DOI QR코드

DOI QR Code

Virulence and Antimicrobial Resistance Gene Profiling of Salmonella Isolated from Swine Meat Samples in Abattoirs and Wet Markets of Metro Manila, Philippines

  • Rance Derrick N. Pavon (Pathogen-Host-Environment Interactions Research Laboratory, Institute of Biology, College of Science, University of the Philippines Diliman) ;
  • Windell L. Rivera (Pathogen-Host-Environment Interactions Research Laboratory, Institute of Biology, College of Science, University of the Philippines Diliman)
  • 투고 : 2023.06.26
  • 심사 : 2023.10.06
  • 발행 : 2023.12.28

초록

Salmonella are Gram-negative pathogenic bacteria commonly found in food animals such as poultry and swine and potentially constitute risks and threats to food safety and public health through transmissible virulence and antimicrobial resistance (AMR) genes. Although there are previous studies in the Philippines regarding genotypic and phenotypic AMR in Salmonella, there are very few on virulence and their associations. Hence, this study collected 700 Salmonella isolates from swine samples in abattoirs and wet markets among four districts in Metro Manila and characterized their genotypic virulence and β-lactam AMR profiles. Gene frequency patterns and statistical associations between virulence and bla genes and comparisons based on location types (abattoirs and wet markets) and districts were also determined. High prevalence (>50%) of virulence genes was detected encompassing Salmonella pathogenicity islands (SPIs) 1-5 suggesting their pathogenic potential, but none possessed plasmid-borne virulence genes spvR and spvC. For bla, blaTEM was detected with high prevalence (>45%) and revealed significant associations to four SPI genes, namely, avrA, hilA, mgtC, and spi4R, which suggest high resistance potential particularly to β-lactam antibiotics and relationships with pathogenicity that remain mechanistically unestablished until now. Lastly, comparisons of location types and districts showed variations in gene prevalence suggesting effects from environmental factors throughout the swine production chain. This study provides vital data on the genotypic virulence and AMR of Salmonella from swine in abattoirs and wet markets that suggest their pathogenicity and resistance potential for policymakers to implement enforced surveillance and regulations for the improvement of the Philippine swine industry.

키워드

과제정보

The authors acknowledge Paolo D.G. Mendoza, Camille Andrea R. Flores, and Alyzza Marie B. Calayag for the technical support. This study was supported financially by the Department of Agriculture-Biotechnology Program Office (DABIOTECH-R1808) of the Philippines.

참고문헌

  1. World Health Organization. 2018. Salmonella (non-typhoidal). Available from https://www.who.int/news-room/fact-sheets/detail/salmonella-(non-typhoidal)#:~:text=Salmonellosis%20is%20a%20disease%20caused,illness%20lasts%202-7%20days. Accessed May 21, 2022.
  2. Casadevall A, Pirofski LA. 1999. Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect. Immun. 67: 3703-3713. https://doi.org/10.1128/IAI.67.8.3703-3713.1999
  3. Foley SL, Johnson TJ, Ricke SC, Nayak R, Danzeisen J. 2013. Salmonella pathogenicity and host adaptation in chicken-associated serovars. Microbiol. Mol. Biol. Rev. 77: 582-607. https://doi.org/10.1128/MMBR.00015-13
  4. Wang M, Qazi IH, Wang L, Zhou G, Han H. 2020. Salmonella virulence and immune escape. Microorganisms 8: 407.
  5. Ng KCS, Rivera WL. 2015. Multiplex PCR-based serogrouping and serotyping of Salmonella enterica from tonsil and jejunum with jejunal lymph nodes of slaughtered swine in Metro Manila, Philippines. J. Food Prot. 78: 873-880. https://doi.org/10.4315/0362-028X.JFP-14-342
  6. Soguilon-del Rosario S, Rivera WL. 2015. Incidence and molecular detection of Salmonella enterica serogroups and spvC virulence gene in raw and processed meats from selected wet markets in Metro Manila, Philippines. Int. J. Philipp. Sci. Technol. 8: 52-55. https://doi.org/10.18191/2015-08-2-025
  7. Paclibare PAP, Calayag AMB, Santos PDM, Rivera WL. 2017. Molecular characterization of Salmonella enterica isolated from raw and processed meats from selected wet markets in Metro Manila, Philippines. Philipp. Agric. Sci. 100: 55-62.
