, FL 32307, USA.
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11
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Raut R, Maharjan P, Fouladkhah AC. Practical Preventive Considerations for Reducing the Public Health Burden of Poultry-Related Salmonellosis. INTERNATIONAL JOURNAL OF ENVIRONMENTAL RESEARCH AND PUBLIC HEALTH 2023; 20:6654. [PMID: 37681794 PMCID: PMC10487474 DOI: 10.3390/ijerph20176654] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 04/25/2023] [Revised: 08/20/2023] [Accepted: 08/23/2023] [Indexed: 09/09/2023]
Abstract
With poultry products as one of the leading reservoirs for the pathogen, in a typical year in the United States, it is estimated that over one million individuals contract non-typhoidal Salmonella infections. Foodborne outbreaks associated with Salmonella infections in poultry, thus, continue to remain a significant risk to public health. Moreover, the further emergence of antimicrobial resistance among various serovars of Salmonella is an additional public health concern. Feeding-based strategies (such as use of prebiotics, probiotics, and/or phytobiotics as well as essential oils), non-feeding-based strategies (such as use of bacteriophages, vaccinations, and in ovo strategies), omics tools and surveillance for identifying antibiotic-resistance genes, post-harvest application of antimicrobials, and biosecurity measures at poultry facilities are practical interventions that could reduce the public health burden of salmonellosis and antibiotic resistance associated with poultry products. With the escalating consumption of poultry products around the globe, the fate, prevalence, and transmission of Salmonella in agricultural settings and various poultry-processing facilities are major public health challenges demanding integrated control measures throughout the food chain. Implementation of practical preventive measures discussed in the current study could appreciably reduce the public health burden of foodborne salmonellosis associated with poultry products.
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Affiliation(s)
- Rabin Raut
- Cooperative Extension Program, Tennessee State University, Nashville, TN 37209, USA;
- Public Health Microbiology Laboratory, Tennessee State University, Nashville, TN 37209, USA
| | - Pramir Maharjan
- Cooperative Extension Program, Tennessee State University, Nashville, TN 37209, USA;
| | - Aliyar Cyrus Fouladkhah
- Public Health Microbiology Laboratory, Tennessee State University, Nashville, TN 37209, USA
- Public Health Microbiology FoundationSM, Nashville, TN 37209, USA
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12
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Münster P, Pöppel L, Antakli A, Müller-Doblies D, Radko D, Kemper N. The Detection of Salmonella Enteritidis on German Layer Farms after Cleaning and Disinfection. Animals (Basel) 2023; 13:2588. [PMID: 37627379 PMCID: PMC10451266 DOI: 10.3390/ani13162588] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/14/2023] [Revised: 08/01/2023] [Accepted: 08/09/2023] [Indexed: 08/27/2023] Open
Abstract
The presence of Salmonella Enteritidis in poultry houses after cleaning and disinfection can pose a potential risk to public health, as Salmonella remains one of the most important causes of foodborne diseases. This study focused on ten German layer farms (including floor-reared and free-range systems) with a recent history of Salmonella Enteritidis, and samples were collected from July 2018 to March 2021 after the cleaning and disinfection process. A total of 244 swab samples were tested for the presence of Salmonella using real-time PCR, followed by a culture of positive samples. Results revealed that 61 out of the 244 swab samples tested positive for Salmonella, indicating a prevalence of 25% in the samples examined. Among the Salmonella-positive swab samples identified with the PCR assay, 65.6% (40 out of 61) were confirmed by the culture. Of the 40 isolates obtained from the culture, 36 were identified as Salmonella Enteritidis, while 4 were categorized as rough Salmonella strains. This study emphasizes the importance of both the surrounding area of the poultry houses in terms of infection carry-over and the meticulous implementation of cleaning and disinfection procedures to eliminate any remaining infection within the houses. To mitigate the risk of further Salmonella spread on layer farms, additional investigations are recommended to focus on the existing transmission pathways of Salmonella and their genetic diversity.
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Affiliation(s)
- Pia Münster
- Elanco Deutschland GmbH, Rathausplatz 12, 61348 Bad Homburg, Germany; (P.M.); (A.A.); (D.R.)
| | - Lars Pöppel
- Institute for Animal Hygiene, Animal Welfare and Farm Animal Behaviors, University of Veterinary Medicine Hannover, Foundation, 30559 Hannover, Germany;
- Praxis Pöppel GmbH, Drubbelstraße 2, 33129 Delbrück, Germany
| | - Ali Antakli
- Elanco Deutschland GmbH, Rathausplatz 12, 61348 Bad Homburg, Germany; (P.M.); (A.A.); (D.R.)
| | - Doris Müller-Doblies
- Elanco Austria GmbH, Quartier Belvedere Central, Gertrude Froehlich Sandner Str. 3, 1100 Vienna, Austria;
| | - Dmytro Radko
- Elanco Deutschland GmbH, Rathausplatz 12, 61348 Bad Homburg, Germany; (P.M.); (A.A.); (D.R.)
| | - Nicole Kemper
- Institute for Animal Hygiene, Animal Welfare and Farm Animal Behaviors, University of Veterinary Medicine Hannover, Foundation, 30559 Hannover, Germany;
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13
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Akinyemi KO, Fakorede CO, Linde J, Methner U, Wareth G, Tomaso H, Neubauer H. Whole genome sequencing of Salmonella enterica serovars isolated from humans, animals, and the environment in Lagos, Nigeria. BMC Microbiol 2023; 23:164. [PMID: 37312043 DOI: 10.1186/s12866-023-02901-1] [Citation(s) in RCA: 12] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/27/2022] [Accepted: 05/17/2023] [Indexed: 06/15/2023] Open
Abstract
BACKGROUND Salmonella infections remain an important public health issue worldwide. Some serovars of non-typhoidal Salmonella (NTS) have been associated with bloodstream infections and gastroenteritis, especially in children in Sub-Saharan Africa with circulating S. enterica serovars with drug resistance and virulence genes. This study identified and verified the clonal relationship of Nigerian NTS strains isolated from humans, animals, and the environment. METHODS In total, 2,522 samples were collected from patients, animals (cattle and poultry), and environmental sources between December 2017 and May 2019. The samples were subjected to a standard microbiological investigation. All the isolates were identified using Microbact 24E, and MALDI-TOF MS. The isolates were serotyped using the Kauffmann-White scheme. Antibiotic susceptibility testing was conducted using the disc diffusion method and the Vitek 2 compact system. Virulence and antimicrobial resistance genes, sequence type, and cluster analysis were investigated using WGS data. RESULTS Forty-eight (48) NTS isolates (1.9%) were obtained. The prevalence of NTS from clinical sources was 0.9%, while 4% was recorded for animal sources. The serovars identified were S. Cotham (n = 17), S. Give (n = 16), S. Mokola (n = 6), S. Abony (n = 4), S. Typhimurium (n = 4), and S. Senftenberg (n = 1). All 48 Salmonella isolates carried intrinsic and acquired resistant genes such as aac.6…Iaa, mdf(A), qnrB, qnrB19 genes and golT, golS, pcoA, and silP, mediated by plasmid Col440I_1, incFIB.B and incFII. Between 100 and 118 virulence gene markers distributed across several Salmonella pathogenicity islands (SPIs), clusters, prophages, and plasmid operons were found in each isolate. WGS revealed that strains of each Salmonella serovar could be assigned to a single 7-gene MLST cluster, and strains within the clusters were identical strains and closely related as defined by the 0 and 10 cgSNPs and likely shared a common ancestor. The dominant sequence types were S. Give ST516 and S. Cotham ST617. CONCLUSION We found identical Salmonella sequence types in human, animal, and environmental samples in the same locality, which demonstrates the great potential of the applied tools to trace back outbreak strains. Strategies to control and prevent the spread of NTS in the context of one's health are essential to prevent possible outbreaks.
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Affiliation(s)
| | | | - Jörg Linde
- Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institute, Jena, Germany
| | - Ulrich Methner
- Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institute, Jena, Germany
| | - Gamal Wareth
- Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institute, Jena, Germany
- Department of Bacteriology, Immunology, and Mycology, Faculty of Veterinary Medicine, Benha University, PO Box 13736, Toukh, Moshtohor, Egypt
- Institute of Infectious Diseases and Infection Control, Jena University Hospital, Am Klinikum 1, 07747, Jena, Germany
| | - Herbert Tomaso
- Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institute, Jena, Germany
| | - Heinrich Neubauer
- Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institute, Jena, Germany
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14
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Murray CE, Varga C, Ouckama R, Guerin MT. Temporal Study of Salmonella enterica Serovars Isolated from Environmental Samples from Ontario Poultry Breeder Flocks between 2009 and 2018. Pathogens 2023; 12:278. [PMID: 36839550 PMCID: PMC9967235 DOI: 10.3390/pathogens12020278] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/13/2023] [Revised: 02/02/2023] [Accepted: 02/02/2023] [Indexed: 02/11/2023] Open
Abstract
This study's goal was to determine the prevalence, temporal trends, seasonal patterns, and temporal clustering of Salmonella enterica isolated from environmental samples from Ontario's poultry breeding flocks between 2009 and 2018. Clusters of common serovars and those of human health concern were identified using a scan statistic. The period prevalence of S. enterica was 25.3% in broiler breeders, 6.4% in layer breeders, and 28.6% in turkey breeders. An overall decreasing trend in S. enterica prevalence was identified in broiler breeders (from 27.8% in 2009 to 22.1% in 2018) and layer breeders (from 15.4% to 4.9%), while an increasing trend was identified in turkey breeders (from 12.0% to 24.5%). The most common serovars varied by commodity. Among broiler breeders, S. enterica serovars Kentucky (42.4% of 682 submissions), Heidelberg (19.2%), and Typhimurium (5.4%) were the most common. Salmonella enterica serovars Thompson (20.0% of 195 submissions) and Infantis (16.4%) were most common among layer breeders, and S. enterica serovars Schwarzengrund (23.6% of 1368 submissions), Senftenberg (12.9%), and Heidelberg and Uganda (9.6% each) were most common among turkey breeders. Salmonella enterica ser. Enteritidis prevalence was highest in submissions from broiler breeders (3.7% of 682 broiler breeder submissions). Temporal clusters of S. enterica serovars were identified for all poultry commodities. Seasonal effects varied by commodity, with most peaks occurring in the fall. Our study provides information on the prevalence and temporality of S. enterica serovars within Ontario's poultry breeder flocks that might guide prevention and control programs at the breeder level.
