Potential impact of antimicrobial resistance in wildlife, environment, and human health

Frontiers in Microbiology

Volumn 5, Issue FEB, 2014, Pages

  Radhouani, Hajer ^a,b   Silva, Nuno ^b   Poeta, Patrícia ^a,b   Torres, Carmen ^c   Correia, Susana ^a,b   Igrejas, Gilberto ^a  

^a UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

^b UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

^c UNIVERSITY OF LA RIOJA   (Spain)

Author keywords

Antimicrobial resistance; Enterococci; Escherichia coli; Phylogenetic groups; Virulence factors; Wild animals

Indexed keywords

BACTERIOCIN; BETA LACTAM ANTIBIOTIC; CARBAPENEM DERIVATIVE; GLYCOPEPTIDE; IMIPENEM; MEROPENEM; PENICILLIN BINDING PROTEIN; TEICOPLANIN; VANCOMYCIN; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; BACTERIUM; CELL PROLIFERATION; ECOLOGICAL FALLACY; ENVIRONMENTAL IMPACT; ESCHERICHIA COLI; GENE MUTATION; GENE SEQUENCE; GENETIC VARIABILITY; HORIZONTAL GENE TRANSFER; HOSPITAL INFECTION; HUMAN; MULTILOCUS ENZYME ELECTROPHORESIS; MULTIPLEX POLYMERASE CHAIN REACTION; NONHUMAN; PHYLOGENY; PREVALENCE; REVIEW; WILDLIFE;

EID: 84897603328     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00023     Document Type: Review

References (165)

