Abstract
The Western European population of wild boar (Sus scrofa) has increased its distribution over the past several decades, and some populations have colonized areas strongly influenced by human activity. Wild boars are known carriers of antibiotic-resistant bacteria acquired from the environment, and urban populations of wild boars may be more exposed than their rural counterparts. In this work, we compared the frequency of antibiotic resistance in indicator bacteria (Escherichia coli, Enterococcus faecalis, Enterococcus faecium) isolated from urban wild boars with that from rural wild boars in NE Spain. We further assessed whether bacterial isolates from the urban wild boars had a higher probability of showing antibiotic resistance when their host was highly associated to urban features. Seventy-two and 100 bacterial isolates from urban and rural habitat, respectively, were screened for antibiotic resistance against a set of antibiotics (13 per bacterial species). We found a significantly higher frequency of E. faecium showing resistance to tetracycline (70.0% vs 36.4%) and high-level resistance to streptomycin (30.0% vs 4.5%) in urban wild boars compared to rural wild boars (p < 0.05). E. faecalis was more frequently resistant to trimethoprim in urban than rural wild boars (33.3% vs 0.0%, p < 0.05). In isolates from urban origin, 55.6% of the likelihood of detecting antibiotic resistance depended only on the bacterial species, being more likely in the enterococci than in E. coli. These results suggest that urban wild boars may be more exposed to certain antibiotic-resistant bacteria or antibiotic resistance genes that they may acquire from the urban environment, although implications are uncertain.
Similar content being viewed by others
References
Alvarez-Perez S, Blanco JL, Harmanus C, Kuijper EJ, Garcia ME (2017) Prevalence and characteristics of Clostridium perfringens and Clostridium difficile in dogs and cats attended in diverse veterinary clinics from the Madrid region. Anaerobe 48:47–55. https://doi.org/10.1016/j.anaerobe.2017.06.023
Apollonio M, Andersen R (2010) European ungulates and their management in the 21st century. Cambridge University Press, Cambridge
Arnold KE, Williams NJ, Bennett M (2017) “Disperse abroad in the land”: the role of wildlife in the dissemination of antimicrobial resistance. Biol Lett 12:20160137. https://doi.org/10.1098/rsbl.2016.0137
Atterby C, Ramey AM, Hall GG, Järhult J, Börjesson S, Bonnedahl J (2016) Increased prevalence of antibiotic-resistant E. coli in gulls sampled in Southcentral Alaska is associated with urban environments. Infect Ecol Epidemiol 19:32334. https://doi.org/10.3402/iee.v6.32334
Bateman PW, Fleming PA (2012) Big city life: carnivores in urban environments. J Zool 287:1–23. https://doi.org/10.1111/j.1469-7998.2011.00887.x
Bieber C, Ruf T (2005) Population dynamics in wild boar Sus scrofa: ecology, elasticity of growth rate and implications for the management of pulsed resource consumers. J Appl Ecol 42:1203–1213. https://doi.org/10.1111/j.1365-2664.2005.01094.x
Bonnedahl J, Drobni M, Gauthier-Clerc M, Hernandez J, Granholm S, Kayser Y, Melhu A, Kahlmeter G, Waldenström J, Johansson A, Olsen B (2009) Dissemination of Escherichia coli with CTX-M type ESBL between humans and yellow-legged gulls in the south of France. PLoS One 4:e5958. https://doi.org/10.1371/journal.pone.0005958
Burnham KP, Anderson DR (1998) Model selection and inference. In: A practical information-theoretic approach. Springer, New York
Cahill S, Llimona F, Gràcia J (2003) spacing and nocturnal activity of wild boar Sus scrofa in a Mediterranean metropolitan park. Wildlife Biol 9:3–13. doi:.https://doi.org/10.2981/wlb.2003.058
Cahill S, Llimona F, Cabañeros L, Casas E, Massei GCF (2010) Wild boar habituation to human and suburban landscapes: local perspectives on an increasingly global phenomenon with complex management implications. In: 8th international symposium on wild boar and other suids. York, United Kingdom