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Affiliation(s)
- Carolyn E. Murray
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada
| | - Csaba Varga
- Department of Pathobiology, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Urbana, IL 61802, USA
| | - Rachel Ouckama
- Maple Lodge Hatcheries Ltd., Port Hope, ON L1A 3V5, Canada
| | - Michele T. Guerin
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada
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15
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Jiang B, Xu H, Zhou Z. Septic arthritis with osteomyelitis due to Salmonella enterica serotype Dublin: A case series. Front Surg 2023; 9:1069141. [PMID: 36684367 PMCID: PMC9852604 DOI: 10.3389/fsurg.2022.1069141] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/13/2022] [Accepted: 11/21/2022] [Indexed: 01/09/2023] Open
Abstract
Background Septic arthritis with osteomyelitis due to Salmonella enterica serotype Dublin is rare. We reviewed and analyzed cases of septic arthritis with osteomyelitis due to Salmonella enterica serotype Dublin seen at our institution. Methods The medical records of all patients diagnosed with Salmonella septic arthritis and/or Salmonella osteomyelitis during 2017-2022 were included. We reviewed the diagnosis, medical history, clinical management, and outcome of all cases. Results Five patients with Salmonella septic arthritis or Salmonella osteomyelitis were identified during the 5-year study period. They were all male; the median age was 53 years (range 15-56). Only one was immunodeficient. All five patients were infected at the hip joint and ipsilateral femur, while two suffered bilateral hip septic arthritis with femoral osteomyelitis. Salmonella Dublin was isolated from the hip joint fluid of all patients. Four presented with fever and constitutional signs within four weeks of symptom onset. Four had positive blood cultures, and only one patient had gastrointestinal symptoms. Four patients underwent surgical debridement as the primary surgical plan, and two underwent secondary two-stage exchange after primary surgical debridement failure. The last patient had a two-stage exchange directly as the first surgical treatment. All patients received intravenous antimicrobial therapy for a median duration of 6 (range 4-12) weeks and oral antimicrobial therapy for a median duration of 4 (range 4-6) weeks. All patients had a median duration of follow-up of 12 months (range 9-25), and none had evidence of recurrence of infection. Conclusions Septic arthritis due to Salmonella Dublin remains rare. It frequently occurs with ipsilateral femur osteomyelitis adjacent to the infected hip joint in our cases. Surgical debridement or two-stage exchange, along with 4-12 weeks of effective intravenous and followed by 4-6 oral antimicrobial therapy, could successfully eradicate the infection.
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Ali MC, Khatun MS, Jahan SI, Das R, Munni YA, Rahman MM, Dash R. In silico design of epitope-based peptide vaccine against non-typhoidal Salmonella through immunoinformatic approaches. J Biomol Struct Dyn 2022; 40:10696-10714. [PMID: 36529187 DOI: 10.1080/07391102.2021.1947381] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/20/2022]
Abstract
Non-typhoidal Salmonella (NTS) is one of the leading bacterial causes of many invasive human infections with a high antibiotic resistance profile. With this concern, the current study aimed to design an effective epitope-based peptide vaccine against NTS species as a successive and substitutive protective measure of invasive NTS disease. To design rationally, the current study considered a comprehensive in silico workflow combination of both immunoinformatics and molecular modeling approaches, including molecular docking and molecular dynamics (MD) simulation. We identified the two most promising T cell epitopes KVLYGIFAI and YGIFAITAL, and three B cell epitopes AAPVQVGEAAGS, TGGGDGSNT, and TGGGDGSNTGTTTT, in the outer membrane of NTS. Using these epitopes, a multiepitope vaccine was subsequently constructed along with appropriate adjuvant and linkers, which showed a good binding affinity and stability with toll-like receptor 2 (TLR2) in both molecular docking and MD simulation. Furthermore, in silico immune simulation described a strong immune response with a high number of antibodies, interferon-γ, and activated B and T cells. This study collectively suggests that predicted vaccine constructs could be considered potential vaccine candidates against common NTS species.Communicated by Ramaswamy H. Sarma.
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Affiliation(s)
- Md Chayan Ali
- Department of Biotechnology & Genetic Engineering, Faculty of Biological Sciences, Islamic University, Kushtia, Bangladesh
| | - Mst Shanzeda Khatun
- Department of Biotechnology & Genetic Engineering, Faculty of Biological Sciences, Islamic University, Kushtia, Bangladesh
| | - Sultana Israt Jahan
- Department of Biotechnology & Genetic Engineering, Noakhali Science and Technology University, Noakhali, Bangladesh
| | - Raju Das
- Department of Physiology, Dongguk University College of Medicine, Gyeongju, Republic of Korea
| | - Yeasmin Akter Munni
- Department of Anatomy, Dongguk University College of Medicine, Gyeongju, Republic of Korea
| | - Md Mafizur Rahman
- Department of Biotechnology & Genetic Engineering, Faculty of Biological Sciences, Islamic University, Kushtia, Bangladesh
| | - Raju Dash
- Department of Anatomy, Dongguk University College of Medicine, Gyeongju, Republic of Korea
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17
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Heating Rate during Shell Egg Thermal Treatment Elicits Stress Responses and Alters Virulence of Salmonella enterica Serovar Enteritidis; Implications for Shell Egg Pasteurization. Appl Environ Microbiol 2022; 88:e0114022. [PMID: 36197091 PMCID: PMC9599327 DOI: 10.1128/aem.01140-22] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/20/2022] Open
Abstract
Thermal pasteurization of shell eggs, at various time-temperature combinations, has been proposed previously and implemented industrially. This study was conducted to determine if shell egg heating rate, which varies with different pasteurization implementations, alters the Salmonella enterica serovar Enteritidis response to different stresses or expression of virulence. Shell eggs, containing Salmonella Enteritidis in yolk, were subjected to a low (2.4°C/min) or a high (3.5°C/min) heating rate during treatments that mimicked the pasteurization temperature come-up stage. The low heating rate protected Salmonella from the following processes: (i) lethal heat at the holding stage, (ii) loss of viability during 8-h cooling after heating, and (iii) sequential antimicrobial ozone treatment. Transcriptional analysis using Salmonella reporter strains revealed that the heat stress response gene grpE was transcribed at 3-fold-higher levels (P = 0.0009) at the low than at the high heating rate. Slow heating also significantly increased the transcription of the Salmonella virulence-related genes sopB (P = 0.0012) and sseA (P = 0.0006) in comparison to fast heating. Salmonella virulence was determined experimentally as 50% lethal dose (LD50) values in an in vivo model. The slow heat treatment mildly increased Salmonella Enteritidis virulence in mice (LD50 of 3.3 log CFU), compared to that in nontreated yolk (LD50 of 3.9 log CFU). However, when ozone application followed the slow heat treatment, Salmonella virulence decreased (LD50 of 4.2 log CFU) compared to that for heat-treated or nontreated yolk. In conclusion, heating shell eggs at a low rate can trigger hazardous responses that may compromise the safety of the final pasteurized products but following the thermal treatment with ozone application may help alleviate these concerns. IMPORTANCE Pasteurization of shell eggs is an important technology designed to protect consumers against Salmonella Enteritidis that contaminates this commodity. A low heating rate is preferred over a high rate during shell egg thermal pasteurization due to product quality concern. However, it is not known whether raising the temperature at different rates, during pasteurizing, would potentially affect product safety determinants. The current study demonstrated that slow heating during the pasteurization come-up stage increased the following risks: (i) resistance of Salmonella to pasteurization holding stage or to subsequent ozone treatment, (ii) recovery of Salmonella during the cooling that followed pasteurization, and (iii) Salmonella's ability to cause disease (i.e., virulence). Our findings inform food processors about potential safety risks to consumers resulting from improper use of processing parameters during shell egg pasteurization. Additionally, treating shell eggs with ozone after heat treatment could alleviate these hazards and protect consumers from natural Salmonella Enteritidis contaminants in shell eggs.
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18
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Khatun MF, Khan MAS, Ahmed MF, Rahman MM, Rahman SR. Assessment of foodborne transmission of
Salmonella enteritidis
in hens and eggs in Bangladesh. Vet Med Sci 2022; 8:2032-2039. [PMID: 35776098 PMCID: PMC9514458 DOI: 10.1002/vms3.874] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/11/2022] Open
Abstract
Objectives Salmonella is considered one of the leading causes of foodborne illnesses worldwide. Information about the transmission of pathogens to poultry and poultry products is necessary to implement control measures for reducing both human exposure and economic loss. The aim of this study was to analyze and evaluate the transmission characteristics of Salmonella enteritidis to laying‐type hen flocks and their laid eggs. Materials and methods For this purpose, 15 pairs of laying hens were used in which each pair consisted of one inoculated and one contact exposed hen. The eggs and cloacal swabs from these hens were subsequently analyzed. Results Of the 15 in‐contact hens tested, 60% were found to be positive for S. enteritidis within 61 days postinoculation, of which 26.7% transmission occurred within the first 31 days postinoculation. Among the collected laid eggs tested, S. enteritidis was detected on 58% eggshells and 5.33% eggs internal contents. We also observed a 33.33% reduction in egg production from S. enteritidis‐infected hens. In a cross‐contamination study, we demonstrated that an experimentally inoculated container can act as a potential source of Salmonella spp. infection. Conclusions Our results will help establish effective monitoring programs to reduce the transmission of Salmonella spp. in poultry and poultry products.
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Affiliation(s)
| | | | - Md Firoz Ahmed
- Department of Microbiology Jahangirnagar University Dhaka Bangladesh
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19
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Pettengill JB, Rand H, Wang SS, Kautter D, Pightling A, Wang Y. Transient and resident pathogens: Intra-facility genetic diversity of Listeria monocytogenes and Salmonella from food production environments. PLoS One 2022; 17:e0268470. [PMID: 36048885 PMCID: PMC9436056 DOI: 10.1371/journal.pone.0268470] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/05/2021] [Accepted: 05/01/2022] [Indexed: 11/18/2022] Open
Abstract
Food production facilities are often routinely tested over time for the presence of foodborne pathogens (e.g., Listeria monocytogenes or Salmonella enterica subsp. enterica). Strains detected in a single sampling event can be classified as transient; positive findings of the same strain across multiple sampling events can be classified as resident pathogens. We analyzed whole-genome sequence (WGS) data from 4,758 isolates (L. monocytogenes = 3,685; Salmonella = 1,073) from environmental samples taken by FDA from 536 U.S. facilities. Our primary objective was to determine the frequency of transient or resident pathogens within food production facilities. Strains were defined as isolates from the same facility that are less than 50 SNP (single-nucleotide polymorphisms) different from one another. Resident pathogens were defined as strains that had more than one isolate collected >59 days apart and from the same facility. We found 1,076 strains (median = 1 and maximum = 21 strains per facility); 180 were resident pathogens, 659 were transient, and 237 came from facilities that had only been sampled once. As a result, 21% of strains (180/ 839) from facilities with positive findings and that were sampled multiple times were found to be resident pathogens; nearly 1 in 4 (23%) of L. monocytogenes strains were found to be resident pathogens compared to 1 in 6 (16%) of Salmonella strains. Our results emphasize the critical importance of preventing the colonization of food production environments by foodborne pathogens, since when colonization does occur, there is an appreciable chance it will become a resident pathogen that presents an ongoing potential to contaminate product.