  8. Azanza MPV, Membrebe, BNQ, Sanchez RGR, Estilo EEC, Dollete UGM, Feliciano RJ, et al. 2019. Foodborne disease outbreaks in the Philippines (2005-2018). Philipp. J. Sci. 148: 323-342.
  9. World Health Organization. 2021. Antimicrobial resistance. Available from https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance. Accessed May 21, 2022.
  10. Miller MB, Gilligan PH. 2012. 290 - Mechanisms and detection of antimicrobial resistance, pp. 1421-1433. In Long SS (ed.). Principles and Practice of Pediatric Infectious Diseases, 4th Ed. Elsevier Churchill Livingstone, London.
  11. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, et al. 2015. Global trends in antimicrobial use in food animals. Proc. Natl. Acad. Sci. USA 112: 5649-5654. https://doi.org/10.1073/pnas.1503141112
  12. Tiseo K, Huber L, Gilbert M, Robinson TP, Van Boeckel TP. 2020. Global trends in antimicrobial use in food animals from 2017 to 2030. Antibiotics (Basel) 9: 918.
  13. Landers TF, Cohen B, Wittum TE, Larson EL. 2012. A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Rep. 127: 4-22. https://doi.org/10.1177/003335491212700103
  14. Peng M, Salaheen, S, Biswas D. 2014. Animal health: Global antibiotic issues. Encyclopedia Agric. Food Syst. 2014: 346-357. https://doi.org/10.1016/B978-0-444-52512-3.00187-X
  15. de Kraker ME, Stewardson AJ, Harbarth S. 2016. Will 10 million people die a year due to antimicrobial resistance by 2050? PLoS Med. 13): e1002184.
  16. Centers for Disease Control and Prevention. 2019. Antibiotic resistance threats in the United States. Available from https://www.cdc.gov/drugresistance/pdf/threats-report/2019-ar-threats-report-508.pdf. Accessed May 21, 2022.
  17. Ng KC, Rivera WL. 2014. Antimicrobial resistance of Salmonella enterica isolates from tonsil and jejunum with lymph node tissues of slaughtered swine in Metro Manila, Philippines. ISRN Microbiol. 2014: 364265.
  18. Calayag AMB, Paclibare PAP, Santos PDM, Bautista CAC, Rivera WL. 2017. Molecular characterization and antimicrobial resistance of Salmonella enterica from swine slaughtered in two different types of Philippine abattoir. Food Microbiol. 65: 51-56. https://doi.org/10.1016/j.fm.2017.01.016
  19. Calayag AMB, Widmer KW, Rivera WL. 2021. Antimicrobial susceptibility and frequency of bla and qnr genes in Salmonella enterica isolated from slaughtered pigs. Antibiotics (Basel) 10: 1442.
  20. de Guzman MLC, Manzano RME, Monjardin JFB. 2016. Antibiotic resistant bacteria in raw chicken meat sold in public market in Quezon city, Philippines. Philipp. J. Health Res. Dev. 20: 43-51.
  21. Paterson DL, Bonomo RA. 2005. Extended-spectrum beta-lactamases: a clinical update. Clin. Microbiol. Rev. 18: 657-686. https://doi.org/10.1128/CMR.18.4.657-686.2005
  22. Rawat D, Nair D. 2010. Extended-spectrum β-lactamases in gram negative bacteria. J. Glob. Infect. Dis. 2: 263-274. https://doi.org/10.4103/0974-777X.68531
  23. Campos J, Mourao J, Peixe L, Antunes P. 2019. Non-typhoidal Salmonella in the pig production chain: A comprehensive analysis of its impact on human health. Pathogens 8: 19.