Cahill S, Llimona F, Cabañeros L, Calomardo F (2012) Characteristics of wild boar (Sus scrofa) habituation to urban areas in the Collserola Natural Park (Barcelona) and comparison with other locations. Anim Biodivers Conserv 35(2):221–233
Castillo-Contreras R, Carvalho J, Serrano E, Mentaberre G, Fernández-Aguilar X, Colom A, González-Crespo C, Lavín S, López-Olvera JR (2018) Urban wild boars prefer fragmented areas with food resources near natural corridors. Sci Total Environ 615:282–288. https://doi.org/10.1016/j.scitotenv.2017.09.277
De Jong A, Thomas V, Simjee S, Godinho K, Schiessl B, Klein U, Butty P, Vallé M, Marion H, Shryock TR (2012) Pan-European monitoring of susceptibility to human-use antimicrobial agents in enteric bacteria isolated from healthy food-producing animals. J Antimicrob Chemother 67:638–665. https://doi.org/10.1093/jac/dkr539
De Jong A, Simjee S, El Garch F, Moyaert H, Rose M, Youala M, Dry M (2018) Antimicrobial susceptibility of enterococci recovered from healthy cattle, pigs and chickens in nine EU countries (EASSA Study) to critically important antibiotics. Vet Microbiol 216:168–175. https://doi.org/10.1016/j.vetmic.2018.02.010
De’ath G, Fabricius KE (2000) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81:3178–3192. https://doi.org/10.2307/177409
Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: modifications due to human-induced stress. Urban Ecosyst 9:5–12. https://doi.org/10.1007/s11252-006-3262-3
Dobiasova H, Dolejska M (2016) Prevalence and diversity of IncX plasmids carrying fluoroquinolone and beta-lactam resistance genes in Escherichia coli originating from diverse sources and geographical areas. J Antimicrob Chemoth 71:2118–2124. https://doi.org/10.1093/jac/dkw144
Dutka-Malen S, Evers S, Courvalin P (1995) Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J Clin Microbiol 33:1434
EUCAST (European Committee on Antimicrobial Susceptibility Testing). Data from the EUCAST MIC distribution website, last accessed 06/2012. http://www.eucast.org
European Food Safety Authority (2008) Report from the Task Force on Zoonoses Data Collection including guidance for harmonized monitoring and reporting of antimicrobial resistance in commensal Escherichia coli and Enterococcus spp. from food animals. EFSA J 141:1–44. https://doi.org/10.2903/j.efsa.2008.141r
European Food Safety Authority (2012) Technical specifications on the harmonised monitoring and reporting of antimicrobial resistance in Salmonella, Campylobacter and indicator Escherichia coli and Enterococcus spp. bacteria transmitted through food. EFSA J 10(2742). https://doi.org/10.2903/j.efsa.2012.2742
European Food Safety Authority and European Centre for Disease Prevention and Control (2012) Summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2010. EFSA J 10:2598. https://doi.org/10.2903/j.efsa.2012.2598
European Food Safety Authority and European Centre for Disease Prevention and Control (2016) The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2014. EFSA J 14(4380). https://doi.org/10.2903/j.efsa.2016.4380
Fessler AT, Calvo N, Gutierrez N, Munoz Bellido JL, Fajardo M, Garduno E, Monecke S, Ehricht R, Kadlec K, Schwarz S (2013) Cfr-mediated linezolid resistance in methicillin-resistant Staphylococcus aureus and Staphylococcus haemolyticus associated with clinical infections in humans: two case reports. J Antimicrob Chemother 69(1):268–270
Furness LE, Campbell A, Zhang LH, Gaze WH, McDonald RA (2017) Wild small mammals as sentinels for the environmental transmission of antimicrobial resistance. Environ Res 154:28–34. https://doi.org/10.1016/j.envres.2016.12.014
