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Antibiotic-Resistant Bacteria in Wildlife

  • Monika DolejskaEmail author
Chapter
  • 25 Downloads
Part of the The Handbook of Environmental Chemistry book series

Abstract

The global dissemination of antibiotic-resistant bacteria (ARB) is one of the most important issues for current medicine, having serious implications for public health. Particular concern has been raised regarding the increasing occurrence of multidrug-resistant bacteria in the environment and wildlife. Wild animals inhabiting human-influenced environments can easily acquire ARB. Synanthropic animals that tend to live close to humans and seek food in cities, landfills or areas with intensive agriculture are more likely to carry ARB in their gut than those in places with limited human footprints. In the past years, wild animals were recognized as vectors and secondary sources of ARB for humans and animals. Moreover, wild birds are capable of long-range movements and may spread antibiotic resistance (AR) across borders or continents. This chapter provides a summary of various aspects of AR in wildlife which is presented with respect to the One Health concept. It highlights the most important sources of AR for wildlife and outlines transmission routes of AR into the environment. Ecological and biological factors of various groups of wild animals driving the occurrence of AR and the role of wild animals as spreaders of resistant bacteria are addressed. An overview of selected resistant pathogens carrying epidemiologically and clinically relevant AR found in wildlife is presented and linked to the situation in humans and livestock. Current gaps in our understanding of AR in wildlife and suggestions for future actions and research activities are also highlighted.

Keywords

Antibiotics Escherichia coli Environmental source One Health Resistance Transmission Wildlife 

Abbreviations

AR

Antibiotic resistance

ARB

Antibiotic-resistant bacteria

ARG

Antibiotic resistance genes

CC

Clonal complex (defined by multilocus sequence typing)

CPE

Carbapenemase-producing Enterobacteriaceae

ESBL

Extended-spectrum beta-lactamase

LA-MRSA

Livestock-associated methicillin-resistant Staphylococcus aureus

MDR

Multidrug resistance

MLST

Multilocus sequence typing

MRSA

Methicillin-resistant Staphylococcus aureus

PCR

Polymerase chain reaction

PFGE

Pulse-field gel electrophoresis

PMQR

Plasmid-mediated quinolone resistance

qPCR

Quantitative PCR

rep-PCR

Repetitive element sequence-based PCR

SSCmec

Staphylococcal cassette chromosome mec

ST

Sequence type

VRE

Vancomycin-resistant enterococci

WGS

Whole-genome sequencing

WWTP

Wastewater treatment plant

Notes

Acknowledgements

Supported by Czech Health Research Council (NV18-09-00605) and the Czech Ministry of Education, Youth and Sports within the National Programme for Sustainability II (LQ1601). I am sincerely grateful to Marco Minoia for his help with figure preparation.

