FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Microbiology spectrum2025; 13(3); e0250124; doi: 10.1128/spectrum.02501-24

Phenotypic and genotypic characterization of antimicrobial resistance and virulence profiles of Salmonella enterica serotypes isolated from necropsied horses in Kentucky.

Abstract: Salmonella is a foodborne pathogen that poses a significant threat to global public health. It affects several animal species, including horses. Salmonella infections in horses can be either asymptomatic or cause severe clinical illness. Infections caused by Salmonella are presently controlled with antibiotics. Due to the formation of biofilms and the emergence of antimicrobial resistance, the treatment has become more complicated. Our study focused on investigating the prevalence of Salmonella enterica in necropsied horses, assessing the capability for biofilm formation, and motility, determining the phenotypic and genotypic profiles of antibiotic resistance, and detecting virulence genes. A total of 2,182 necropsied horses were tested for the presence of Salmonella. Intestinal samples were enriched in selenite broth and cultured on hektoen and eosin methylene blue agar plates, whereas other samples were directly cultured on aforementioned plates. Confirmation of the serotypes was performed according to the Kauffmann-White-Le Minor Scheme followed by biofilm formation screening using crystal violet assay. The resistance profile of the isolates was determined by broth microdilution assay using the Sensititre️ Vet (Equine EQUIN2F). The genotypic antimicrobial resistance (AMR) and virulence profiles were detected using polymerase chain reaction (PCR). The overall prevalence of Salmonella was 1.19% (26/2182), with 11 different serotypes identified. Salmonella Typhimurium was the most prevalent serotype with 19.2% prevalence. All of the isolates were identified as biofilm producers and motile. Virulence genes related to invasion (invA, hilA, mgtC, and spiA), biofilm formation (csgA and csgB), and motility (filA, motA, flgG, figG, flgH, fimC, fimD, and fimH) of Salmonella were detected among 100% of the isolates. An overall 11.4% of the isolates were identified as multidrug-resistant (MDR), with resistance to gentamicin, amikacin, ampicillin, ceftazidime, ceftiofur, chloramphenicol, and trimethoprim/sulfamethoxazole. We found that beta-lactamase-producing genes blaTEM, blaCTXM, and blaSHV2 were identified in 11.5% of the isolates, while only 3.8% carried the blaOXA-9 gene. The presence of MDR pathogenic Salmonella in horses is alarming for human and animal health, especially when they have a high affinity for forming biofilm. Our study found horses as potential sources of pathogenic Salmonella transmission to humans. Thus, it is important to perform continuous monitoring and surveillance studies to track the source of infection and develop preventive measures. Objective: This study focuses on understanding how Salmonella, specifically isolated from horses, can resist antibiotics and cause disease. Salmonella is a well-known foodborne pathogen that can pose risks not only to animals but also to humans. By studying the bacteria from necropsied horses, the research aims to uncover how certain Salmonella strains develop resistance to antibiotics and which genetic factors make them more dangerous. In addition to antibiotic resistance, the research explores the biofilm-forming ability of these strains, which enhances their survival in harsh environments. The study also investigates their motility, a factor that contributes to the spread of infection. The findings can improve treatment strategies for horses and help prevent the transmission of resistant bacteria to other animals as well as humans. Ultimately, the research could contribute to better management of antibiotic resistance in both veterinary and public health contexts, helping to safeguard animal welfare and public health.
Get Full Text
Publication Date: 2025-01-23 PubMed ID: 39846771PubMed Central: PMC11878045DOI: 10.1128/spectrum.02501-24Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study explores the phenotypic and genotypic characteristics of antibiotic-resistant Salmonella enterica strains isolated from horses. It also analyzes different disease-causing profiles of these bacteria, shedding light on how these strains resist antibiotics and cause illness.

Methodology

  • The researchers tested 2,182 necropsied horses in Kentucky for the presence of Salmonella enterica, focusing on the bacteria’s capacity for biofilm formation, motility, phenotypic and genotypic profiles of antibiotic resistance, and the presence of virulence genes.
  • The examination was conducted using samples enriched in selenite broth and cultured on Hektoen and eosin methylene blue agar plates. Other samples were directly cultured on these plates without enrichment.
  • Serotypes (variation within a species) confirmation was done according to the Kauffmann-White-Le Minor Scheme, followed by screening for biofilm formation using crystal violet assay, a common technique for visualizing biofilms.
  • The Sensititre Vet (Equine EQUIN2F) was used to determine the antibiotic resistance profile of the isolates via a broth microdilution assay.
  • Finally, the resistances and virulence profiles were identified at the genetic level through polymerase chain reaction (PCR), a well-established method for amplifying targeted sections of DNA for further analysis.

