Journal of Veterinary Science

  • 제24권6호
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  • Pages.82.1-82.12
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  • 2023
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  • 1229-845X(pISSN)
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  • 1976-555X(eISSN)
대한수의학회 (The Korean Society of Veterinary Science)
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Virulence gene profiles and antimicrobial susceptibility of Salmonella Brancaster from chicken

  • Evie Khoo (Department of Veterinary Pathology and Microbiology, Faculty of Veterinary Medicine, Universiti Putra Malaysia) ;
  • Roseliza Roslee (Bacteriology Section, Veterinary Research Institute) ;
  • Zunita Zakaria (Department of Veterinary Pathology and Microbiology, Faculty of Veterinary Medicine, Universiti Putra Malaysia) ;
  • Nur Indah Ahmad (Department of Veterinary Pathology and Microbiology, Faculty of Veterinary Medicine, Universiti Putra Malaysia)
  • 투고 : 2023.03.07
  • 심사 : 2023.09.25
  • 발행 : 2023.11.30
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초록

Background: The current conventional serotyping based on antigen-antisera agglutination could not provide a better understanding of the potential pathogenicity of Salmonella enterica subsp. enterica serovar Brancaster. Surveillance data from Malaysian poultry farms indicated an increase in its presence over the years. Objective: This study aims to investigate the virulence determinants and antimicrobial resistance in S. Brancaster isolated from chickens in Malaysia. Methods: One hundred strains of archived S. Brancaster isolated from chicken cloacal swabs and raw chicken meat from 2017 to 2022 were studied. Two sets of multiplex polymerase chain reaction (PCR) were conducted to identify eight virulence genes associated with pathogenicity in Salmonella (invasion protein gene [invA], Salmonella invasion protein gene [sipB], Salmonella-induced filament gene [sifA], cytolethal-distending toxin B gene [cdtB], Salmonella iron transporter gene [sitC], Salmonella pathogenicity islands gene [spiA], Salmonella plasmid virulence gene [spvB], and inositol phosphate phosphatase gene [sopB]). Antimicrobial susceptibility assessment was conducted by disc diffusion method on nine selected antibiotics for the S. Brancaster isolates. S. Brancaster, with the phenotypic ACSSuT-resistance pattern (ampicillin, chloramphenicol, streptomycin, sulphonamides, and tetracycline), was subjected to PCR to detect the corresponding resistance gene(s). Results: Virulence genes detected in S. Brancaster in this study were invA, sitC, spiA, sipB, sopB, sifA, cdtB, and spvB. A total of 36 antibiogram patterns of S. Brancaster with a high level of multidrug resistance were observed, with ampicillin exhibiting the highest resistance. Over a third of the isolates displayed ACSSuT-resistance, and seven resistance genes (β-lactamase temoneira [blaTEM], florfenicol/chloramphenicol resistance gene [floR], streptomycin resistance gene [strA], aminoglycoside nucleotidyltransferase gene [ant(3")-Ia], sulfonamides resistance gene [sul-1, sul-2], and tetracycline resistance gene [tetA]) were detected. Conclusion: Multidrug-resistant S. Brancaster from chickens harbored an array of virulence-associated genes similar to other clinically significant and invasive non-typhoidal Salmonella serovars, placing it as another significant foodborne zoonosis.

키워드

과제정보

The authors would like to acknowledge the Director-General of Department of Veterinary Services (DVS), the Director of the Veterinary Research Division, and DVS for granting permission to conduct and publish this study.