References

  1. 1.
    ECDC (2018) European Center for Infectious Diseases and Control. Surveillance of antimicrobial resistance in Europe – Annual report of the European Antimicrobial Resistance Surveillance Network (EARS-Net) 2017. ECDC, StockholmGoogle Scholar
  2. 2.
    EFSA ECDC (2019) European Food Safety Authority and European Centre for Disease Prevention and Control. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J 17:278Google Scholar
  3. 3.
    Kraemer SA, Ramachandran A, Perron GG (2019) Antibiotic pollution in the environment: from microbial ecology to public policy. Microorganisms 7(6):180Google Scholar
  4. 4.
    Wellington EM, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM, Johnson-Rollings AS, Jones DL, Lee NM, Otten W, Thomas CM, Williams AP (2013) The role of the natural environment in the emergence of antibiotic resistance in gram-negative bacteria. Lancet Infect Dis 13:155–165Google Scholar
  5. 5.
    Guenther S, Ewers C, Wieler LH (2011) Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution? Front Microbiol 2:246Google Scholar
  6. 6.
    Dolejska M, Papagiannitsis CC (2018) Plasmid-mediated resistance is going wild. Plasmid 99:99–111Google Scholar
  7. 7.
    Bonnedahl J, Jarhult JD (2014) Antibiotic resistance in wild birds. Ups J Med Sci 119:113–116Google Scholar
  8. 8.
    Coertze RD, Bezuidenhout CC (2019) Global distribution and current research of AmpC beta-lactamase genes in aquatic environments: A systematic review. Environ Pollut 252:1633–1642Google Scholar
  9. 9.
    Karkman A, Do TT, Walsh F, Virta MPJ (2018) Antibiotic-resistance genes in waste water. Trends Microbiol 26:220–228Google Scholar
  10. 10.
    Manaia CM, Macedo G, Fatta-Kassinos D, Nunes OC (2016) Antibiotic resistance in urban aquatic environments: can it be controlled? Appl Microbiol Biotechnol 100:1543–1557Google Scholar
  11. 11.
    Almakki A, Jumas-Bilak E, Marchandin H, Licznar-Fajardo P (2019) Antibiotic resistance in urban runoff. Sci Total Environ 667:64–76Google Scholar
  12. 12.
    Hessman J, Atterby C, Olsen B, Jarhult JD (2018) High prevalence and temporal variation of extended spectrum beta-lactamase-producing bacteria in urban Swedish mallards. Microb Drug Resist 24:822–829Google Scholar
  13. 13.
    Sandegren L, Stedt J, Lustig U, Bonnedahl J, Andersson DI, Jarhult JD (2018) Long-term carriage and rapid transmission of extended spectrum beta-lactamase-producing E. coli within a flock of mallards in the absence of antibiotic selection. Environ Microbiol Rep 10:576–582Google Scholar
  14. 14.
    Nelson M, Jones SH, Edwards C, Ellis JC (2008) Characterization of Escherichia coli populations from gulls, landfill trash, and wastewater using ribotyping. Dis Aquat Org 81:53–63Google Scholar
  15. 15.
    Varela AR, Manageiro V, Ferreira E, Augusta Guimaraes M, da Costa PM, Canica M, Manaia CM (2015) Molecular evidence of the close relatedness of clinical, gull and wastewater isolates of quinolone-resistant Escherichia coli. J Glob Antimicrob Resist 3:286–289Google Scholar
  16. 16.
    Cole D, Drum DJ, Stalknecht DE, White DG, Lee MD, Ayers S, Sobsey M, Maurer JJ (2005) Free-living Canada geese and antimicrobial resistance. Emerg Infect Dis 11:935–938Google Scholar
  17. 17.
    Marcelino VR, Wille M, Hurt AC, Gonzalez-Acuna D, Klaassen M, Schlub TE, Eden JS, Shi M, Iredell JR, Sorrell TC, Holmes EC (2019) Meta-transcriptomics reveals a diverse antibiotic resistance gene pool in avian microbiomes. BMC Biol 17:31Google Scholar
  18. 18.
    Butterfield J, Coulson JC, Kearsey SV, Monaghan P, McCoy JH, Spain GE (1983) The herring gull Larus argentatus as a carrier of salmonella. Epidemiol Infect 91:429–436Google Scholar
  19. 19.
    Converse RR, Kinzelman JL, Sams EA, Hudgens E, Dufour AP, Ryu H, Santo-Domingo JW, Kelty CA, Shanks OC, Siefring SD, Haugland RA, Wade TJ (2012) Dramatic improvements in beach water quality following gull removal. Environ Sci Technol 46:10206–10213Google Scholar
  20. 20.
    Burgmann H, Frigon D, Gaze WH, Manaia CM, Pruden A, Singer AC, Smets BF, Zhang T (2018) Water and sanitation: an essential battlefront in the war on antimicrobial resistance. FEMS Microbiol Ecol 94:fiy101Google Scholar
  21. 21.
    Furness LE, Campbell A, Zhang L, Gaze WH, McDonald RA (2017) Wild small mammals as sentinels for the environmental transmission of antimicrobial resistance. Environ Res 154:28–34Google Scholar
  22. 22.
    Guenther S, Grobbel M, Beutlich J, Guerra B, Ulrich RG, Wieler LH, Ewers C (2010) Detection of pandemic B2-O25-ST131 Escherichia coli harbouring the CTX-M-9 extended-spectrum beta-lactamase type in a feral urban brown rat (Rattus norvegicus). J Antimicrob Chemother 65:582–584Google Scholar
  23. 23.
    Plaza PI, Lambertucci SA (2017) How are garbage dumps impacting vertebrate demography, health, and conservation? Glob Ecol Conserv 12:9–20Google Scholar
  24. 24.
    Smith GC, Carlile N (1993) Food and feeding ecology of breeding silver gulls (Larus novaehollandiae) in urban Australia. Colon Waterbirds 16:9–16Google Scholar
  25. 25.
    De Giacomo U, Guerrieri G (2018) The feeding behavior of the black kite (Milvus migrans) in the rubbish dump of Rome. J Raptor Res 42:110–118Google Scholar
  26. 26.
    Novaes WG, Cintra R (2013) Factors influencing the selection of communal roost sites by the black vulture Coragyps Atratus (Aves: Cathartidae) in an urban area in Central Amazon. Zoologia (Curitiba) 30:607–614Google Scholar
  27. 27.
    Marzluff JM, Neatherlin E (2006) Corvid response to human settlements and campgrounds: causes, consequences, and challenges for conservation. Biol Conserv 30:301–314Google Scholar
  28. 28.
    Gould NP, Andelt WF (2013) Effect of anthropogenically developed areas on spatial distribution of island foxes. J Mammal 94:662–671Google Scholar
  29. 29.
    Rotics S, Turjeman S, Kaatz M, Resheff YS, Zurrel D, Sapir N, Eggers U, Fiedler W, Flack A, Jeltsch F, Wikelski M, Nathan R (2017) Wintering in Europe instead of Africa enhances juvenile survival in a long-distance migrant. Anim Behav 126:79–88Google Scholar
  30. 30.
    Ahlstrom CA, Bonnedahl J, Woksepp H, Hernandez J, Reed JA, Tibbitts L, Olsen B, Douglas DC, Ramey AM (2019) Satellite tracking of gulls and genomic characterization of faecal bacteria reveals environmentally mediated acquisition and dispersal of antimicrobial-resistant Escherichia coli on the Kenai Peninsula, Alaska. Mol Ecol 28:2531–2545Google Scholar
  31. 31.
    Dolejska M, Masarikova M, Dobiasova H, Jamborova I, Karpiskova R, Havlicek M, Carlile N, Priddel D, Cizek A, Literak I (2016) High prevalence of Salmonella and IMP-4-producing Enterobacteriaceae in the silver gull on Five Islands, Australia. J Antimicrob Chemother 71:63–70Google Scholar
  32. 32.
    Ramos R, Cerda-Cuellar M, Ramirez F, Jover L, Ruiz X (2010) Influence of refuse sites on the prevalence of Campylobacter spp. and Salmonella serovars in seagulls. Appl Environ Microbiol 76:3052–3056Google Scholar
  33. 33.
    Benskin CM, Wilson K, Jones K, Hartley IR (2009) Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev Camb Philos Soc 84:349–373Google Scholar
  34. 34.
    Thieriot E, Patenaude-Monette M, Molina P, Giroux JF (2015) The efficiency of an integrated program using falconry to deter gulls from landfills. Animals 5:214–225Google Scholar
  35. 35.
    Thanner S, Drissner D, Walsh F (2016) Antimicrobial resistance in agriculture. MBio 7:e02227–e02215Google Scholar
  36. 36.
    Jechalke S, Heuer H, Siemens J, Amelung W, Smalla K (2014) Fate and effects of veterinary antibiotics in soil. Trends Microbiol 22:536–545Google Scholar
  37. 37.
    Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci U S A 110:3435–3440Google Scholar
  38. 38.
    Kozak GK, Boerlin P, Janecko N, Reid-Smith RJ, Jardine C (2009) Antimicrobial resistance in Escherichia coli isolates from swine and wild small mammals in the proximity of swine farms and in natural environments in Ontario, Canada. Appl Environ Microbiol 75:559–566Google Scholar
  39. 39.
    Rogers SW, Shaffer CE, Langen TA, Jahne M, Welsh R (2018) Antibiotic-resistant genes and pathogens shed by wild deer correlate with land application of residuals. EcoHealth 15:409–425Google Scholar
  40. 40.