Key Findings

  • Out of the tested horses, 1.19% (26/2182) were found to be harboring Salmonella enterica, with 11 different serotypes identified, Typhimurium being the most prevalent.
  • All of the isolates were found to be capable of producing biofilms, a feature facilitating survival in adverse conditions, and were motile, allowing them to spread in the host organism.
  • Virulence genes related to invasion, biofilm formation, and motility of Salmonella were present in all the isolates, indicating these strains’ high pathogenic potential.
  • Approximately 11.4% of isolates were multidrug-resistant, demonstrating resistance to numerous antibiotics like gentamicin, amikacin, ampicillin, ceftazidime, ceftiofur, chloramphenicol, and trimethoprim/sulfamethoxazole.
  • Some of these isolates produced beta-lactamase, an enzyme that can break down certain antibiotics, rendering them ineffective.

Significance

  • The presence of multidrug-resistant, pathogenic Salmonella enterica in horses is concerning for both animal and human health, especially given their aptitude for biofilm formation.
  • This study underscores the possibility that horses may act as a source for transmitting pathogenic Salmonella to humans.
  • Continuous monitoring and research studies are required to identify the source of infection and develop preventive measures.
  • The findings could improve treatment strategies for horses and help prevent the spread of resistant bacteria, thereby aiding in the better management of antibiotic resistance in veterinary and public health sectors.

Cite This Article

APA
Kabir A, Kelley WG, Glover C, Erol E, Helmy YA. (2025). Phenotypic and genotypic characterization of antimicrobial resistance and virulence profiles of Salmonella enterica serotypes isolated from necropsied horses in Kentucky. Microbiol Spectr, 13(3), e0250124. https://doi.org/10.1128/spectrum.02501-24

Publication

Microbiology spectrum
ISSN: 2165-0497
NlmUniqueID: 101634614
Country: United States
Language: English
Volume: 13
Issue: 3
Pages: e0250124

Researcher Affiliations

Kabir, Ajran
  • Department of Veterinary Science, Martin-Gatton College of Agriculture, Food, and Environment, University of Kentucky, Lexington, Kentucky, USA.
Kelley, William G
  • Department of Veterinary Science, Martin-Gatton College of Agriculture, Food, and Environment, University of Kentucky, Lexington, Kentucky, USA.
Glover, Cheyenne
  • Department of Veterinary Science, Martin-Gatton College of Agriculture, Food, and Environment, University of Kentucky, Lexington, Kentucky, USA.
  • College of Veterinary Medicine, Lincoln Memorial University, Harrogate, Tennessee, USA.
Erol, Erdal
  • Veterinary Diagnostic Laboratory, Martin-Gatton College of Agriculture, Food, and Environment, University of Kentucky, Lexington, Kentucky, USA.
Helmy, Yosra A
  • Department of Veterinary Science, Martin-Gatton College of Agriculture, Food, and Environment, University of Kentucky, Lexington, Kentucky, USA.

MeSH Terms

  • Animals
  • Horses / microbiology
  • Salmonella enterica / drug effects
  • Salmonella enterica / genetics
  • Salmonella enterica / isolation & purification
  • Salmonella enterica / pathogenicity
  • Salmonella enterica / classification
  • Salmonella Infections, Animal / microbiology
  • Salmonella Infections, Animal / epidemiology
  • Horse Diseases / microbiology
  • Horse Diseases / epidemiology
  • Anti-Bacterial Agents / pharmacology
  • Serogroup
  • Genotype
  • Biofilms / growth & development
  • Microbial Sensitivity Tests
  • Virulence / genetics
  • Kentucky / epidemiology
  • Virulence Factors / genetics
  • Phenotype
  • Drug Resistance, Bacterial
  • Drug Resistance, Multiple, Bacterial / genetics
  • Prevalence