Harveson PM, Lopez RR, Collier BA, Silvy NJ (2007) Impacts of urbanization on Florida Key deer behavior and population dynamics. Biol Conserv 134:321–331. https://doi.org/10.1016/j.biocon.2006.07.022
Heininger A, Bider M, Schmidt S, Unertl K, Botzenhart K, Doring G (1999) PCR and blood culture for detection of Escherichia coli bacteremia in rats. J Clin Microbiol 37:2479–2482
Hernández J, González-Acuña D (2016) Anthropogenic antibiotic resistance genes mobilization to the polar regions. Infect Ecol Epidemiol 6:32112
Hölzel CS, Harms KS, Schwaiger K, Bauer J (2010) Resistance to linezolid in a porcine Clostridium perfringens strain carrying a mutation in the rplD gene encoding the ribosomal protein L4. Antimicrob Agents Ch 54:1351–1353. https://doi.org/10.1128/AAC.01208-09
Idescat (2013) Cens de població i habitatges 2011. Available at https://www.idescat.cat
Jardine CM, Janecko N, Allan M, Boerlin P, Chalmers G, Kozak G, McEwen S, Reid-Smith RJ (2012) Antimicrobial resistance in Escherichia coli isolates from raccoons (Procyon lotor) in southern Ontario, Canada. Appl Environ Microbiol 78:3873–3879. https://doi.org/10.1128/AEM.00705-12
Jiménez-Valverde A (2012) Insights into the area under the receiver operating characteristic curve (AUC) as a discrimination measure in species distribution modelling. Glob Ecol Biogeogr 21:498–507. https://doi.org/10.1111/j.1466-8238.2011.00683.x
Jobbins SE, Alexander KA (2015) From whence they came—antibiotic-resistant Escherichia coli in African wildlife. J Wildlife Dis 51:811–820. https://doi.org/10.7589/2014-11-257
Literak I, Dolejska M, Radimersky T, Klimes J, Friedman M, Aarestrup FM, Hasman H, Cizek A (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. https://doi.org/10.1111/j.1365-2672.2009.04572.x
Llimona F, Cahill S, Tenés A, Camps D, Bonet-Arbolí V, Cabañeros L (2007) El estudio de los mamíferos en relación a la gestión de áreas periurbanas. El caso de la región metropolitana de Barcelona Galemys 19:215–234
Lowry H, Lill A, Wong BBM (2013) Behavioural responses of wildlife to urban environments. Biol Rev 88:537–549. https://doi.org/10.1111/brv.12012
Lozano C, Gonzalez-Barrio D, Camacho MC, Lima-Barbero JF, De la Puente J, Hofle U, Torres C (2016) Characterization of fecal vancomycin-resistant enterococci with acquired and intrinsic resistance mechanisms in wild animals, Spain. Microb Ecol 72:813–820. https://doi.org/10.1007/s00248-015-0648-x
Luniak M (2004) Synurbization - the adaptation of animal wildlife to urban development. In: Shaw WW, Harris LK, VanDruff L (Eds). Proceedings of the 4th international symposium on urban wildlife conservation, 1999, Tucson, Arizona, USA
Massei G, Kindberg J, Licoppe A, Gačić D, Šprem N, Kamler J, Baubet E, Hohmann U, Monaco A, Ozoliņš J, Cellina S, Podgórski T, Fonseca C, Markov N, Pokorny B, Rosell C, Náhlik A (2015) Wild boar populations up, numbers of hunters down? A review of trends and implications for Europe. Pest Manag Sci 71:492–500. https://doi.org/10.1002/ps.3965
McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260. https://doi.org/10.1016/j.biocon.2005.09.005
Meka VG, Gold HS (2004) Antimicrobial resistance to linezolid. Clin Infect Dis 39(7):1010–1015
Mentaberre G, Romero B, de Juan L, Navarro-Gonzalez N, Velarde R, Mateos A, Marco I, Olivé-Boix X, Domínguez L, Lavín S, Serrano E (2014) Long-term monitoring of wild boar harvesting and cattle removal for bovine tuberculosis control in free ranging populations. PLoS One 9:e88824. https://doi.org/10.1371/journal.pone.0088824
Morelle K, Podgórski T, Prévot C, Keuling O, Lehaire F, Lejeune P (2015) Towards understanding wild boar Sus scrofa movement: a synthetic movement ecology approach. Mammal Rev 45(1):15–29. https://doi.org/10.1111/mam.12028
Navarro-Gonzalez N, Mentaberre G, Porrero CM, Serrano E, Mateos A, López-Martín JM, Lavín S, Domínguez L (2012) Effect of cattle on Salmonella carriage, diversity and antimicrobial resistance in free-ranging wild boar (Sus scrofa) in northeastern Spain. PLoS One 7:e51614. https://doi.org/10.1371/journal.pone.0051614