    Zurek L, Ghosh A (2014) Insects represent a link between food animal farms and the urban environment for antibiotic resistance traits. Appl Environ Microbiol 80:3562–3567Google Scholar
  41. 41.
    Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993Google Scholar
  42. 42.
    Arnold KE, Williams NJ, Bennett M (2016) ‘Disperse abroad in the land’: the role of wildlife in the dissemination of antimicrobial resistance. Biol Lett 12:20160137Google Scholar
  43. 43.
    Grond K, Sandercock BK, Jumpponen A, Zeglin LH (2018) The avian gut microbiota: community, physiology and function in wild birds. J Avian Biol 49:e01788Google Scholar
  44. 44.
    Pearce DS, Hoover BA, Jennings S, Nevitt GA, Docherty KM (2017) Morphological and genetic factors shape the microbiome of a seabird species (Oceanodroma leucorhoa) more than environmental and social factors. Microbiome 5:146Google Scholar
  45. 45.
    Chi X, Gao H, Wu G, Qin W, Song P, Wang L, Chen J, Cai Z, Zhang T (2019) Comparison of gut microbiota diversity between wild and captive bharals (Pseudois nayaur). BMC Vet 15:243Google Scholar
  46. 46.
    Cizek A, Literak I, Hejlicek K, Treml F, Smola J (1994) Salmonella contamination of the environment and its incidence in wild birds. Zentralbl Veterinarmed B 41:320–327Google Scholar
  47. 47.
    Donaldson SC, Straley BA, Hegde NV, Sawant AA, DebRoy C, Jayarao BM (2006) Molecular epidemiology of ceftiofur-resistant Escherichia coli isolates from dairy calves. Appl Environ Microbiol 72:3940–3948Google Scholar
  48. 48.
    Meale SJ, Chaucheyras-Durand F, Berends H, Guan LL, Steele MA (2017) From pre- to postweaning: transformation of the young calf’s gastrointestinal tract. J Dairy Sci 100:5984–5995Google Scholar
  49. 49.
    Mir RA, Weppelmann TA, Teng L, Kirpich A, Elzo MA, Driver JD, Jeong KC (2018) Colonization dynamics of cefotaxime resistant bacteria in beef cattle raised without cephalosporin antibiotics. Front Microbiol 9:500Google Scholar
  50. 50.
    Girdwood RW, Fricker CR, Munro D, Shedden CB, Monaghan P (1985) The incidence and significance of salmonella carriage by gulls (Larus spp.) in Scotland. Epidemiol Infect 95:229–241Google Scholar
  51. 51.
    Literak I, Smola J (1996) Survival of salmonellas in a colony of common black-headed gulls Larus ridibundus between two nesting periods. Colon Waterbirds 19:268–269Google Scholar
  52. 52.
    Ribas A, Saijuntha W, Agatsuma T, Prantlova V, Poonlaphdecha S (2016) Rodents as a source of Salmonella contamination in wet markets in Thailand. Vector Borne Zoonotic Dis 16:537–540Google Scholar
  53. 53.
    Laidler MR, Tourdjman M, Buser GL, Hostetler T, Repp KK, Leman R, Samadpour M, Keene WE (2013) Escherichia coli O157:H7 infections associated with consumption of locally grown strawberries contaminated by deer. Clin Infect Dis 57:1129–1134Google Scholar
  54. 54.
    Macovei L, Miles B, Zurek L (2008) Potential of houseflies to contaminate ready-to-eat food with antibiotic-resistant enterococci. J Food Prot 71:435–439Google Scholar
  55. 55.
    Brown VR, Bowen RA, Bosco-Lauth AM (2018) Zoonotic pathogens from feral swine that pose a significant threat to public health. Transbound Emerg Dis 65:649–659Google Scholar
  56. 56.
    Alderisio KA, DeLuca N (1999) Seasonal enumeration of fecal coliform bacteria from the feces of ring-billed gulls (Larus delawarensis) and Canada geese (Branta canadensis). Appl Environ Microbiol 65:5628–5630Google Scholar
  57. 57.
    Varslot M, Resell J, Fostad IG (1996) Water-borne outbreaks of Campylobacter gastroenteritis due to pink-footed geese in Norway in 1994 and 1995. Tidsskrift for den Norske Legeforening 116:3366–3369Google Scholar
  58. 58.
    Whitman RL, Nevers MB (2003) Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michigan beach. Appl Environ Microbiol 69:5555–5562Google Scholar
  59. 59.
    Alm EW, Daniels-Witt QR, Learman DR, Ryu H, Jordan DW, Gehring TM, Santo Domingo J (2018) Potential for gulls to transport bacteria from human waste sites to beaches. Sci Total Environ 615:123–130Google Scholar
  60. 60.
    Gill FB (ed) (1994) Ornithology, 2nd edn. Freeman, New YorkGoogle Scholar
  61. 61.
    Reed KD, Meece JK, Henkel JS, Shukla SK (2003) Birds, migration and emerging zoonoses: west nile virus, lyme disease, influenza A and enteropathogens. Clin Med Res 1:5–12Google Scholar
  62. 62.
    Anonymous (2016) Role for migratory wild birds in the global spread of avian influenza H5N8. Science 354:213–217Google Scholar
  63. 63.
    Risely A, Waite DW (2018) Active migration is associated with specific and consistent changes to gut microbiota in Calidris shorebirds. J Anim Ecol 87:428–437Google Scholar
  64. 64.
    Sjolund M, Bonnedahl J, Hernandez J, Bengtsson S, Cederbrant G, Pinhassi J, Kahlmeter G, Olsen B (2008) Dissemination of multidrug-resistant bacteria into the Arctic. Emerg Infect Dis 14:70–72Google Scholar
  65. 65.
    Hernandez J, Gonzalez-Acuna D (2016) Anthropogenic antibiotic resistance genes mobilization to the polar regions. Infect Ecol Epidemiol 6:32112Google Scholar
  66. 66.
    Guenther S, Aschenbrenner K, Stamm I, Bethe A, Semmler T, Stubbe A, Stubbe M, Batsajkhan N, Glupczynski Y, Wieler LH, Ewers C (2012) Comparable high rates of extended-spectrum-beta-lactamase-producing Escherichia coli in birds of prey from Germany and Mongolia. PLoS One 7:e53039Google Scholar
  67. 67.
    Loncaric I, Stalder GL, Mehinagic K, Rosengarten R, Hoelzl F, Knauer F, Walzer C (2013) Comparison of ESBL--and AmpC producing Enterobacteriaceae and methicillin-resistant Staphylococcus aureus (MRSA) isolated from migratory and resident population of rooks (Corvus frugilegus) in Austria. PLoS One 8:e84048Google Scholar
  68. 68.
    Mathys DA, Mathys BA, Mollenkopf DF, Daniels JB, Wittum TE (2017) Enterobacteriaceae harboring AmpC (blaCMY) and ESBL (blaCTX-M) in migratory and nonmigratory wild songbird populations on Ohio dairies. Vector Borne Zoonotic Dis 17:254–259Google Scholar
  69. 69.
    Bonnedahl J, Stedt J, Waldenstrom J, Svensson L, Drobni M, Olsen B (2015) Comparison of Extended-Spectrum beta-Lactamase (ESBL) CTX-M genotypes in Franklin gulls from Canada and Chile. PLoS One 10:e0141315Google Scholar
  70. 70.
    Liakopoulos A, Olsen B, Geurts Y, Artursson K, Berg C, Mevius DJ, Bonnedahl J (2016) Molecular characterization of extended-spectrum-Cephalosporin-resistant Enterobacteriaceae from wild kelp gulls in South America. Antimicrob Agents Chemother 60:6924–6927Google Scholar
  71. 71.
    Ghafourian S, Sadeghifard N, Soheili S, Sekawi Z (2015) Extended spectrum beta-lactamases: definition, classification and epidemiology. Curr Issues Mol Biol 17:11–21Google Scholar
  72. 72.
    Jacoby GA (2009) AmpC beta-lactamases. Clin Microbiol Rev 22:161–182, Table of ContentsGoogle Scholar
  73. 73.
    Chong Y, Shimoda S, Shimono N (2018) Current epidemiology, genetic evolution and clinical impact of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae. Infect Genet Evol 61:185–188Google Scholar
  74. 74.
    Madec JY, Haenni M, Nordmann P, Poirel L (2017) Extended-spectrum beta-lactamase/AmpC- and carbapenemase-producing Enterobacteriaceae in animals: a threat for humans? Clin Microbiol Infect 23:826–833Google Scholar
  75. 75.
    Wang J, Ma Z-B, Zeng Z-L, Yang X-W, Huang Y, Liu J-H (2017) The role of wildlife (wild birds) in the global transmission of antimicrobial resistance genes. Zool Res 38:55–80Google Scholar
  76. 76.
    Costa D, Poeta P, Saenz Y, Vinue L, Rojo-Bezares B, Jouini A, Zarazaga M, Rodrigues J, Torres C (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 58:1311–1312Google Scholar
  77. 77.
    Jamborova I, Dolejska M, Zurek L, Townsend AK, Clark AB, Ellis JC, Papousek I, Cizek A, Literak I (2017) Plasmid-mediated resistance to cephalosporins and quinolones in Escherichia coli from American crows in the USA. Environ Microbiol 19:2025–2036Google Scholar
  78. 78.
    Jamborova I, Janecko N, Halova D, Sedmik J, Mezerova K, Papousek I, Kutilova I, Dolejska M, Cizek A, Literak I (2018) Molecular characterization of plasmid-mediated AmpC beta-lactamase- and extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae among corvids (Corvus brachyrhynchos and Corvus corax) roosting in Canada. FEMS Microbiol Ecol 94:fiy166Google Scholar
  79. 79.
