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Journal of Microbiology

, Volume 57, Issue 4, pp 271–280 | Cite as

Genomic surveillance links livestock production with the emergence and spread of multi-drug resistant non-typhoidal Salmonella in Mexico

  • Enrique Jesús Delgado-SuárezEmail author
  • Rocío Ortíz-López
  • Wondwossen A. Gebreyes
  • Marc W. Allard
  • Francisco Barona-Gómez
  • María Salud Rubio-Lozano
Microbial Genetics, Genomics and Molecular Biology
  • 110 Downloads

Abstract

Multi-drug resistant (MDR) non-typhoidal Salmonella (NTS) is increasingly common worldwide. While food animals are thought to contribute to the growing antimicrobial resistance (AMR) problem, limited data is documenting this relationship, especially in low and middle-income countries (LMIC). Herein, we aimed to assess the role of non-clinical NTS of bovine origin as reservoirs of AMR genes of human clinical significance. We evaluated the phenotypic and genotypic AMR profiles in a set of 44 bovine-associated NTS. For comparative purposes, we also included genotypic AMR data of additional isolates from Mexico (n = 1,067) that are publicly available. The most frequent AMR phenotypes in our isolates involved tetracycline (40/44), trimethoprim-sulfamethoxazole (26/44), chloramphenicol (19/44), ampicillin (18/44), streptomycin (16/44), and carbenicillin (13/44), while nearly 70% of the strains were MDR. These phenotypes were correlated with a widespread distribution of AMR genes (i.e. tetA, aadA, dfrA12, dfrA17, sul1, sul2, bla-TEM-1, blaCARB-2) against multiple antibiotic classes, with some of them contributed by plasmids and/or class-1 integrons. We observed different AMR genotypes for betalactams and tetracycline resistance, providing evidence of convergent evolution and adaptive AMR. The probability of MDR genotype occurrence was higher in meat-associated isolates than in those from other sources (odds ratio 11.2, 95% confidence interval 4.5–27.9, P < 0.0001). The study shows that beef cattle are a significant source of MDR NTS in Mexico, highlighting the role of animal production on the emergence and spread of MDR Salmonella in LMIC.

Keywords

antimicrobial resistance Salmonella genomics beef production 

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Supplementary material

12275_2019_8421_MOESM1_ESM.pdf (1.9 mb)
Supplementary material, approximately 1.94 MB.
12275_2019_8421_MOESM2_ESM.xlsx (13 kb)
Supplementary material, approximately 12.5 KB.
12275_2019_8421_MOESM3_ESM.xlsx (96 kb)
Supplementary data Table S2. Database of isolates from Mexico with AMR genotypes that were publicly available at NCBI as of July 24 2018
12275_2019_8421_MOESM4_ESM.xlsx (20 kb)
Supplementary data Table S3. Summary of genome assembly and annotation results

