Antibiotic resistance in Salmonella enterica isolated from dairy calves in Uruguay

  • M. L. Casaux
  • R. D. Caffarena
  • C. O. Schild
  • F. Giannitti
  • Franklin Riet-Correa
  • Martín FragaEmail author
Veterinary Microbiology - Short Communication


Salmonella enterica is an important animal and human pathogen that can cause enteritis and septicaemia in calves. Generally, antibiotics are prescribed for the treatment of salmonellosis in dairy calves. Here, we report the isolation of antibiotic resistant S. enterica serotypes from calves, including multidrug-resistant isolates. A total of 544 faecal samples from live healthy and diarrheic dairy calves from 29 commercial dairy farms and organ samples from 19 deceased calves that succumbed to salmonellosis in 12 commercial dairy farms in Uruguay were processed for selective S. enterica culture. In total, 41 isolates were serotyped, and susceptibility to 14 antibiotics, from 9 classes of compounds, was evaluated by disk-diffusion test. The minimum inhibitory concentration (MIC) was determined by microdilution. Salmonella Typhimurium was the most frequent serotype, followed by S. Dublin and S. Anatum. Whether determined by diffusion assay or microdilution, resistance to tetracycline, streptomycin and ampicillin were the most frequently pattern found. Based on MIC, 5 isolates were resistant to at least one antibiotic, 21 were resistant to 2 antibiotics, and 14 were multidrug-resistant (resistant to at least one antibiotic in 3 different categories of antibiotics). Eleven different resistance patterns were found. Multidrug resistance in S. enterica is a concern for animal and public health not only because of its zoonotic potential but also due to the possibility of transfer resistance determinants to other bacterial genera. This represents the first report of the antibiotic resistance in S. enterica in dairy farms in Uruguay.


Salmonella Typhimurium Salmonella Dublin Salmonella Anatum Antibiotic resistance Dairy calves 



The authors thank Cecilia Monesiglio from INIA for technical assistance with microbiological routine, and Laura Betancor and Arací Martínez from the “Instituto de Higiene, Facultad de Medicina, UdelaR” for Salmonella serotyping.

Data availability statement

The datasets generated during and/or analysed during the current study are available from the corresponding author on request.

Funding information

This work was partially funded by INIA’s grant PL-15, and project FMV-104922 from the Uruguayan “Agencia Nacional de Investigación e Innovación” (ANII). M.L. Casaux received master’s scholarships from ANII (POS_NAC_2016_1_130296).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

42770_2019_151_MOESM1_ESM.docx (18 kb)
Table S1 (DOCX 18 kb)