    Bevan ER, Jones AM, Hawkey PM (2017) Global epidemiology of CTX-M beta-lactamases: temporal and geographical shifts in genotype. J Antimicrob Chemother 72:2145–2155Google Scholar
  80. 80.
    Atterby C, Borjesson S, Ny S, Jarhult JD, Byfors S, Bonnedahl J (2017) ESBL-producing Escherichia coli in Swedish gulls-A case of environmental pollution from humans? PLoS One 12:e0190380Google Scholar
  81. 81.
    Atterby C, Ramey AM, Hall GG, Jarhult J, Borjesson 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 6:32334Google Scholar
  82. 82.
    Tausova D, Dolejska M, Cizek A, Hanusova L, Hrusakova J, Svoboda O, Camlik G, Literak I (2012) Escherichia coli with extended-spectrum beta-lactamase and plasmid-mediated quinolone resistance genes in great cormorants and mallards in Central Europe. J Antimicrob Chemother 67:1103–1107Google Scholar
  83. 83.
    Garmyn A, Haesebrouck F, Hellebuyck T, Smet A, Pasmans F, Butaye P, Martel A (2011) Presence of extended-spectrum beta-lactamase-producing Escherichia coli in wild geese. J Antimicrob Chemother 66:1643–1644Google Scholar
  84. 84.
    Mohsin M, Raza S, Schaufler K, Roschanski N, Sarwar F, Semmler T, Schierack P, Guenther S (2017) High prevalence of CTX-M-15-type ESBL-producing E. coil from migratory avian species in Pakistan. Front Microbiol 8:2476Google Scholar
  85. 85.
    Pinto L, Radhouani H, Coelho C, da Costa PM, Simoes R, Brandao RML, Torres C, Igrejas G, Poeta P (2010) Genetic detection of extended-spectrum beta-lactamase-containing Escherichia coli isolates from birds of prey from Serra da Estrela natural reserve in Portugal. Appl Environ Microbiol 76:4118–4120Google Scholar
  86. 86.
    Jamborova I, Dolejska M, Vojtech J, Guenther S, Uricariu R, Drozdowska J, Papousek I, Pasekova K, Meissner W, Hordowski J, Cizek A, Literak I (2015) Plasmid-mediated resistance to cephalosporins and fluoroquinolones in various Escherichia coli sequence types isolated from rooks wintering in Europe. Appl Environ Microbiol 81:648–657Google Scholar
  87. 87.
    Hasan B, Olsen B, Alam A, Akter L, Melhus A (2015) Dissemination of the multidrug-resistant extended-spectrum beta-lactamase-producing Escherichia coli O25b-ST131 clone and the role of house crow (Corvus splendens) foraging on hospital waste in Bangladesh. Clin Microbiol Infect 21:1000-e1Google Scholar
  88. 88.
    Poeta P, Radhouani H, Pinto L, Martinho A, Rego V, Rodrigues R, Goncalves A, Rodrigues J, Estepa V, Torres C, Igrejas G (2009) Wild boars as reservoirs of extended-spectrum beta-lactamase (ESBL) producing Escherichia coli of different phylogenetic groups. J Basic Microbiol 49:584–588Google Scholar
  89. 89.
    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 108:1702–1711Google Scholar
  90. 90.
    Bachiri T, Bakour S, Ladjouzi R, Thongpan L, Rolain JM, Touati A (2017) High rates of CTX-M-15-producing Escherichia coli and Klebsiella pneumoniae in wild boars and Barbary macaques in Algeria. J Glob Antimicrob Resist 8:35–40Google Scholar
  91. 91.
    Alonso CA, Alcala L, Simon C, Torres C (2017) Novel sequence types of extended-spectrum and acquired AmpC beta-lactamase producing Escherichia coli and Escherichia clade V isolated from wild mammals. FEMS Microbiol Ecol 93:fiy066Google Scholar
  92. 92.
    Ho PL, Chow KH, Lai EL, Lo WU, Yeung MK, Chan J, Chan PY, Yuen KY (2011) Extensive dissemination of CTX-M-producing Escherichia coli with multidrug resistance to ‘critically important’ antibiotics among food animals in Hong Kong, 2008-10. J Antimicrob Chemother 66:765–768Google Scholar
  93. 93.
    Ho PL, Lo WU, Lai EL, Law PY, Leung SM, Wang Y, Chow KH (2015) Clonal diversity of CTX-M-producing, multidrug-resistant Escherichia coli from rodents. J Med Microbiol 64:185–190Google Scholar
  94. 94.
    Guenther S, Bethe A, Fruth A, Semmler T, Ulrich RG, Wieler LH, Ewers C (2012) Frequent combination of antimicrobial multiresistance and extraintestinal pathogenicity in Escherichia coli Isolates from Urban Rats (Rattus norvegicus) in Berlin, Germany. PLoS One 7:e50331Google Scholar
  95. 95.
    Sola-Gines M, Gonzalez-Lopez JJ, Cameron-Veas K, Piedra-Carrasco N, Cerda-Cuellar M, Migura-Garcia L (2015) Houseflies (Musca domestica) as vectors for extended-spectrum beta-Lactamase-producing Escherichia coli on Spanish broiler farms. Appl Environ Microbiol 81:3604–3611Google Scholar
  96. 96.
    Blaak H, van Hoek AH, Hamidjaja RA, van der Plaats RQ, Kerkhof-de Heer L, de Roda Husman AM, Schets FM (2015) Distribution, numbers, and diversity of ESBL-producing E. coli in the poultry farm environment. PLoS One 10:e0135402Google Scholar
  97. 97.
    von Salviati C, Laube H, Guerra B, Roesler U, Friese A (2015) Emission of ESBL/AmpC-producing Escherichia coli from pig fattening farms to surrounding areas. Vet Microbiol 175:77–84Google Scholar
  98. 98.
    Usui M, Iwasa T, Fukuda A, Sato T, Okubo T, Tamura Y (2013) The role of flies in spreading the extended-spectrum beta-lactamase gene from cattle. Microb Drug Resist 19:415–420Google Scholar
  99. 99.
    Songe MM, Hang’ombe BM, Knight-Jones TJ, Grace D (2016) Antimicrobial resistant enteropathogenic Escherichia coli and Salmonella spp. in houseflies infesting fish in food markets in Zambia. Int J Environ Res Public Health 14:21Google Scholar
  100. 100.
    Loucif L, Gacemi-Kirane D, Cherak Z, Chamlal N, Grainat N, Rolain JM (2016) First report of German cockroaches (Blattella germanica) as reservoirs of CTX-M-15 extended-spectrum-beta-lactamase- and OXA-48 carbapenemase-producing Enterobacteriaceae in Batna University Hospital, Algeria. Antimicrob Agents Chemother 60:6377–6380Google Scholar
  101. 101.
    Brahmi S, Touati A, Dunyach-Remy C, Sotto A, Pantel A, Lavigne JP (2018) High prevalence of extended-spectrum beta-lactamase-producing enterobacteriaceae in wild fish from the Mediterranean Sea in Algeria. Microb Drug Resist 24:290–298Google Scholar
  102. 102.
    Poeta P, Radhouani H, Igrejas G, Goncalves A, Carvalho C, Rodrigues J, Vinue L, Somalo S, Torres C (2008) Seagulls of the Berlengas natural reserve of Portugal as carriers of fecal Escherichia coli harboring CTX-M and TEM extended-spectrum beta-lactamases. Appl Environ Microbiol 74:7439–7441Google Scholar
  103. 103.
    Bonnedahl J, Drobni M, Gauthier-Clerc M, Hernandez J, Granholm S, Kayser Y, Melhus A, Kahlmeter G, Waldenstrom 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:e5958Google Scholar
  104. 104.
    Dolejska M, Bierosova B, Kohoutova L, Literak I, Cizek A (2009) Antibiotic-resistant Salmonella and Escherichia coli isolates with integrons and extended-spectrum beta-lactamases in surface water and sympatric black-headed gulls. J Appl Microbiol 106:1941–1950Google Scholar
  105. 105.
    Bonnedahl J, Drobni P, Johansson A, Hernandez J, Melhus A, Stedt J, Olsen B, Drobni M (2010) Characterization, and comparison, of human clinical and black-headed gull (Larus ridibundus) extended-spectrum beta-lactamase-producing bacterial isolates from Kalmar, on the southeast coast of Sweden. J Antimicrob Chemother 65:1939–1944Google Scholar
  106. 106.
    Hernandez J, Bonnedahl J, Eliasson I, Wallensten A, Comstedt P, Johansson A, Granholm S, Melhus A, Olsen B, Drobni M (2010) Globally disseminated human pathogenic Escherichia coli of O25b-ST131 clone, harbouring blaCTX-M-15, found in Glaucous-winged gull at remote Commander Islands, Russia. Environ Microbiol Rep 2:329–332Google Scholar
  107. 107.
    Literak I, Dolejska M, Janoszowska D, Hrusakova J, Meissner W, Rzyska H, Bzoma S, Cizek A (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 76:8126–8134Google Scholar
  108. 108.
    Simoes RR, Poirel L, Da Costa PM, Nordmann P (2010) Seagulls and beaches as reservoirs for multidrug-resistant Escherichia coli. Emerg Infect Dis 16:110–112Google Scholar
  109. 109.
    Wallensten A, Hernandez J, Ardiles K, Gonzalez-Acuna D, Drobni M, Olsen B (2011) Extended spectrum beta-lactamases detected in Escherichia coli from gulls in Stockholm, Sweden. Infect Ecol Epidemiol 1:7030Google Scholar
  110. 110.
    Poirel L, Potron A, De La Cuesta C, Cleary T, Nordmann P, Munoz-Priceb LS (2012) Wild coastline birds as reservoirs of broad-spectrum-beta-lactamase-producing Enterobacteriaceae in Miami Beach, Florida. Antimicrob Agents Chemother 56:2756–2758Google Scholar
  111. 111.