1. Adams, J. (2004). Microbial evolution in laboratory environments. Res. Microbiol. 155, 311-318. doi: 10.1016/j.resmic.2004.01.013
2. Allen, H. K., Donato, J., Wang, H. H., Cloud-Hansen, K. A., Davies, J., and Handelsman, J. (2010). Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8, 251-259. doi: 10.1038/nrmicro2312
3. Allen, S. E., Boerlin, P., Janecko, N., Lumsden, J. S., Barker, I. K., Pearl, D. L., et al. (2011). Antimicrobial resistance in generic Escherichia coli isolates from wild small mammals living in swine farm, residential, landfill, and natural environments in southern Ontario, Canada. Appl. Environ. Microbiol. 77, 882-888. doi: 10.1128/AEM.01111-10
4. American Academy of Microbiology. (2009). Antibiotic Resistance: An Ecological Perspective on an Old Problem. Washington, DC: American Academy of Microbiology.
5. Anderson, J. F., Parrish, T. D., Akhtar, M., Zurek, L., and Hirt, H. (2008). Antibiotic resistance of enterococci in American bison (Bison bison) from a nature preserve compared to that of enterococci in pastured cattle. Appl. Environ. Microbiol. 74, 1726-1730. doi: 10.1128/AEM.02164-07
6. Arias, C. A., and Murray, B. E. (2012). The rise of the Enterococcus: beyond vancomycin resistance. Nat. Rev. Microbiol. 10, 266-278. doi: 10.1038/nrmicro2761
7. Arthur, M., Reynolds, P., and Courvalin, P. (1996). Glycopeptide resistance in enterococci. Trends Microbiol. 4, 401-407. doi: 10.1016/0966-842X(96)10063-9
8. Baldy-Chudzik, K., Mackiewicz, P., and Stosik, M. (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. doi: 10.1016/j.vetmic.2008.02.019
9. Barrick, J. E., Yu, D. S., Yoon, S. H., Jeong, H., Oh, T. K., Schneider, D., et al. (2009). Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461, 1243-1247. doi: 10.1038/nature08480
10. Barros, J., Andrade, M., Radhouani, H., Lopez, M., Igrejas, G., Poeta, P., et al. (2012). Detection of vanA-containing Enterococcus species in faecal microbiota of gilthead seabream (Sparus aurata). Microbes Environ. 27, 509-511. doi: 10.1264/jsme2.ME11346
11. Barros, J., Igrejas, G., Andrade, M., Radhouani, H., Lopez, M., Torres, C., et al. (2011). Gilthead seabream (Sparus aurata) carrying antibiotic resistant enterococci. A potential bioindicator of marine contamination? Mar. Pollut. Bull. 62, 1245-1248. doi: 10.1016/j.marpolbul.2011.03.021
12. Bingen, E., Picard, B., Brahimi, N., Mathy, S., Desjardins, P., Elion, J., et al. (1998). Phylogenetic analysis of Escherichia coli strains causing neonatal meningitis suggests horizontal gene transfer from a predominant pool of highly virulent B2 group strains. J. Infect. Dis. 177, 642-650. doi: 10.1086/514217
13. Bonnedahl, J., Drobni, M., Gauthier-Clerc, M., Hernandez, J., Granholm, S., Kayser, Y., et al. (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. doi: 10.1371/journal.pone.0005958
14. Botti, V., Navillod, F. V., Domenis, L., Orusa, R., Pepe, E., Robetto, S., et al. (2013). Salmonella spp. and antibiotic-resistant strains in wild mammals and birds in north-western Italy from 2002 to 2010. Vet. Ital. 49, 195-202.
15. Cabello, F. C. (2006). Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ. Microbiol. 8, 1137-1144. doi: 10.1111/j.1462-2920.2006.01054.x
16. Canton, R., Akova, M., Carmeli, Y., Giske, C. G., Glupczynski, Y., Gniadkowski, M., et al. (2012). Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin. Microbiol. Infect. 18, 413-431. doi: 10.1111/j.1469-0691.2012.03821.x
17. Carlos, C., Pires, M. M., Stoppe, N. C., Hachich, E. M., Sato, M. I., Gomes, T. A., et al. (2010). Escherichia coli phylogenetic group determination and its application in the identification of the major animal source of fecal contamination. BMC Microbiol. 10:161. doi: 10.1186/1471-2180-10-161
18. Chao, L., and Levin, B. R. (1981). Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc. Natl. Acad. Sci. U.S.A. 78, 6324-6328. doi: 10.1073/pnas.78.10.6324
