Effect of Cattle on Salmonella Carriage, Diversity and Antimicrobial Resistance in Free-Ranging Wild Boar (Sus scrofa) in Northeastern Spain

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Navarro Gonzalez, Nora ^a   Mentaberre, Gregorio ^a   Porrero, Concepción M ^b   Serrano, Emmanuel ^a,c   Mateos, Ana ^b   López Martín, José M ^a,d   Lavín, Santiago ^a   Domínguez, Lucas ^b  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c UNIVERSITY OF LLEIDA   (Spain)

^d Generalitat de Catalunya ^*  (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; AMOXICILLIN PLUS CLAVULANIC ACID; AMPICILLIN; CEFOTAXIME; CEFOXITIN; CEFTAZIDIME; CHLORAMPHENICOL; CIPROFLOXACIN; FLORFENICOL; GENTAMICIN; IMIPENEM; KANAMYCIN; NALIDIXIC ACID; STREPTOMYCIN; SULFAMETHOXAZOLE;

AGE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; CATTLE; CONTROLLED STUDY; DISEASE CARRIER; HABITAT STRUCTURE; HERD; HOST PATHOGEN INTERACTION; LIVESTOCK; MICROBIAL DIVERSITY; NONHUMAN; SALMONELLA; SALMONELLA ENTERITIDIS; SALMONELLA MBANDAKA; SPAIN; SPECIES RICHNESS; WILD BOAR;

ANIMALS; ANTI-INFECTIVE AGENTS; BIODIVERSITY; CATTLE; DISEASE RESERVOIRS; DRUG RESISTANCE, MICROBIAL; FECES; FEMALE; MALE; SALMONELLA; SALMONELLA INFECTIONS, ANIMAL; SPAIN; SUS SCROFA; SWINE; SWINE DISEASES;

BOS; SALMONELLA; SALMONELLA ENTERITIDIS; SUS SCROFA;

EID: 84871325427     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051614     Document Type: Article

References (54)