    Hernandez J, Johansson A, Stedt J, Bengtsson S, Porczak A, Granholm S, Gonzalez-Acuna D, Olsen B, Bonnedahl J, Drobni M (2013) Characterization and comparison of extended-spectrum beta-lactamase (ESBL) resistance genotypes and population structure of Escherichia coli isolated from Franklin’s gulls (Leucophaeus pipixcan) and humans in Chile. PLoS One 8:e76150Google Scholar
  112. 112.
    Veldman K, van Tulden P, Kant A, Testerink J, Mevius D (2013) Characteristics of cefotaxime-resistant Escherichia coli from wild birds in the Netherlands. Appl Environ Microbiol 79:7556–7561Google Scholar
  113. 113.
    Bonnedahl J, Hernandez J, Stedt J, Waldenstrom J, Olsen B, Drobni M (2014) Extended-spectrum beta-lactamases in Escherichia coli and Klebsiella pneumoniae in Gulls, Alaska, USA. Emerg Infect Dis 20:897–899Google Scholar
  114. 114.
    Hasan B, Melhus A, Sandegren L, Alam M, Olsen B (2014) The gull (Chroicocephalus brunnicephalus) as an environmental bioindicator and reservoir for antibiotic resistance on the coastlines of the Bay of Bengal. Microb Drug Resist 20:466–471Google Scholar
  115. 115.
    Baez J, Hernandez-Garcia M, Guamparito C, Diaz S, Olave A, Guerrero K, Canton R, Baquero F, Gahona J, Valenzuela N, Del Campo R, Silva J (2015) Molecular characterization and genetic diversity of ESBL-producing Escherichia coli colonizing the migratory Franklin’s gulls (Leucophaeus pipixcan) in Antofagasta, North of Chile. Microb Drug Resist 21:111–116Google Scholar
  116. 116.
    Stedt J, Bonnedahl J, Hernandez J, Waldenstrom J, McMahon BJ, Tolf C, Olsen B, Drobni M (2015) Carriage of CTX-M type extended spectrum beta-lactamases (ESBLs) in gulls across Europe. Acta Vet Scand 57:74Google Scholar
  117. 117.
    Vergara A, Pitart C, Montalvo T, Roca I, Sabate S, Carlos Hurtado J, Planell R, Marco F, Ramirez B, Peracho V, de Simon M, Vila J (2017) Prevalence of extended-spectrum-beta-lactamase- and/or carbapenemase-producing Escherichia coli Isolated from yellow-legged gulls from Barcelona, Spain. Antimicrob Agents Chemother 61:e02071-16Google Scholar
  118. 118.
    Mukerji S, Stegger M, Truswell AV, Laird T, Jordan D, Abraham RJ, Harb A, Barton M, O’Dea M, Abraham S (2019) Resistance to critically important antimicrobials in Australian silver gulls (Chroicocephalus novaehollandiae) and evidence of anthropogenic origins. J Antimicrob Chemother 74(9):2566–2574Google Scholar
  119. 119.
    Bonomo RA, Burd EM, Conly J, Limbago BM, Poirel L, Segre JA, Westblade LF (2018) Carbapenemase-producing organisms: a global scourge. Clin Infect Dis 66:1290–1297Google Scholar
  120. 120.
    Koeck R, Daniels-Haardt I, Becker K, Mellmann A, Friedrich AW, Mevius D, Schwarz S, Jurke A (2018) Carbapenem-resistant Enterobacteriaceae in wildlife, food-producing, and companion animals: a systematic review. Clin Microbiol Infect 24:1241–1250Google Scholar
  121. 121.
    Khan FA, Soderquist B, Jass J (2019) Prevalence and diversity of antibiotic resistance genes in Swedish aquatic environments impacted by household and hospital wastewater. Front Microbiol 10:688Google Scholar
  122. 122.
    Diab M, Hamze M, Bonnet R, Saras E, Madec JY, Haenni M (2018) Extended-spectrum beta-lactamase (ESBL)- and carbapenemase-producing Enterobacteriaceae in water sources in Lebanon. Vet Microbiol 217:97–103Google Scholar
  123. 123.
    Walsh TR, Weeks J, Livermore DM, Toleman MA (2011) Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect Dis 11:355–362Google Scholar
  124. 124.
    Cahill N, O’Connor L, Mahon B, Varley A, McGrath E, Ryan P, Cormican M, Brehony C, Jolley KA, Maiden MC, Brisse S, Morris D (2019) Hospital effluent: a reservoir for carbapenemase-producing Enterobacterales? Sci Total Environ 672:618–624Google Scholar
  125. 125.
    Fischer J, Schmoger S, Jahn S, Helmuth R, Guerra B (2013) NDM-1 carbapenemase-producing Salmonella enterica subsp enterica serovar Corvallis isolated from a wild bird in Germany. J Antimicrob Chemother 68:2954–2956Google Scholar
  126. 126.
    Vittecoq M, Laurens C, Brazier L, Durand P, Elguero E, Arnal A, Thomas F, Aberkane S, Renaud N, Prugnolle F, Solassol J, Jean-Pierre H, Godreuil S, Renaud F (2017) VIM-1 carbapenemase-producing Escherichia coli in gulls from southern France. Ecol Evol 7:1224–1232Google Scholar
  127. 127.
    Aberkane S, Compain F, Barraud O, Ouedraogo AS, Bouzinbi N, Vittecoq M, Jean-Pierre H, Decre D, Godreuil S (2015) Non-O1/Non-O139 Vibrio cholerae Avian isolate from France cocarrying the bla(VIM-1) and bla(VIM-4) Genes. Antimicrob Agents Chemother 59:6594–6596Google Scholar
  128. 128.
    Bachiri T, Bakour S, Lalaoui R, Belkebla N, Allouache M, Rolain JM, Touati A (2018) Occurrence of carbapenemase-producing Enterobacteriaceae isolates in the wildlife: first report of OXA-48 in Wild Boars in Algeria. Microb Drug Resist 24:337–345Google Scholar
  129. 129.
    Oteo J, Mencia A, Bautista V, Pastor N, Lara N, Gonzalez-Gonzalez F, Garcia-Pena FJ, Campos J (2018) Colonization with Enterobacteriaceae-producing ESBLs, AmpCs, and OXA-48 in Wild Avian Species, Spain 2015-2016. Microb Drug Resist 24:932–938Google Scholar
  130. 130.
    Wang Y, Zhang R, Li J, Wu Z, Yin W, Schwarz S, Tyrrell JM, Zheng Y, Wang S, Shen Z, Liu Z, Liu J, Lei L, Li M, Zhang Q, Wu C, Zhang Q, Wu Y, Walsh TR, Shen J (2017) Comprehensive resistome analysis reveals the prevalence of NDM and MCR-1 in Chinese poultry production. Nat Microbiol 2:16260Google Scholar
  131. 131.
    Fischer J, San Jose M, Roschanski N, Schmoger S, Baumann B, Irrgang A, Friese A, Roesler U, Helmuth R, Guerra B (2017) Spread and persistence of VIM-1 Carbapenemase-producing Enterobacteriaceae in three German swine farms in 2011 and 2012. Vet Microbiol 200:118–123Google Scholar
  132. 132.
    Guenther S, Semmler T, Stubbe A, Stubbe M, Wieler LH, Schaufler K (2017) Chromosomally encoded ESBL genes in Escherichia coli of ST38 from Mongolian wild birds. J Antimicrob Chemother 72:1310–1313Google Scholar
  133. 133.
    Ahlstrom CA, Ramey AM, Woksepp H, Bonnedahl J (2019) Repeated detection of carbapenemase-producing Escherichia coli in gulls inhabiting Alaska, USA. Antimicrob Agents Chemother 63:e00758–e00719Google Scholar
  134. 134.
    Poirel L, Jayol A, Nordmann P (2017) Polymyxins: antibacterial activity, susceptibility testing, and resistance mechanisms encoded by plasmids or chromosomes. Clin Microbiol Rev 30:557–596Google Scholar
  135. 135.
    EMA (2016) European Medicines Agency. Updated advice on the use of colistin products in animals within the European Union: development of resistance and possible impact on human and animal health. EMA, LondonGoogle Scholar
  136. 136.
    Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu JH, Shen J (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 16:161–168Google Scholar
  137. 137.
    Falagas ME, Kasiakou SK (2005) Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clin Infect Dis 40:1333–1341Google Scholar
  138. 138.
    Cizmeci Z, Aktas E, Otlu B (2017) Molecular characterization of carbapenem- resistant Enterobacteriaceae yields increasing rates of NDM-1 carbapenemases and colistin resistance in an OXA-48- endemic area. J Chemother 29:344–350Google Scholar
  139. 139.
    Pena I, Picazo JJ, Rodriguez-Avial C, Rodriguez-Avial I (2014) Carbapenemase-producing Enterobacteriaceae in a tertiary hospital in Madrid, Spain: high percentage of colistin resistance among VIM-1-producing Klebsiella pneumoniae ST11 isolates. Int J Antimicrob Agents 43:460–464Google Scholar
  140. 140.
    Bakthavatchalam YD, Pragasam AK, Biswas I, Veeraraghavan B (2018) Polymyxin susceptibility testing, interpretative breakpoints and resistance mechanisms: An update. J Glob Antimicrob Resist 12:124–136Google Scholar
  141. 141.
    Walsh TR, Wu Y (2016) China bans colistin as a feed additive for animals. Lancet Infect Dis 16:1102–1103Google Scholar
  142. 142.
    Sun J, Zhang H, Liu YH, Feng Y (2018) Towards understanding MCR-like colistin resistance. Trends Microbiol 26:794–808Google Scholar
  143. 143.
    Yang YQ, Li YX, Lei CW, Zhang AY, Wang HN (2018) Novel plasmid-mediated colistin resistance gene mcr-7.1 in Klebsiella pneumoniae. J Antimicrob Chemother 73:1791–1795Google Scholar
  144. 144.