19. Chenoweth, C., and Schaberg, D. (1990). The epidemiology of enterococci. Eur. J. Clin. Microbiol. Infect. Dis. 9, 80-89.
20. Ciftci, A., Findik, A., Ica, T., Bas, B., Onuk, E. E., and Gungordu, S. (2009). Slime production and antibiotic resistance of Enterococcus faecalis isolated from arthritis in chickens. J. Vet. Med. Sci. 71, 849-853. doi: 10.1292/jvms.71.849
21. Clermont, O., Bonacorsi, S., and Bingen, E. (2000). Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66, 4555-4558. doi: 10.1128/AEM.66.10.4555-4558.2000
22. Cole, D., Drum, D. J., Stalknecht, D. E., White, D. G., Lee, M. D., Ayers, S., et al. (2005). Free-living Canada geese and antimicrobial resistance. Emerg. Infect. Dis. 11, 935-938. doi: 10.3201/eid1106.040717
23. Conrad, T. M., Lewis, N. E., and Palsson, B. O. (2011). Microbial laboratory evolution in the era of genome-scale science. Mol. Syst. Biol. 7, 509. doi: 10.1038/msb.2011.42
24. Coque, T. M., Novais, A., Carattoli, A., Poirel, L., Pitout, J., Peixe, L., et al. (2008). Dissemination of clonally related Escherichia coli strains expressing extended-spectrum beta-lactamase CTX-M-15. Emerg. Infect. Dis. 14, 195-200. doi: 10.3201/eid1402.070350
25. Costa, D., Poeta, P., Saenz, Y., Vinue, L., Rojo-Bezares, B., Jouini, A., et al. (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. doi: 10.1093/jac/dkl415
26. Dagan, T., and Martin, W. (2007). Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution. Proc. Natl. Acad. Sci. U.S.A. 104, 870-875. doi: 10.1073/pnas.0606318104
27. Davies, J., and Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74, 417-433. doi: 10.1128/MMBR.00016-10
28. Deschamps, C., Clermont, O., Hipeaux, M. C., Arlet, G., Denamur, E., and Branger, C. (2009). Multiple acquisitions of CTX-M plasmids in the rare D2 genotype of Escherichia coli provide evidence for convergent evolution. Microbiology 155, 1656-1668. doi: 10.1099/mic.0.023234-0
29. Devriese, L. A., and Pot, B. (1995). "The genus Enterococcus," in The Lactic Acid Bacteria: The Genera of Lactic Acid Bacteria, Vol. 2, eds B. J. B. Wood and W. H. Holzapfel (London: Blackie Academic), 327-367. doi: 10.1007/978-1-4615-5817-0_10
30. Dolejska, M., Bierosova, B., Kohoutova, L., Literak, I., and 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, 1941-1950. doi: 10.1111/j.1365-2672.2009.04155.x
31. Dolejska, M., Cizek, A., and Literak, I. (2007). High prevalence of antimicrobial-resistant genes and integrons in Escherichia coli isolates from Black-headed Gulls in the Czech Republic. J. Appl. Microbiol. 103, 11-19. doi: 10.1111/j.1365-2672.2006.03241.x
32. Drobni, M., Bonnedahl, J., Hernandez, J., Haemig, P., and Olsen, B. (2009). Vancomycin-resistant enterococci, Point Barrow, Alaska, USA. Emerg. Infect. Dis. 15, 838-839. doi: 10.3201/eid1505.081219
33. Duriez, P., Clermont, O., Bonacorsi, S., Bingen, E., Chaventre, A., Elion, J., et al. (2001). Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology 147, 1671-1676.
34. Eaton, T. J., and Gasson, M. J. (2001). Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl. Environ. Microbiol. 67, 1628-1635. doi: 10.1128/AEM.67.4.1628-1635.2001
35. Escobar-Paramo, P., Le Menac'h, A., Le Gall, T., Amorin, C., Gouriou, S., Picard, B., et al. (2006). Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environ. Microbiol. 8, 1975-1984. doi: 10.1111/j.1462-2920.2006.01077.x
36. Figueiredo, N., Radhouani, H., Goncalves, A., Rodrigues, J., Carvalho, C., Igrejas, G., et al. (2009). Genetic characterization of vancomycin-resistant enterococci isolates from wild rabbits. J. Basic Microbiol. 49, 491-494. doi: 10.1002/jobm.200800387
37. Fischer, J., Schmoger, S., Jahn, S., Helmuth, R., and Guerra, B. (2013). NDM-1 carbapenemase-producing Salmonella enterica subsp. enterica serovar Corvallis isolated from a wild bird in Germany. J. Antimicrob. Chemother. 68, 2954-2956. doi: 10.1093/jac/dkt260