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Affiliation(s)
- James B. Pettengill
- Biostatistics and Bioinformatics Staff, Office of Analytics and Outreach, Center for Food Safety and Applied Nutrition, US Food and Drug Administration, College Park, MD, United States of America
- * E-mail:
| | - Hugh Rand
- Biostatistics and Bioinformatics Staff, Office of Analytics and Outreach, Center for Food Safety and Applied Nutrition, US Food and Drug Administration, College Park, MD, United States of America
| | - Shizhen S. Wang
- Biostatistics and Bioinformatics Staff, Office of Analytics and Outreach, Center for Food Safety and Applied Nutrition, US Food and Drug Administration, College Park, MD, United States of America
| | - Donald Kautter
- Division Of Plant Products & Beverages, Office of Food Safety, Center for Food Safety and Applied Nutrition; US Food and Drug Administration, College Park, MD, United States of America
| | - Arthur Pightling
- Biostatistics and Bioinformatics Staff, Office of Analytics and Outreach, Center for Food Safety and Applied Nutrition, US Food and Drug Administration, College Park, MD, United States of America
| | - Yu Wang
- Biostatistics and Bioinformatics Staff, Office of Analytics and Outreach, Center for Food Safety and Applied Nutrition, US Food and Drug Administration, College Park, MD, United States of America
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20
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da Silva Pires PG, Bavaresco C, Moraes PDO. Hundred years of knowledge on table egg refrigeration. WORLD POULTRY SCI J 2022. [DOI: 10.1080/00439339.2022.2105276] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/15/2022]
Affiliation(s)
- Paula Gabriela da Silva Pires
- Faculdade de Agronomia, Department of Animal Science, Universidade Federal Do Rio Grande Do Sul, Campus of Porto Alegre-RS, Brazil
| | | | - Priscila de Oliveira Moraes
- School of Agricultural Sciences, Department of Animal Sciences and Rural Development, Universidade Federal de Santa Catarina, Campus of Florianópolis, Brazil
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21
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Xu Y, Abdelhamid AG, Sabag-Daigle A, Sovic MG, Ahmer BM, Yousef AE. The Role of Egg Yolk in Modulating the Virulence of Salmonella Enterica Serovar Enteritidis. Front Cell Infect Microbiol 2022; 12:903979. [PMID: 35774398 PMCID: PMC9237210 DOI: 10.3389/fcimb.2022.903979] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/24/2022] [Accepted: 04/15/2022] [Indexed: 11/13/2022] Open
Abstract
Contribution of food vehicles to pathogenicity of disease-causing microorganisms is an important but overlooked research field. The current study was initiated to reveal the relationship between virulence of Salmonella enterica serovar Enteritidis and egg yolk as a hosting medium. Mice were orally challenged with Salmonella Enteritidis cultured in egg yolk or tryptic soy broth (TSB). Additionally, mice were challenged with Salmonella Enteritidis cultured in TSB, followed by administration of sterile egg yolk, to discern the difference between pre-growth of the pathogen and its mere presence in egg yolk during infection. The pathogen's Lethal dose 50 (LD50) was the lowest when grown in yolk (2.8×102 CFU), compared to 1.1×103 CFU in TSB, and 4.6×103 CFU in TSB followed by administration of sterile yolk. Additionally, mice that orally received Salmonella Enteritidis grown in egg yolk expressed a high death rate. These findings were supported by transcriptional analysis results. Expression of promoters of virulence-related genes (sopB and sseA) in genetically modified Salmonella Enteritidis reporter strains was significantly higher (p < 0.05) when the bacterium was grown in the yolk, compared to that grown in TSB. Sequencing of RNA (RNA-seq) revealed 204 differentially transcribed genes in Salmonella Enteritidis grown in yolk vs. TSB. Yolk-grown Salmonella Enteritidis exhibited upregulated virulence pathways, including type III secretion systems, epithelial cell invasion, and infection processes; these observations were confirmed by RT-qPCR results. The transcriptomic analysis suggested that upregulation of virulence machinery of Salmonella Enteritidis grown in egg yolk was related to increased iron uptake, biotin utilization, flagellar biosynthesis, and export of virulence proteins encoded on Salmonella pathogenicity island 1, 2, 4, and 5. These biological responses may have acted in concert to increase the virulence of Salmonella infection in mice. In conclusion, growth in egg yolk enhanced Salmonella Enteritidis virulence, indicating the significance of this food vehicle to the risk assessment of salmonellosis.
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Affiliation(s)
- Yumin Xu
- Department of Food Science and Technology, The Ohio State University, Columbus, OH, United States
| | - Ahmed G. Abdelhamid
- Department of Food Science and Technology, The Ohio State University, Columbus, OH, United States
- Botany and Microbiology Department, Faculty of Science, Benha University, Benha, Egypt
| | - Anice Sabag-Daigle
- Department of Microbial Infection and Immunity, The Ohio State University, Columbus, OH, United States
| | - Michael G. Sovic
- Center for Applied Plant Sciences, The Ohio State University, Columbus, OH, United States
| | - Brian M.M. Ahmer
- Department of Microbial Infection and Immunity, The Ohio State University, Columbus, OH, United States
| | - Ahmed E. Yousef
- Department of Food Science and Technology, The Ohio State University, Columbus, OH, United States
- Department of Microbiology, The Ohio State University, Columbus, OH, United States
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22
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Stilz CR, Cavallo S, Garman K, Dunn JR. Salmonella Enteritidis Outbreaks Associated with Egg-Producing Farms Not Regulated by Food and Drug Administration's Egg Safety Rule. Foodborne Pathog Dis 2022; 19:529-534. [DOI: 10.1089/fpd.2022.0025] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/12/2022] Open
Affiliation(s)
- Charles Robert Stilz
- Department of Biomedical and Diagnostic Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, Tennessee, USA
| | - Steffany Cavallo
- Communicable and Environmental Diseases and Emergency Preparedness Division, Tennessee Department of Health, Nashville, Tennessee, USA
| | - Katie Garman
- Communicable and Environmental Diseases and Emergency Preparedness Division, Tennessee Department of Health, Nashville, Tennessee, USA
| | - John R. Dunn
- Communicable and Environmental Diseases and Emergency Preparedness Division, Tennessee Department of Health, Nashville, Tennessee, USA
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23
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Jiang M, Yang C, Kwan PSL, Zhang L, Fan H, Jin Y, Sun L, Chen H, Li B, Chen Q, Wu Y, Guo Y, Shi Y, Liao M, Shi X, Liu J, Jiang L, Cai R, Deng Y, Sun Q, Yang R, Zhang Q, Cui Y, Hu Q. Rapid Multilateral and Integrated Public Health Response to a Cross-City Outbreak of Salmonella Enteritidis Infections Combining Analytical, Molecular, and Genomic Epidemiological Analysis. Front Microbiol 2022; 13:772489. [PMID: 35602015 PMCID: PMC9117964 DOI: 10.3389/fmicb.2022.772489] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/08/2021] [Accepted: 03/28/2022] [Indexed: 11/13/2022] Open
Abstract
On September 21, 2019, the Shenzhen and Dongguan Centers for Disease Control and Prevention received notification of a large cluster of suspected gastroenteritis involving primarily children who sought medical care at hospitals throughout two adjacent cities in China, Shenzhen, and Dongguan. A joint outbreak response was promptly initiated across jurisdictions in a concerted effort between clinical microbiologists, epidemiologists, and public health scientists. Concurrently, multiplex PCRs were used for rapid laboratory diagnosis of suspected cases; epidemiological investigations were conducted to identify the outbreak source, complemented by near real-time multicenter whole-genome analyses completed within 34 h. Epidemiological evidence indicated that all patients had consumed egg sandwiches served on September 20 as snacks to children and staff at a nursery in Dongguan, located near Shenzhen. Salmonella Enteritidis was isolated from case-patients, food handlers, kitchenware, and sandwiches with kitchen-made mayonnaise. Whole-genome single-nucleotide polymorphism (SNP)-based phylogenetic analysis demonstrated a well-supported cluster with pairwise distances of ≤1 SNP between genomes for outbreak-associated isolates, providing the definitive link between all samples. In comparison with historical isolates from the same geographical region, the minimum pairwise distance was >14 SNPs, suggesting a non-local outbreak source. Genomic source tracing revealed the possible transmission dynamics of a S. Enteritidis clone throughout a multi-provincial egg distribution network. The efficiency and scale with which multidisciplinary and integrated approaches were coordinated in this foodborne disease outbreak response was unprecedented in China, leading to the timely intervention of a large cross-jurisdiction Salmonella outbreak.
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Affiliation(s)
- Min Jiang
- Shenzhen Major Infectious Disease Control Key Laboratory, Shenzhen Center for Disease Control and Prevention, Shenzhen, China
| | - Chao Yang
- Shenzhen Major Infectious Disease Control Key Laboratory, Shenzhen Center for Disease Control and Prevention, Shenzhen, China
| | - Patrick S L Kwan
- Shenzhen Major Infectious Disease Control Key Laboratory, Shenzhen Center for Disease Control and Prevention, Shenzhen, China
| | - Liping Zhang
- Microbiology Laboratory, Dongguan Center for Disease Control and Prevention, Guangdong, China
| | - Hang Fan
- State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China
| | - Yujuan Jin
- Microbiology Laboratory, Longgang District Center for Disease Control and Prevention, Shenzhen, China
| | - Lifang Sun
- Department of Laboratory Medicine, Shenzhen Children's Hospital, Shenzhen, China
| | - Hongyu Chen
- Department of Laboratory Medicine, Shenzhen Children's Hospital, Shenzhen, China
| | - Baisheng Li
- Microbiology Laboratory, Guangdong Center for Disease Control and Prevention, Guangdong, China
| | - Qiuxia Chen
- Microbiology Laboratory, Guangdong Center for Disease Control and Prevention, Guangdong, China
| | - Yarong Wu
- State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China
| | - Yan Guo
- State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China
| | - Yuanguo Shi
- Division of Biohazard Inspection and Testing, Shenzhen Institute of Quality & Safety Inspection and Research, Shenzhen, China
| | - Min Liao
- Division of Biohazard Inspection and Testing, Shenzhen Institute of Quality & Safety Inspection and Research, Shenzhen, China
| | - Xiaolu Shi
- Shenzhen Major Infectious Disease Control Key Laboratory, Shenzhen Center for Disease Control and Prevention, Shenzhen, China
| | - Jianping Liu
- Shenzhen Major Infectious Disease Control Key Laboratory, Shenzhen Center for Disease Control and Prevention, Shenzhen, China
| | - Lijuan Jiang
- Shenzhen Major Infectious Disease Control Key Laboratory, Shenzhen Center for Disease Control and Prevention, Shenzhen, China
| | - Rui Cai
- Shenzhen Major Infectious Disease Control Key Laboratory, Shenzhen Center for Disease Control and Prevention, Shenzhen, China
| | - Yinhua Deng
- Shenzhen Major Infectious Disease Control Key Laboratory, Shenzhen Center for Disease Control and Prevention, Shenzhen, China
| | - Qun Sun
- Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China
| | - Ruifu Yang
- State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China
| | - Qiaoli Zhang
- Microbiology Laboratory, Dongguan Center for Disease Control and Prevention, Guangdong, China
| | - Yujun Cui
- State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China
| | - Qinghua Hu
- Shenzhen Major Infectious Disease Control Key Laboratory, Shenzhen Center for Disease Control and Prevention, Shenzhen, China
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24
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El-Saadony MT, Salem HM, El-Tahan AM, Abd El-Mageed TA, Soliman SM, Khafaga AF, Swelum AA, Ahmed AE, Alshammari FA, Abd El-Hack ME. The control of poultry salmonellosis using organic agents: an updated overview. Poult Sci 2022; 101:101716. [PMID: 35176704 PMCID: PMC8857471 DOI: 10.1016/j.psj.2022.101716] [Citation(s) in RCA: 48] [Impact Index Per Article: 16.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/05/2021] [Revised: 12/29/2021] [Accepted: 01/05/2022] [Indexed: 02/06/2023] Open
Abstract
Salmonellosis is a severe problem that threatens the poultry sector worldwide right now. Salmonella gallinarium and Salmonella pullorum (Fowl typhoid) are the most pathogenic serovars in avian species leading to systemic infection resulting in severe economic losses in the poultry industry. Nontyphoidal serotypes of Salmonella (Paratyphoid disease) constitute a public health hazard for their involvement in food poisoning problems in addition to their zoonotic importance. Also, Salmonella species distribution is particularly extensive. They resisted environmental conditions that made it difficult to control their spread for a long time. Therefore, the current review aimed to through light on Salmonellosis in poultry with particular references to its pathogenesis, economic importance, immune response to Salmonella, Salmonella antibiotics resistance, possible methods for prevention and control of such problems using promising antibiotics alternatives including probiotics, prebiotics, symbiotics, organic acids, essential oils, cinnamaldehyde, chitosan, nanoparticles, and vaccines.