  1. 1.
    Grimont PAD, Weill FX (2007) Antigenic formulae of the Salmonella serovars. WHO Collaborating Centre for Reference and Research on Salmonella, 9th edition. Institut Pasteur, ParisGoogle Scholar
  2. 2.
    Cho Y, Yoon KJ (2014) An overview of calf diarrhea-infectious etiology, diagnosis, and intervention. J Vet Med Sci 15:1–17Google Scholar
  3. 3.
    Uzal FA, Plattner BL, Hostetter JM (2016) Chapter 1 - Alimentary System. In: Grant Maxie M (ed) Jubb, Kennedy & Palmer’s pathology of domestic animals: Volume 2, 6th edn. Elsevier, St Louis, pp 1–257Google Scholar
  4. 4.
    Carrique-Mas JJ, Willmington JA, Papadopoulou C, Watson EN, Davies RH (2008) Salmonella infection in cattle in Great Britain, 2003 to 2008. Vet Rec 67:560–565Google Scholar
  5. 5.
    Costa LF, Paixão TA, Tsolis RM, Bäumler AJ, Santos RL (2012) Salmonellosis in cattle: advantages of being an experimental model. Res Vet Sci 93:1–6CrossRefGoogle Scholar
  6. 6.
    Constable PD (2004) Antimicrobial use in the treatment of calf diarrhea. J Vet Intern Med 18:8–17CrossRefGoogle Scholar
  7. 7.
    Mohler VL, Izzo MM, House JK (2009) Salmonella in calves. Vet Clin North Am Food Anim Pract 25:37–54CrossRefGoogle Scholar
  8. 8.
    Pribul BR, Festivo ML, Rodrigues MS, Costa RG, Rodrigues EC, de Souza MM, Rodrigues DD (2017) Characteristics of quinolone resistance in Salmonella spp. isolates from the food chain in Brazil. Front Microbiol 8:299CrossRefGoogle Scholar
  9. 9.
    Tang KL, Caffrey NP, Nóbrega DB, Cork SC, Ronksley PE, Barkema HW, Polachek AJ, Ganshorn H, Sharma N, Kellner JD, Ghali WA (2017) Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis. Lancet Planet Health 1:e316–e327CrossRefGoogle Scholar
  10. 10.
    World Health Organization (2017) WHO guidelines on use of medically important antimicrobials in food-producing animals: policy brief. Accessed 14 Jan 2019
  11. 11.
    Eguale T, Engidawork E, Gebreyes WA, Asrat D, Alemayehu H, Medhin G, Johnson RP, Gunn JS (2016) Fecal prevalence, serotype distribution and antimicrobial resistance of Salmonellae in dairy cattle in central Ethiopia. BMC Microbiol 16:1–11CrossRefGoogle Scholar
  12. 12.
    McGuirk SM (2008) Disease management of dairy calves and heifers. Vet Clin North Am Food Anim Pract 24:139–153CrossRefGoogle Scholar
  13. 13.
    Cramer MC, Stanton AL (2015) Associations between health status and the probability of approaching a novel object or stationary human in preweaned group-housed dairy calves. J Dairy Sci 98:7298–7308CrossRefGoogle Scholar
  14. 14.
    Octavia S, Lan R (2014) The Family Enterobacteriaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: Gammaproteobacteria. Springer, Berlin, pp 225–286Google Scholar
  15. 15.
    Clinical and Laboratory Standards Institute (2018) Performance standards for antimicrobial susceptibility testing; 25th informational supplement, M100-S28. Wayne, PA, USAGoogle Scholar
  16. 16.
    Clinical and Laboratory Standards Institute (2015) Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. VET01S. Wayne, PA, USAGoogle Scholar
  17. 17.
    The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 9.0, 2019.
  18. 18.
    NARMS. The National Antimicrobial Resistance Monitoring System: enteric Bacteria. In: NARMS Integrated Report: 2012–2013: National Antimicrobial Resistance Monitoring System; 201Google Scholar
  19. 19.
    Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18:268–281CrossRefGoogle Scholar
  20. 20.
    Hammer Ø, Harper DA, Ryan DD (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol Electron 178kb T Harper Geol Museum 4:5–7Google Scholar
  21. 21.
    Davidson KE, Byrne BA, Pires AFA, Magdesian KG, Pereira RV (2018) Antimicrobial resistance trends in fecal Salmonella isolates from northern California dairy cattle admitted to a veterinary teaching hospital, 2002-2016. PLoS One 13:1–18CrossRefGoogle Scholar
  22. 22.
    Bilbao GN, Malena R, Passucci JA, Pinto de Almeida Castro AM, Paolicchi F, Soto P, Cantón J, Monteavaro CE (2019) Detección de serovares de Salmonella en terneros de crianza artificial de la región lechera Mar y Sierras, Argentina. Rev Argent Microbiol. CrossRefGoogle Scholar
