Microbial Ecology

, Volume 61, Issue 4, pp 811–820 | Cite as

Geographical and Temporal Dissemination of Salmonellae Isolated from Domestic Animal Hosts in the Culiacan Valley, Mexico

  • Maribel Jiménez
  • Jaime Martínez-Urtaza
  • Cristobal ChaidezEmail author
Environmental Microbiology


The prevalence and diversity of salmonellae from domestic animal hosts were investigated in the Culiacan Valley, Mexico. A total of 240 farm animal feces (cows, chicken, and sheep) were evaluated for Salmonella spp. presence from July 2008 to June 2009. Salmonella enterica subsp. enterica strains were isolated from 76 samples (31.7%), and 20 serotypes were identified being Salmonella Oranienburg (25%), Salmonella Give (14%), Salmonella Saintpaul (12%), and Salmonella Minnesota (11%) the most frequent isolates. Twenty-four percent (18/76) of the isolates were resistant to ampicillin. Salmonella Oranienburg, Salmonella Minnesota, Salmonella Give, Salmonella Agona, Salmonella Weltevreden, and Salmonella Newport serotypes showed multiple pulsed-field electrophoresis patterns. Salmonella Oranienburg was the dominant serotype in the Culiacan Valley; however, no specific distribution patterns were detected in animal sources or sampling sites. The genetic diversity of salmonellae could be an evidence of the continuous animal exposition to the bacteria. Also, Salmonella adaptation in asymptomatic animals could be justified by the development of natural host immunity. This study provides novel information about Salmonella population distribution in domestic animals living at tropical areas. The presence of asymptomatic carriers may be critical to understand the routes of transmission of Salmonella in areas of high disease prevalence.


PFGE Type Animal Feces Prevalent Serotype Microbial Source Tracking Sheep Feces 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors thank Marisol Castañeda, Célida Martínez, and Ariel Ramírez from CIAD Culiacan for sample recovery and Salmonella isolation. Also, we thank Silvia Carles, Estela Nuñez, Isa Mayán, and Sandra Fernandez from USC for technical assistance in Salmonella characterization.