Grant Funding

  • KL2 TR001996 / NCATS NIH HHS
  • P20 GM130456 / NIGMS NIH HHS

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 70 references
  1. nCDC . 2024. Salmonella, on centers for disease control and prevention. Available from: https://www.cdc.gov/salmonella/index.html
  2. Schott II HC, Ewart SL, Walker RD, Dwyer RM, Dietrich S, Eberhart SW, Kusey J, Stick JA, Derksen FJ. An outbreak of salmonellosis among horses at a veterinary teaching hospital.. javma 2001;218:1152–1159.
    doi: 10.2460/javma.2001.218.1152pubmed: 11318368google scholar: lookup
  3. nWHO . 2018. Salmonella (non-typhoidal), on World Health Organization. Available from: https://www.who.int/news-room/fact-sheets/detail/salmonella-(non-typhoidal)#:~:text=Key%20facts%201%20Salmonella%20is%201%20of%204,have%20emerged%2C%20affecting%20the%20food%20chain.%20More%20items
  4. Zhang S, Yin Y, Jones MB, Zhang Z, Deatherage Kaiser BL, Dinsmore BA, Fitzgerald C, Fields PI, Deng X. Salmonella serotype determination utilizing high-throughput genome sequencing data.. J Clin Microbiol 2015;53:1685–1692.
    doi: 10.1128/JCM.00323-15pmc: PMC4400759pubmed: 25762776google scholar: lookup
  5. Lamichhane B, Mawad AMM, Saleh M, Kelley WG, Harrington PJ 2nd, 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.
    doi: 10.3390/antibiotics13010076pmc: PMC10812683pubmed: 38247636google scholar: lookup
  6. Javed R, Taku AK, Gangil R, Sharma RK. Molecular characterization of virulence genes of Streptococcus equi subsp. equi and Streptococcus equi subsp. zooepidemicus in equines.. Vet World 2016;9:875–881.
    doi: 10.14202/vetworld.2016.875-881pmc: PMC5021838pubmed: 27651677google scholar: lookup
  7. Burgess BA. Salmonella in horses.. Vet Clin North Am Equine Pract 2023;39:25–35.
    doi: 10.1016/j.cveq.2022.11.005pubmed: 36737292google scholar: lookup
  8. Ernst NS, Hernandez JA, MacKay RJ, Brown MP, Gaskin JM, Nguyen AD, Giguere S, Colahan PT, Troedsson MR, Haines GR, Addison IR, Miller BJ. Risk factors associated with fecal Salmonella shedding among hospitalized horses with signs of gastrointestinal tract disease.. J Am Vet Med Assoc 2004;225:275–281.
    doi: 10.2460/javma.2004.225.275pubmed: 15323386google scholar: lookup
  9. Kim LM, Morley PS, Traub-Dargatz JL, Salman MD, Gentry-Weeks C. Factors associated with Salmonella shedding among equine colic patients at a veterinary teaching hospital.. J Am Vet Med Assoc 2001;218:740–748.
    doi: 10.2460/javma.2001.218.740pubmed: 11280409google scholar: lookup
  10. Dargatz DA, Traub-Dargatz JL. Multidrug-resistant Salmonella and nosocomial infections.. Vet Clin North Am Equine Pract 2004;20:587–600.
    doi: 10.1016/j.cveq.2004.07.008pubmed: 15519820google scholar: lookup
  11. Soza-Ossandón P, Rivera D, Tardone R, Riquelme-Neira R, García P, Hamilton-West C, Adell AD, González-Rocha G, Moreno-Switt AI. Widespread environmental presence of multidrug-resistant Salmonella in an equine veterinary hospital that received local and international horses.. Front Vet Sci 2020;7:346.
    doi: 10.3389/fvets.2020.00346pmc: PMC7366320pubmed: 32754619google scholar: lookup
  12. Rothers KL, Hackett ES, Mason GL, Nelson BB. Atypical Salmonellosis in a horse: implications for hospital safety.. Case Rep Vet Med 2020;2020:7062408.
    doi: 10.1155/2020/7062408pmc: PMC7292965pubmed: 32566354google scholar: lookup
  13. Ward MP, Brady TH, Couëtil LL, Liljebjelke K, Maurer JJ, Wu CC. Investigation and control of an outbreak of salmonellosis caused by multidrug-resistant Salmonella typhimurium in a population of hospitalized horses.. Vet Microbiol 2005;107:233–240.
    doi: 10.1016/j.vetmic.2005.01.019pubmed: 15863282google scholar: lookup
  14. Grandolfo E, Parisi A, Ricci A, Lorusso E, Siena R, Trotta A, Buonavoglia D, Martella V, Corrente M. High mortality in foals associated with Salmonella enterica subsp. enterica Abortusequi infection in Italy.. J Vet Diagn Invest 2018;30:483–485.