    Wang X, Wang Y, Zhou Y, Li J, Yin W, Wang S (2018) Emergence of a novel mobile colistin resistance gene, mcr-8, in NDM-producing Klebsiella pneumoniae. Emerg Microbes Infect 7:122Google Scholar
  145. 145.
    Ruzauskas M, Vaskeviciute L (2016) Detection of the mcr-1 gene in Escherichia coli prevalent in the migratory bird species Larus argentatus. J Antimicrob Chemother 71:2333–2334Google Scholar
  146. 146.
    Liakopoulos A, Mevius DJ, Olsen B, Bonnedahl J (2016) The colistin resistance mcr-1 gene is going wild. J Antimicrob Chemother 71:2335–2336Google Scholar
  147. 147.
    Quiroga C, Nastro M, Di Conza J (2019) Current scenario of plasmid-mediated colistin resistance in Latin America. Rev Argent Microbiol 51:93–100Google Scholar
  148. 148.
    Bachiri T, Lalaoui R, Bakour S, Allouache M, Belkebla N, Rolain JM, Touati A (2018) First report of the plasmid-mediated colistin resistance gene mcr-1 in Escherichia coli ST405 Isolated from Wildlife in Bejaia, Algeria. Microb Drug Resist 24:890–895Google Scholar
  149. 149.
    Mohsin M, Raza S, Roschanski N, Schaufler K, Guenther S (2016) First description of plasmid-mediated colistin-resistant extended-spectrum beta-lactamase-producing Escherichia coli in a wild migratory bird from Asia. Int J Antimicrob Agents 48:463–464Google Scholar
  150. 150.
    Tarabai H, Valcek A, Jamborova I, Vazhov SV, Karyakin IV, Raab R, Literak I, Dolejska M (2019) Plasmid-mediated mcr-1 colistin resistance in Escherichia coli from a Black Kite in Russia. Antimicrob Agents Chemother 63(9):e01266-19Google Scholar
  151. 151.
    Shen Z, Wang Y, Shen Y, Shen J, Wu C (2016) Early emergence of mcr-1 in Escherichia coli from food-producing animals. Lancet Infect Dis 16:293Google Scholar
  152. 152.
    Yang QE, Tansawai U, Andrey DO, Wang S, Wang Y, Sands K, Kiddee A, Assawatheptawee K, Bunchu N, Hassan B, Walsh TR, Niumsup PR (2019) Environmental dissemination of mcr-1 positive Enterobacteriaceae by Chrysomya spp. (common blowfly): An increasing public health risk. Environ Int 122:281–290Google Scholar
  153. 153.
    Zhang J, Wang J, Chen L, Yassin AK, Kelly P, Butaye P, Li J, Gong J, Cattley R, Qi K, Wang C (2018) Housefly (Musca domestica) and Blow Fly (Protophormia terraenovae) as vectors of bacteria carrying colistin resistance genes. Appl Environ Microbiol 84:e01736-17Google Scholar
  154. 154.
    Sellera FP, Fernandes MR, Sartori L, Carvalho MP, Esposito F, Nascimento CL, Dutra GH, Mamizuka EM, Perez-Chaparro PJ, McCulloch JA, Lincopan N (2017) Escherichia coli carrying IncX4 plasmid-mediated mcr-1 and blaCTX-M genes in infected migratory Magellanic penguins (Spheniscus magellanicus). J Antimicrob Chemother 72:1255–1256Google Scholar
  155. 155.
    Wu J, Huang Y, Rao D, Zhang Y, Yang K (2018) Evidence for environmental dissemination of antibiotic resistance mediated by wild birds. Front Microbiol 9:745Google Scholar
  156. 156.
    Aeksiri N, Toanan W, Sawikan S, Suwannarit R, Pungpomin P, Khieokhajonkhet A, Niumsup PR (2019) First detection and genomic insight into mcr-1 encoding plasmid-mediated colistin-resistance gene in Escherichia coli ST101 Isolated from the migratory bird species Hirundo rustica in Thailand. Microb Drug Resist 25(10):1437–1144Google Scholar
  157. 157.
    Ahlstrom CA, Ramey AM, Woksepp H, Bonnedahl J (2019) Early emergence of mcr-1-positive Enterobacteriaceae in gulls from Spain and Portugal. Environ Microbiol Rep 11(5):669–671Google Scholar
  158. 158.
    Jacoby GA, Strahilevitz J, Hooper DC (2014) Plasmid-mediated quinolone resistance. Microbiol Spectr 2:685–711Google Scholar
  159. 159.
    Veldman K, Cavaco LM, Mevius D, Battisti A, Franco A, Botteldoorn N, Bruneau M, Perrin-Guyomard A, Cerny T, De Frutos Escobar C, Guerra B, Schroeter A, Gutierrez M, Hopkins K, Myllyniemi AL, Sunde M, Wasyl D, Aarestrup FM (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 66:1278–1286Google Scholar
  160. 160.
    Dotto G, Giacomelli M, Grilli G, Ferrazzi V, Carattoli A, Fortini D, Piccirillo A (2014) High prevalence of oqxAB in Escherichia coli isolates from domestic and wild lagomorphs in Italy. Microb Drug Resist 20:118–123Google Scholar
  161. 161.
    Oh JY, Kwon YK, Tamang MD, Jang HK, Jeong OM, Lee HS, Kang MS (2016) Plasmid-mediated quinolone resistance in Escherichia coli Isolates from wild birds and chickens in South Korea. Microb Drug Resist 22:69–79Google Scholar
  162. 162.
    Literak I, Micudova M, Tausova D, Cizek A, Dolejska M, Papousek I, Prochazka J, Vojtech J, Borleis F, Guardone L, Guenther S, Hordowski J, Lejas C, Meissner W, Marcos BF, Tucakov M (2012) Plasmid-mediated quinolone resistance genes in fecal bacteria from rooks commonly wintering throughout Europe. Microb Drug Resist 18:567–573Google Scholar
  163. 163.
    Halova D, Papousek I, Jamborova I, Masarikova M, Cizek A, Janecko N, Oravcova V, Zurek L, Clark AB, Townsend A, Ellis JC, Literak I (2014) Plasmid-mediated quinolone resistance genes in Enterobacteriaceae from American crows: high prevalence of bacteria with variable qnrB genes. Antimicrob Agents Chemother 58:1257–1258Google Scholar
  164. 164.
    Wasyl D, Zajac M, Lalak A, Skarzynska M, Samcik I, Kwit R, Jablonski A, Bocian L, Wozniakowski G, Hoszowski A, Szulowski K (2018) Antimicrobial resistance in Escherichia coli isolated from wild animals in Poland. Microb Drug Resist 24:807–815Google Scholar
  165. 165.
    Wasyl D (2014) Prevalence and characterization of quinolone resistance mechanisms in commensal Escherichia coli isolated from slaughter animals in Poland, 2009-2012. Microb Drug Resist 20:544–549Google Scholar
  166. 166.
    Roderova M, Halova D, Papousek I, Dolejska M, Masarikova M, Hanulik V, Pudova V, Broz P, Htoutou-Sedlakova M, Sauer P, Bardon J, Cizek A, Kolar M, Literak I (2016) Characteristics of quinolone resistance in Escherichia coli isolates from humans, animals, and the environment in the Czech Republic. Front Microbiol 7:2147Google Scholar
  167. 167.
    Literak I, Reitschmied T, Bujnakova D, Dolejska M, Cizek A, Bardon J, Pokludova L, Alexa P, Halova D, Jamborova I (2013) Broilers as a source of quinolone-resistant and extraintestinal pathogenic Escherichia coli in the Czech Republic. Microb Drug Resist 19:57–63Google Scholar
  168. 168.
    Courvalin P (2006) Vancomycin resistance in gram-positive cocci. Clin Infect Dis 42(Suppl 1):S25–S34Google Scholar
  169. 169.
    Xu X, Lin D, Yan G, Ye X, Wu S, Guo Y, Zhu D, Hu F, Zhang Y, Wang F, Jacoby GA, Wang M (2010) vanM, a new glycopeptide resistance gene cluster found in Enterococcus faecium. Antimicrob Agents Chemother 54:4643–4647Google Scholar
  170. 170.
    Nilsson O (2012) Vancomycin resistant enterococci in farm animals – occurrence and importance. Infect Ecol Epidemiol 2:16959Google Scholar
  171. 171.
    Klare I, Badstubner D, Konstabel C, Bohme G, Claus H, Witte W (1999) Decreased incidence of VanA-type vancomycin-resistant enterococci isolated from poultry meat and from fecal samples of humans in the community after discontinuation of avoparcin usage in animal husbandry. Microb Drug Resist 5:45–52Google Scholar
  172. 172.
    Ahmed MO, Baptiste KE (2018) Vancomycin-resistant Enterococci: a review of antimicrobial resistance mechanisms and perspectives of human and animal health. Microb Drug Resist 24:590–606Google Scholar
  173. 173.
    Guzman Prieto AM, van Schaik W, Rogers MR, Coque TM, Baquero F, Corander J, Willems RJ (2016) Global emergence and dissemination of Enterococci as Nosocomial Pathogens: attack of the clones? Front Microbiol 7:788Google Scholar
  174. 174.
    Radhouani H, Pinto L, Coelho C, Sargo R, Araujo C, Lopez M, Torres C, Igrejas G, Poeta P (2010) MLST and a genetic study of antibiotic resistance and virulence factors in vanA-containing Enterococcus from buzzards (Buteo buteo). Lett Appl Microbiol 50:537–541Google Scholar
  175. 175.
    Radhouani H, Poeta P, Pinto L, Miranda J, Coelho C, Carvalho C, Rodrigues J, Lopez M, Torres C, Vitorino R, Domingues P, Igrejas G (2010) Proteomic characterization of vanA-containing Enterococcus recovered from Seagulls at the Berlengas Natural Reserve, W Portugal. Proteome Sci 8:48Google Scholar
  176. 176.
    Silva N, Igrejas G, Rodrigues P, Rodrigues T, Goncalves A, Felgar AC, Pacheco R, Goncalves D, Cunha R, Poeta P (2011) Molecular characterization of vancomycin-resistant enterococci and extended-spectrum beta-lactamase-containing Escherichia coli isolates in wild birds from the Azores Archipelago. Avian Pathol 40:473–479Google Scholar