38. Fisher, K., and Phillips, C. (2009). The ecology, epidemiology and virulence of Enterococcus. Microbiology 155, 1749-1757. doi: 10.1099/mic.0.026385-0
39. Franz, C. M., Muscholl-Silberhorn, A. B., Yousif, N. M., Vancanneyt, M., Swings, J., and Holzapfel, W. H. (2001). Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl. Environ. Microbiol. 67, 4385-4389. doi: 10.1128/AEM.67.9.4385-4389.2001
40. Freitas, A. R., Coque, T. M., Novais, C., Hammerum, A. M., Lester, C. H., Zervos, M. J., et al. (2011). Human and swine hosts share vancomycin-resistant Enterococcus faecium CC17 and CC5 and Enterococcus faecalis CC2 clonal clusters harboring Tn1546 on indistinguishable plasmids. J. Clin. Microbiol. 49, 925-931. doi: 10.1128/JCM.01750-10
41. Gakuya, F. M., Kyule, M. N., Gathura, P. B., and Kariuki, S. (2001). Antimicrobial susceptibility and plasmids from Escherichia coli isolated from rats. East Afr. Med. J. 78, 518-522. doi: 10.4314/eamj.v78i10.8960
42. Galloway-Pena, J., Roh, J. H., Latorre, M., Qin, X., and Murray, B. E. (2012). Genomic and SNP analyses demonstrate a distant separation of the hospital and community-associated clades of Enterococcus faecium. PLoS ONE 7:e30187. doi: 10.1371/journal.pone.0030187
43. Garmyn, A., Haesebrouck, F., Hellebuyck, T., Smet, A., Pasmans, F., Butaye, P., et al. (2011). Presence of extended-spectrum beta-lactamase-producing Escherichia coli in wild geese. J. Antimicrob. Chemother. 66, 1643-1644. doi: 10.1093/jac/dkr148
44. Gaukler, S. M., Linz, G. M., Sherwood, J. S., Dyer, N. W., Bleier, W. J., Wannemuehler, Y. M., et al. (2009). Escherichia coli, Salmonella, and Mycobacterium avium subsp. paratuberculosis in wild European starlings at a Kansas cattle feedlot. Avian Dis. 53, 544-551. doi: 10.1637/8920-050809-Reg.1
45. Gilliver, M. A., Bennett, M., Begon, M., Hazel, S. M., and Hart, C. A. (1999). Antibiotic resistance found in wild rodents. Nature 401, 233-234. doi: 10.1038/45724
46. Gin, A. S., and Zhanel, G. G. (1996). Vancomycin-resistant enterococci. Ann. Pharmacother. 30, 615-624.
47. Giridhara Upadhyaya, P. M., Ravikumar, K. L., and Umapathy, B. L. (2009). Review of virulence factors of Enterococcus: an emerging nosocomial pathogen. Indian J. Med. Microbiol. 27, 301-305. doi: 10.4103/0255-0857.55437
48. Gonçalves, A., Igrejas, G., Radhouani, H., Correia, S., Pacheco, R., Santos, T., et al. (2013a). Antimicrobial resistance in faecal enterococci and Escherichia coli isolates recovered from Iberian wolf. Lett. Appl. Microbiol. 56, 268-274. doi: 10.1111/lam.12044
49. Gonçalves, A., Igrejas, G., Radhouani, H., Santos, T., Monteiro, R., Pacheco, R., et al. (2013b). Detection of antibiotic resistant enterococci and Escherichia coli in free range Iberian Lynx (Lynx pardinus). Sci. Total Environ. 456-457., 115-119. doi: 10.1016/j.scitotenv.2013.03.073
50. Gonçalves, A., Igrejas, G., Radhouani, H., Santos, T., Monteiro, R., Marinho, C., et al. (2013c). Iberian Lynx (Lynx pardinus) from the captive breeding program as reservoir of antimicrobial resistant enterococci and Escherichia coli isolates. J. Integr. OMICS 3, 2. doi: 10.5584/jiomics.v3i2.142
51. Gonçalves, A., Igrejas, G., Radhouani, H., Estepa, V., Alcaide, E., Zorrilla, I., et al. (2012a). Detection of extended-spectrum beta-lactamase-producing Escherichia coli isolates in faecal samples of Iberian lynx. Lett. Appl. Microbiol. 54, 73-77. doi: 10.1111/j.1472-765X.2011.03173.x
52. Gonçalves, A., Igrejas, G., Radhouani, H., Estepa, V., Pacheco, R., Monteiro, R., et al. (2012b). Iberian wolf as a reservoir of extended-spectrum beta-lactamase-producing Escherichia coli of the TEM, SHV, and CTX-M groups. Microb. Drug Resist. 18, 215-219. doi: 10.1089/mdr.2011.0145
