Antimicrobial resistance was tested in Escherichia coli isolated from feces (n = 660) of red deer, roe deer, fallow deer, European bison, and wild boar shot in regional forests in Poland during two winter hunting seasons. Indicator E. coli (n = 542) was resistant against 11 of 14 tested compounds, mostly sulfamethoxazole, streptomycin, ampicillin, trimethoprim, and tetracycline (1.3–6.6% range). No significant differences were observed between boar and ruminant isolates. Most of deer and bison isolates showed no resistance. Selective screening of wildlife samples revealed 1.7% prevalence of cephalosporin-resistant E. coli found mostly in wild boars. They produced extended-spectrum beta-lactamases (blaCTX-M-1, blaCTX-M-15) and plasmid–mediated AmpC-type cephalosporinase (blaCMY-2). The majority of the isolates originated from boars shot in a narrow time frame and space; therefore, common antimicrobial selection pressure in the environment was assumed. Three E. coli isolates carried plasmid–mediated quinolone resistance genes (qnrS1/S3). No transferable colistin resistance mechanisms were found in two resistant E. coli. Transferability of resistance was proved in a single pAmpC-positive isolate carrying IncI1-alpha 95 kb plasmid. No cephalosporin-resistant E. coli harbored pathogenicity markers; therefore, they might be considered a vector of resistance determinants, but not a pathogen themselves.
Get full access to this article
View all access options for this article.
References
1.
AllenH.K., DonatoJ., WangH.H., Cloud-HansenK.A., DaviesJ., and HandelsmanJ.. 2010. Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol., 8:251–259.
2.
LabroM.T., and BryskierJ.M.. 2014. Antibacterial resistance: an emerging “zoonosis”?. Expert Rev. Anti Infect. Ther., 12:1441–1461.
3.
LiuY.-Y., WangY., WalshT.R., YiL.-X., ZhangR., SpencerJ., DoiY., TianG., DongB., HuangX., YuL.-F., GuD., RenH., ChenX., LvL., HeD., ZhouH., LiangZ., LiuJ.-H., and ShenJ.. 2016. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect. Dis., 16:161–168.
4.
NesmeJ., and SimonetP.. 2015. The soil resistome: a critical review on antibiotic resistance origins, ecology and dissemination potential in telluric bacteria. Environ. Microbiol., 17:913–930.
5.
BhullarK., WaglechnerN., PawlowskiA., KotevaK., BanksE.D., JohnstonM.D., BartonH.A., and WrightG.D.. 2012. Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS One, 7:e34953.
DjordjevicS.P., StokesH.W., and Roy ChowdhuryP.. 2013. Mobile elements, zoonotic pathogens and commensal bacteria: conduits for the delivery of resistance genes into humans, production animals and soil microbiota. Front Microbiol., 4:86.
ManageiroV., ClementeL., Jones-DiasD., AlbuquerqueT., FerreiraE., and CaniçaM.. 2015. CTX-M-15-producing Escherichia coli in dolphin, Portugal. Emerg. Infect. Dis., 21:2249.
10.
JanatovaM., AlbrechtovaK., PetrzelkovaK.J., DolejskaM., PapousekI., MasarikovaM., CizekA., ToddA., ShuttK., KalousovaB., Profousova-PsenkovaI., ModryD., and LiterakI.. 2014. Antimicrobial-resistant Enterobacteriaceae from humans and wildlife in Dzanga-Sangha Protected Area, Central African Republic. Vet. Microbiol., 171:422–431.
11.
HendriksenR.S., MikoleitM., KornschoberC., RickertR.L., DuyneS.V., KjelsoC., HasmanH., CormicanM., MeviusD., ThrelfallJ., AnguloF.J., and AarestrupF.M.. 2009. Emergence of multidrug-resistant Salmonella Concord infections in Europe and the United States in children adopted from Ethiopia, 2003–2007. Pediatr. Infect. Dis. J., 28:814–818.
12.
RadhouaniH., SilvaN., PoetaP., TorresC., CorreiaS., and IgrejasG.. 2014. Potential impact of antimicrobial resistance in wildlife, environment, and human health. Front Microbiol., 5:23.
13.
DolejskaM., VillaL., MinoiaM., GuardabassiL., and CarattoliA.. 2014. Complete sequences of IncHI1 plasmids carrying blaCTX-M-1 and qnrS1 in equine Escherichia coli provide new insights into plasmid evolution. J. Antimicrob. Chemother., 69:2388–2393.
14.
JohnsonT.J., BielakE.M., FortiniD., HansenL.H., HasmanH., DebroyC., NolanL.K., and CarattoliA.. 2012. Expansion of the IncX plasmid family for improved identification and typing of novel plasmids in drug-resistant Enterobacteriaceae. Plasmid, 68:43–50.