    doi: 10.1177/1040638717753965pmc: PMC6505811pubmed: 29322884google scholar: lookup
  15. McCain CS, Powell KC. Asymptomatic salmonellosis in healthy adult horses.. J Vet Diagn Invest 1990;2:236–237.
    doi: 10.1177/104063879000200318pubmed: 2094454google scholar: lookup
  16. Helmy YA, Kabir A, Saleh M, Kennedy LA, Burns L, Johnson B. Draft genome sequence analysis of multidrug-resistant Salmonella enterica subsp. enterica serovar Mbandaka harboring colistin resistance gene mcr-9.1 isolated from foals in Kentucky, USA.. Microbiol Resour Announc 2024;13:e00737–24.
    doi: 10.1128/mra.00737-24pmc: PMC11556123pubmed: 39373480google scholar: lookup
  17. Helmy YA, Taha-Abdelaziz K, Hawwas H-H, Ghosh S, AlKafaas SS, Moawad MMM, Saied EM, Kassem II, Mawad AMM. Antimicrobial resistance and recent alternatives to antibiotics for the control of bacterial pathogens with an emphasis on foodborne pathogens.. Antibiotics (Basel) 2023;12:274.
    doi: 10.3390/antibiotics12020274pmc: PMC9952301pubmed: 36830185google scholar: lookup
  18. House JK, Smith BP. Salmonella in horses.. .
  19. Abebe E, Gugsa G, Ahmed M. Review on major food-borne zoonotic bacterial pathogens.. J Trop Med 2020;2020:4674235.
    doi: 10.1155/2020/4674235pmc: PMC7341400pubmed: 32684938google scholar: lookup
  20. Kabir A, Lamichhane B, Habib T, Adams A, El-Sheikh Ali H, Slovis NM, Troedsson MHT, Helmy YA. Antimicrobial resistance in equines: a growing threat to horse health and beyond-a comprehensive review.. Antibiotics (Basel) 2024;13:713.
    doi: 10.3390/antibiotics13080713pmc: PMC11350719pubmed: 39200013google scholar: lookup
  21. Bhandari M, Poelstra JW, Kauffman M, Varghese B, Helmy YA, Scaria J, Rajashekara G. Genomic diversity, antimicrobial resistance, plasmidome, and virulence profiles of Salmonella isolated from small specialty crop farms revealed by whole-genome sequencing.. Antibiotics (Basel) 2023;12:1637.
    doi: 10.3390/antibiotics12111637pmc: PMC10668983pubmed: 37998839google scholar: lookup
  22. Rahman MM, Hossain H, Chowdhury MSR, Hossain MM, Saleh A, Binsuwaidan R, Noreddin A, Helmy YA, El Zowalaty ME. Molecular characterization of multidrug-resistant and extended-spectrum β-lactamases-producing Salmonella enterica serovars Enteritidis and Typhimurium isolated from raw meat in retail markets.. Antibiotics (Basel) 2024;13:586.
    doi: 10.3390/antibiotics13070586pmc: PMC11274296pubmed: 39061268google scholar: lookup
  23. Zha L, Garrett S, Sun J. Salmonella infection in chronic inflammation and gastrointestinal cancer.. Diseases 2019;7:28.
    doi: 10.3390/diseases7010028pmc: PMC6473780pubmed: 30857369google scholar: lookup
  24. Helmy YA, El-Adawy H, Abdelwhab EM. A comprehensive review of common bacterial, parasitic and viral zoonoses at the human-animal interface in Egypt.. Pathogens 2017;6:33.
    doi: 10.3390/pathogens6030033pmc: PMC5617990pubmed: 28754024google scholar: lookup
  25. Dougnon TV, Legba B, Deguenon E, Hounmanou G, Agbankpe J, Amadou A, Fabiyi K, Assogba P, Hounsa E, Aniambossou A, De SOUZA M, Bankole HS, Baba-moussa L, Dougnon TJ. Pathogenicity, epidemiology and virulence factors of Salmonella species: a review.. N Sci Biol 2017;9:460–466.
    doi: 10.15835/nsb9410125google scholar: lookup
  26. Simm R, Ahmad I, Rhen M, Le Guyon S, Römling U. Regulation of biofilm formation in Salmonella enterica serovar Typhimurium.. Future Microbiol 2014;9:1261–1282.
    doi: 10.2217/fmb.14.88pubmed: 25437188google scholar: lookup
  27. Stepanovic S, Cirkovic I, Ranin L, Svabic-Vlahovic M. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface.. Lett Appl Microbiol 2004;38:428–432.
    doi: 10.1111/j.1472-765X.2004.01513.xpubmed: 15059216google scholar: lookup
  28. Ibarra JA, Steele-Mortimer O. Salmonella--the ultimate insider. Salmonella virulence factors that modulate intracellular survival.. Cell Microbiol 2009;11:1579–1586.