  1. 1.
    Aksakal A, Boynukara B, Solmaz H, Ilhan Z, Kutlu I, Gulhan T (2009) Occurrence and antibiotic susceptibility of Salmonella serotypes in apparently healthy slaughtered sheep in Van, Turkey. J Anim Vet Adv 8:1455–1460Google Scholar
  2. 2.
    Alaniz-de la O R, Ríos-Ibarra ML, Rosas-Barbosa BT, Juan-Morales AL (1997) Resistencia a antimicrobianos de cepas de Salmonella aisladas de fuentes animales. Vet Méx 28:215–220Google Scholar
  3. 3.
    Alemayehu D, Molla B, Muckle A (2003) Prevalence and antimicrobial resistance pattern of Salmonella isolates from apparently healthy slaughtered cattle in Ethiopia. Trop Anim Health Prod 35:309–319PubMedCrossRefGoogle Scholar
  4. 4.
    Andrews JM (2007) BSAC standardized disc susceptibility testing method (version 6). J Antimicrob Chemother 60:20–41PubMedCrossRefGoogle Scholar
  5. 5.
    Archambault M, Petrov P, Hendriksen RS, Asseva G, Bangtrakulnonth A, Hasman H, Aarestrup FM (2006) Molecular characterization and occurrence of extended-spectrum beta-lactamase resistance genes among Salmonella enterica serovar Corvallis from Thailand, Bulgaria, and Denmark. Microb Drug Resist 12:192–198PubMedCrossRefGoogle Scholar
  6. 6.
    Benavides-Plascencia L, Aldama-Ojeda AL, Vázquez HJ (2005) Vigilancia de los niveles de uso de antibióticos y perfiles de resistencia bacteriana en hospitales de tercer nivel de la Ciudad de México. Salud Pública Méx 47:219–226PubMedCrossRefGoogle Scholar
  7. 7.
    Berrang ME, Bailey JS, Altekruse SF, Shaw WK, Patel BL, Meinersmann RJ, Fedorka-Cray PJ (2009) Prevalence, serotype, and antimicrobial resistance of Salmonella on broiler carcasses postpick and postchill in 20 U.S. processing plants. J Food Prot 72:1610–1615PubMedGoogle Scholar
  8. 8.
    Boerling, Reid-Smith RJ (2008) Antimicrobial resistance: its emergence and transmission. Anim Health Res Rev 9:115–126CrossRefGoogle Scholar
  9. 9.
    Centers for Disease Control and Prevention (CDC) (2002) Standardized molecular subtyping of foodborne bacterial pathogens by pulsed-field gel electrophoresis. Centers for Diseases Control and Prevention, AtlantaGoogle Scholar
  10. 10.
    Chávez-de la Peña ME, Higuera-Iglesias AL, Huertas-Jiménez MA, Báez-Martínez R, Morales-de León J, Arteaga-Cabello F, Rangel-Frausto MS, Ponce S (2001) Brote por Salmonella Enteritidis en trabajadores de un hospital. Salud Púbica Méx 43:211–216CrossRefGoogle Scholar
  11. 11.
    Clinical and Laboratory Standards Institute (CLSI) (2008) Performance standards for antimicrobial disk and diffusion susceptibility testing for bacteria isolated from animals; approved standard. 3rd edn. Document M31-A3. CLSI, WayneGoogle Scholar
  12. 12.
    Commission for Environmental Cooperation (CEC) (2003) Comparative standards for intensive livestock operations in Canada, Mexico, and the United States. Available at
  13. 13.
    Cox JM, Pavic A (2010) Advances in enteropathogen control in poultry production. J Appl Microbiol 108:745–755PubMedCrossRefGoogle Scholar
  14. 14.
    Dargatz DA, Fedorka-Cray PJ, Ladely SR, Kopral CA, Ferris KE, Headrick ML (2003) Prevalence and antimicrobial susceptibility of Salmonella spp. isolates from US cattle in feedlots in 1999 and 2000. J Appl Microbiol 95:753–761PubMedCrossRefGoogle Scholar
  15. 15.
    Dirección General de Epidemiología (DGEPI) (2009) Casos por enfermedades infecciosas y parasitarias del aparato digestivo. Vigilancia epidemiológica semana 52, 2009. Available at
  16. 16.
    Dorr PM, Tadesse DA, Zewde BM, Fry P, Thakur S, Gebreyes WA (2009) Longitudinal study of Salmonella dispersion and the role of environmental contamination in commercial swine production systems. Appl Environ Microbiol 75:1478–1486PubMedCrossRefGoogle Scholar
  17. 17.
    Dreser A, Wirtz VJ, Corbett KK, Echániz G (2008) Uso de antibióticos en México: revisión de problemas y políticas. Salud Púb Méx 50:S480–S487CrossRefGoogle Scholar
  18. 18.
    European Centre for Disease Prevention and Control (ECDC) (2008) Food- and Waterborne Diseases and Zoonoses Surveillance Network Quarterly Salmonella Report Q1 2008, January–March 2008. Available at
  19. 19.
    Esaki H, Morioka A, Ishihara K, Kojima A, Shiroki S, Tamura Y, Takahashi T (2004) Antimicrobial susceptibility of Salmonella isolated from cattle, swine and poultry (2001–2002): report from the Japanese Veterinary Antimicrobial Resistance Monitoring Program. J Antimicrob Chemother 53:266–270PubMedCrossRefGoogle Scholar
  20. 20.
    Fluckey WM, Loneragan WG, Warner R, Brashears MM (2007) Antimicrobial drug resistance of Salmonella and Escherichia coli isolates from cattle feces, hides, and carcasses. J Food Prot 70:551–556PubMedGoogle Scholar
  21. 21.