  24. Huynh TTT, Aarnink AJA, Drucker A, Verstegen MWA. 2006. Pig production in Cambodia, Laos, Philippines, and Vietnam: A review. Asian J. Agric. Rural Dev. 3: 69-90.
  25. Lapus ZM. 2009. Swine production in the Philippines. Available from https://www.pig333.com/articles/swine-production-in-the-philippines-2-2_1489/. Accessed May 21, 2022.
  26. Barroga TRM, Morales RG, Benigno CC, Castro SJM, Caniban MM, Cabullo MFB, et al. 2020. Antimicrobials used in backyard and commercial poultry and swine farms in the Philippines: A qualitative pilot study. Front. Vet. Sci. 7: 329.
  27. Chiu CH, Ou JT. 1996. Rapid identification of Salmonella serovars in feces by specific detection of virulence genes, invA and spvC, by an enrichment broth culture-multiplex PCR combination assay. J. Clin. Microbiol. 34: 2619-2622. https://doi.org/10.1128/jcm.34.10.2619-2622.1996
  28. Pavon RDN, Rivera WL. 2021. Molecular serotyping by phylogenetic analyses of a 1498bp segment of the invA gene of Salmonella. ASM Sci. J. 14. doi: 10.32802/asmscj.2020.602.
  29. Borges KA, Furian TQ, Borsoi A, Moraes HLS, Salle CTP, Nascimento VP. 2013. Detection of virulence-associated genes in Salmonella Enteritidis isolates from chicken in South of Brazil. Pesq. Vet. Bras. 33: 1416-1422. . https://doi.org/10.1590/S0100-736X2013001200004
  30. Fazl AA, Salehi TZ, Jamshidian M, Amini K, Jangjou AH. 2013. Molecular detection of invA, ssaP, sseC and pipB genes in Salmonella Typhimurium isolated from human and poultry in Iran. Afr. J. Microbiol. Res. 7: 1104-1108.
  31. Sanchez-Jimenez MM, Cardona-Castro NM, Canu N, Uzzau S, Rubino S. 2010. Distribution of pathogenicity islands among Colombian isolates of Salmonella. J. Infect. Dev. Ctries. 4: 555-559. https://doi.org/10.3855/jidc.670
  32. Soto SM, Rodriguez I, Rodicio MR, Vila J, Mendoza MC. 2006. Detection of virulence determinants in clinical strains of Salmonella enterica serovar Enteritidis and mapping on macrorestriction profiles. J. Med. Microbiol. 55: 365-373. https://doi.org/10.1099/jmm.0.46257-0
  33. Knodler LA, Celli J, Hardt W-D, Vallance BA, Yip C, Finlay BB. 2002. Salmonella effectors within a single pathogenicity island are differentially expressed and translocated by separate type III secretion systems. Mol. Microbiol. 43: 1089-1103. https://doi.org/10.1046/j.1365-2958.2002.02820.x
  34. Derakhshandeh A, Firouzi R, Khoshbakht R. 2012. Association of three plasmid-encoded spv genes among different Salmonella serotypes isolated from different origins. Indian J. Microbiol. 53: 106-110. https://doi.org/10.1007/s12088-012-0316-5
  35. Pavon RDN, Mendoza PDG, Flores CAR, Calayag AMB, Rivera WL. 2022. Genotypic virulence profiles and associations in Salmonella isolated from meat samples in wet markets and abattoirs of Metro Manila, Philippines. BMC Microbiol. 22: 292.
  36. Monstein HJ, Ostholm-Balkhed A, Nilsson MV, Nilsson M, Dornbusch K, Nilsson LE. 2007. Multiplex PCR amplification assay for the detection of blaSHV, blaTEM and blaCTX-M genes in Enterobacteriaceae. APMIS 115: 1400-1408. https://doi.org/10.1111/j.1600-0463.2007.00722.x
  37. Byomi A, Zidan S, Ghada H, Sakr M, EL-Waraqi S. 2019. Characterization of Salmonella spp. isolated from poultry giblets, calves and human beings in Menoufiya governorate. JCVR. 2: 78-94.