Navarro-Gonzalez N, Porrero MC, Mentaberre G, Serrano E, Mateos A, Dominguez L, Lavin S (2013a) Antimicrobial resistance in Indicator Escherichia coli isolates from free-ranging livestock and sympatric wild ungulates in a natural environment (northeastern Spain). Appl Environ Microbiol 79:6184–6186. https://doi.org/10.1128/AEM.01745-13
Navarro-Gonzalez N, Casas-Díaz E, Porrero CM, Mateos A, Domínguez L, Lavín S, Serrano E (2013b) Food-borne zoonotic pathogens and antimicrobial resistance of indicator bacteria in urban wild boars in Barcelona, Spain. Vet Microbiol 167:686–689. https://doi.org/10.1016/j.vetmic.2013.07.037
Papich MG (2016) Linezolid. In: Papich MG (ed) Saunders handbook of veterinary drugs (4th edition). W.B. Saunders, St. Louis, pp 451–452
Poeta P, Costa D, Igrejas G, Rodrigues J, Torres C (2007) Phenotypic and genotypic characterization of antimicrobial resistance in faecal enterococci from wild boars (Sus scrofa). Vet Microbiol 125:368–374
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Sacristán C, Esperon F, Herrera-Leon S, Iglesias I, Neves E, Nogal V, Munoz MJ, de la Torre A (2014) Virulence genes, antibiotic resistance and integrons in Escherichia coli strains isolated from synanthropic birds from Spain. Avian Pathol 43:172–175. https://doi.org/10.1080/03079457.2014.897683
Sáez-Royuela C, Tellería JL (1986) The increased population of the wild boar (Sus scrofa L.) in Europe. Mammal Rev 16(2):97–101. https://doi.org/10.1111/j.1365-2907.1986.tb00027.x
Skurnik D, Ruimy R, Andremont A, Amorin C, Rouquet P, Picard B, Denamur E (2006) Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J Antimicrob Chemoth 57:1215–1219. https://doi.org/10.1093/jac/dkl122
Stillfried M, Gras P, Börner K, Göritz F, Painer J, Röllig K, Wenzler M, Hofer H, Ortmann S, Kramer-Schadt S (2017) Secrets of success in a landscape of fear: urban wild boar adjust risk perception and tolerate disturbance. Front Ecol Evol 5(157). https://doi.org/10.3389/fevo.2017.00157
Therneau T, Atkinson B, Ripley B (2013) Package “rpart”: recursive partitioning and regression trees. R package version 4:1–10 https://CRAN.R-project.org/package=rpart
Vittecoq M, Godreuil S, Prugnolle F, Durand P, Brazier L, Renaud N, Arnal A, Aberkane S, Jean-Pierre H, Gauthier-Leclerc M, Thomas F, Renaud F (2016) Antimicrobial resistance in wildlife. J Appl Ecol 53:519–529. https://doi.org/10.1111/1365-2664.12596
Wasyl D, Zajac M, Lalak A, Skarzynska M, Samcik I, Kwit R, Jablonski A, Bocian L, Wozniakowski G, Hoszowski A, Szulowsk K (2017) Antimicrobial resistance in Escherichia coli isolated from wild animals in Poland. Microb Drug Resist 24:807–815. https://doi.org/10.1089/mdr.2017.0148
Wheeler E, Hong P-Y, Bedon LC, Mackie RI (2012) Carriage of antibiotic-resistant enteric bacteria varies among sites in Galápagos reptiles. J Wildlife Dis 48:56–67. https://doi.org/10.7589/0090-3558-48.1.56
Acknowledgements
We are grateful to the Collserola Natural Park staff for their help in obtaining the samples and information necessary for this work. E. Serrano (SFRH/BPD/96637/2013) and R. T. Torres (SFRH/BPD/112482/2015) were supported by a post-doctoral grant from Fundação para a Ciência e a Tecnologia, Portugal. R. Castillo-Contreras was supported by a PhD grant (2016FI_B 00425) co-financed by Generalitat de Catalunya (Secretaria d’Universitats i Recerca del Departament d’Economia i Coneixement) and European Social Fund (ESF).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Navarro-Gonzalez, N., Castillo-Contreras, R., Casas-Díaz, E. et al. Carriage of antibiotic-resistant bacteria in urban versus rural wild boars. Eur J Wildl Res 64, 60 (2018). https://doi.org/10.1007/s10344-018-1221-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10344-018-1221-y