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Affiliation(s)
- Mohamed T El-Saadony
- Department of Agricultural Microbiology, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt
| | - Heba M Salem
- Department of Poultry Diseases, Faculty of Veterinary Medicine, Cairo University 12211, Giza, Egypt
| | - Amira M El-Tahan
- Plant Production Department, Arid Lands Cultivation Research Institute, The City of Scientific Research and Technological Applications, Alexandria, Egypt
| | - Taia A Abd El-Mageed
- Soil and Water Department, Faculty of Agriculture, Fayoum University, Fayoum 63514, Egypt
| | - Soliman M Soliman
- Department of Medicine and Infectious Diseases, Faculty of Veterinary Medicine, Cairo University 1221, Giza, Egypt
| | - Asmaa F Khafaga
- Department of Pathology, Faculty of Veterinary Medicine, Alexandria University, Edfina 22758, Egypt
| | - Ayman A Swelum
- Department of Animal production, College of Food and Agriculture Sciences, King Saud University, Riyadh 11451, Saudi Arabia; Department of Theriogenology, Faculty of Veterinary Medicine, Zagazig University, Sharkia 44519, Egypt
| | - Ahmed E Ahmed
- Biology Department, College of Science, King Khalid University 61413 Abha, Saudi Arabia; Department of Theriogenology, Faculty of Veterinary Medicine, South Valley University 83523 Qena, Egypt
| | - Fahdah A Alshammari
- Department of Biology, College of Sciences and Literature, Northern Border University, Rafha 76312, Saudi Arabia
| | - Mohamed E Abd El-Hack
- Poultry Department, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt.
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25
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Murphy CM, Weller DL, Reiter MS, Bardsley CA, Eifert J, Ponder M, Rideout SL, Strawn LK. Anaerobic soil disinfestation, amendment-type, and irrigation regimen influence Salmonella survival and die-off in agricultural soils. J Appl Microbiol 2022; 132:2342-2354. [PMID: 34637586 PMCID: PMC8860855 DOI: 10.1111/jam.15324] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/25/2021] [Revised: 09/27/2021] [Accepted: 10/04/2021] [Indexed: 11/29/2022]
Abstract
AIMS This study investigated Salmonella concentrations following combinations of horticultural practices including anaerobic soil disinfestation (ASD), soil amendment type and irrigation regimen. METHODS AND RESULTS Sandy-loam soil was inoculated with a five-serovar Salmonella cocktail (5.5 ± 0.2 log CFU per gram) and subjected to one of six treatments: (i) no soil amendment, ASD (ASD control), (ii) no soil amendment, no-ASD (non-ASD control) and (iii-vi) soil amended with pelletized poultry litter, rye, rapeseed or hairy vetch with ASD. The effect of irrigation regimen was determined by collecting samples 3 and 7 days after irrigation. Twenty-five-gram soil samples were collected pre-ASD, post-soil saturation (i.e. ASD-process), and at 14 time-points post-ASD, and Salmonella levels enumerated. Log-linear models examined the effect of amendment type and irrigation regimen on Salmonella die-off during and post-ASD. During ASD, Salmonella concentrations significantly decreased in all treatments (range: -0.2 to -2.7 log CFU per gram), albeit the smallest decrease (-0.2 log CFU per gram observed in the pelletized poultry litter) was of negligible magnitude. Salmonella die-off rates varied by amendment with an average post-ASD rate of -0.05 log CFU per gram day (CI = -0.05, -0.04). Salmonella concentrations remained highest over the 42 days post-ASD in pelletized poultry litter, followed by rapeseed, and hairy vetch treatments. Findings suggested ASD was not able to eliminate Salmonella in soil, and certain soil amendments facilitated enhanced Salmonella survival. Salmonella serovar distribution differed by treatment with pelletized poultry litter supporting S. Newport survival, compared with other serovars. Irrigation appeared to assist Salmonella survival with concentrations being 0.14 log CFU per gram (CI = 0.05, 0.23) greater 3 days, compared with 7 days post-irrigation. CONCLUSIONS ASD does not eliminate Salmonella in soil, and may in fact, depending on the soil amendment used, facilitate Salmonella survival. SIGNIFICANCE AND IMPACT OF THE STUDY Synergistic and antagonistic effects on food safety hazards of implementing horticultural practices should be considered.
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Affiliation(s)
- Claire M. Murphy
- Department of Food Science and Technology, Virginia Tech, Blacksburg, VA 24061, USA
| | - Daniel L. Weller
- Department of Biostatistics and Computational Biology, University of Rochester, Rochester, NY, 14627, USA
| | - Mark S. Reiter
- Eastern Shore Agricultural Research and Extension Center, Virginia Tech, Painter, VA 23420, USA
| | - Cameron A. Bardsley
- Department of Food Science and Technology, Virginia Tech, Blacksburg, VA 24061, USA
| | - Joseph Eifert
- Department of Food Science and Technology, Virginia Tech, Blacksburg, VA 24061, USA
| | - Monica Ponder
- Department of Food Science and Technology, Virginia Tech, Blacksburg, VA 24061, USA
| | - Steve L. Rideout
- School of Plant and Environmental Sciences, Virginia Tech, Blacksburg, VA 24061, USA
| | - Laura K. Strawn
- Department of Food Science and Technology, Virginia Tech, Blacksburg, VA 24061, USA,Author for correspondence. Laura K. Strawn, Department of Food Science and Technology, Virginia Tech, 1230 Washington Street, SW, Blacksburg, VA 24061, USA. Tel: 540-231-6806; Fax: 540-231-9293;
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Medina-Santana JL, Ortega-Paredes D, de Janon S, Burnett E, Ishida M, Sauders B, Stevens M, Vinueza-Burgos C. Investigating the dynamics of Salmonella contamination in integrated poultry companies using a whole genome sequencing approach. Poult Sci 2022; 101:101611. [PMID: 34953378 PMCID: PMC8715213 DOI: 10.1016/j.psj.2021.101611] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/16/2021] [Revised: 11/08/2021] [Accepted: 11/09/2021] [Indexed: 11/22/2022] Open
Abstract
The study of non-typhoid Salmonella in broiler integrations has been limited by the resolution of typing techniques. Although serotyping of Salmonella isolates is used as a traditional approach, it is not of enough resolution to clearly understand the dynamics of this pathogen within poultry companies. The aim of this research was to investigate the epidemiology and population dynamics of Salmonella serotypes in 2 poultry integrations using a whole genome sequencing approach. Two hundred and forty-three Salmonella isolates recovered from the broiler production chain of 2 integrated poultry companies were whole genome sequenced and analyzed with dedicated databases and bioinformatic software. The analyses of sequences revealed that S. Infantis was the most frequent serotype (82.3%). Most isolates showed a potential for resistance against medically important antibiotics and disinfectants. Furthermore, 97.5% of isolates harbored the pESI-like mega plasmid, that plays an important role in the global dissemination of AMR. SNP tree analysis showed that there were clones that are niche-specific while other ones were distributed throughout the broiler production chains. In this study, we demonstrated the potential of whole genome sequencing analysis for a comprehensive understanding of Salmonella distribution in integrated poultry companies. Data obtained with these techniques allow determination of the presence of genetic factors that play an important role in the environmental fitness and pathogenicity of Salmonella.
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Affiliation(s)
- José L Medina-Santana
- 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 170103, Ecuador
| | - David Ortega-Paredes
- 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 170103, Ecuador
| | - Sofia de Janon
- 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 170103, Ecuador
| | - Elton Burnett
- Institute of Parasitology, McGill University, Montreal, QC H9X3V9, Canada
| | - Maria Ishida
- Division of Food Laboratory, New York State Department of Agriculture and Markets, Albany, NY 12206, USA
| | - Brian Sauders
- Division of Food Laboratory, New York State Department of Agriculture and Markets, Albany, NY 12206, USA
| | | | - Christian Vinueza-Burgos
- 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 170103, Ecuador.
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Tanui CK, Karanth S, Njage PM, Meng J, Pradhan AK. Machine learning-based predictive modeling to identify genotypic traits associated with Salmonella enterica disease endpoints in isolates from ground chicken. Lebensm Wiss Technol 2022. [DOI: 10.1016/j.lwt.2021.112701] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/12/2022]
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Sheen JM, Lin FJ, Yang YH, Kuo KC. Increased non-typhoidal Salmonella hospitalizations in transfusion-naïve thalassemia children: a nationwide population-based cohort study. Pediatr Res 2022; 91:1858-1863. [PMID: 34148067 PMCID: PMC9270223 DOI: 10.1038/s41390-021-01602-7] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/09/2020] [Revised: 03/09/2021] [Accepted: 05/20/2021] [Indexed: 02/04/2023]
Abstract
INTRODUCTION Although non-typhoidal Salmonella (NTS) infection usually causes self-limited enterocolitis, several risk factors have been found to predispose individuals to more severe NTS infections. However, few studies have discussed the association between NTS infection and pediatric thalassemia populations. MATERIAL AND METHODS A nationwide population-based retrospective cohort study was conducted using medical records of the selected children from the Taiwan National Health Insurance Research Database. Immunocompromised individuals or patients with a history of transfusion or splenectomy were excluded. One thalassemia patient was matched with four non-thalassemia patients based on their year of birth, sex, and urbanization level. RESULTS In this cohort, 912 patients with thalassemia and 3648 comparison cohort were analyzed. The mean age of NTS hospitalization was 2.0 ± 1.4 in thalassemia cohort and 2.6 ± 2.4 in non-thalassemia cohort. Transfusion-naïve thalassemia children were proved to have a higher rate of NTS hospitalization (6.90 vs 4.11 per 1000 person-year; p = 0.0004) than the non-thalassemia cohort, with an adjusted hazard ratio (HR) of 1.68 (95% confidence interval [CI] = 1.26-2.24). CONCLUSION Our research shows that transfusion-naïve thalassemia is associated with an increased risk of NTS hospitalization. Further prospective study comparing the incidence and severity of NTS infection among children with and without thalassemia is needed. IMPACT Pediatric transfusion-naïve thalassemia patients have an 1.68-fold increased risk for hospitalization due to non-typhoidal Salmonella (NTS) infection. This is the first nationwide population-based cohort study based on an extremely large database that shows pediatric transfusion-naïve thalassemia patients have an increased risk for NTS hospitalizations. Besides the previously known risk factors such as extremes of age, sickle cell disease, or immunosuppressing conditions, clinicians must also take thalassemia as a possible risk factor for more severe NTS disease.
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Affiliation(s)
- Jiunn-Ming Sheen
- grid.145695.a0000 0004 1798 0922Department of Pediatrics, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan ,grid.454212.40000 0004 1756 1410Department of Pediatrics, Chiayi Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Chiayi, Taiwan
| | - Fang-Ju Lin
- grid.145695.a0000 0004 1798 0922Department of Pediatrics, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Yao-Hsu Yang
- grid.454212.40000 0004 1756 1410Department of Traditional Chinese Medicine, Chang Gung Memorial Hospital, Chiayi, Taiwan ,grid.19188.390000 0004 0546 0241Institute of Occupational Medicine and Industrial Hygiene, National Taiwan University College of Public Health, Taipei, Taiwan
| | - Kuang-Che Kuo
- Department of Pediatrics, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan.