    doi: 10.1111/j.1462-5822.2009.01368.xpmc: PMC2774479pubmed: 19775254google scholar: lookup
  29. Kalai Chelvam K, Chai LC, Thong KL. Variations in motility and biofilm formation of Salmonella enterica serovar Typhi.. Gut Pathog 2014;6:1–10.
    doi: 10.1186/1757-4749-6-2pmc: PMC3922113pubmed: 24499680google scholar: lookup
  30. Bogomolnaya LM, Aldrich L, Ragoza Y, Talamantes M, Andrews KD, McClelland M, Andrews-Polymenis HL. Identification of novel factors involved in modulating motility of Salmonella enterica serotype Typhimurium.. PLoS One 2014;9:e111513.
    doi: 10.1371/journal.pone.0111513pmc: PMC4219756pubmed: 25369209google scholar: lookup
  31. Mughini-Gras L, Pijnacker R, Duijster J, Heck M, Wit B, Veldman K, Franz E. Changing epidemiology of invasive non-typhoid Salmonella infection: a nationwide population-based registry study.. Clin Microbiol Infect 2020;26:941.
    doi: 10.1016/j.cmi.2019.11.015pubmed: 31760114google scholar: lookup
  32. Leon IM, Lawhon SD, Norman KN, Threadgill DS, Ohta N, Vinasco J, Scott HM. Serotype diversity and antimicrobial resistance among Salmonella enterica isolates from patients at an equine referral hospital.. Appl Environ Microbiol 2018;84:e02829-17.
    doi: 10.1128/AEM.02829-17pmc: PMC6007101pubmed: 29678910google scholar: lookup
  33. Xiang Y, Li F, Dong N, Tian S, Zhang H, Du X, Zhou X, Xu X, Yang H, Xie J, Yang C, Liu H, Qiu S, Song H, Sun Y. Investigation of a Salmonellosis outbreak caused by multidrug resistant Salmonella typhimurium in China.. Front Microbiol 2020;11:801.
    doi: 10.3389/fmicb.2020.00801pmc: PMC7200987pubmed: 32411120google scholar: lookup
  34. Jajere SM. A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance.. Vet World 2019;12:504–521.
    doi: 10.14202/vetworld.2019.504-521pmc: PMC6515828pubmed: 31190705google scholar: lookup
  35. Wu S, Hulme JP. Recent advances in the detection of antibiotic and multi-drug resistant Salmonella: an update.. IJMS 2021;22:3499.
    doi: 10.3390/ijms22073499pmc: PMC8037659pubmed: 33800682google scholar: lookup
  36. Cummings KJ, Perkins GA, Khatibzadeh SM, Warnick LD, Aprea VA, Altier C. Antimicrobial resistance trends among Salmonella isolates obtained from horses in the northeastern United States (2001-2013).. Am J Vet Res 2016;77:505–513.
    doi: 10.2460/ajvr.77.5.505pubmed: 27111018google scholar: lookup
  37. van Duijkeren E, Wannet WJB, Heck MEOC, van Pelt W, Sloet van Oldruitenborgh-Oosterbaan MM, Smit JAH, Houwers DJ. Sero types, phage types and antibiotic susceptibilities of Salmonella strains isolated from horses in the Netherlands from 1993 to 2000.. Vet Microbiol 2002;86:203–212.
    doi: 10.1016/s0378-1135(02)00007-xpubmed: 11900955google scholar: lookup
  38. nCenter AHD . 2019. Multi-drug resistant Salmonella in horses. Available from: https://www.vet.cornell.edu/animal-health-diagnostic-center/news/multi-drug-resistant-salmonella-horses
  39. Popa GL, Papa MI. Salmonella spp. infection - a continuous threat worldwide.. Germs 2021;11:88–96.
    doi: 10.18683/germs.2021.1244pmc: PMC8057844pubmed: 33898345google scholar: lookup
  40. Goni JI, Hendrix K, Kritchevsky J. Recovery of Salmonella bacterial isolates from pooled fecal samples from horses.. J Vet Intern Med 2023;37:323–327.
    doi: 10.1111/jvim.16586pmc: PMC9889685pubmed: 36433697google scholar: lookup
  41. Hailu W, Helmy YA, Carney-Knisely G, Kauffman M, Fraga D, Rajashekara G. Prevalence and antimicrobial resistance profiles of foodborne pathogens isolated from dairy cattle and poultry manure amended farms in Northeastern Ohio, the United States.. Antibiotics (Basel) 2021;10:1450.
    doi: 10.3390/antibiotics10121450pmc: PMC8698512pubmed: 34943663google scholar: lookup
  42. Santos PDM, Widmer KW, Rivera WL. PCR-based detection and serovar identification of Salmonella in retail meat collected from wet markets in Metro Manila, Philippines.. PLoS One 2020;15:e0239457.