    Foley SL, Lynne AM, Nayak R (2008) Salmonella challenges: prevalence in swine and poultry and potential pathogenicity of such isolates. J Anim Sci 86:E149–E162PubMedCrossRefGoogle Scholar
  22. 22.
    Food and Agriculture Organization of the United Nations (FAOSTAT) (2007) The agricultural trade domain covers detailed food and agriculture exports and imports. Available at
  23. 23.
    Galanis E, Lo Fo Wong DM, Patrick ME, Binsztein N, Cieslik A, Chalermchikit T, Aidara-Kane A, Ellis A, Angulo FJ, Wegener HC (2006) Web-based surveillance and global Salmonella distribution, 2000–2002. Emerg Infect Dis 12:381–388PubMedCrossRefGoogle Scholar
  24. 24.
    Global Foodborne Infections Network Country Databank (GFN) (2010) Available at,1&_dad=portal&_schema=PORTAL
  25. 25.
    Gutiérrez-Cogco L, Montiel VE, Aguilera PP, González AM (2000) Serotipos de Salmonella identificados en los servicios de salud de México. Salud Pública Méx 42:490–495PubMedCrossRefGoogle Scholar
  26. 26.
    Gyles CL (2008) Antimicrobial resistance in selected bacteria from poultry. Anim Health Res Rev 9:149–158PubMedCrossRefGoogle Scholar
  27. 27.
    Keen JE, Durso LM, Meehan TP (2007) Isolation of Salmonella enterica and Shiga-toxigenic Escherichia coli O157 from feces of animals in public contact areas of United States zoological parks. Appl Environ Microbiol 73:362–365PubMedCrossRefGoogle Scholar
  28. 28.
    Lan R, Reeves PR, Octavia S (2009) Population structure, origins and evolution of major Salmonella enterica clones. Infect Genet Evol 9:996–1005PubMedCrossRefGoogle Scholar
  29. 29.
    López O, León J, Jiménez M, Chaidez C (2009) Detección y resistencia a antibióticos de Escherichia coli y Salmonella en agua y suelo agrícola. Rev Fitotecnia Mex 32:119–126Google Scholar
  30. 30.
    Malorny B, Hoorfar J, Bunge C, Helmuth R (2003) Multicenter validation of the analytical accuracy of Salmonella PCR: towards an international standard. Appl Environ Microbiol 69:290–296PubMedCrossRefGoogle Scholar
  31. 31.
    Morbidity and Mortality Weekly Report (MMWR) (2006) Surveillance for foodborne-disease outbreaks—United States, 1998–2002. Surveillance Summaries 55, 1–34. Available at
  32. 32.
    Morbidity and Mortality Weekly Report (MMWR) (2008) Preliminary FoodNet Data on the incidence of infection with pathogens transmitted commonly through food—10 states, 2007. Surveillance Summaries 57, 366–370. Available at
  33. 33.
    National Antimicrobial Resistance Monitoring System (NARMS) (2007) Retail meat annual report. Available at
  34. 34.
    Panamerican Health Organization (PAHO) (2006) Informe Anual de la Red de Monitoreo/Vigilancia de la Resistencia a los Antibióticos. Available at
  35. 35.
    Perron GG, Quessy S, Bell G (2008) A reservoir of drug-resistant pathogenic bacteria in asymptomatic hosts. PLoS ONE 3:e3749PubMedCrossRefGoogle Scholar
  36. 36.
    Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA) (2007) Guía de Plaguicidas Autorizados de Uso Agrícola. Comisión Nacional de Sanidad Agropecuaria, Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria. Available at
  37. 37.
    Setti I, Rodriguez-Castro A, Pata MP, Cadarso-Suarez C, Yacoubi B, Bensmael L, Moukrim A, Martinez-Urtaza J (2009) Characteristics and dynamics of Salmonella contamination along the coast of Agadir, Morocco. Appl Environ Microbiol 75:7700–7709PubMedCrossRefGoogle Scholar
  38. 38.
    Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernard S, Casadesús J, Platt DJ, Olsen JE (2000) Host adapted serotypes of Salmonella enterica. Epidemiol Infect 125:229–255PubMedCrossRefGoogle Scholar
  39. 39.
    White DG, Zhao S, Singh R, McDermott PF (2004) Antimicrobial resistance among gram-negative foodborne bacterial pathogens associated with foods of animal origin. Foodborne Pathog Dis 1(3):137–152PubMedGoogle Scholar
  40. 40.
    Winfield MD, Groisman EA (2003) Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl Environ Microbiol 69:3687–3694PubMedCrossRefGoogle Scholar
  41. 41.
    World Health Organization (WHO) (2006) Global Salm-Surv strategic planning meeting 2006–2010: report of a WHO meeting. Winnipeg, Canada, 14–15 Sep 2005. Available at
  42. 42.
    Zaidi MB, Calva JJ, Estrada-Garcia MT, Leon V, Vazquez G, Figueroa G, Lopez E, Contreras J, Abbott J, Zhao S, McDermott P, Tollefson L (2008) Integrated food chain surveillance system for Salmonella spp. in Mexico. Emerg Infect Dis 14:429–435PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Maribel Jiménez
    • 1
  • Jaime Martínez-Urtaza
    • 2
  • Cristobal Chaidez
    • 1
    • 3
    Email author
  1. 1.Centro de Investigación en Alimentación y Desarrollo ACCuliacanMexico
  2. 2.Instituto de AcuiculturaUniversidad de Santiago de CompostelaSantiago de CompostelaSpain
  3. 3.Food and Environmental Microbiology Lab. CIADCuliacanMexico

Personalised recommendations