53. Gonçalves, A., Igrejas, G., Radhouani, H., Lopez, M., Guerra, A., Petrucci-Fonseca, F., et al. (2011). Detection of vancomycin-resistant enterococci from faecal samples of Iberian wolf and Iberian lynx, including Enterococcus faecium strains of CC17 and the new singleton ST573. Sci. Total Environ. 410-411, 266-268. doi: 10.1016/j.scitotenv.2011.09.074
54. Gordon, D. M., and Cowling, A. (2003). The distribution and genetic structure of Escherichia coli in Australian vertebrates: host and geographic effects. Microbiology 149, 3575-3586. doi: 10.1099/mic.0.26486-0
55. Goullet, P., and Picard, B. (1989). Comparative electrophoretic polymorphism of esterases and other enzymes in Escherichia coli. J. Gen. Microbiol. 135, 135-143.
56. Grobbel, M., Lubke-Becker, A., Alesik, E., Schwarz, S., Wallmann, J., Werckenthin, C., et al. (2007). Antimicrobial susceptibility of Escherichia coli from swine, horses, dogs and cats as determined in the BfT-GermVet monitoring program 2004-2006. Berl. Munch. Tierarztl. Wochenschr. 120, 391-401.
57. Grobbel, M., Wittstatt, U., Guenther, S., and Ewers, C. (2012). Urban red foxes (Vulpes vulpes) and their possible role in the transmission of 3rd generation beta-lactam resistant E. coli to the environment," in Proceedings of 3rd ASM Conference on Antimicrobial resistance in Zoonotic Bacteria and Foodborne Pathogens in Animals, Humans, and the Environment, Aix-en-Provence, France.
58. Guenther, S., Ewers, C., and Wieler, L. H. (2011). Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution? Front. Microbiol. 2:246. doi: 10.3389/fmicb.2011.00246
59. Guenther, S., Grobbel, M., Beutlich, J., Guerra, B., Ulrich, R. G., Wieler, L. H., et al. (2010a). 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, 582-584. doi: 10.1093/jac/dkp496
60. Guenther, S., Grobbel, M., Heidemanns, K., Schlegel, M., Ulrich, R. G., Ewers, C., et al. (2010b). First insights into antimicrobial resistance among faecal Escherichia coli isolates from small wild mammals in rural areas. Sci. Total Environ. 408, 3519-3522. doi: 10.1016/j.scitotenv.2010.05.005
61. Hernandez, J., Bonnedahl, J., Eliasson, I., Wallensten, A., Comstedt, P., Johansson, A., et al. (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, 329-332. doi: 10.1111/j.1758-2229.2010.00142.x
62. Herzer, P. J., Inouye, S., Inouye, M., and Whittam, T. S. (1990). Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J. Bacteriol. 172, 6175-6181.
63. Ho, P. L., Chow, K. H., Lai, E. L., Lo, W. U., Yeung, M. K., Chan, J., et al. (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, 765-768. doi: 10.1093/jac/dkq539
64. Ishihara, S., Bitner, J. J., Farley, G. H., and Gillock, E. T. (2013). Vancomycin-resistant gram-positive cocci isolated from the saliva of wild songbirds. Curr. Microbiol. 66, 337-343. doi: 10.1007/s00284-012-0278-1
65. Jaureguy, F., Landraud, L., Passet, V., Diancourt, L., Frapy, E., Guigon, G., et al. (2008). Phylogenetic and genomic diversity of human bacteremic Escherichia coli strains. BMC Genomics 9:560. doi: 10.1186/1471-2164-9-560
66. Jett, B. D., Huycke, M. M., and Gilmore, M. S. (1994). Virulence of enterococci. Clin. Microbiol. Rev. 7, 462-478.
67. Johnson, J. R. (2002). Escherichia Coli: Virulence Mechanisms of a Versatile Pathogen. London: Academic Press.
68. Johnson, J. R., Delavari, P., Kuskowski, M., and Stell, A. L. (2001). Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J. Infect. Dis. 183, 78-88. doi: 10.1086/317656
69. Johnson, J. R., Goullet, P., Picard, B., Moseley, S. L., Roberts, P. L., and Stamm, W. E. (1991). Association of carboxylesterase B electrophoretic pattern with presence and expression of urovirulence factor determinants and antimicrobial resistance among strains of Escherichia coli that cause urosepsis. Infect. Immun. 59, 2311-2315.