    doi: 10.1371/journal.pone.0239457pmc: PMC7526908pubmed: 32997676google scholar: lookup
  43. Pulido-Landínez M, Sánchez-Ingunza R, Guard J, Pinheiro do Nascimento V. Assignment of serotype to Salmonella enterica isolates obtained from poultry and their environment in southern Brazil.. Lett Appl Microbiol 2013;57:288–294.
    doi: 10.1111/lam.12110pmc: PMC4260173pubmed: 23734786google scholar: lookup
  44. O’Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis.. Mol Microbiol 1998;28:449–461.
    doi: 10.1046/j.1365-2958.1998.00797.xpubmed: 9632250google scholar: lookup
  45. Xu Z, Liang Y, Lin S, Chen D, Li B, Li L, Deng Y. Crystal violet and XTT assays on Staphylococcus aureus biofilm quantification.. Curr Microbiol 2016;73:474–482.
    doi: 10.1007/s00284-016-1081-1pubmed: 27324342google scholar: lookup
  46. Brunelle BW, Bearson BL, Bearson SMD, Casey TA. Multidrug-resistant Salmonella enterica serovar Typhimurium isolates are resistant to antibiotics that influence their swimming and swarming motility.. mSphere 2017;2:00306–00317.
    doi: 10.1128/mSphere.00306-17pmc: PMC5663980pubmed: 29104932google scholar: lookup
  47. Gu Z, Hübschmann D. Make interactive complex heatmaps in R.. Bioinformatics 2022;38:1460–1462.
    doi: 10.1093/bioinformatics/btab806pmc: PMC8826183pubmed: 34864868google scholar: lookup
  48. Wei T, Simko V, Levy M, Xie Y, Jin Y, Zemla J. Package ‘corrplot’.. 2017;56.
  49. nCouncil TAH . 2023. Results from the 2023 national equine economic impact study released. Available from: https://horsecouncil.org/press-releases/results-from-the-2023-national-equine-economic-impact-study-released. Retrievedn5 Aug 2024.
  50. Kohnen AB, Wiedenheft AM, Traub-Dargatz JL, Short DM, Cook KL, Lantz K, Morningstar-Shaw B, Lawrence JP, House S, Marshall KL, Rao S. Antimicrobial susceptibility of Salmonella and Escherichia coli from equids sampled in the NAHMS 2015-16 equine study and association of management factors with resistance.. Prev Vet Med 2023;213:105857.
    doi: 10.1016/j.prevetmed.2023.105857pubmed: 36773374google scholar: lookup
  51. Kilcoyne I, Magdesian KG, Guerra M, Dechant JE, Spier SJ, Kass PH. Prevalence of and risk factors associated with Salmonella shedding among equids presented to a veterinary teaching hospital for colic (2013-2018).. Equine Vet J 2023;55:446–455.
    doi: 10.1111/evj.13864pubmed: 35861656google scholar: lookup
  52. van Rensburg IB, Jardine JE, Carstens JH, van der Walt ML. The prevalence of intestinal Salmonella infection in horses submitted for necropsy.. Onderstepoort J Vet Res 1995;62:65–67.
    pubmed: 8539039
  53. Li Q. Mechanisms for the invasion and dissemination of Salmonella.. Can J Infect Dis Med Microbiol 2022;2022:1–12.
    doi: 10.1155/2022/2655801pmc: PMC9203224pubmed: 35722038google scholar: lookup
  54. Astorga R, Arenas A, Tarradas C, Mozos E, Zafra R, Pérez J. Outbreak of peracute septicaemic salmonellosis in horses associated with concurrent Salmonella enteritidis and Mucor species infection.. Vet Rec 2004;155:240–242.
    doi: 10.1136/vr.155.8.240pubmed: 15384508google scholar: lookup
  55. Balducci E, Papi F, Capialbi DE, Del Bino L. Polysaccharides’ structures and functions in biofilm architecture of antimicrobial-resistant (AMR) pathogens.. Int J Mol Sci 2023;24:4030.
    doi: 10.3390/ijms24044030pmc: PMC9965654pubmed: 36835442google scholar: lookup
  56. Petrin S, Mancin M, Losasso C, Deotto S, Olsen JE, Barco L. Effect of pH and salinity on the ability of Salmonella serotypes to form biofilm.. Front Microbiol 2022;13:821679.
    doi: 10.3389/fmicb.2022.821679pmc: PMC9021792pubmed: 35464965google scholar: lookup
  57. Dimakopoulou-Papazoglou D, Lianou A, Koutsoumanis KP. Modelling biofilm formation of Salmonella enterica ser. Newport as a function of pH and water activity.. Food Microbiol 2016;53:76–81.
    doi: 10.1016/j.fm.2015.09.002pubmed: 26678133google scholar: lookup