  38. Siddiky NA, Sarker MS, Khan MSR, Begum R, Kabir ME, Karim MR, et al. 2021. Virulence and antimicrobial resistance profiles of Salmonella enterica serovars isolated from chicken at wet markets in Dhaka, Bangladesh. Microorganisms 9: 952.
  39. Kong-Ngoen T, Santajit S, Tunyong W, Pumirat P, Sookrung N, Chaicumpa W, et al. 2022. Antimicrobial resistance and virulence of non-typhoidal Salmonella from retail foods marketed in Bangkok, Thailand. Foods. 11: 661.
  40. Boddicker JD, Knosp BM, Jones BD. 2003. Transcription of the Salmonella invasion gene activator, hilA, requires HilD activation in the absence of negative regulators. J. Bacteriol. 185: 525-533. https://doi.org/10.1128/JB.185.2.525-533.2003
  41. Ramatla TA, Mphuthi N, Ramaili T, Taioe MO, Thekisoe OMM, Syakalima M. 2020. Molecular detection of virulence genes in Salmonella spp. isolated from chicken faeces in Mafikeng, South Africa. J. S. Afr. Vet. Assoc. 91: e1-e7. https://doi.org/10.4102/jsava.v91i0.1994
  42. Thung TY, Radu S, Mahyudin NA, Rukayadi Y, Zakaria Z, Mazlan N, et al. 2018. Prevalence, virulence genes and antimicrobial resistance profiles of Salmonella serovars from retail beef in Selangor, Malaysia. Front. Microbiol. 8: 2697.
  43. Elkenany R, Elsayed MM, Zakaria AI, El-Sayed SA, Rizk MA. 2019. Antimicrobial resistance profiles and virulence genotyping of Salmonella enterica serovars recovered from broiler chickens and chicken carcasses in Egypt. BMC Vet. Res. 15: 124.
  44. Ahmed HA, El-Hofy FI, Shafik SM, Abdelrahman MA, Elsaid GA. 2016. Characterization of virulence-associated genes, antimicrobial resistance genes, and class 1 integrons in Salmonella enterica serovar Typhimurium isolates from chicken meat and humans in Egypt. Foodborne Pathog. Dis. 13: 281-288. https://doi.org/10.1089/fpd.2015.2097
  45. Joaquim P, Herrera M, Dupuis A, Chacana P. 2021. Virulence genes and antimicrobial susceptibility in Salmonella enterica serotypes isolated from swine production in Argentina. Rev. Argent. Microbiol. 53: 233-239. https://doi.org/10.1016/j.ram.2020.10.001
  46. Shittu OB, Uzairue LI, Ojo OE, Obuotor TM, Folorunso JB, Raheem-Ademola RR, et al. 2022. Antimicrobial resistance and virulence genes in Salmonella enterica serovars isolated from droppings of layer chicken in two farms in Nigeria. J. Appl. Microbiol. 132: 3891-3906. https://doi.org/10.1111/jam.15477
  47. Liao AP, Petrof EO, Kuppireddi S, Zhao Y, Xia Y, Claud EC, et al. 2008. Salmonella type III effector AvrA stabilizes cell tight junctions to inhibit inflammation in intestinal epithelial cells. PLoS One 3: e2369.
  48. Yin C, Liu Z, Xian H, Jiao Y, Yuan Y, Li Y, et al. 2020. AvrA exerts inhibition of NF-κB pathway in its naive Salmonella serotype through suppression of p-JNK and beclin-1 molecules. Int. J. Mol. Sci. 21: 6063.
  49. Hower S, McCormack R, Bartra SS, Alonso P, Podack ER, Shembade N, et al. 2021. LPS modifications and AvrA activity of Salmonella enterica serovar Typhimurium are required to prevent Perforin-2 expression by infected fibroblasts and intestinal epithelial cells. Microb. Pathog. 154: 104852.