15.
CarattoliA.2011. Plasmids in Gram negatives: molecular typing of resistance plasmids. Int. J. Med. Microbiol., 301:654–658.
16.
Garcillan-BarciaM.P., AlvaradoA., and de la CruzF.. 2011. Identification of bacterial plasmids based on mobility and plasmid population biology. FEMS Microbiol. Rev., 35:936–956.
17.
KaplanE., OffekM., JurkevitchE., and CytrynE.. 2013. Characterization of fluoroquinolone resistance and qnr diversity in Enterobacteriaceae from municipal biosolids. Front Microbiol., 4:144.
18.
VeldmanK., CavacoL.M., MeviusD., BattistiA., FrancoA., BotteldoornN., BruneauM., Perrin-GuyomardA., CernyT., De Frutos EscobarC., GuerraB., SchroeterA., GutierrezM., HopkinsK., MyllyniemiA.L., SundeM., WasylD., and AarestrupF.M.. 2011. International collaborative study on the occurrence of plasmid-mediated quinolone resistance in Salmonella enterica and Escherichia coli isolated from animals, humans, food and the environment in 13 European countries. J. Antimicrob. Chemother., 66:1278–1286.
19.
SeiffertS.N., HiltyM., PerretenV., and EndimianiA.. 2013. Extended-spectrum cephalosporin-resistant gram-negative organisms in livestock: an emerging problem for human health? Drug Resist. Updates., 16:22–45.
20.
TrottD.2012. Beta-lactam resistance in Gram-negative pathogens isolated from animals. Curr. Pharm. Des., 19:239–249.
21.
Martinez-MartinezL., Eliecer CanoM., Manuel Rodriguez-MartinezJ., CalvoJ., and PascualA.. 2008. Plasmid-mediated quinolone resistance. Expert Rev. Anti Infect. Ther., 6:685–711.
22.
DolejskaM., VillaL., HasmanH., HansenL., and CarattoliA.. 2013. Characterization of IncN plasmids carrying blaCTX-M-1 and qnr genes in Escherichia coli and Salmonella from animals, the environment and humans. J. Antimicrob. Chemother., 68:333–339.
23.
LiterakI., DolejskaM., JanoszowskaD., HrusakovaJ., MeissnerW., RzyskaH., BzomaS., and CizekA.. 2010. Antibiotic-resistant Escherichia coli bacteria, including strains with genes encoding the extended-spectrum beta-lactamase and QnrS, in waterbirds on the Baltic Sea Coast of Poland. Appl. Environ. Microbiol., 76:8126–8134.
24.
World Health Organization. 2017. Critically Important Antimicrobials for Human Medicine, 5th rev. WHO, Geneva.
25.
ChenJ., and GriffithsM.W.. 1998. PCR differentiation of Escherichia coli from other gram-negative bacteria using primers derived from the nucleotide sequences flanking the gene encoding the universal stress protein. Lett. Appl. Microbiol., 27:369–371.
26.
WasylD., HoszowskiA., ZającM., and SzulowskiK.. 2013. Antimicrobial resistance in commensal Escherichia coli isolated from animals at slaughter. Front Microbiol., 4:221.
27.
WasylD.2014. Prevalence and characterization of quinolone resistance mechanisms in commensal Escherichia coli isolated from slaughter animals in Poland, 2009–2012. Microb. Drug Resist., 20:544–549.
28.
WasylD., and HoszowskiA.. 2012. First isolation of ESBL-producing Salmonella and emergence of multiresistant Salmonella Kentucky in turkey in Poland. Food Res. Int., 45:958–961.
29.
XavierB.B., LammensC., RuhalR., Kumar-SinghS., ButayeP., GoossensH., and Malhotra-KumarS.. Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Euro Surveill. 2016; 21:pii=30280. DOI: http://dx.doi.org/10.2807/1560-7917.ES.2016.21.27.30280
ArandaK.R., FabbricottiS.H., Fagundes-NetoU., and ScaletskyI.C.. 2007. Single multiplex assay to identify simultaneously enteropathogenic, enteroaggregative, enterotoxigenic, enteroinvasive and Shiga toxin-producing Escherichia coli strains in Brazilian children. FEMS Microbiol. Lett., 267:145–150.
32.
SchierackP., RomerA., JoresJ., KasparH., GuentherS., FilterM., EichbergJ., and WielerL.H.. 2009. Isolation and characterization of intestinal Escherichia coli clones from wild boars in Germany. Appl. Environ. Microbiol., 75:695–702.
33.
Navarro-GonzalezN., PorreroM.C., MentaberreG., SerranoE., MateosA., DominguezL., and LavinS.. 2013. 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.
34.