References

  1. An, R., Alshalchi, S., Breimhurst, P., Munoz-Aguayo, J., Flores-Figueroa, C., and Vidovic, S. 2017. Strong influence of livestock environments on the emergence and dissemination of distinct multidrug-resistant phenotypes among the population of non-typhoidal Salmonella. PLoS One 12, e0179005.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Antunes, P., Machado, J., and Peixe, L. 2006. Characterization of antimicrobial resistance and class 1 and 2 integrons in Salmonella enterica isolates from different sources in Portugal. J. Antimicrob. Chemother. 58, 297–304.CrossRefPubMedGoogle Scholar
  3. Baron, S., Hadjadj, L., Rolain, J.M., and Olaitan, A.O. 2016. Molecular mechanisms of polymyxin resistance: Knowns and unknowns. Int. J. Antimicrob. Agents 48, 583–591.CrossRefPubMedGoogle Scholar
  4. Bauer, A.W., Kirby, W.M., Sherris, J.C., and Turck, M. 1966. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 45, 493–496.CrossRefGoogle Scholar
  5. Brichta-Harhay, D.M., Arthur, T.M., Bosilevac, J.M., Kalchayanand, N., Shackelford, S.D., Wheeler, T.L., and Koohmaraie, M. 2011. Diversity of multidrug-resistant Salmonella enterica strains associated with cattle at harvest in the United States. Appl. Environ. Microbiol. 77, 1783–1796.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Carattoli, A., Zankari, E., García-Fernández, A., Larsen, M.V., Lund, O., Villa, L., Aarestrup, F.M., and Hasman, H. 2014. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58, 3895–3903.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552.CrossRefPubMedGoogle Scholar
  8. Chang, H.H., Cohen, T., Grad, Y.H., Hanage, W.P., O’Brien, T.F., and Lipsitch, M. 2015. Origin and proliferation of multiple-drug resistance in bacterial pathogens. Microbiol. Mol. Biol. Rev. 79, 101–116.CrossRefPubMedPubMedCentralGoogle Scholar
  9. CLSI. 2012. Clinical and laboratory standards institute. Performance standards for antimicrobial disk susceptibility tests; Approved standard-Eleventh edition. CLSI document M02-A11. CLSI, Wayne, PA, USA.Google Scholar
  10. Delgado-Suárez, E.J., Selem-Mojica, N., Ortiz-Lopez, R., Gebreyes, W.A., Allard, M.W., Barona-Gomez, F., and Rubio-Lozano, M.S. 2018. Whole genome sequencing reveals widespread distribution of typhoidal toxin genes and VirB/D4 plasmids in bovineassociated nontyphoidal Salmonella. Sci. Rep. 8, 9864.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dhanani, A.S., Block, G., Dewar, K., Forgetta, V., Topp, E., Beiko, R.G., and Diarra, M.S. 2015. Genomic comparison of non-typhoidal Salmonella enterica serovars Typhimurium, Enteritidis, Heidelberg, Hadar and Kentucky isolates from broiler chickens. PLoS One 10, e0128773.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Edgar, R. and Bibi, E. 1997. MdfA, an Escherichia coli multidrug resistance protein with an extraordinarily broad spectrum of drug recognition. J. Bacteriol. 179, 2274–2280.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gouy, M., Guindon, S., and Gascuel, O. 2010. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27, 221–224.CrossRefPubMedGoogle Scholar
  14. Hoffmann, S., Batz, M.B., and Morris, J.G.Jr. 2012. Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens. J. Food Prot. 75, 1292–1302.CrossRefPubMedGoogle Scholar
  15. Jia, B., Raphenya, A.R., Alcock, B., Waglechner, N., Guo, P., Tsang, K.K., Lago, B.A., Dave, B.M., Pereira, S., Sharma, A.N., et al. 2017. CARD 2017: Expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 45, D566–D573.CrossRefPubMedGoogle Scholar
  16. Junod, T., López-Martín, J., and Gädicke, P. 2013. Antimicrobial susceptibility of animal and food isolates of Salmonella enterica. Rev. Med. Chile 141, 298–304.CrossRefPubMedGoogle Scholar
  17. Kalambhe, D.G., Zade, N.N., Chaudhari, S.P., Shinde, S.V., Khan, W., and Patil, A.R. 2016. Isolation, antibiogram and pathogenicity of Salmonella spp. recovered from slaughtered food animals in Nagpur region of Central India. Vet. World 9, 176–181.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Karczmarczyk, M., Martins, M., McCusker, M., Mattar, S., Amaral, L., Leonard, N., Aarestrup, F.M., and Fanning, S. 2010. Characterization of antimicrobial resistance in Salmonella enterica food and animal isolates from Colombia: identification of a qnrB19- mediated quinolone resistance marker in two novel serovars. FEMS Microbiol. Lett. 313, 10–19.CrossRefPubMedGoogle Scholar