  50. Wu H, Jones RM, Neish AS. 2012. The Salmonella effector AvrA mediates bacterial intracellular survival during infection in vivo. Cell Microbiol. 14: 28-39. https://doi.org/10.1111/j.1462-5822.2011.01694.x
  51. Lu R, Wu S, Zhang YG, Xia Y, Liu X, Zheng Y, et al. 2014. Enteric bacterial protein AvrA promotes colonic tumorigenesis and activates colonic beta-catenin signaling pathway. Oncogenesis 3: e105.
  52. Zou W, Al-Khaldi SF, Branham WS, Han T, Fuscoe JC, Han J, et al. 2011. Microarray analysis of virulence gene profiles in Salmonella serovars from food/food animal environment. J. Infect. Dev. Ctries. 5: 94-105. https://doi.org/10.3855/jidc.1396
  53. Suez J, Porwollik S, Dagan A, Marzel A, Schorr YI, Desai PT, et al. 2013. Virulence gene profiling and pathogenicity characterization of non-typhoidal Salmonella accounted for invasive disease in humans. PLoS One 8: e58449.
  54. Astolfi-Ferreira CS, Pequini MRS, Nunez LFN, Parra SHS, Chacon R, Torre DID, et al. 2017. A comparative survey between non-systemic Salmonella spp. (paratyphoid group) and systemic Salmonella Pullorum and S. Gallinarum with a focus on virulence genes. Pesqui. Vet. Bras. 37: 1064-1068. https://doi.org/10.1590/s0100-736x2017001000004
  55. Lee JW, Lee EJ. 2015. Regulation and function of the Salmonella MgtC virulence protein. J. Microbiol. 53: 667-672. https://doi.org/10.1007/s12275-015-5283-1
  56. Park M, Kim H, Nam D, Kweon DH, Shin D. 2019. The mgtCBR mRNA leader secures growth of Salmonella in both host and non-host environments. Front. Microbiol. 10: 2831.
  57. Nguyen Thi H, Pham TT, Turchi B, Fratini F, Ebani VV, Cerri D, et al. 2020. Characterization of Salmonella spp. isolates from swine: Virulence and antimicrobial resistance. Animals (Basel) 10: 2418.
  58. Obayes MS, Al-Bermani OK, Rahim SA. 2020. Genetic detection of invA, sipB, sopB and sseC genes in Salmonella spp. isolated from diarrheic children patients. EurAsian J. Biosci. 14: 3085-3091.
  59. Li S, Zhang Z, Pace L, Lillehoj H, Zhang S. 2009. Functions exerted by the virulence-associated type-three secretion systems during Salmonella enterica serovar Enteritidis invasion into and survival within chicken oviduct epithelial cells and macrophages. Avian Pathol. 38: 97-106. https://doi.org/10.1080/03079450902737771
  60. Maze A, Glatter T, Bumann D. 2014. The central metabolism regulator EIIAGlc switches Salmonella from growth arrest to acute virulence through activation of virulence factor secretion. Cell Rep. 7: 1426-1433. https://doi.org/10.1016/j.celrep.2014.04.022
  61. Freeman JA, Rappl C, Kuhle V, Hensel M, Miller SI. 2002. SpiC is required for translocation of Salmonella pathogenicity island 2 effectors and secretion of translocon proteins SseB and SseC. J. Bacteriol. 184: 4971-4980. https://doi.org/10.1128/JB.184.18.4971-4980.2002
  62. Bhowmick PP, Devegowda D, Ruwandeepika HAD, Karunasagar I, Karunasagar I. 2011. Presence of Salmonella pathogenicity island 2 genes in seafood-associated Salmonella serovars and the role of the sseC gene in survival of Salmonella enterica serovar Weltevreden in epithelial cells. Microbiology (Reading) 157(Pt 1): 160-168. https://doi.org/10.1099/mic.0.043596-0
  63. Parvathi A, Vijayan J, Murali G, Chandran P. 2011. Comparative virulence genotyping and antimicrobial susceptibility profiling of environmental and clinical Salmonella enterica from Cochin, India. Curr. Microbiol. 62: 21-26. https://doi.org/10.1007/s00284-010-9665-7
  64. El sayed AESM, Abdel-Azeem MW, Sultan S, Yousif AA. 2016. Detection of five major pathogenicity islands in Salmonella serovars isolated from broiler chicken. Nat. Sci. 14: 103-110.