  58. Steenackers H, Hermans K, Vanderleyden J, De Keersmaecker SCJ. Salmonella biofilms: an overview on occurrence, structure, regulation and eradication.. Food Res Int 2012;45:502–531.
    doi: 10.1016/j.foodres.2011.01.038google scholar: lookup
  59. Mahadwar G, Chauhan KR, Bhagavathy GV, Murphy C, Smith AD, Bhagwat AA. Swarm motility of Salmonella enterica serovar Typhimurium is inhibited by compounds from fruit peel extracts.. Lett Appl Microbiol 2015;60:334–340.
    doi: 10.1111/lam.12364pubmed: 25422036google scholar: lookup
  60. Wang Q, Frye JG, McClelland M, Harshey RM. Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity genes.. Mol Microbiol 2004;52:169–187.
    doi: 10.1111/j.1365-2958.2003.03977.xpubmed: 15049819google scholar: lookup
  61. Mirold S, Ehrbar K, Weissmüller A, Prager R, Tschäpe H, Rüssmann H, Hardt WD. Salmonella host cell invasion emerged by acquisition of a mosaic of separate genetic elements, including Salmonella pathogenicity island 1 (SPI1), SPI5, and sopE2.. J Bacteriol 2001;183:2348–2358.
    doi: 10.1128/JB.183.7.2348-2358.2001pmc: PMC95144pubmed: 11244077google scholar: lookup
  62. Bertelloni F, Tosi G, Massi P, Fiorentini L, Parigi M, Cerri D, Ebani VV. Some pathogenic characters of paratyphoid Salmonella enterica strains isolated from poultry.. Asian Pac J Trop Med 2017;10:1161–1166.
    doi: 10.1016/j.apjtm.2017.10.023pubmed: 29268972google scholar: lookup
  63. Bajaj V, Hwang C, Lee CA. hilA is a novel ompR/toxR family member that activates the expression of Salmonella typhimurium invasion genes.. Mol Microbiol 1995;18:715–727.
    doi: 10.1111/j.1365-2958.1995.mmi_18040715.xpubmed: 8817493google scholar: lookup
  64. Gong H, Vu G-P, Bai Y, Yang E, Liu F, Lu S. Differential expression of Salmonella type III secretion system factors InvJ, PrgJ, SipC, SipD, SopA and SopB in cultures and in mice.. Microbiology (Reading) 2010;156:116–127.
    doi: 10.1099/mic.0.032318-0pmc: PMC2889428pubmed: 19762438google scholar: lookup
  65. Giacomodonato MN, Uzzau S, Bacciu D, Caccuri R, Sarnacki SH, Rubino S, Cerquetti MC. SipA, SopA, SopB, SopD and SopE2 effector proteins of Salmonella enterica serovar Typhimurium are synthesized at late stages of infection in mice.. Microbiology (Reading) 2007;153:1221–1228.
    doi: 10.1099/mic.0.2006/002758-0pubmed: 17379731google scholar: lookup
  66. Pal S, Dey S, Batabyal K, Banerjee A, Joardar SN, Samanta I, Isore DP. Characterization of Salmonella gallinarum isolates from backyard poultry by polymerase chain reaction detection of invasion (invA) and Salmonella plasmid virulence (spvC) genes.. Vet World 2017;10:814–817.
    doi: 10.14202/vetworld.2017.814-817pmc: PMC5553153pubmed: 28831228google scholar: lookup
  67. Knych HK, Magdesian KG. Equine antimicrobial therapy: current and past issues facing practitioners.. J Vet Pharmacol Ther 2021;44:270–279.
    doi: 10.1111/jvp.12964pubmed: 33650183google scholar: lookup
  68. Primeau CA, Bharat A, Janecko N, Carson CA, Mulvey M, Reid-Smith R, McEwen S, McWhirter JE, Parmley EJ. Integrated surveillance of extended-spectrum beta-lactamase (ESBL)-producing Salmonella and Escherichia coli from humans and animal species raised for human consumption in Canada from 2012 to 2017 .. Epidemiol Infect 2023;151:e14.
    doi: 10.1017/S0950268822001509pmc: PMC9990382pubmed: 36698196google scholar: lookup
  69. Srednik ME, Morningstar-Shaw BR, Hicks JA, Tong C, Mackie TA, Schlater LK. Whole-genome sequencing and phylogenetic analysis capture the emergence of a multi-drug resistant Salmonella enterica serovar Infantis clone from diagnostic animal samples in the United States.. Front Microbiol 2023;14:1166908.
    doi: 10.3389/fmicb.2023.1166908pmc: PMC10272548pubmed: 37333652google scholar: lookup
  70. Salipante SJ, Hall BG. Determining the limits of the evolutionary potential of an antibiotic resistance gene.. Mol Biol Evol 2003;20:653–659.
    doi: 10.1093/molbev/msg074pubmed: 12679553google scholar: lookup