1. Gortázar C, Ferroglio E, Höfle U, Frölich K, Vicente J, (2007) Diseases shared between wildlife and livestock: A european perspective. Eur J Wildl Res 53: 241-256.
2. Boehm M, White PCL, Chambers J, Smith L, Hutchings MR, (2007) Wild deer as a source of infection for livestock and humans in the UK. Vet J 174: 260-276.
3. Meng XJ, Lindsay DS, Sriranganathan N, (2009) Wild boars as sources for infectious diseases in livestock and humans. Philos Trans R Soc Lond B Biol Sci 364: 2697-2707.
4. Wacheck S, Fredriksson-Ahomaa M, Konig M, Stolle A, Stephan R, (2010) Wild boars as an important reservoir for foodborne pathogens. Foodborne Pathog Dis 7: 307-312.
5. Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, et al. (2000) Host adapted serotypes of Salmonella enterica. Epidemiol Infect 125: 229-255.
6. Murray CJ, (1991) Salmonellae in the environment. Rev Sci Tech 10: 765-785.
7. Davies RH, Breslin M, (2003) Persistence of Salmonella Enteritidis phage type 4 in the environment and arthropod vectors on an empty free-range chicken farm. Environ Microbiol 5: 79-84.
8. Garber L, Smeltzer M, Fedorka-Cray P, Ladely S, Ferris K, (2003) Salmonella enterica serotype Enteritidis in table egg layer house environments and in mice in US layer houses and associated risk factors. Avian Dis 47: 134-142.
9. Liebana E, Garcia-Migura L, Clouting C, Clifton-Hadley FA, Breslin M, et al. (2003) Molecular fingerprinting evidence of the contribution of wildlife vectors in the maintenance of Salmonella Enteritidis infection in layer farms. J Appl Microbiol 94: 1024-1029.
10. Glawischnig W, Khaschabi D, Schopf K, Schonbauer M, (2000) An outbreak of Salmonella Dublin in chamois (Rupicapra rupicapra). Wien Tierarztl Monatsschr 87: 21-25.
11. Hilbert F, Smulders FJM, Chopra-Dewasthaly R, Paulsen P, (2012) Salmonella in the wildlife-human interface. Food Res Int 45: 603-608.
12. Paulsen P, Smulders FJM, Hilbert F, (2012) Salmonella in meat from hunted game: A central European perspective. Food Res Int 45: 609-616.
13. Foley SL, Lynne AM, (2008) Food animal-associated Salmonella challenges: Pathogenicity and antimicrobial resistance. J Anim Sci 86: E173-E187.
14. Dolejska M, Cizek A, Literak I, (2007) High prevalence of antimicrobial-resistant genes and integrons in Escherichia coli isolates from black-headed gulls in the Czech Republic. J Appl Microbiol 103: 11-19.
15. Literak I, Dolejska M, Radimersky T, Klimes J, Friedman M, et al. (2010) Antimicrobial-resistant faecal Escherichia coli in wild mammals in central Europe: Multiresistant Escherichia coli producing extended-spectrum beta-lactamases in wild boars. J Appl Microbiol 108: 1702-1711.
16. Skurnik D, Ruimy R, Andremont A, Amorin C, Rouquet P, et al. (2006) Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J Antimicrob Chemother 57: 1215-1219.
17. Lankau EW, Bedon LC, Mackie RI, (2012) Salmonella strains isolated from Galapagos iguanas show spatial structuring of serovar and genomic diversity. Plos One 7: e37302.
18. Patton TG, Scupham AJ, Bearson SMD, Carlson SA, (2009) Characterization of fecal microbiota from a Salmonella endemic cattle herd as determined by oligonucleotide fingerprinting of rDNA genes. Vet Microbiol 136: 285-292.
19. Santos FBO, Sheldon BW, Santos AA Jr, Ferket PR, Lee MD, et al. (2007) Determination of ileum microbial diversity of broilers fed triticale- or corn-based diets and colonized by Salmonella. J Appl Poult Res 16: 563-573.
20. Perron GG, Quessy S, Letellier A, Bell G, (2007) Genotypic diversity and antimicrobial resistance in asymptomatic Salmonella enterica serotype Typhimurium DT104. Infect Genet Evol 7: 223-228.
21. Daszak P, Cunningham AA, Hyatt AD, (2000) Wildlife ecology- emerging infectious diseases of wildlife- threats to biodiversity and human health. Science 287: 443-449.
22. Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek J, Dobson AP (2002) Ecology of wildlife diseases. Oxford: Oxford University Press.
23. Winfield MD, Groisman EA, (2003) Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl Environ Microbiol 69: 3687-3694.
24. European Environment Agency (2007) CLC2006 technical guidelines. EEA Technical report No. 17/2007.
25. Boitani l, Mattei L, (1992) Aging wild boar (Sus scrofa) by tooth eruption. In: Spitz F, Janeau G, Gonzalez G, Aulagnier S, editors. Ongulés/Ungulates. Paris-Toulouse: S.F.E.P.M.-I.R.G. M: 419-421.
26. International Organization for Standardization (2007) Detection of Salmonella spp. in animal faeces and in environmental samples from the primary production stage. 6579: 2002.