참고문헌

  1. Popa GL, Papa MI. Salmonella spp. infection - a continuous threat worldwide. Germs. 2021;11(1):88-96. https://doi.org/10.18683/germs.2021.1244
  2. Mohan A, Munusamy C, Tan YC, Muthuvelu S, Hashim R, Chien SL, et al. Invasive Salmonella infections among children in Bintulu, Sarawak, Malaysian Borneo: a 6-year retrospective review. BMC Infect Dis. 2019;19(1):330.
  3. Modarressi S, Thong KL. Isolation and molecular subtyping of Salmonella enterica from chicken, beef and street foods in Malaysia. Sci Res Essays. 2010;5(18):2713-2720. 
  4. Chuah LO, Shamila Syuhada AK, Mohamad Suhaimi I, Farah Hanim T, Rusul G. Genetic relatedness, antimicrobial resistance and biofilm formation of Salmonella isolated from naturally contaminated poultry and their processing environment in northern Malaysia. Food Res Int. 2018;105:743-751. https://doi.org/10.1016/j.foodres.2017.11.066
  5. Hinden E, Taylor J, Walther WW. An outbreak due to Salmonella brancaster. Lancet. 1952;260(6724):64-66. https://doi.org/10.1016/S0140-6736(52)92107-7
  6. Dieye Y, Hull DM, Wane AA, Harden L, Fall C, Sambe-Ba B, et al. Genomics of human and chicken Salmonella isolates in Senegal: broilers as a source of antimicrobial resistance and potentially invasive nontyphoidal salmonellosis infections. PLoS One. 2022;17(3):e0266025.
  7. Zwe YH, Tang VC, Aung KT, Gutierrez RA, Ng LC, Yuk HG. Prevalence, sequence types, antibiotic resistance and, gyrA mutations of Salmonella isolated from retail fresh chicken meat in Singapore. Food Control. 2018;90:233-240. https://doi.org/10.1016/j.foodcont.2018.03.004
  8. Chang YJ, Chen CL, Yang HP, Chiu CH. Prevalence, serotypes, and antimicrobial resistance patterns of non-typhoid Salmonella in food in northern Taiwan. Pathogens. 2022;11(6):705.
  9. Anderson TC, Nguyen TA, Adams JK, Garrett NM, Bopp CA, Baker JB, et al. Multistate outbreak of human Salmonella Typhimurium infections linked to live poultry from agricultural feed stores and mail-order hatcheries, United States 2013. One Health. 2016;2:144-149. https://doi.org/10.1016/j.onehlt.2016.08.002
  10. Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629-655. https://doi.org/10.1016/S0140-6736(21)02724-0
  11. Chin PS, Yu CY, Ang GY, Yin WF, Chan KG. Draft genome sequence of multidrug-resistant Salmonella enterica serovar Brancaster strain PS01 isolated from chicken meat, Malaysia. J Glob Antimicrob Resist. 2017;9:41-42. https://doi.org/10.1016/j.jgar.2016.12.017
  12. Wang M, Qazi IH, Wang L, Zhou G, Han H. Salmonella virulence and immune escape. Microorganisms. 2020;8(3):407.
  13. Chattaway MA, Langridge GC, Wain J. Salmonella nomenclature in the genomic era: a time for change. Sci Rep. 2021;11(1):7494.
  14. Kim JE, Lee YJ. Molecular characterization of antimicrobial resistant non-typhoidal Salmonella from poultry industries in Korea. Ir Vet J. 2017;70(1):20.
  15. Grimont PAD, Weill FX. Antigenic Formulae of the Salmonella Serovars. 9th ed. Geneva: World Health Organization; 2007.
  16. Abatcha MG, Effarizah ME, Rusul G. Prevalence, antimicrobial resistance, resistance genes and class 1 integrons of Salmonella serovars in leafy vegetables, chicken carcasses and related processing environments in Malaysian fresh food markets. Food Control. 2018;91:170-180. https://doi.org/10.1016/j.foodcont.2018.02.039
  17. Skyberg JA, Logue CM, Nolan LK. Virulence genotyping of Salmonella spp. with multiplex PCR. Avian Dis. 2006;50(1):77-81. https://doi.org/10.1637/7417.1
  18. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing. CLSI supplement M100. 30th ed. Wayne: Clinical and Laboratory Standards Institute; 2020. 
  19. Bacci C, Boni E, Alpigiani I, Lanzoni E, Bonardi S, Brindani F. Phenotypic and genotypic features of antibiotic resistance in Salmonella enterica isolated from chicken meat and chicken and quail carcasses. Int J Food Microbiol. 2012;160(1):16-23. https://doi.org/10.1016/j.ijfoodmicro.2012.09.014