  23. 23.
    Izzo M, Mohler V, House JK (2011) Antimicrobial susceptibility of Salmonella isolates recovered from calves with diarrhoea in Australia. Aust Vet J 89:402–408CrossRefGoogle Scholar
  24. 24.
    Centers for Disease Control and Prevention (2017) Salmonella Anatum Infections Linked to Maradol Papayas. Accessed 14 Jan 2019
  25. 25.
    Nielsen LR (2013) Review of pathogenesis and diagnostic methods of immediate relevance for epidemiology and control of Salmonella Dublin in cattle. Vet Microbiol 162:1–9CrossRefGoogle Scholar
  26. 26.
    Constable PD, Hinchcliff KW, Stanley H, Done SH, Grünberg W (2017) Veterinary medicine: a textbook of the diseases of cattle, horses, sheep, pigs, and goat. 11th ed. Elsevier, St Louis, pp 357–373Google Scholar
  27. 27.
    Costa RA, Casaux ML, Caffarena RD, Macías-Rioseco M, Schild CO, Fraga M, Riet-Correa F, Giannitti F (2018) Urocystitis and ureteritis in Holstein calves with septicaemia caused by Salmonella enterica serotype Dublin. J Comp Pathol 164:32–36CrossRefGoogle Scholar
  28. 28.
    Pezzella C, Ricci A, DiGiannatale E, Luzzi I, Carattoli A (2004) Tetracycline and streptomycin resistance genes, transposons, and plasmids in Salmonella enterica isolates from animals in Italy. Antimicrob Agents Chemother 48:903–908CrossRefGoogle Scholar
  29. 29.
    Yang SJ, Park KY, Kim SH, No KM, Besser TE, Yoo HS, Kim SH, Lee BK, Park YH (2002) Antimicrobial resistance in Salmonella enterica serovars Enteritidis and Typhimurium isolated from animals in Korea: comparison of phenotypic and genotypic resistance characterization. Vet Microbiol 86:295–301CrossRefGoogle Scholar
  30. 30.
    Hong S, Rovira A, Davies P, Ahlstrom C, Muellner P, Rendahl A, Olsen K, Bender JB, Wells S, Perez A, Alvarez J (2016) Serotypes and antimicrobial resistance in salmonella enterica recovered from clinical samples from cattle and swine in Minnesota, 2006 to 2015. PLoS One 11:1–20Google Scholar
  31. 31.
    Cantón R, Ruiz-Garbajosa P (2011) Co-resistance: an opportunity for the bacteria and resistance genes. Curr Opin Pharmacol 11:477–485CrossRefGoogle Scholar
  32. 32.
    World Health Organization; Food and agriculture organization of the United Nations; world organisation for animal health (2016) antimicrobial resistance a manual for developing national action plans (Ver.1). doi:, 1998
  33. 33.
    Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17:7–15CrossRefGoogle Scholar
  34. 34.
    Da Costa PM, Loureiro L, Matos AJF (2013) Transfer of multidrug-resistant bacteria between intermingled ecological niches: the interface between humans, animals and the environment. Int J Environ Res Public Health 10:278–294CrossRefGoogle Scholar
  35. 35.
    Cordeiro NF, Yim L, Betancor L, Cejas D, García-Fulgueiras V, Mota MI, Varela G, Anzalone L, Algorta G, Gutkind G, Ayala JA, Chabalgoity JA, Vignoli R (2013) Identification of the first blaCMY-2 gene in Salmonella enterica serovar Typhimurium isolates obtained from cases of paediatric diarrhoea illness detected in South America. J Glob Antimicrob Resist 1:143–148CrossRefGoogle Scholar
  36. 36.
    Cordeiro NF, Nabón A, García-Fulgueiras V, Álvez M, Sirok A, Camou T, Vignoli R (2016) Analysis of plasmid-mediated quinolone and oxyimino-cephalosporin resistance mechanisms in Uruguayan Salmonella enterica isolates from 2011–2013. J Glob Antimicrob Resist 6:165–171CrossRefGoogle Scholar
  37. 37.
    Sasías S, Martínez-Sanguiné A, Betancor L, Martínez A, D'Alessandro B, Iriarte A, Chabalgoity JA, Yim L (2018) A naturally occurring deletion in FliE from Salmonella enterica serovar Dublin results in an aflagellate phenotype and defective proinflammatory properties. Infect Immun 86:1–20Google Scholar

Copyright information

© Sociedade Brasileira de Microbiologia 2019

Authors and Affiliations

  1. 1.Instituto Nacional de Investigación Agropecuaria (INIA), Plataforma de Investigación en Salud AnimalEstación Experimental INIA La EstanzuelaColoniaUruguay
  2. 2.Facultad de VeterinariaUniversidad de la RepúblicaMontevideoUruguay

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