27. Grimont PAD, Weill F, editors (2007) Antigenic formulas of the Salmonella serovars. Paris: WHO Collaborating Centre for Reference and Research on Salmonella, Insitut Pasteur.
28. Anderson ES, Ward LR, Saxe MJ, de Sa JD, (1977) Bacteriophage-typing designations of Salmonella Typhimurium. J Hyg 78: 297-300.
29. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extension in ecology with R. New York: Springer. 1-530 p.
30. Thulke H, Eisinger D, Freuling C, Froehlich A, Globig A, et al. (2009) Situation-based surveillance: Adapting investigations to actual epidemic situations. J Wildl Dis 45: 1089-1103.
31. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: A practical information-theoretic approach. New York: Springer-Verlag. 1-488 p.
32. Johnson DH, (2002) The role of hypothesis testing in wildlife science. J Wildl Manage 66: 272-276.
33. Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. New York, USA: Springer. 1-672 p.
34. Anderson DR, Burnham KP, Thomson WL, (2000) Null hypothesis testing: Problems, prevalence, and an alternative. J Wildl Manage 64: 912-923.
35. Anderson DR, Burnham KP, White GA, (2001) Kullback-Leibler information in resolving natural resource conflicts when definitive data exist. Wildlife Soc B 29: 1260-1270.
36. Hurlbert SH, (1971) Nonconcept of species diversity- critique and alternative parameters. Ecology 52: 577-586.
37. R Development Core Team 2.14.0 (2011) A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org. Accessed 3 October 2011.
38. Stevenson M, Nunes T, Sanchez J, Thornton R, Reiczigel J, et al. (2012) epiR: An R package for the analysis of epidemiological data. R package version 0.9-43.
39. Gotelli NJ, Entsminger GL. EcoSim 7.72. acquired intelligence, inc. http://www.uvm.edu/~ngotelli/EcoSim/EcoSim.html. Accessed 12 April 2012.
40. Mentaberre G, Porrero MC, Navarro-Gonzalez N, Serrano E, Domínguez L,et al. Cattle drive Salmonella infection in the wildlife-livestock interface. Zoonoses Public Hlth, In press.
41. EFSA (2012) The European union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks. EFSA Journal 10: 2597.
42. Navarro-Gonzalez N, Velarde R, Porrero MC, Mentaberre G, Serrano E,et al. Lack of evidence of spill-over of Salmonella enterica between cattle and sympatric Iberian ibex (Capra pyrenaica) from a protected area in Catalonia, NE spain. Transbound Emerg Dis, In press.
43. Vieira-Pinto M, Morais L, Caleja C, Themudo P, Torres C, et al. (2011) Salmonella sp in game (Sus scrofa and Oryctolagus cuniculus). Foodborne Pathog Dis 8: 739-740.
44. Millan J, Aduriz G, Moreno B, Juste RA, Barral M, (2004) Salmonella isolates from wild birds and mammals in the Basque country (Spain). Rev Sci Tech 23: 905-911.
45. Schley L, Roper TJ, (2003) Diet of wild boar Sus scrofa in Western Europe, with particular reference to consumption of agricultural crops. Mamm Rev 33: 43-56.
46. Fedorka-Cray P, Kelley L, Stabel T, Gray J, Laufer J, (1995) Alternate routes of invasion may affect pathogenesis of Salmonella Typhimurium in swine. Infect Immun 63: 2658-2664.
47. Skov MN, Madsen JJ, Rahbek C, Lodal J, Jespersen JB, et al. (2008) Transmission of Salmonella between wildlife and meat-production animals in Denmark. J Appl Microbiol 105: 1558-1568.
48. Carlson JC, Franklin AB, Hyatt DR, Pettit SE, Linz GM, (2011) The role of starlings in the spread of Salmonella within concentrated animal feeding operations. J Appl Ecol 48: 479-486.
49. Methner U, Heller M, Bocklisch H, (2010) Salmonella enterica subspecies enterica serovar Choleraesuis in a wild boar population in Germany. Eur J Wildl Res 56: 493-502.
50. Singer RS, Mayer AE, Hanson TE, Isaacson RE, (2009) Do microbial interactions and cultivation media decrease the accuracy of Salmonella surveillance systems and outbreak investigations? J Food Prot 72: 707-713.
51. Gorski L, (2012) Selective enrichment media bias the types of Salmonella enterica strains isolated from mixed strain cultures and complex enrichment broths. PloS One 7: e34722.
52. EFSA (2010) The community summary report on antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European union in 2008. EFSA Journal 8: 1658.
53. VAV (2005) Red de vigilancia veterinaria de resistencias a antibióticos. Number 12. http://www.vigilanciasanitaria.es/vav/. Accessed 2012 July 18.
54. Caleja C, de Toro M, Goncalves A, Themudo P, Vieira-Pinto M, et al. (2011) Antimicrobial resistance and class I integrons in Salmonella enterica isolates from wild boars and bisaro pigs. Int Microbiol 14: 19-24.