70. Johnson, J. R., Orskov, I., Orskov, F., Goullet, P., Picard, B., Moseley, S. L., et al. (1994). O, K, and H antigen predict virulence factors, carboxylesterase B pattern, antimicrobial resistance, and host compromise among Escherichia coli strains causing urosepsis. J. Infect. Dis. 169, 119-126. doi: 10.1093/infdis/169.1.119
71. Johnson, J. R., and Stell, A. L. (2000). Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J. Infect. Dis. 181, 261-272. doi: 10.1086/315217
72. Kozak, G. K., Boerlin, P., Janecko, N., Reid-Smith, R. J., and 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, 559-566. doi: 10.1128/AEM.01821-08
73. Kummerer, K., and Henninger, A. (2003). Promoting resistance by the emission of antibiotics from hospitals and households into effluent. Clin. Microbiol. Infect. 9, 1203-1214. doi: 10.1111/j.1469-0691.2003.00739.x
74. Lebreton, F., Van Schaik, W., Mcguire, A. M., Godfrey, P., Griggs, A., Mazumdar, V., et al. (2013). Emergence of epidemic multidrug-resistant Enterococcus faecium from animal and commensal strains. MBio 4, pii: e00534-13. doi: 10.1128/mBio.00534-13
75. Leclercq, R. (1997). Enterococci acquire new kinds of resistance. Clin. Infect. Dis. 24(Suppl. 1), S80-S84. doi: 10.1093/clinids/24.Supplement_1.S80
76. Lee, D. K., Kim, Y., Park, K. S., Yang, J. W., Kim, K., and Ha, N. J. (2007). Antimicrobial activity of mupirocin, daptomycin, linezolid, quinupristin/dalfopristin and tigecycline against vancomycin-resistant enterococci (VRE) from clinical isolates in Korea (1998 and 2005). J. Biochem. Mol. Biol. 40, 881-887. doi: 10.5483/BMBRep.2007.40.6.881
77. Lescat, M., Hoede, C., Clermont, O., Garry, L., Darlu, P., Tuffery, P., et al. (2009). aes, the gene encoding the esterase B in Escherichia coli, is a powerful phylogenetic marker of the species. BMC Microbiol. 9:273. doi: 10.1186/1471-2180-9-273
78. Lescat, M., Clermont, O., Woerther, P. L., Glodt, J., Dion, S., Skurnik, D., et al. (2013). Commensal Escherichia coli strains in Guiana reveal a high genetic diversity with host-dependant population structure. Environ. Microbiol. Rep. 5, 49-57. doi: 10.1111/j.1758-2229.2012.00374.x
79. Lillehaug, A., Bergsjo, B., Schau, J., Bruheim, T., Vikoren, T., and Handeland, K. (2005). Campylobacter spp., Salmonella spp., verocytotoxic Escherichia coli, and antibiotic resistance in indicator organisms in wild cervids. Acta Vet. Scand. 46, 23-32. doi: 10.1186/1751-0147-46-23
80. Literak, I., Dolejska, M., Janoszowska, D., Hrusakova, J., Meissner, W., Rzyska, H., et al. (2010a). 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. doi: 10.1128/AEM.01446-10
81. Literak, I., Dolejska, M., Radimersky, T., Klimes, J., Friedman, M., Aarestrup, F. M., et al. (2010b). 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. doi: 10.1111/j.1365-2672.2009.04572.x
82. Liti, G., Carter, D. M., Moses, A. M., Warringer, J., Parts, L., James, S. A., et al. (2009). Population genomics of domestic and wild yeasts. Nature 458, 337-341. doi: 10.1038/nature07743
83. Machado, E., Coque, T. M., Canton, R., Sousa, J. C., and Peixe, L. (2008). Antibiotic resistance integrons and extended-spectrum β-lactamases among Enterobacteriaceae isolates recovered from chickens and swine in Portugal. J. Antimicrob. Chemother. 62, 296-302. doi: 10.1093/jac/dkn179
84. MacLean, D., Jones, J. D., and Studholme, D. J. (2009). Application of "next-generation" sequencing technologies to microbial genetics. Nat. Rev. Microbiol. 7, 287-296. doi: 10.1038/nrmicro2088
85. Mallon, D. J. P., Corkill, J. E., Hazel, S. M., Wilson, J. S., French, N. P., Bennett, M., et al. (2002). Excretion of vancomycin-resistant enterococci by wild mammals. Emerg. Infect. Dis. 8, 636-638. doi: 10.3201/eid0806.010247
86. Mammeri, H., Galleni, M., and Nordmann, P. (2009). Role of the Ser-287-Asn replacement in the hydrolysis spectrum extension of AmpC beta-lactamases in Escherichia coli. Antimicrob. Agents Chemother. 53, 323-326. doi: 10.1128/AAC.00608-08