  20. Hur J, Kim JH, Park JH, Lee YJ, Lee JH. Molecular and virulence characteristics of multi-drug resistant Salmonella Enteritidis strains isolated from poultry. Vet J. 2011;189(3):306-311. https://doi.org/10.1016/j.tvjl.2010.07.017
  21. Ng LK, Martin I, Alfa M, Mulvey M. Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes. 2001;15(4):209-215. https://doi.org/10.1006/mcpr.2001.0363
  22. Shang K, Wei B, Jang HK, Kang M. Phenotypic characteristics and genotypic correlation of antimicrobial resistant (AMR) Salmonella isolates from a poultry slaughterhouse and its downstream retail markets. Food Control. 2019;100:35-45. https://doi.org/10.1016/j.foodcont.2018.12.046
  23. Mughini-Gras L, van Hoek AH, Cuperus T, Dam-Deisz C, van Overbeek W, van den Beld M, et al. Prevalence, risk factors and genetic traits of Salmonella Infantis in Dutch broiler flocks. Vet Microbiol. 2021;258(109120):109120.
  24. Suez J, Porwollik S, Dagan A, Marzel A, Schorr YI, Desai PT, et al. Virulence gene profiling and pathogenicity characterization of non-typhoidal Salmonella accounted for invasive disease in humans. PLoS One. 2013;8(3):e58449.
  25. Liu Y, Jiang J, Ed-Dra A, Li X, Peng X, Xia L, et al. Prevalence and genomic investigation of Salmonella isolates recovered from animal food-chain in Xinjiang, China. Food Res Int. 2021;142(110198):110198.
  26. Rodriguez-Rivera LD, Bowen BM, den Bakker HC, Duhamel GE, Wiedmann M. Characterization of the cytolethal distending toxin (typhoid toxin) in non-typhoidal Salmonella serovars. Gut Pathog. 2015;7(1):19.
  27. Guiney DG, Fierer J. The role of the spv genes in Salmonella pathogenesis. Front Microbiol. 2011;2:129.
  28. Kuang D, Xu X, Meng J, Yang X, Jin H, Shi W, et al. Antimicrobial susceptibility, virulence gene profiles and molecular subtypes of Salmonella Newport isolated from humans and other sources. Infect Genet Evol. 2015;36:294-299. https://doi.org/10.1016/j.meegid.2015.10.003
  29. Garcia-Pastor L, Puerta-Fernandez E, Casadesus J. Bistability and phase variation in Salmonella enterica. Biochim Biophys Acta Gene Regul Mech. 2019;1862(7):752-758. https://doi.org/10.1016/j.bbagrm.2018.01.003
  30. V T Nair D, Venkitanarayanan K, Kollanoor Johny A. Antibiotic-resistant Salmonella in the food supply and the potential role of antibiotic alternatives for control. Foods. 2018;7(10):1-24.
  31. Ifeanyi CI, Bassey BE, Ikeneche NF, Al-Gallas N. Molecular characterization and antibiotic resistance of Salmonella in children with acute gastroenteritis in Abuja, Nigeria. J Infect Dev Ctries. 2014;8(6):712-719. https://doi.org/10.3855/jidc.4185
  32. McMillan EA, Gupta SK, Williams LE, Jove T, Hiott LM, Woodley TA, et al. Antimicrobial resistance genes, cassettes, and plasmids present in Salmonella enterica associated with United States food animals. Front Microbiol. 2019;10:832.
  33. Given C, Penttinen R, Jalasvuori M. Plasmid viability depends on the ecological setting of hosts within a multiplasmid community. Microbiol Spectr. 2022;10(2):e0013322. 
  34. Campioni F, Gomes CN, Bergamini AM, Rodrigues DP, Falcao JP. Partial correlation between phenotypic and genotypic antimicrobial resistance of Salmonella enterica serovar Enteritidis strains from Brazil. Microb Drug Resist. 2020;26(12):1466-1471. https://doi.org/10.1089/mdr.2019.0477
  35. Manyi-Loh C, Mamphweli S, Meyer E, Okoh A. Antibiotic use in agriculture and its consequential resistance in environmental sources: potential public health implications. Molecules. 2018;23(4):795.
  36. Rachel WJ, Marni S, Zurina R, Ani Y, Rozanah Asmah A. Antibiotic usage in myGAP poultry farms in Malaysia. Malays J Vet Res. 2020;11(2):22-31. 
  37. World Organisation for Animal Health. Malaysia country report on the current situations of the use of antimicrobial agents as growth promoter in 2019 OIE Regional Workshop on Animal Feed Safety [Internet]. Paris: World Organisation for Animal Health; https://rr-asia.woah.org/wp-content/uploads/2020/01/malaysia.pdf. Updated 2020. Accessed 2023 May 31.