  65. Kaur J, Jain SK. 2012. Role of antigens and virulence factors of Salmonella enterica serovar Typhi in its pathogenesis. Microbiol. Res. 167: 199-210. https://doi.org/10.1016/j.micres.2011.08.001
  66. Srisanga S, Angkititrakul S, Sringam P, Le Ho PT, T Vo AT, Chuanchuen R. 2017. Phenotypic and genotypic antimicrobial resistance and virulence genes of Salmonella enterica isolated from pet dogs and cats. J. Vet. Sci. 18: 273-281. https://doi.org/10.4142/jvs.2017.18.3.273
  67. Addwebi TM, Call DR, Shah DH. 2014. Contribution of Salmonella Enteritidis virulence factors to intestinal colonization and systemic dissemination in 1-day-old chickens. Poult. Sci. 93: 871-881. https://doi.org/10.3382/ps.2013-03710
  68. Gopinath A, Allen TA, Bridgwater CJ, Young CM, Worley MJ. 2019. The Salmonella type III effector SpvC triggers the reverse transmigration of infected cells into the bloodstream. PLoS One 14: e0226126.
  69. Chakraborty S, Roychoudhury P, Samanta I, Subudhi PK, Lalhruaipuii L, Das M, et al. 2020. Molecular detection of biofilm, virulence and antimicrobial resistance associated genes of Salmonella serovars isolated from pig and chicken of Mizoram, India. Indian J. Anim. Res. 54: 608-613.
  70. El-Sharkawy H, Tahoun A, El-Gohary AEA, El-Abasy M, El-Khayat F, Gillespie T, et al. 2017. Epidemiological, molecular characterization and antibiotic resistance of Salmonella enterica serovars isolated from chicken farms in Egypt. Gut Pathog. 9: 8.
  71. Zhang YL, Huang FY, Gan LL, Yu X, Cai D-J, Fang J, et al. 2021. High prevalence of blaCTX-M and blaSHV among ESBL producing E. coli isolates from beef cattle in China's Sichuan-Chongqing Circle. Sci. Rep. 11: 13725.
  72. Adamu I, Ishaleku D, Obande G. 2018. High occurrence blaCTX-M, blaSHV, and blaTEM genes in extended-spectrum β-lactamase-positive strains of Salmonella Typhimurium in Nasarawa state: results of a point prevalence survey. Int. J. Infect. Dis. 73: 128.
  73. Nair S, Day M, Godbole G, Saluja T, Langridge GC, Dallman TJ, et al. 2020. Genomic surveillance detects Salmonella enterica serovar Paratyphi A harbouring blaCTX-M-15 from a traveller returning from Bangladesh. PLoS One 15: e0228250.
  74. Dor Z, Shnaiderman-Torban A, Kondratyeva K, Davidovich-Cohen M, Rokney A, Steinman A, et al. 2020. Emergence and spread of different ESBL-producing Salmonella enterica serovars in hospitalized horses sharing a highly transferable IncM2 CTX-M-3-encoding plasmid. Front. Microbiol. 11: 616032.
  75. Pitout JD, DeVinney R. 2017. Escherichia coli ST131: A multidrug-resistant clone primed for global domination. F1000Res. 6: F1000 Faculty Rev-195.
  76. Geisinger E, Isberg RR. 2017. Interplay between antibiotic resistance and virulence during disease promoted by multidrug-resistant bacteria. J. Infect. Dis. 215(suppl_1): S9-S17. https://doi.org/10.1093/infdis/jiw402
  77. Gerlach RG, Hensel M. 2007. Salmonella pathogenicity islands in host specificity, host pathogen-interactions and antibiotics resistance of Salmonella enterica. Berl. Munch. Tierarztl. Wochenschr. 120: 317-327.