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Zakaria Z, Hassan L, Sharif Z, Ahmad N, Mohd Ali R, Amir Husin S, Mohamed Sohaimi N, Abu Bakar S, Garba B. Virulence Gene Profile, Antimicrobial Resistance and Multilocus Sequence Typing of Salmonella enterica Subsp. enterica Serovar Enteritidis from Chickens and Chicken Products. Animals (Basel) 2022; 12:ani12010097. [PMID: 35011203 PMCID: PMC8749576 DOI: 10.3390/ani12010097] [Citation(s) in RCA: 10] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/11/2021] [Revised: 11/01/2021] [Accepted: 11/04/2021] [Indexed: 01/19/2023] Open
Abstract
This study was undertaken to determine the virulence, antimicrobial resistance and molecular subtypes of Salmonella in the Central Region of Peninsular Malaysia. A total of 45 Salmonella Enteritidis were detected from live chicken (cloacal swab), and chicken products (fresh and ready-to-eat meat) samples upon cultural isolation and serotyping. Similarly, an antimicrobial susceptibility test based on the Kirby Bauer disk diffusion method as well as antimicrobial resistance AMR genes, virulence determinants and multilocus sequence typing (MLST) typing were conducted after the Whole Genome Sequencing and analysis of the isolates. The results indicate that sequence types ST1925 (63.7%), and ST11 (26.5%) were the predominant out of the seven sequence types identified (ST292, ST329, ST365, ST423 and ST2132). The phenotypic antimicrobial profile corresponds to the genotypic characterization in that the majority of the isolates that exhibited tetracycline, gentamycin and aminoglycoside resistance; they also possessed the tetC and blaTEM β-Lactam resistance genes. However, isolates from cloacal swabs showed the highest number of resistance genes compared to the chicken products (fresh and ready-to-eat meat) samples. Furthermore, most of the virulence genes were found to cluster in the Salmonella pathogenicity island (SPI). In this study, all the isolates were found to possess SPI-1, which codes for the type III secretion system, which functions as actin-binding proteins (SptP and SopE). The virulence plasmid (VP) genes (spvB, spvC) were present in all genotypes except ST365. The findings of this study, particularly with regard to the molecular subtypes and AMR profiles of the Salmonella Enteritidis serotype shows multidrug-resistance features as well as genetic characteristics indicative of high pathogenicity.
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Affiliation(s)
- Zunita Zakaria
- Institute of Bioscience, Universiti Putra Malaysia, Serdang 43400, Malaysia
- Department of Veterinary Pathology and Microbiology, Faculty of Veterinary Medicine, Universiti Putra Malaysia, Serdang 43400, Malaysia;
- Correspondence:
| | - Latiffah Hassan
- Department of Veterinary Laboratory Diagnostics, Faculty of Veterinary Medicine, Universiti Putra Malaysia, Serdang 43400, Malaysia; (L.H.); (N.M.S.)
| | - Zawiyah Sharif
- Food Safety and Quality Division, Ministry of Health, Putrajaya 62675, Malaysia; (Z.S.); (S.A.B.)
| | - Norazah Ahmad
- Veterinary Public Health Division, Department of Veterinary Services Malaysia, Putrajaya 62630, Malaysia; (N.A.); (R.M.A.)
| | - Rohaya Mohd Ali
- Veterinary Public Health Division, Department of Veterinary Services Malaysia, Putrajaya 62630, Malaysia; (N.A.); (R.M.A.)
| | - Suraya Amir Husin
- Medical Development Division, Ministry of Health, Putrajaya 62590, Malaysia;
| | - Norfitriah Mohamed Sohaimi
- Department of Veterinary Laboratory Diagnostics, Faculty of Veterinary Medicine, Universiti Putra Malaysia, Serdang 43400, Malaysia; (L.H.); (N.M.S.)
| | - Shafini Abu Bakar
- Food Safety and Quality Division, Ministry of Health, Putrajaya 62675, Malaysia; (Z.S.); (S.A.B.)
| | - Bashiru Garba
- Department of Veterinary Pathology and Microbiology, Faculty of Veterinary Medicine, Universiti Putra Malaysia, Serdang 43400, Malaysia;
- Faculty of Veterinary Medicine, Usmanu Danfodiyo University, Sultan Abubakar Road, City Campus Complex, Sokoto 840212, Nigeria
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Mihajilov-Krstev T, Joković N, Tamindžija D, Tamaš I, Stanković N, Stojanović-Radić Z, Volarić A, Radnović D. Decontamination of Salmonella enterica spp. on shell eggs by Allium cepa L. dry scales extracts. KRAGUJEVAC JOURNAL OF SCIENCE 2022. [DOI: 10.5937/kgjsci2244127m] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/02/2022] Open
Abstract
Salmonellae are a major global diarrheal diseases agent and are commonly found in a variety of foods. However, eggs appear to be one of the most important sources of infection ultimately leading to salmonellosis. Here we investigate a potential utilization of onion (Allium cepa L.) dry scales extracts and decoction for disinfection of eggshells contaminated with Salmonella enterica spp. Antimicrobial activity was screened by a microplate dilution method against 32 environmental and 1 reference Salmonella strains, at 106 and 103 CFU/ml starting cell concentration. Also, the efficacy of egg submersion treatment was tested. At high contamination level of 106 Salmonella cells per ml, extracts exhibited MIC and MBC values in the range of 0.08-2.50 mg/ml and 0.31-10.0 mg/ml, respectively. Ethanol extract had the most potent antibacterial activity followed by methanol, ethyl-acetate and acetone extracts. Pure decoction had MIC and MBC in the range of 250-500 mg/ml. When testing a lower level of contamination (103 CFU/ml) which is more similar to real life levels, MIC and MBCs were 8 to 14 times lower. Submersion of artificially contaminated eggs in ethanol extracts and decoctions resulted in the complete elimination of Salmonella after 8 minutes of exposure. Thus, a reduction of a minimum of 3.71 log units was achieved during the 8 minutes of treatment. Having in mind natural levels of Salmonella eggshell counts are far lower it can be implied that such treatment could be highly effective in practical application. Results show that tested onion dry scale decontamination solutions are an efficient, cost-effective and eco-friendly options for eggshell decontamination, and are especially promising for use in organic egg production.
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Murray CE, Varga C, Ouckama R, Guerin MT. Temporal Study of Salmonella enterica Serovars Isolated from Fluff Samples from Ontario Poultry Hatcheries between 2009 and 2018. Pathogens 2021; 11:9. [PMID: 35055957 PMCID: PMC8781519 DOI: 10.3390/pathogens11010009] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/30/2021] [Revised: 12/17/2021] [Accepted: 12/19/2021] [Indexed: 11/26/2022] Open
Abstract
The objectives of this study were to determine the prevalence, temporal trends, seasonal patterns, and temporal clustering of Salmonella enterica isolated from fluff samples from poultry hatcheries in Ontario between 2009 and 2018. A scan statistic was used to identify clusters of common serovars and those of human health concern. A multi-level logistic regression model was used to identify factors (poultry commodity, year, season) associated with S. enterica presence. The period prevalence of S. enterica was 7.5% in broiler hatcheries, 1.6% in layer hatcheries, 7.6% in turkey hatcheries, 29.7% in waterfowl hatcheries, and 13.8% in game-bird hatcheries. An overall increasing trend in S. enterica prevalence was identified in waterfowl and game-bird hatcheries, while a decreasing trend was identified in broiler and turkey hatcheries. Overall, the most common S. enterica serovars were Kentucky, Enteritidis, Heidelberg, and Senftenberg. Salmonella enterica ser. Enteritidis was the most common serovar in waterfowl hatcheries. Temporal clusters were identified for all poultry commodities. Seasonal effects varied by commodity, with the highest odds of S. enterica occurring in the summer and fall. Our study offers information on the prevalence and temporality of S. enterica serovars that might guide prevention and control programs at the hatchery level.
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Affiliation(s)
- Carolyn E. Murray
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada;
| | - Csaba Varga
- Department of Pathobiology, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Urbana, IL 61802, USA;
| | - Rachel Ouckama
- Maple Lodge Hatcheries Ltd., Port Hope, ON L1A 3V5, Canada;
| | - Michele T. Guerin
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada;
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Holt PS. Centennial Review: A revisiting of hen welfare and egg safety consequences of mandatory outdoor access for organic egg production. Poult Sci 2021; 100:101436. [PMID: 34768045 PMCID: PMC8592875 DOI: 10.1016/j.psj.2021.101436] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/13/2021] [Accepted: 07/26/2021] [Indexed: 11/10/2022] Open
Abstract
Mandating free range husbandry as a requirement for organic egg designation remains a prevailing sentiment within a segment of the organic community. The proponents maintain that such management practice ensures high hen welfare and enhanced wholesomeness of the egg. However, evidence from the field, especially in the European Union (EU), contradicts these assumptions. In many cases, hens allowed outdoor access were more subject to increased injury from predators and from flock mates, disease was more prevalent and generally more severe, and, as a result, higher mortality was routinely observed in these individuals compared with those raised indoors. The safety of eggs from free range hens is also questionable. Outdoor access compromises biosecurity efforts to curtail interaction of hens with rodents and wild birds, increasing the risk of flock Salmonella enterica serovar Enteritidis infection and consequent production of Salmonella-contaminated eggs. Even more serious, soil contaminated with dioxins and polychlorinated biphenyls, carcinogenic industrial by-products widespread in the environment, can be ingested by hens foraging outdoors. These compounds will subsequently be deposited into the egg yolks, many times at high levels, creating a serious food safety issue for the consuming public. Such findings provide evidence that hens exposed to a free-range environment may exhibit neither an enhanced welfare nor produce the safe wholesome egg that consumers expect.
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Affiliation(s)
- Peter S Holt
- Holt Consulting, P.O. Box 869, Winterville, GA 30683, USA.
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33
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Zhang Y, Song L, Hou L, Cao Z, Vongsangnak W, Zhu G, Xu Q, Chen G. Dual Transcriptomic Analyses Unveil Host-Pathogen Interactions Between Salmonella enterica Serovar Enteritidis and Laying Ducks ( Anas platyrhynchos). Front Microbiol 2021; 12:705712. [PMID: 34421865 PMCID: PMC8374152 DOI: 10.3389/fmicb.2021.705712] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/06/2021] [Accepted: 07/13/2021] [Indexed: 12/13/2022] Open
Abstract
Salmonella enteritidis (SE) is a pathogen that can readily infect ovarian tissues and colonize the granulosa cell layer such that it can be transmitted via eggs from infected poultry to humans in whom it can cause food poisoning. Ducks are an important egg-laying species that are susceptible to SE infection, yet the host–pathogen interactions between SE and ducks have not been thoroughly studied to date. Herein, we performed dual RNA-sequencing analyses of these two organisms in a time-resolved infection model of duck granulosa cells (dGCs) by SE. In total, 10,510 genes were significantly differentially expressed in host dGCs, and 265 genes were differentially expressed in SE over the course of infection. These differentially expressed genes (DEGs) of dGCs were enriched in the cytokine–cytokine receptor interaction pathway via KEGG analyses, and the DEGs in SE were enriched in the two-component system, bacterial secretion system, and metabolism of pathogen factors pathways as determined. A subsequent weighted gene co-expression network analysis revealed that the cytokine–cytokine receptor interaction pathway is mostly enriched at 6 h post-infection (hpi). Moreover, a number of pathogenic factors identified in the pathogen–host interaction database (PHI-base) are upregulated in SE, including genes encoding the pathogenicity island/component, type III secretion, and regulators of systemic infection. Furthermore, an intracellular network associated with the regulation of SE infection in ducks was constructed, and 16 cytokine response-related dGCs DEGs (including IL15, CD40, and CCR7) and 17 pathogenesis-related factors (including sseL, ompR, and fliC) were identified, respectively. Overall, these results not only offer new insights into the mechanisms underlying host–pathogen interactions between SE and ducks, but they may also aid in the selection of potential targets for antimicrobial drug development.