Citations

This article has been cited 7 times.
  1. Pavon RDN, Mora JFB, Nagpala MJM, Codia A, Pantua HD, Rivera WL. Microarray-Based Serotyping and Molecular Characterization of Virulence and Antimicrobial Resistance of Salmonella enterica from Swine Meat Samples in Abattoirs and Wet Markets of Metro Manila, Philippines. Foods 2026 Jan 6;15(2).
    doi: 10.3390/foods15020187pubmed: 41596787google scholar: lookup
  2. Rossi GAM, Sellera FP, Ferraz CM, Carvalho RS, Oliveira APL, Marques CA, Fávaro EBR, Rosa RDS, Silva LAM, Cardozo MV, Stehling EG, Furlan JPR. Antimicrobial-Resistant Enteric Gram-Negative Bacteria Isolated from a Fatal Diarrhea in a Horse: Genomic Characterization of CTX-M-2-Producing Escherichia coli. Antibiotics (Basel) 2025 Nov 21;14(12).
    doi: 10.3390/antibiotics14121185pubmed: 41463689google scholar: lookup
  3. Phayakka P, Vongkamjan K, Khrongsee P, Subramaniam K, Mordmueng A, Pelyuntha W. Detection, Genomic Characterization, and Antibiotic Susceptibility of Salmonella Anatum SPBM3 Isolated from Plant-Based Meat. Foods 2025 Oct 30;14(21).
    doi: 10.3390/foods14213710pubmed: 41227682google scholar: lookup
  4. Saleh M, Verma A, Shaaban KA, Helmy YA. Antibiotic Alternatives and Next-Generation Therapeutics for Salmonella Control: A One Health Approach to Combating Antimicrobial Resistance. Antibiotics (Basel) 2025 Oct 21;14(10).
    doi: 10.3390/antibiotics14101054pubmed: 41148746google scholar: lookup
  5. He T, Huang M, Sun Y, Ding Y, Zhou N, Fu M, Li T. A newly discovered sRNA is involved in the virulence regulation of Salmonella pullorum. Front Vet Sci 2025;12:1651294.
    doi: 10.3389/fvets.2025.1651294pubmed: 41059458google scholar: lookup
  6. Fahmy NA, Karna S, Bhusal A, Kabir A, Erol E, Helmy YA. Multidrug Resistance and Virulence Traits of Salmonella enterica Isolated from Cattle: Genotypic and Phenotypic Insights. Antibiotics (Basel) 2025 Jul 8;14(7).
    doi: 10.3390/antibiotics14070689pubmed: 40723992google scholar: lookup
  7. He T, Ding Y, Sun Y, Li T. Advances in sRNA-mediated regulation of Salmonella infection in the host. Front Cell Infect Microbiol 2025;15:1503337.
    doi: 10.3389/fcimb.2025.1503337pubmed: 40444151google scholar: lookup
Subscribe to our newsletter
Join 99,658 horse owners like you who receive our email updates on horse health and nutrition.