  177. 177.
    Sellin M, Palmgren H, Broman T, Bergstrom S, Olsen B (2000) Involving ornithologists in the surveillance of vancomycin-resistant enterococci. Emerg Infect Dis 6:87–88Google Scholar
  178. 178.
    Silva V, Igrejas G, Carvalho I, Peixoto F, Cardoso L, Pereira JE, Del Campo R, Poeta P (2018) Genetic characterization of vanA-Enterococcus faecium isolates from wild red-legged partridges in Portugal. Microb Drug Resist 24:89–94Google Scholar
  179. 179.
    Oravcova V, Ghosh A, Zurek L, Bardon J, Guenther S, Cizek A, Literak I (2013) Vancomycin-resistant enterococci in rooks (Corvus frugilegus) wintering throughout Europe. Environ Microbiol 15:548–556Google Scholar
  180. 180.
    Coque TM, Tomayko JF, Ricke SC, Okhyusen PC, Murray BE (1996) Vancomycin-resistant enterococci from nosocomial, community, and animal sources in the United States. Antimicrob Agents Chemother 40:2605–2609Google Scholar
  181. 181.
    Rana SW, Kumar A, Walia SK, Berven K, Cumper K, Walia SK (2011) Isolation of Tn1546-like elements in vancomycin-resistant Enterococcus faecium isolated from wood frogs: an emerging risk for zoonotic bacterial infections to humans. J Appl Microbiol 110:35–43Google Scholar
  182. 182.
    Oravcova V, Zurek L, Townsend A, Clark AB, Ellis JC, Cizek A, Literak I (2014) American crows as carriers of vancomycin-resistant enterococci with vanA gene. Environ Microbiol 16:939–949Google Scholar
  183. 183.
    Ghosh A, Kukanich K, Brown CE, Zurek L (2012) Resident cats in small animal veterinary hospitals carry multi-drug resistant Enterococci and are likely involved in cross-contamination of the hospital environment. Front Microbiol 3:62Google Scholar
  184. 184.
    CDDEP (2013) CDDEP – The Center for Disease Dynamics, Economics and Policy (2013) Maps of regional trends – Vancomycin-resistant Enterococcus. CDDEP, Washington. URL: http://www.cddep.org/resistancemap/bug-drug/VRE#.UUc2G6zcB3sGoogle Scholar
  185. 185.
    Gandra S, Barysauskas CM, Mack DA, Barton B, Finberg R, Ellison 3rd RT (2014) Impact of contact precautions on falls, pressure ulcers and transmission of MRSA and VRE in hospitalized patients. J Hosp Infect 88:170–176Google Scholar
  186. 186.
    Roberts MC, No DB, Marzluff JM, Delap JH, Turner R (2016) Vancomycin resistant Enterococcus spp. from crows and their environment in metropolitan Washington State, USA: Is there a correlation between VRE positive crows and the environment? Vet Microbiol 194:48–54Google Scholar
  187. 187.
    Drobni M, Bonnedahl J, Hernandez J, Haemig P, Olsen B (2009) Vancomycin-resistant enterococci, Point Barrow, Alaska, USA. Emerg Infect Dis 15:838–839Google Scholar
  188. 188.
    Poeta P, Costa D, Igrejas G, Rojo-Bezares B, Saenz Y, Zarazaga M, Ruiz-Larrea F, Rodrigues J, Torres C (2007) Characterization of vanA-containing Enterococcus faecium isolates carrying Tn5397-like and Tn916/Tn1545-like transposons in wild boars (Sus Scrofa). Microb Drug Resist 13:151–156Google Scholar
  189. 189.
    Lozano C, Gonzalez-Barrio D, Garcia JT, Ceballos S, Olea PP, Ruiz-Fons F, Torres C (2015) Detection of vancomycin-resistant Enterococcus faecalis ST6-vanB2 and E. faecium ST915-vanA in faecal samples of wild Rattus rattus in Spain. Vet Microbiol 177:168–174Google Scholar
  190. 190.
    Turner NA, Sharma-Kuinkel BK, Maskarinec SA, Eichenberger EM, Shah PP, Carugati M, Holland TL, Fowler Jr VG (2019) Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nat Rev Microbiol 17:203–218Google Scholar
  191. 191.
    Aires-de-Sousa M (2017) Methicillin-resistant Staphylococcus aureus among animals: current overview. Clin Microbiol Infect 23:373–380Google Scholar
  192. 192.
    Katayama Y, Ito T, Hiramatsu K (2000) A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 44:1549–1555Google Scholar
  193. 193.
    Garcia-Alvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, Walpole E, Brooks K, Pickard DJ, Teale C, Parkhill J, Bentley SD, Edwards GF, Girvan EK, Kearns AM, Pichon B, Hill RL, Larsen AR, Skov RL, Peacock SJ, Maskell DJ, Holmes MA (2011) Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis 11:595–603Google Scholar
  194. 194.
    Nowakiewicz A, Ziolkowska G, Zieba P, Gnat S, Wojtanowicz-Markiewicz K, Troscianczyk A (2016) Coagulase-positive Staphylococcus isolated from wildlife: Identification, molecular characterization and evaluation of resistance profiles with focus on a methicillin-resistant strain. Comp Immunol Microbiol Infect Dis 44:21–28Google Scholar
  195. 195.
    Carson M, Meredith AL, Shaw DJ, Giotis ES, Lloyd DH, Loeffler A (2012) Foxes as a potential wildlife reservoir for mecA-positive Staphylococci. Vector Borne Zoonotic Dis 12:583–587Google Scholar
  196. 196.
    Monecke S, Gavier-Widen D, Hotzel H, Peters M, Guenther S, Lazaris A, Loncaric I, Muller E, Reissig A, Ruppelt-Lorz A, Shore AC, Walter B, Coleman DC, Ehricht R (2016) Diversity of Staphylococcus aureus isolates in European Wildlife. PLoS One 11:e0168433Google Scholar
  197. 197.
    Kmet V, Cuvalova A, Stanko M (2018) Small mammals as sentinels of antimicrobial-resistant staphylococci. Folia Microbiol (Praha) 63:665–668Google Scholar
  198. 198.
    Sousa M, Silva N, Manageiro V, Ramos S, Coelho A, Goncalves D, Canica M, Torres C, Igrejas G, Poeta P (2017) First report on MRSA CC398 recovered from wild boars in the north of Portugal. Are we facing a problem? Sci Total Environ 596–597:26–31Google Scholar
  199. 199.
    Wardyn SE, Kauffman LK, Smith TC (2012) Methicillin-resistant Staphylococcus aureus in central Iowa wildlife. J Wildl Dis 48:1069–1073Google Scholar
  200. 200.
    Gomez P, Gonzalez-Barrio D, Benito D, Garcia JT, Vinuela J, Zarazaga M, Ruiz-Fons F, Torres C (2014) Detection of methicillin-resistant Staphylococcus aureus (MRSA) carrying the mecC gene in wild small mammals in Spain. J Antimicrob Chemother 69:2061–2064Google Scholar
  201. 201.
    Gomez P, Lozano C, Gonzalez-Barrio D, Zarazaga M, Ruiz-Fons F, Torres C (2015) High prevalence of methicillin-resistant Staphylococcus aureus (MRSA) carrying the mecC gene in a semi-extensive red deer (Cervus elaphus hispanicus) farm in Southern Spain. Vet Microbiol 177:326–331Google Scholar
  202. 202.
    Loncaric I, Kubber-Heiss A, Posautz A, Stalder GL, Hoffmann D, Rosengarten R, Walzer C (2014) mecC- and mecA-positive meticillin-resistant Staphylococcus aureus (MRSA) isolated from livestock sharing habitat with wildlife previously tested positive for mecC-positive MRSA. Vet Dermatol 25:147–148Google Scholar
  203. 203.
    Monecke S, Gavier-Widen D, Mattsson R, Rangstrup-Christensen L, Lazaris A, Coleman DC, Shore AC, Ehricht R (2013) Detection of mecC-positive Staphylococcus aureus (CC130-MRSA-XI) in diseased European hedgehogs (Erinaceus europaeus) in Sweden. PLoS One 8:e66166Google Scholar
  204. 204.
    Mrochen DM, Schulz D, Fischer S, Jeske K, El Gohary H, Reil D, Imholt C, Trube P, Suchomel J, Tricaud E, Jacob J, Heroldova M, Broker BM, Strommenger B, Walther B, Ulrich RG, Holtfreter S (2018) Wild rodents and shrews are natural hosts of Staphylococcus aureus. Int J Med Microbiol 308:590–597Google Scholar
  205. 205.
    Loncaric I, Kubber-Heiss A, Posautz A, Stalder GL, Hoffmann D, Rosengarten R, Walzer C (2013) Characterization of methicillin-resistant Staphylococcus spp. carrying the mecC gene, isolated from wildlife. J Antimicrob Chemother 68:2222–2225Google Scholar
  206. 206.
    Bengtsson B, Persson L, Ekstrom K, Unnerstad HE, Uhlhorn H, Borjesson S (2017) High occurrence of mecC-MRSA in wild hedgehogs (Erinaceus europaeus) in Sweden. Vet Microbiol 207:103–107Google Scholar
  207. 207.
    McDermott PF, Zhao S, Tate H (2018) Antimicrobial resistance in Nontyphoidal Salmonella. In: Schwarz S, Cavaco LM, Shen J (eds) Antimicrobial resistance in bacteria from livestock and companion animals. ASM Press, Washington DC, p 400Google Scholar
  208. 208.
    Gopee NV, Adesiyun AA, Caesar K (2000) Retrospective and longitudinal study of salmonellosis in captive wildlife in Trinidad. J Wildl Dis 36:284–293Google Scholar
  209. 209.
    Refsum T, Handeland K, Baggesen DL, Holstad G, Kapperud G (2002) Salmonellae in avian wildlife in Norway from 1969 to 2000. Appl Environ Microbiol 68:5595–5599Google Scholar