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Affiliation(s)
- Yu Zhang
- Joint International Research Laboratory of Agriculture and Agri-Product Safety, The Ministry of Education, Yangzhou University, Yangzhou, China.,College of Animal Science and Technology, Yangzhou University, Yangzhou, China
| | - Lina Song
- Joint International Research Laboratory of Agriculture and Agri-Product Safety, The Ministry of Education, Yangzhou University, Yangzhou, China.,College of Animal Science and Technology, Yangzhou University, Yangzhou, China
| | - Lie Hou
- College of Animal Science and Technology, Yangzhou University, Yangzhou, China
| | - Zhengfeng Cao
- College of Animal Science and Technology, Yangzhou University, Yangzhou, China
| | - Wanwipa Vongsangnak
- Department of Zoology, Faculty of Science, Kasetsart University, Bangkok, Thailand
| | - Guoqiang Zhu
- Joint International Research Laboratory of Agriculture and Agri-Product Safety, The Ministry of Education, Yangzhou University, Yangzhou, China
| | - Qi Xu
- Joint International Research Laboratory of Agriculture and Agri-Product Safety, The Ministry of Education, Yangzhou University, Yangzhou, China.,College of Animal Science and Technology, Yangzhou University, Yangzhou, China
| | - Guohong Chen
- Joint International Research Laboratory of Agriculture and Agri-Product Safety, The Ministry of Education, Yangzhou University, Yangzhou, China.,College of Animal Science and Technology, Yangzhou University, Yangzhou, China
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35
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Abstract
Acute bacterial gastroenteritis is among the most common infections worldwide, with millions of infections annually in the United States. Much of the illness is foodborne, occurring as both sporadic cases and large multistate outbreaks. Pathogen evolution through genetic exchange of virulence traits and antibiotic resistance determinants poses challenges for empiric therapy. Culture-independent diagnostic tests in clinical laboratories afford rapid diagnosis and expanded identification of pathogens. However, cultures remain important to generate sensitivity data and strain archiving for outbreak investigations. Most infections are self-limited, permitting judicious selection of antibiotic use in more severe forms of illness.
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Affiliation(s)
- James M Fleckenstein
- Department of Medicine, Division of Infectious Diseases, Washington University in Saint Louis, School of Medicine, Campus Box 8051, 660 South Euclid Avenue, Saint Louis, MO 63110, USA; Infectious Disease Section, Medicine Service, Veterans Affairs Saint Louis Health Care System, 915 North Grand Boulevard, Saint Louis, MO 63106, USA.
| | - F Matthew Kuhlmann
- Department of Medicine, Division of Infectious Diseases, Washington University in Saint Louis, School of Medicine, Campus Box 8051, 660 South Euclid Avenue, Saint Louis, MO 63110, USA
| | - Alaullah Sheikh
- Department of Medicine, Division of Infectious Diseases, Washington University in Saint Louis, School of Medicine, Campus Box 8051, 660 South Euclid Avenue, Saint Louis, MO 63110, USA
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36
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Overview of the Use of Probiotics in Poultry Production. Animals (Basel) 2021; 11:ani11061620. [PMID: 34072694 PMCID: PMC8230106 DOI: 10.3390/ani11061620] [Citation(s) in RCA: 46] [Impact Index Per Article: 11.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/23/2021] [Revised: 05/17/2021] [Accepted: 05/27/2021] [Indexed: 12/18/2022] Open
Abstract
Simple Summary Probiotics are feed additives that have gained popularity in poultry production following the ban of antibiotic growth promoters (AGP). They are one of the more universal feed additives and can be easily combine with other additives. Probiotics, above all, have many advantages, including stimulation of the host microflora or immunomodulation. The statement “immunity comes from the intestines” has become more important in the poultry industry because probiotics have proven helpful in the fight against diseases of bacterial origin and against zoonoses. Positive effects on the organism have already been studied at the cellular level, where probiotics were responsible for changes in gene expression, leading to alleviation of heat stress. In addition to the health benefits, the utility value of the animals increases. The numerous advantages are overshadowed by a few drawbacks, which include the possibility of lowering semen quality in roosters and the diversity of production processes affecting the persistence of the probiotic. In addition to bird health, probiotics have improved the taste and quality of poultry products. Future prospects are promising as scientists are working to maximize the positive effects of probiotics by increasing the integrity of probiotics within the bird organism, taking into account, among others, bacterial metabolites. Abstract In recent years, probiotics have become more popular in the world of dietary supplements and feed additives within the poultry industry, acting as antibiotic substitutes. Above all, probiotics are universal feed additives that can be used in conjunction with other additives to promote improved performance and health. Their positive effects can be observed directly in the gastrointestinal tract and indirectly in immunomodulation of the poultry immune system. Nutritional effects seen in flocks given probiotics include increased laying and egg quality, increased daily increments, and improved feed conversion ratio (FCR). There has also been an improvement in the quality of meat. This suggests producers can improve production results through the use of probiotics. In addition to these production effects, bird immunity is improved by allowing the organism to better protect itself against pathogens and stress. The lack of accuracy in the formulation of non-European preparations needs to be further developed due to unknown interactions between probiotic bacteria strains as well as their metabolites. The versatility of probiotics and the fact that the bacteria used in their production are an integral part of animal digestive tracts make them a safe feed additives. Despite restrictions from the European Union, probiotics have potential to improve production and health within the poultry industry and beyond. The following article will review the use of probiotics in poultry production.
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Cardoso MJ, Nicolau AI, Borda D, Nielsen L, Maia RL, Møretrø T, Ferreira V, Knøchel S, Langsrud S, Teixeira P. Salmonella in eggs: From shopping to consumption-A review providing an evidence-based analysis of risk factors. Compr Rev Food Sci Food Saf 2021; 20:2716-2741. [PMID: 33960652 DOI: 10.1111/1541-4337.12753] [Citation(s) in RCA: 28] [Impact Index Per Article: 7.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/17/2020] [Revised: 02/20/2021] [Accepted: 03/16/2021] [Indexed: 11/28/2022]
Abstract
Nontyphoidal salmonellae are among the most prevalent foodborne pathogens causing gastrointestinal infections worldwide. A high number of cases and outbreaks of salmonellosis are associated with the consumption of eggs and egg products, and several of these occur at the household level. The aim of the current study is to critically evaluate the current status of knowledge on Salmonella in eggs from a consumer's perspective, analyzing the hazard occurrence and the good practices that should be applied to reduce salmonellosis risk. Following a HACCP (Hazard Analysis and Critical Control Point) based approach, some steps along the food journey were identified as Critical Consumer Handling (CCH)-steps in which consumers, through their behavior or choice, can significantly reduce the level of Salmonella in eggs and egg products. From shopping/collecting to consumption, each of these steps is discussed in this review to provide an evidence-based overview of risk factors of human salmonellosis related to egg consumption. The main message to consumers is to choose Salmonella-free eggs (those that some official entity or producer guarantees that does not contain Salmonella), when available, especially for dishes that are not fully heat treated. Second, as guaranteed Salmonella-free eggs are only available in a few countries, refrigerated storage from the point of collection and proper cooking will significantly reduce the risk of salmonellosis. This will require a revision of the actual recommendations/regulations, as not all ensure that eggs are maintained at temperatures that prevent growth of Salmonella from collection until the time of purchasing.
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Affiliation(s)
- Maria João Cardoso
- Universidade Católica Portuguesa, CBQF - Centro de Biotecnologia e Química Fina - Laboratório Associado, Escola Superior de Biotecnologia, Porto, Portugal
| | - Anca Ioana Nicolau
- Faculty of Food Science and Engineering, Dunarea de Jos University of Galati, Galati, Romania
| | - Daniela Borda
- Faculty of Food Science and Engineering, Dunarea de Jos University of Galati, Galati, Romania
| | - Line Nielsen
- Department of Food Science, University of Copenhagen, Copenhagen, Denmark
| | - Rui Leandro Maia
- UFP Energy, Environment and Health Research Unit (FP-ENAS), University Fernando Pessoa, Porto, Portugal
| | - Trond Møretrø
- Norwegian Institute of Food, Fisheries and Aquaculture Research, Ås, Norway
| | - Vânia Ferreira
- Universidade Católica Portuguesa, CBQF - Centro de Biotecnologia e Química Fina - Laboratório Associado, Escola Superior de Biotecnologia, Porto, Portugal
| | - Susanne Knøchel
- Department of Food Science, University of Copenhagen, Copenhagen, Denmark
| | - Solveig Langsrud
- Norwegian Institute of Food, Fisheries and Aquaculture Research, Ås, Norway
| | - Paula Teixeira
- Universidade Católica Portuguesa, CBQF - Centro de Biotecnologia e Química Fina - Laboratório Associado, Escola Superior de Biotecnologia, Porto, Portugal
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Low-energy X-ray inactivation of Salmonella Enteritidis on shell eggs in mono-/co-culture biofilms with Pseudomonas fluorescens. Food Control 2021. [DOI: 10.1016/j.foodcont.2020.107742] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022]
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Zhu J, Zhang D, Zhou X, Cui Y, Jiao S, Shi X. Development of a pasteurization method based on radio frequency heating to ensure microbiological safety of liquid egg. Food Control 2021. [DOI: 10.1016/j.foodcont.2019.107035] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/01/2022]
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Sabzali S, Bouzari M. Isolation, identification and some characteristics of two lytic bacteriophages against Salmonella enterica serovar Paratyphi B and S. enterica serovar Typhimurium from various food sources. FEMS Microbiol Lett 2021; 368:6217424. [PMID: 33830213 DOI: 10.1093/femsle/fnab037] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/16/2019] [Accepted: 04/06/2021] [Indexed: 12/12/2022] Open
Abstract
Salmonellosis is an important worldwide food-borne disease. Increasing resistance to Salmonella spp. has been reported in recent years, and now the prevalence of multidrug-resistant Salmonella spp. is a worldwide problem. This necessitates alternative approaches like phage therapy. This study aimed to isolate bacteriophages specific for Salmonella enterica serovar Paratyphi B and S. enterica serovar Typhimurium isolated from different sources (chicken meat, beef and eggshells). The antibiotic resistance profiles of the bacteria were determined by phenotypic and genotypic methods. The prevalence of extended-spectrum β-lactamase genes was examined by polymerase chain reaction. In total, 75% of the isolated Salmonella strains were resistant to tetracycline, whereas 70% of them were resistant to azithromycin. All of the isolates from beef were resistant to nalidixic acid. The most common extended-spectrum β-lactamase genes among the isolates were blaSHV (15%) followed by blaTEM (10%) and blaCTX (5%). Two specific bacteriophages were isolated and characterized. The host range for vB_SparS-ui was Salmonella Paratyphi B, S. enterica serovar Paratyphi A and S. enterica, while that for vB_StyS-sam phage was Salmonella Typhimurium and S. enterica serovar Enteritidis. The characteristics of the isolated phages indicate that they are proper candidates to be used to control some foodstuff contaminations and also phage therapy of infected animals.