  19. Lin, D., Chen, K., Wai-Chi Chan, E., and Chen, S. 2015. Increasing prevalence of ciprofloxacin-resistant food-borne Salmonella strains harboring multiple PMQR elements but not target gene mutations. Sci. Rep. 5, 14754.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Lujan, S.A., Guogas, L.M., Ragonese, H., Matson, S.W., and Redinbo, M.R. 2007. Disrupting antibiotic resistance propagation by inhibiting the conjugative DNA relaxase. Proc. Natl. Acad. Sci. USA 104, 12282–12287.CrossRefPubMedGoogle Scholar
  21. McEwen, S.A. and Fedorka-Cray, P.J. 2002. Antimicrobial use and resistance in animals. Clin. Infect. Dis. 34 (Suppl 3), S93–S106.CrossRefPubMedGoogle Scholar
  22. Meng, H., Zhang, Z., Chen, M., Su, Y., Li, L., Miyoshi, S., Yan, H., and Shi, L. 2011. Characterization and horizontal transfer of class 1 integrons in Salmonella strains isolated from food products of animal origin. Int. J. Food Microbiol. 149, 274–277.CrossRefPubMedGoogle Scholar
  23. Mir, R.A., Weppelmann, T.A., Johnson, J.A., Archer, D., Morris, J.G.Jr., and Jeong, K.C. 2016. Identification and characterization of cefotaxime resistant bacteria in beef cattle. PLoS One 11, e0163279.CrossRefPubMedPubMedCentralGoogle Scholar
  24. OECD. 2016. Antimicrobial resistance. Policy insights. Available online: https://doi.org/www.oecd.org/health/health-systems/AMR-Policy-Insights-November2016.pdf (accessed on 5 October 2018).
  25. Perez-Montaño, J.A., González-Aguilar, D., Barba, J., Pacheco-Gallardo, C., Campos-Bravo, C.A., García, S., Heredia, N.L., and Cabrera-Díaz, E. 2012. Frequency and antimicrobial resistance of Salmonella serotypes on beef carcasses at small abattoirs in Jalisco State, Mexico. J. Food Prot. 75, 867–873.CrossRefPubMedGoogle Scholar
  26. Poole, K. 2012. Bacterial stress responses as determinants of antimicrobial resistance. J. Antimicrob. Chemother. 67, 2069–2089.CrossRefPubMedGoogle Scholar
  27. Qiu, H., Gong, J., Butaye, P., Lu, G., Huang, K., Zhu, G., Zhang, J., Hathcock, T., Cheng, D., and Wang, C. 2018. CRISPR/Cas9/ sgRNA-mediated targeted gene modification confirms the causeeffect relationship between gyrA mutation and quinolone resistance in Escherichia coli. FEMS Microbiol. Lett. 365, fny127.CrossRefGoogle Scholar
  28. Quesada, A., Porrero, M.C., Tellez, S., Palomo, G., Garcia, M., and Dominguez, L. 2015. Polymorphism of genes encoding PmrAB in colistin-resistant strains of Escherichia coli and Salmonella enterica isolated from poultry and swine. J. Antimicrob. Chemother. 70, 71–74.CrossRefPubMedGoogle Scholar
  29. Quesada, A., Reginatto, G.A., Ruiz Español, A., Colantonio, L.D., and Burrone, M.S. 2016. Antimicrobial resistance of Salmonella spp. isolated animal food for human consumption. Rev. Perú. Med. Exp. Salud Pública 33, 32.CrossRefPubMedGoogle Scholar
  30. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A., and Huelsenbeck, J.P. 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542.CrossRefPubMedPubMedCentralGoogle Scholar
  31. SAGARPA. 2018. Productos químico-farmacéuticos vigentes 2017. Available online: https://doi.org/www.gob.mx/senasica/acciones-y-programas/regulacion-de-productos-veterinarios (accessed on 5 October 2018).
  32. Schmidt, J.W., Agga, G.E., Bosilevac, J.M., Brichta-Harhay, D.M., Shackelford, S.D., Wang, R., Wheeler, T.L., and Arthur, T.M. 2015. Occurrence of antimicrobial-resistant Escherichia coli and Salmonella enterica in the beef cattle production and processing continuum. Appl. Environ. Microbiol. 81, 713–725.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Sibhat, B., Molla Zewde, B., Zerihun, A., Muckle, A., Cole, L., Boerlin, P., Wilkie, E., Perets, A., Mistry, K., and Gebreyes, W.A. 2011. Salmonella serovars and antimicrobial resistance profiles in beef cattle, slaughterhouse personnel and slaughterhouse environment in Ethiopia. Zoonoses Public Health 58, 102–109.CrossRefPubMedGoogle Scholar