  210. 210.
    Methner U, Merbach S, Peters M (2018) Salmonella enterica subspecies enterica serovar Choleraesuis in a German wild boar population: occurrence and characterisation. Acta Vet Scand 60:65Google Scholar
  211. 211.
    Kocabiyik AL, Cangul IT, Alasonyalilar A, Dedicova D, Karpiskova R (2006) Isolation of Salmonella Enteritidis phage type 21b from a Eurasian eagle-owl (Bubo bubo). J Wildl Dis 42:696–698Google Scholar
  212. 212.
    Molina-Lopez RA, Valverdu N, Martin M, Mateu E, Obon E, Cerda-Cuellar M, Darwich L (2011) Wild raptors as carriers of antimicrobial-resistant Salmonella and Campylobacter strains. Vet Rec 168:565Google Scholar
  213. 213.
    Daoust PY, Busby DG, Ferns L, Goltz J, McBurney S, Poppe C, Whitney H (2000) Salmonellosis in songbirds in the Canadian Atlantic provinces during winter-summer 1997-98. Can Vet J 41:54–59Google Scholar
  214. 214.
    Hudson CR, Quist C, Lee MD, Keyes K, Dodson SV, Morales C, Sanchez S, White DG, Maurer JJ (2000) Genetic relatedness of Salmonella isolates from nondomestic birds in Southeastern United States. J Clin Microbiol 38:1860–1865Google Scholar
  215. 215.
    Perez J, Astorga R, Carrasco L, Mendez A, Perea A, Sierra MA (1999) Outbreak of salmonellosis in farmed European wild boars (Sus scrofa ferus). Vet Rec 145:464–465Google Scholar
  216. 216.
    Simpson KMJ, Hill-Cawthorne GA, Ward MP, Mor SM (2018) Diversity of Salmonella serotypes from humans, food, domestic animals and wildlife in New South Wales, Australia. BMC Infect Dis 18:623Google Scholar
  217. 217.
    Alley MR, Connolly JH, Fenwick SG, Mackereth GF, Leyland MJ, Rogers LE, Haycock M, Nicol C, Reed CE (2002) An epidemic of salmonellosis caused by Salmonella Typhimurium DT160 in wild birds and humans in New Zealand. N Z Vet J 50:170–176Google Scholar
  218. 218.
    Kapperud G, Stenwig H, Lassen J (1998) Epidemiology of Salmonella typhimurium O:4-12 infection in Norway: evidence of transmission from an avian wildlife reservoir. Am J Epidemiol 147:774–782Google Scholar
  219. 219.
    Ashbolt R, Kirk MD (2006) Salmonella Mississippi infections in Tasmania: the role of native Australian animals and untreated drinking water. Epidemiol Infect 134:1257–1265Google Scholar
  220. 220.
    Andres-Barranco S, Vico JP, Garrido V, Samper S, Herrera-Leon S, de Frutos C, Mainar-Jaime RC (2014) Role of wild bird and rodents in the epidemiology of subclinical salmonellosis in finishing pigs. Foodborne Pathog Dis 11:689–697Google Scholar
  221. 221.
    Umali DV, Lapuz RR, Suzuki T, Shirota K, Katoh H (2012) Transmission and shedding patterns of Salmonella in naturally infected captive wild roof rats (Rattus rattus) from a Salmonella-contaminated layer farm. Avian Dis 56:288–294Google Scholar
  222. 222.
    Fenlon DR (1981) Seagulls (Larus spp.) as vectors of salmonellae: an investigation into the range of serotypes and numbers of salmonellae in gull faeces. Epidemiol Infect 86:195–202Google Scholar
  223. 223.
    Migura-Garcia L, Ramos R, Cerda-Cuellar M (2017) Antimicrobial resistance of Salmonella Serovars and Campylobacter spp. isolated from an opportunistic gull species, Yellow-legged Gull (Larus michahellis). J Wildl Dis 53:148–152Google Scholar
  224. 224.
    Masarikova M, Manga I, Cizek A, Dolejska M, Oravcova V, Myskova P, Karpiskova R, Literak I (2016) Salmonella enterica resistant to antimicrobials in wastewater effluents and black-headed gulls in the Czech Republic, 2012. Sci Total Environ 542:102–107Google Scholar
  225. 225.
    Palmgren H, Aspan A, Broman T, Bengtsson K, Blomquist L, Bergstrom S, Sellin M, Wollin R, Olsen B (2006) Salmonella in Black-headed gulls (Larus ridibundus); prevalence, genotypes and influence on Salmonella epidemiology. Epidemiol Infect 134:635–644Google Scholar
  226. 226.
    Antilles N, Garcia-Migura L, Joensen KG, Leekitcharoenphon P, Aarestrup FM, Cerda-Cuellar M, Hendriksen RS (2015) Audouin’s gull, a potential vehicle of an extended spectrum beta-lactamase producing Salmonella Agona. FEMS Microbiol Lett 362:1–4Google Scholar
  227. 227.
    Blanco G (2018) Supplementary feeding as a source of multiresistant Salmonella in endangered Egyptian vultures. Transbound Emerg Dis 65:806–816Google Scholar
  228. 228.
    Botti V, Navillod FV, Domenis L, Orusa R, Pepe E, Robetto S, Guidetti C (2013) Salmonella spp. and antibiotic-resistant strains in wild mammals and birds in north-western Italy from 2002 to 2010. Vet Ital 49:195–202Google Scholar
  229. 229.
    Zottola T, Montagnaro S, Magnapera C, Sasso S, De Martino L, Bragagnolo A, D’Amici L, Condoleo R, Pisanelli G, Iovane G, Pagnini U (2013) Prevalence and antimicrobial susceptibility of salmonella in European wild boar (Sus scrofa); Latium Region – Italy. Comp Immunol Microbiol Infect Dis 36:161–168Google Scholar
  230. 230.
    Caleja C, de Toro M, Goncalves A, Themudo P, Vieira-Pinto M, Monteiro D, Rodrigues J, Saenz Y, Carvalho C, Igrejas G, Torres C, Poeta P (2011) Antimicrobial resistance and class I integrons in Salmonella enterica isolates from wild boars and Bisaro pigs. Int Microbiol 14:19–24Google Scholar
  231. 231.
    van den Bogaard AE, Stobberingh EE (2000) Epidemiology of resistance to antibiotics. Links between animals and humans. Int J Antimicrob Agents 14:327–335Google Scholar
  232. 232.
    Dale AP, Woodford N (2015) Extra-intestinal pathogenic Escherichia coli (ExPEC): disease, carriage and clones. J Infect 71:615–626Google Scholar
  233. 233.
    Rwego IB, Isabirye-Basuta G, Gillespie TR, Goldberg TL (2008) Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conserv Biol 22:1600–1607Google Scholar
  234. 234.
    Fratamico PM, DebRoy C, Liu Y, Needleman DS, Baranzoni GM, Feng P (2016) Advances in molecular serotyping and subtyping of Escherichia coli. Front Microbiol 7:644Google Scholar
  235. 235.
    Jamborova I, Johnston BD, Papousek I, Kachlikova K, Micenkova L, Clabots C, Skalova A, Chudejova K, Dolejska M, Literak I, Johnson JR (2018) Extensive genetic commonality among wildlife, wastewater, community, and nosocomial isolates of Escherichia coli sequence Type 131 (H30R1 and H30Rx Subclones) that carry blaCTX-M-27 or blaCTX-M-15. Antimicrob Agents Chemother 62:e00519-18Google Scholar
  236. 236.
    Ewers C, Bethe A, Semmler T, Guenther S, Wieler LH (2012) Extended-spectrum ss-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin Microbiol Infect 18:646–655Google Scholar
  237. 237.
    Schaufler K, Nowak K, Duex A, Semmler T, Villa L, Kourouma L, Bangoura K, Wieler LH, Leendertz FH, Guenther S (2018) Clinically relevant ESBL-producing K. pneumoniae ST307 and E. coli ST38 in an Urban West African Rat Population. Front Microbiol 9:150Google Scholar
  238. 238.
    Schaufler K, Semmler T, Wieler LH, Woehrmann M, Baddam R, Ahmed N, Mueller K, Kola A, Fruth A, Ewers C, Guenther S (2016) Clonal spread and interspecies transmission of clinically relevant ESBL-producing Escherichia coli of ST410-another successful pandemic clone? FEMS Microbiol Ecol 92:fiv155Google Scholar
  239. 239.
    Literak I, Dolejska M, Rybarikova J, Cizek A, Strejckova P, Vyskocilova M, Friedman M, Klimes J (2009) Highly variable patterns of antimicrobial resistance in commensal Escherichia coli isolates from pigs, sympatric rodents, and flies. Microb Drug Resist 15:229–237Google Scholar
  240. 240.
    Schurch AC, van Schaik W (2017) Challenges and opportunities for whole-genome sequencing-based surveillance of antibiotic resistance. Ann N Y Acad Sci 1388:108–120Google Scholar
  241. 241.
    Schaufler K, Semmler T, Wieler LH, Trott DJ, Pitout J, Peirano G, Bonnedahl J, Dolejska M, Literak I, Fuchs S, Ahmed N, Grobbel M, Torres C, McNally A, Pickard D, Ewers C, Croucher NJ, Corander J, Guenther S (2019) Genomic and functional analysis of emerging virulent and multi-drug resistant E. coli lineage ST648. Antimicrob Agents Chemother 63(6):e00243-19Google Scholar
  242. 242.
    Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60:1136–1151Google Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences BrnoBrnoCzech Republic
  2. 2.Central European Institute of Technology (CEITEC), University of Veterinary and Pharmaceutical Sciences BrnoBrnoCzech Republic

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