DiasD., TorresR.T., KronvallG., FonsecaC., MendoS., and CaetanoT.. 2015. Assessment of antibiotic resistance of Escherichia coli isolates and screening of Salmonella spp. in wild ungulates from Portugal. Res. Microbiol., 166:584–593.
35.
CarrollD., WangJ., FanningS., and McMahonB.J.. 2015. Antimicrobial resistance in wildlife: implications for public health. Zoon. Publ. Health., 62:534–542.
36.
LiterakI., DolejskaM., RadimerskyT., KlimesJ., FriedmanM., AarestrupF.M., HasmanH., and CizekA.. 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.
37.
RödigerS., KramerT., FrömmelU., WeinreichJ., RoggenbuckD., GuentherS., SchauflerK., SchröderC., and SchierackP.. 2015. Intestinal Escherichia coli colonization in a mallard duck population over four consecutive winter seasons. Environ. Microbiol., 17:3352–3361.
38.
LalakA., WasylD., ZającM., SkarżyńskaM., HoszowskiA., SamcikI., WoźniakowskiG., and SzulowskiK.. 2016. Mechanisms of cephalosporin resistance in indicator Escherichia coli isolated from food animals. Vet. Microbiol., 2:69–73.
39.
GuentherS., EwersC., and WielerL.H.. 2011. Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution?. Front Microbiol. 2:246.
40.
PoetaP., RadhouaniH., PintoL., MartinhoA., RegoV., RodriguesR., GoncalvesA., RodriguesJ., EstepaV., TorresC., and IgrejasG.. 2009. Wild boars as reservoirs of extended-spectrum beta-lactamase (ESBL) producing Escherichia coli of different phylogenetic groups. J. Basic Microbiol., 49:584–588.
41.
CostaD., PoetaP., SaenzY., VinueL., Rojo-BezaresB., JouiniA., ZarazagaM., RodriguesJ., and TorresC.. 2006. Detection of Escherichia coli harbouring extended-spectrum beta-lactamases of the CTX-M, TEM and SHV classes in faecal samples of wild animals in Portugal. J. Antimicrob. Chemother., 58:1311–1312.
42.
GnatS., TrościańczykA., NowakiewiczA., Majer-DziedzicB., ZiółkowskaG., DziedzicR., ZiębaP., and TeodorowskiO.. 2015. Experimental studies of microbial populations and incidence of zoonotic pathogens in the faeces of red deer (Cervus elaphus). Lett. Appl. Microbiol., 61:446–452.
43.
CantonR., Gonzalez-AlbaJ.M., and GalanJ.C.. 2012. CTX-M enzymes: origin and diffusion. Front Microbiol., 3:110.
44.
WasylD., HasmanH., CavacoL.M., and AarestrupF.M.. 2012. Prevalence and characterization of cephalosporin resistance in nonpathogenic Escherichia coli from food-producing animals slaughtered in Poland. Microb. Drug Resist., 18:79–82.
45.
LivermoreD.M., CantonR., GniadkowskiM., NordmannP., RossoliniG.M., ArletG., AyalaJ., CoqueT.M., Kern-ZdanowiczI., LuzzaroF., PoirelL., and WoodfordN.. 2007. CTX-M: changing the face of ESBLs in Europe. J. Antimicrob. Chemother., 59:165–174.
46.
Baldy-ChudzikK., MackiewiczP., and StosikM.. 2008. Phylogenetic background, virulence gene profiles, and genomic diversity in commensal Escherichia coli isolated from ten mammal species living in one zoo. Vet. Microbiol., 131:173–184.
47.
GaoL., HuJ., ZhangX., WeiL., LiS., MiaoZ., and ChaiT.. 2015. Application of swine manure on agricultural fields contributes to extended-spectrum β-lactamase-producing Escherichia coli spread in Tai'an, China. Front Microbiol., 6:313.
48.
WadY.M., KimK.R., KimS.-C., KimK., LeeS.R., LeeS.S., and OkY.S.. 2015. Monitoring antibiotic residues and corresponding antibiotic resistance genes in an agroecosystem. J. Chemistr., 2015:974843.
49.
HeuerH., SchmittH., and SmallaK.. 2011. Antibiotic resistance gene spread due to manure application on agricultural fields. Curr. Opin. Microbiol., 14:236–243.
50.
MakowskaN., KoczuraR., and MokrackaJ.. 2015. Class 1 integrase, sulfonamide and tetracycline resistance genes in wastewater treatment plant and surface water. Chemosphere, 144:1665–1673.
51.
Navarro-GonzalezN., PorreroM.C., MentaberreG., SerranoE., MateosA., CabalA., DominguezL., and LavinS.. 2015. Escherichia coli O157:H7 in wild boars (Sus scrofa) and Iberian ibex (Capra pyrenaica) sharing pastures with free-ranging livestock in a natural environment in Spain. Vet. Q., 35:102–106.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