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Affiliation(s)
- Somaieh Sabzali
- Department of Cell and Molecular Biology & Microbiology, Faculty of Biological Science and Technology, University of Isfahan, 81746-73441, Isfahan, Iran
| | - Majid Bouzari
- Department of Cell and Molecular Biology & Microbiology, Faculty of Biological Science and Technology, University of Isfahan, 81746-73441, Isfahan, Iran
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Prevalence and Molecular Characterization of Salmonella Isolated from Broiler Farms at the Tolima Region-Colombia. Animals (Basel) 2021; 11:ani11040970. [PMID: 33807224 PMCID: PMC8067184 DOI: 10.3390/ani11040970] [Citation(s) in RCA: 12] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/20/2021] [Revised: 03/08/2021] [Accepted: 03/09/2021] [Indexed: 12/14/2022] Open
Abstract
Simple Summary Salmonella spp. is a major foodborne pathogen with a worldwide distribution that is responsible for salmonellosis in animals and humans. Salmonella contamination of poultry and derivative products occurs at different levels. The aim of this study was to estimate the prevalence of Salmonella in broilers farms and to conduct a phenotypic and molecular characterization of Salmonella isolates. The prevalence at the broiler farm level was 26.67%, and all isolates were found to belong to the serovar Salmonella Paratyphi B. These results suggest a common source of Salmonella contamination between broiler farms, presumably via feed, parent flocks or hatchery machines. Salmonella Paratyphi B is present in different segments of the poultry chain in the Tolima region. Additional studies are needed to identify the main source of Salmonella in broilers, chicken carcasses, and eggs commercialized in the Tolima region. Abstract Salmonella is an important animal and human pathogen responsible for Salmonellosis, and it is frequently associated with the consumption of contaminated poultry products. The aim of this study was to estimate the prevalence of Salmonella in the poultry farms and to determine the genetic relationship. A total of 135 samples collected from fifteen broiler farms, including cloacal, feed, water, environmental and farm operator faeces samples were subjected to microbiological isolation. Molecular confirmation of Salmonella isolates was carried out by amplification of the invA gene, discrimination of d-tartrate-fermenting Salmonella isolates using multiplex PCR, and subsequently analysed by pulsed-field gel electrophoresis (PFGE). A survey questionnaire was conducted to identify potential risk factors for Salmonella presence in broiler farms. The prevalence of Salmonella at the farm level was 26.67%, and Salmonella isolates were serotyped as S. Paratyphi B and all isolates were d-tartrate-fermenting (dT+). PFGE showed three highly similar clusters and one significantly different Salmonella isolate. S. Paratyphi B continued to be present in different links of the poultry chain in the Tolima region, and identification of its main source is necessary to control its dissemination.
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Cui L, Liu Q, Jiang Z, Song Y, Yi S, Qiu J, Hao G, Sun S. Characteristics of Salmonella From Chinese Native Chicken Breeds Fed on Conventional or Antibiotic-Free Diets. Front Vet Sci 2021; 8:607491. [PMID: 33834046 PMCID: PMC8021795 DOI: 10.3389/fvets.2021.607491] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/17/2020] [Accepted: 02/28/2021] [Indexed: 11/13/2022] Open
Abstract
Salmonella is a common food-borne Gram-negative pathogen with multiple serotypes. Pullorum disease, caused by Salmonella Pullorum, seriously threatens the poultry industry. Many previous studies were focused on the epidemiological characteristics of Salmonella infections in conventional antibiotic use poultry. However, little is known about Salmonella infections in chicken flocks fed on antibiotic-free diets. Herein, we investigated and compared Salmonella infections in three Chinese native breeders fed on antibiotic-free diets, including the Luhua, Langya, and Qingjiaoma chickens, and one conventional breeder, the Bairi chicken, via analyzing 360 dead embryos in 2019. The results showed that the main Salmonella serotypes detected in a total of 155 isolates were S. Pullorum (82.6%) and S. Enteritidis (17.4%). Coinfection with two serotypes of Salmonella was specifically found in Bairi chicken. The sequence type (ST) in S. Pullorum was ST92 (n = 96) and ST2151 (n = 32), whereas only ST11 (n = 27) was found in S. Enteritidis. The Salmonella isolates from three breeder flocks fed on antibiotic-free diets exhibited phenotypic heterogeneity with a great variety of drug resistance spectrum. Most of the isolates among three chicken breeds Luhua (64.9%, 50/77), Langya (60%, 12/20) and Qingjiaoma (58.3%, 7/12) fed on antibiotic-free diets were resistant to only one antibiotic (erythromycin), whereas the rate of resistance to one antibiotic in conventional Bairi chicken isolates was only 4.3% (2/46). The multidrug-resistance rate in Salmonella isolates from layer flocks fed on antibiotic-free diets (20.2%, 22/109) was significantly (P < 0.0001) lower than that from chickens fed on conventional diets (93.5%, 43/46). However, high rate of resistance to erythromycin (97.4%~100%) and streptomycin (26%~41.7%) were also found among three breeder flocks fed on antibiotic-free diets, indicating resistance to these antibiotics likely spread before antibiotic-free feeding in poultry farms. The findings of this study supplement the epidemiological data of salmonellosis and provide an example of the characteristics of Salmonella in the chicken flocks without direct antibiotic selective pressure.
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Affiliation(s)
- Lulu Cui
- Department of Preventive Veterinary Medicine, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
| | - Qingxiao Liu
- Department of Preventive Veterinary Medicine, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
| | - Zhiyu Jiang
- Department of Preventive Veterinary Medicine, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
| | - Yan Song
- Department of Preventive Veterinary Medicine, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
| | - Shoujing Yi
- Department of Preventive Veterinary Medicine, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
| | - Jianhua Qiu
- Department of Preventive Veterinary Medicine, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
| | - Guijuan Hao
- Department of Preventive Veterinary Medicine, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
| | - Shuhong Sun
- Department of Preventive Veterinary Medicine, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
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Gingerich E, Frana T, Logue CM, Smith DP, Pavlidis HO, Chaney WE. Effect of Feeding a Postbiotic Derived from Saccharomyces cerevisiae Fermentation as a Preharvest Food Safety Hurdle for Reducing Salmonella Enteritidis in the Ceca of Layer Pullets. J Food Prot 2021; 84:275-280. [PMID: 32977331 DOI: 10.4315/jfp-20-330] [Citation(s) in RCA: 18] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/14/2020] [Accepted: 09/21/2020] [Indexed: 12/27/2022]
Abstract
ABSTRACT Salmonella Enteritidis is responsible for a significant proportion of foodborne salmonellosis in the United States and continues to be attributable to table eggs despite increased federal oversight. Technologies, including feed additives, continue to be evaluated for preharvest application and their potential food safety benefits. Diamond V Original XPC, a Saccharomyces cerevisiae fermentation-based postbiotic (SCFP), was evaluated for its effectiveness in reducing Salmonella Enteritidis (SE) colonization in young layer pullets. A total of 40 day-old Hy-Line W-36 layer pullets were equally divided and randomly assigned to one of two dietary treatments, with SCFP or without SCFP (PCON), and orally gavaged on day 28 with SE at 106 CFU/mL. Another 20 day-old pullets were fed the same control feed without SCFP and blank inoculated on day 28 with 1 mL of sterile phosphate-buffered saline to serve as a negative control. Qualitative and quantitative analyses of cecal contents for Salmonella were performed for all birds on day 32. The prevalence of SE in the ceca of all directly challenged birds was 100%; however, the SE concentration in birds fed SCFP diet (3.35 log CFU/g) was significantly lower (P < 0.0001) than that of the PCON birds not fed SCFP (4.49 log CFU/g). The proportion of birds with enumerable SE concentrations was lower in SCFP-fed pullets (57.9%) than in the PCON pullets (95.0%). These data suggest that inclusion of SCFP in the diet may aid in the reduction of SE within the ceca of commercial laying hens and could serve as an additional preharvest food safety hurdle. HIGHLIGHTS
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Affiliation(s)
- E Gingerich
- Diamond V, Cargill Health Technologies, 2525 60th Avenue SW, Cedar Rapids, Iowa 52404
| | - T Frana
- Department of Veterinary Diagnostic and Production Animal Medicine, 2203 Lloyd Veterinary Medical Center, Iowa State University, Ames, Iowa 50011
| | - C M Logue
- Department of Population Health, College of Veterinary Medicine, University of Georgia, 501 D. W. Brooks Drive, Athens, Georgia 30605, USA
| | - D P Smith
- Diamond V, Cargill Health Technologies, 2525 60th Avenue SW, Cedar Rapids, Iowa 52404
| | - H O Pavlidis
- Diamond V, Cargill Health Technologies, 2525 60th Avenue SW, Cedar Rapids, Iowa 52404
| | - W E Chaney
- Diamond V, Cargill Health Technologies, 2525 60th Avenue SW, Cedar Rapids, Iowa 52404
- (ORCID: https://orcid.org/0000-0002-4707-4854 [W.E.C.])
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Using stochastic dynamic modelling to estimate the sensitivity of current and alternative surveillance program of Salmonella in conventional broiler production. Sci Rep 2020; 10:19441. [PMID: 33173102 PMCID: PMC7655952 DOI: 10.1038/s41598-020-76514-3] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/02/2020] [Accepted: 10/27/2020] [Indexed: 11/08/2022] Open
Abstract
Since 2018, the EU commission has declared the Danish broiler industry to be Salmonella free. However, there is continuous Salmonella pressure from the environment, and a number of parent flocks and broiler flocks become infected annually. When a parent flock becomes infected, the infection can be transmitted vertically to the broiler flocks, before the parent flock is detected and destroyed, including the eggs at the hatchery. To address this issue, we developed stochastic dynamic modelling of transmission of Salmonella in parent flocks and combined that with the relation between flock prevalence and test sensitivity for environmental samples in the flock. Results suggested that after 10 and 100 infected hens were seeded, the likelihood of detecting an infected parent flock within the three first weeks after the infection was strongly influenced by the taking of five boot swabs (95% CI 70–100) instead of two (95% CI 40–100) or the supplementing of the two boot swabs by a dust sample (95% CI 43–100). Results suggest that the likelihood of detecting the broiler flock as infected in the program was estimated to at least 99% in broiler flock even if only one chicken was initially infected. These findings are of relevance for managing parent flocks and eggs at the hatchery in case of Salmonella infection in parent flocks in the Danish poultry.
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Soyer F, Keman D, Eroğlu E, Türe H. Synergistic antimicrobial effects of activated lactoferrin and rosemary extract in vitro and potential application in meat storage. JOURNAL OF FOOD SCIENCE AND TECHNOLOGY 2020; 57:4395-4403. [PMID: 33087953 DOI: 10.1007/s13197-020-04476-5] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Revised: 04/10/2020] [Accepted: 04/23/2020] [Indexed: 11/24/2022]
Abstract
This study aimed to explore the antimicrobial effects of activated lactoferrin (ALF) and rosemary extract (RE) on Escherichia coli O157:H7, Salmonella Enteritidis and Listeria monocytogenes, and to investigate their application potential in the meat storage. Minimum inhibitory concentrations (MICs) of ALF, RE and ALF-RE combinations were determined via microtiter plate assay. MICs of ALF were 1% for E. coli O157:H7; 0.5% for S. Enteritidis and 0.1% for L. monocytogenes. While 15% RE inhibited L. monocytogenes; 30% RE partially inhibited E. coli O157:H7 and S. Enteritidis growth. Synergistic effect of ALF and RE on the inhibition of E. coli O157:H7 increased the activity of ALF two to three folds. Food application of antimicrobials was performed by dipping of meat samples. Both ALF and RE were found effective in the prevention of L. monocytogenes growth about two logs. According to the data, choice of natural antimicrobials may be promising in food preservation.