  34. Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Soding, J., et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega. Mol. Syst. Biol. 7, 539.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Strahilevitz, J., Jacoby, G.A., Hooper, D.C., and Robicsek, A. 2009. Plasmid-mediated quinolone resistance: A multifaceted threat. Clin. Microbiol. Rev. 22, 664–689.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Swick, M.C., Morgan-Linnell, S.K., Carlson, K.M., and Zechiedrich, L. 2011. Expression of multidrug efflux pump genes acrAB-tolC, mdfA, and norE in Escherichia coli clinical isolates as a function of fluoroquinolone and multidrug resistance. Antimicrob. Agents Chemother. 55, 921–924.CrossRefPubMedGoogle Scholar
  37. Talbot, E.A., Gagnon, E.R., and Greenblatt, J. 2006. Common ground for the control of multidrug-resistant Salmonella in ground beef. Clin. Infect. Dis. 42, 1455–1462.CrossRefPubMedGoogle Scholar
  38. Van, T.T., Nguyen, H.N., Smooker, P.M., and Coloe, P.J. 2012. The antibiotic resistance characteristics of non-typhoidal Salmonella enterica isolated from food-producing animals, retail meat and humans in South East Asia. Int. J. Food Microbiol. 154, 98–106.CrossRefPubMedGoogle Scholar
  39. Varela-Guerrero, J.A., Talavera-Rojas, M., Gutierrez-Castillo Adel, C., Reyes-Rodriguez, N.E., and Vazquez-Guadarrama, J. 2013. Phenotypic-genotypic resistance in Salmonella spp. isolated from cattle carcasses from the north central zone of the State of Mexico. Trop. Anim. Health Prod. 45, 995–1000.CrossRefPubMedGoogle Scholar
  40. WHO. 2015. WHO estimates of the global burden of foodborne diseases. Foodborne disease burden epidemiology reference group 2007–2015. Available online: https://doi.org/www.who.int/foodsafety/areas_work/foodborne-diseases/ferg/en/ (accessed on 5 October 2018).
  41. WHO. 2017. WHO list of critically important antimicrobials for human medicine 5th revision. Available online: https://doi.org/who.int/foodsafety/publications/antimicrobials-fifth/en/ (accessed on 5 October 2018).
  42. Williams, J.J. and Hergenrother, P.J. 2008. Exposing plasmids as the Achilles’ heel of drug-resistant bacteria. Curr. Opin. Chem. Biol. 12, 389–399.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Zankari, E., Allesoe, R., Joensen, K.G., Cavaco, L.M., Lund, O., and Aarestrup, F.M. 2017. PointFinder: a novel web tool for WGSbased detection of antimicrobial resistance associated with chromosomal point mutations in bacterial pathogens. J. Antimicrob. Chemother. 72, 2764–2768.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Zankari, E., Hasman, H., Cosentino, S., Vestergaard, M., Rasmussen, S., Lund, O., Aarestrup, F.M., and Larsen, M.V. 2012. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 2640–2644.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Zhang, S., Yin, Y., Jones, M.B., Zhang, Z., Deatherage Kaiser, B.L., Dinsmore, B.A., Fitzgerald, C., Fields, P.I., and Deng, X. 2015. Salmonella serotype determination utilizing high-throughput genome sequencing data. J. Clin. Microbiol. 53, 1685–1692.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Microbiological Society of Korea 2019

Authors and Affiliations

  • Enrique Jesús Delgado-Suárez
    • 1
    Email author
  • Rocío Ortíz-López
    • 2
  • Wondwossen A. Gebreyes
    • 3
  • Marc W. Allard
    • 4
  • Francisco Barona-Gómez
    • 5
  • María Salud Rubio-Lozano
    • 1
  1. 1.Facultad de Medicina Veterinaria y ZootecniaUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  2. 2.Tecnológico de Monterrey, School of Medicine and Health SciencesMonterreyMexico
  3. 3.College of Veterinary MedicineThe Ohio State UniversityColumbusUSA
  4. 4.Office of Regulatory Science, Center for Food Safety and Applied NutritionU. S. Food and Drug AdministrationCollege ParkUSA
  5. 5.Evolution of Metabolic Diversity LaboratoryUnidad de Genómica Avanzada (Langebio), Cinvestav-IPNIrapuato, GuanajuatoMexico

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