  78. Liaquat S, Sarwar Y, Ali A, Haque A, Farooq M, Martinez-Ballesteros I, et al. 2018. Virulotyping of Salmonella enterica serovar Typhi isolates from Pakistan: Absence of complete SPI-10 in Vi negative isolates. PLoS Negl. Trop. Dis. 12: e0006839.
  79. Osman KM, Marouf SH, Alatfeehy N. 2013. Antimicrobial resistance and virulence-associated genes of Salmonella enterica subsp. enterica serotypes Muenster, Florian, Omuna, and Noya strains isolated from clinically diarrheic humans in Egypt. Microb. Drug Resist. 19: 370-377. https://doi.org/10.1089/mdr.2012.0151
  80. Higgins D, Mukherjee N, Pal C, Sulaiman IM, Jiang Y, Hanna S, et al. 2020. Association of virulence and antibiotic resistance in Salmonella-statistical and computational insights into a selected set of clinical isolates. Microorganisms 8: 1465.
  81. Brunelle BW, Bearson SM, Bearson BL. 2013. Tetracycline accelerates the temporally-regulated invasion response in specific isolates of multidrug-resistant Salmonella enterica serovar Typhimurium. BMC Microbiol. 13: 202.
  82. Brunelle BW, Bearson BL, Bearson SM. 2015. Chloramphenicol and tetracycline decrease motility and increase invasion and attachment gene expression in specific isolates of multidrugresistant Salmonella enterica serovar Typhimurium. Front. Microbiol. 5: 801.
  83. Chuanchuen R, Ajariyakhajorn K, Koowatananukul C, Wannaprasat W, Khemtong S, Samngamnim S. 2010. Antimicrobial resistance and virulence genes in Salmonella enterica isolates from dairy cows. Foodborne Pathog. Dis. 7: 63-69. https://doi.org/10.1089/fpd.2009.0341
  84. Yue M, Li X, Liu D, Hu X. 2020. Serotypes, antibiotic resistance, and virulence genes of Salmonella in children with diarrhea. J. Clin. Lab. Anal. 34: e23525.
  85. Johansson MHK, Bortolaia V, Tansirichaiya S, Aarestrup FM, Roberts AP, Petersen TN. 2021. Detection of mobile genetic elements associated with antibiotic resistance in Salmonella enterica using a newly developed web tool: MobileElementFinder. J. Antimicrob. Chemother. 76: 101-109. https://doi.org/10.1093/jac/dkaa390
  86. Mangat CS, Bekal S, Irwin RJ, Mulvey MR. 2017. A novel hybrid plasmid carrying multiple antimicrobial resistance and virulence genes in Salmonella enterica serovar Dublin. Antimicrob. Agents Chemother. 61: e02601-e02616. https://doi.org/10.1128/AAC.02601-16
  87. Vinueza-Burgos C, Baquero M, Medina J, De Zutter L. 2019. Occurrence, genotypes and antimicrobial susceptibility of Salmonella collected from the broiler production chain within an integrated poultry company. Int. J. Food Microbiol. 299: 1-7. https://doi.org/10.1016/j.ijfoodmicro.2019.03.014
  88. Liu Y, Jiang J, Ed-Dra A, Li X, Peng X, Xia L, et al. 2021. Prevalence and genomic investigation of Salmonella isolates recovered from animal food-chain in Xinjiang, China. Food Res. Int. 142: 110198.
  89. Li Y, Li K, Peng K, Wang Z, Song H, Li R. 2022. Distribution, antimicrobial resistance and genomic characterization of Salmonella along the pork production chain in Jiangsu, China. LWT 163: 113516.
  90. Khan AS, Pierneef RE, Gonzalez-Escalona N, Maguire M, Li C, Tyson GH, et al. 2022. Molecular characterization of Salmonella detected along the broiler production chain in Trinidad and Tobago. Microorganisms 10: 570.