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Affiliation(s)
- Ferda Soyer
- Department of Molecular Biology and Genetics, Izmir Institute of Technology, 35430 Izmir, Turkey
| | - Deniz Keman
- Department of Molecular Biology and Genetics, Izmir Institute of Technology, 35430 Izmir, Turkey
| | - Erdal Eroğlu
- Department of Molecular Biology and Genetics, Izmir Institute of Technology, 35430 Izmir, Turkey.,Present Address: Department of Bioengineering, Manisa Celal Bayar University, 45140 Manisa, Turkey
| | - Hasan Türe
- Department of Molecular Biology and Genetics, Izmir Institute of Technology, 35430 Izmir, Turkey.,Present Address: Department of Marine Sciences, Ordu University, 52200 Ordu, Turkey
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Castro-Vargas RE, Herrera-Sánchez MP, Rodríguez-Hernández R, Rondón-Barragán IS. Antibiotic resistance in Salmonella spp. isolated from poultry: A global overview. Vet World 2020; 13:2070-2084. [PMID: 33281339 PMCID: PMC7704309 DOI: 10.14202/vetworld.2020.2070-2084] [Citation(s) in RCA: 88] [Impact Index Per Article: 17.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/30/2020] [Accepted: 08/05/2020] [Indexed: 01/05/2023] Open
Abstract
Salmonella enterica is the most important foodborne pathogen, and it is often associated with the contamination of poultry products. Annually, Salmonella causes around 93 million cases of gastroenteritis and 155,000 deaths worldwide. Antimicrobial therapy is the first choice of treatment for this bacterial infection; however, antimicrobial resistance has become a problem due to the misuse of antibiotics both in human medicine and animal production. It has been predicted that by 2050, antibiotic-resistant pathogens will cause around 10 million deaths worldwide, and the WHO has suggested the need to usher in the post-antibiotic era. The purpose of this review is to discuss and update the status of Salmonella antibiotic resistance, in particular, its prevalence, serotypes, and antibiotic resistance patterns in response to critical antimicrobials used in human medicine and the poultry industry. Based on our review, the median prevalence values of Salmonella in broiler chickens, raw chicken meat, and in eggs and egg-laying hens were 40.5% ( interquartile range [IQR] 11.5-58.2%), 30% (IQR 20-43.5%), and 40% (IQR 14.2-51.5%), respectively. The most common serotype was Salmonella Enteritidis, followed by Salmonella Typhimurium. The highest antibiotic resistance levels within the poultry production chain were found for nalidixic acid and ampicillin. These findings highlight the need for government entities, poultry researchers, and producers to find ways to reduce the impact of antibiotic use in poultry, focusing especially on active surveillance and finding alternatives to antibiotics.
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Affiliation(s)
- Rafael Enrique Castro-Vargas
- Research Group in Immunology and Pathogenesis, Faculty of Veterinary Medicine and Zootechnics, University of Tolima, Santa Helena Highs, Ibagué, Tolima, Colombia
- Poultry Research Group, Faculty of Veterinary Medicine and Zootechnics, University of Tolima, Santa Helena Highs, Ibagué, Tolima, Colombia
| | - María Paula Herrera-Sánchez
- Research Group in Immunology and Pathogenesis, Faculty of Veterinary Medicine and Zootechnics, University of Tolima, Santa Helena Highs, Ibagué, Tolima, Colombia
- Poultry Research Group, Faculty of Veterinary Medicine and Zootechnics, University of Tolima, Santa Helena Highs, Ibagué, Tolima, Colombia
| | - Roy Rodríguez-Hernández
- Poultry Research Group, Faculty of Veterinary Medicine and Zootechnics, University of Tolima, Santa Helena Highs, Ibagué, Tolima, Colombia
| | - Iang Schroniltgen Rondón-Barragán
- Research Group in Immunology and Pathogenesis, Faculty of Veterinary Medicine and Zootechnics, University of Tolima, Santa Helena Highs, Ibagué, Tolima, Colombia
- Poultry Research Group, Faculty of Veterinary Medicine and Zootechnics, University of Tolima, Santa Helena Highs, Ibagué, Tolima, Colombia
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Insights into the Oxidative Stress Response of Salmonella enterica serovar Enteritidis Revealed by the Next Generation Sequencing Approach. Antioxidants (Basel) 2020; 9:antiox9090849. [PMID: 32927804 PMCID: PMC7555449 DOI: 10.3390/antiox9090849] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/28/2020] [Revised: 08/27/2020] [Accepted: 09/05/2020] [Indexed: 12/14/2022] Open
Abstract
As a facultative intracellular pathogen, Salmonella Enteritidis must develop an effective oxidative stress response to survive exposure to reactive oxygen species within the host. To study this defense mechanism, we carried out a series of oxidative stress assays in parallel with a comparative transcriptome analyses using a next generation sequencing approach. It was shown that the expression of 45% of the genome was significantly altered upon exposure to H2O2. Quantitatively the most significant (≥100 fold) gene expression alterations were observed among genes encoding the sulfur utilization factor of Fe-S cluster formation and iron homeostasis. Our data point out the multifaceted nature of the oxidative stress response. It includes not only numerous mechanisms of DNA and protein repair and redox homeostasis, but also the key genes associated with osmotic stress, multidrug efflux, stringent stress, decrease influx of small molecules, manganese and phosphate starvation stress responses. Importantly, this study revealed that oxidatively stressed S. Enteritidis cells simultaneously repressed key motility encoding genes and induced a wide range of adhesin- and salmonellae-essential virulence-encoding genes, that are critical for the biofilm formation and intracellular survival, respectively. This finding indicates a potential intrinsic link between oxidative stress and pathogenicity in non-typhoidal Salmonella that needs to be empirically evaluated.
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Guard J, Rothrock M, Jones D, Gast R. Low Dose Infection of Hens in Lay with Salmonella enterica Serovar Enteritidis from Different Genomic Clades. Avian Dis 2020; 64:7-15. [PMID: 32267120 DOI: 10.1637/0005-2086-64.1.7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/24/2019] [Accepted: 09/25/2019] [Indexed: 11/05/2022]
Abstract
Salmonella enterica serovar Enteritidis is the leading cause of salmonellosis in people, and modeling of infections in chickens is used to identify intervention strategies. A review of 80 manuscripts encompassing 119 experiments indicated that the mean dose of infection was 108 CFU per bird. Experiments of less than 106 CFU were primarily conducted in immature birds. To address a lack of information on the impact of low dosages on the hen at lay, two experiments were conducted in triplicate. Experiment A addressed issues associated with vaccination; thus, hens were infected intramuscularly at 103, 105, and 107 CFU. For Experiment B, which was focused more on colonization and invasion, hens were infected orally with 5 × 103 CFU with 4 strains from different genomic clades. Samples from liver, spleen, ovarian pedicle, and paired ceca in both experiments were cultured 5, 6, 7, and 8 days postinfection. Eggshell microbiome taxa were assessed in Experiment B. Results indicated that dosages of 103 CFU in both experiments produced enough positive samples to be used within models. The intramuscular route resulted in approximately twice as many positive samples as the oral route. The kinetics of infection appeared to differ between low and high dosages suggestive of a J-curve response. These results could impact risk assessments if the hen at lay has a nonlinear response to infectious dose.
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Affiliation(s)
- Jean Guard
- United States Department of Agriculture, United States National Poultry Research Center, Athens, GA 30605,
| | - Michael Rothrock
- United States Department of Agriculture, United States National Poultry Research Center, Athens, GA 30605
| | - Deana Jones
- United States Department of Agriculture, United States National Poultry Research Center, Athens, GA 30605
| | - Richard Gast
- United States Department of Agriculture, United States National Poultry Research Center, Athens, GA 30605
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Chen Z, Kuang D, Xu X, González-Escalona N, Erickson DL, Brown E, Meng J. Genomic analyses of multidrug-resistant Salmonella Indiana, Typhimurium, and Enteritidis isolates using MinION and MiSeq sequencing technologies. PLoS One 2020; 15:e0235641. [PMID: 32614888 PMCID: PMC7332006 DOI: 10.1371/journal.pone.0235641] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/26/2020] [Accepted: 06/19/2020] [Indexed: 01/04/2023] Open
Abstract
We sequenced 25 isolates of phenotypically multidrug-resistant Salmonella Indiana (n = 11), Typhimurium (n = 8), and Enteritidis (n = 6) using both MinION long-read [SQK-LSK109 and flow cell (R9.4.1)] and MiSeq short-read (Nextera XT and MiSeq Reagent Kit v2) sequencing technologies to determine the advantages of each approach in terms of the characteristics of genome structure, antimicrobial resistance (AMR), virulence potential, whole-genome phylogeny, and pan-genome. The MinION reads were base-called in real-time using MinKnow 3.4.8 integrated with Guppy 3.0.7. The long-read-only assembly, Illumina-only assembly, and hybrid assembly pipelines of Unicycler 0.4.8 were used to generate the MinION, MiSeq, and hybrid assemblies, respectively. The MinION assemblies were highly contiguous compared to the MiSeq assemblies but lacked accuracy, a deficiency that was mitigated by adding the MiSeq short reads through the Unicycler hybrid assembly which corrected erroneous single nucleotide polymorphisms (SNPs). The MinION assemblies provided similar predictions of AMR and virulence potential compared to the MiSeq and hybrid assemblies, although they produced more total false negatives of AMR genotypes, primarily due to failure in identifying tetracycline resistance genes in 11 of the 19 MinION assemblies of tetracycline-resistant isolates. The MinION assemblies displayed a large genetic distance from their corresponding MiSeq and hybrid assemblies on the whole-genome phylogenetic tree, indicating that the lower read accuracy of MinION sequencing caused incorrect clustering. The pan-genome of the MinION assemblies contained significantly more accessory genes and less core genes compared to the MiSeq and hybrid assemblies, suggesting that although these assemblies were more contiguous, their sequencing errors reduced accurate genome annotations. Our research demonstrates that MinION sequencing by itself provides an efficient assessment of the genome structure, antimicrobial resistance, and virulence potential of Salmonella; however, it is not sufficient for whole-genome phylogenetic and pan-genome analyses. MinION in combination with MiSeq facilitated the most accurate genomic analyses.
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Affiliation(s)
- Zhao Chen
- Joint Institute for Food Safety and Applied Nutrition, Center for Food Safety and Security Systems, University of Maryland, College Park, Maryland, United States of Amrica
| | - Dai Kuang
- Ruijin Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
| | - Xuebin Xu
- Shanghai Municipal Center for Disease Control and Prevention, Shanghai, China
| | - Narjol González-Escalona
- Center for Food Safety and Applied Nutrition, U.S. Food and Drug Administration, College Park, Maryland, United States of America
| | - David L. Erickson
- Joint Institute for Food Safety and Applied Nutrition, Center for Food Safety and Security Systems, University of Maryland, College Park, Maryland, United States of Amrica
| | - Eric Brown
- Center for Food Safety and Applied Nutrition, U.S. Food and Drug Administration, College Park, Maryland, United States of America
| | - Jianghong Meng
- Joint Institute for Food Safety and Applied Nutrition, Center for Food Safety and Security Systems, University of Maryland, College Park, Maryland, United States of Amrica
- * E-mail:
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