87. Mardis, E. R. (2008). The impact of next-generation sequencing technology on genetics. Trends Genet. 24, 133-141. doi: 10.1016/j.tig.2007.12.007
88. Marinho, C., Silva, N., Pombo, S., Santos, T., Monteiro, R., Goncalves, A., et al. (2013). Echinoderms from Azores islands: an unexpected source of antibiotic resistant Enterococcus spp. and Escherichia coli isolates. Mar. Pollut. Bull. 69, 122-127. doi: 10.1016/j.marpolbul.2013.01.017
89. Martel, J. L., Tardy, F., Sanders, P., and Boisseau, J. (2001). New trends in regulatory rules and surveillance of antimicrobial resistance in bacteria of animal origin. Vet. Res. 32, 381-392. doi: 10.1051/vetres:2001131
90. Martin, M. F., and Liras, P. (1989). Organization and expression of genes involved in the biosynthesis of antibiotics and other secondary metabolites. Annu. Rev. Microbiol. 43, 173-206. doi: 10.1146/annurev.mi.43.100189.001133
91. Martinez, J. L. (2009). The role of natural environments in the evolution of resistance traits in pathogenic bacteria. Proc. Biol. Sci. 276, 2521-2530. doi: 10.1098/rspb.2009.0320
92. Middleton, J. H., and Ambrose, A. (2005). Enumeration and antibiotic resistance patterns of fecal indicator organisms isolated from migratory Canada geese (Branta canadensis). J. Wildl. Dis. 41, 334-341. doi: 10.7589/0090-3558-41.2.334
93. Miller, C., Kong, J., Tran, T. T., Arias, C. A., Saxer, G., and Shamoo, Y. (2013). Adaptation of Enterococcus faecalis to daptomycin reveals an ordered progression to resistance. Antimicrob. Agents Chemother. 57, 5373-5383. doi: 10.1128/AAC.01473-13
94. Murray, B. E. (1990). The life and times of the Enterococcus. Clin. Microbiol. Rev. 3, 46-65.
95. Naas, T., Oxacelay, C., and Nordmann, P. (2007). Identification of CTX-M-type extended-spectrum-beta-lactamase genes using real-time PCR and pyrosequencing. Antimicrob. Agents Chemother. 51, 223-230. doi: 10.1128/AAC.00611-06
96. Navarro-Gonzalez, N., Casas-Diaz, E., Porrero, C. M., Mateos, A., Dominguez, L., Lavin, S., et al. (2013). Food-borne zoonotic pathogens and antimicrobial resistance of indicator bacteria in urban wild boars in Barcelona, Spain. Vet. Microbiol. 167, 686-689. doi: 10.1016/j.vetmic.2013.07.037
97. Nelson, M., Jones, S. H., Edwards, C., and Ellis, J. C. (2008). Characterization of Escherichia coli populations from gulls, landfill trash, and wastewater using ribotyping. Dis. Aquat. Organ. 81, 53-63. doi: 10.3354/dao01937
98. Nordmann, P., Cuzon, G., and Naas, T. (2009). The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect. Dis. 9, 228-236. doi: 10.1016/S1473-3099(09)70054-4
99. Nordmann, P., Naas, T., and Poirel, L. (2011). Global spread of Carbapenemase-producing Enterobacteriaceae. Emerg. Infect. Dis. 17, 1791-1798. doi: 10.3201/eid1710.110655
100. Novais, C., Freitas, A. R., Silveira, E., Antunes, P., Silva, R., Coque, T. M., et al. (2013). Spread of multidrug-resistant Enterococcus to animals and humans: an underestimated role for the pig farm environment. J. Antimicrob. Chemother. 68, 2746-2754. doi: 10.1093/jac/dkt289
101. Oravcova, V., Ghosh, A., Zurek, L., Bardon, J., Guenther, S., Cizek, A., et al. (2013a). Vancomycin-resistant enterococci in rooks (Corvus frugilegus) wintering throughout Europe. Environ. Microbiol. 15, 548-556. doi: 10.1111/1462-2920.12002
102. Oravcova, V., Zurek, L., Townsend, A., Clark, A. B., Ellis, J. C., Cizek, A., et al. (2013b). American crows as carriers of vancomycin-resistant enterococci with vanA gene. Environ. Microbiol. doi: 10.1111/1462-2920.12213 [Epub ahead of print].
103. Pallecchi, L., Bartoloni, A., Paradisi, F., and Rossolini, G. M. (2008). Antibiotic resistance in the absence of antimicrobial use: mechanisms and implications. Expert Rev. Anti Infect. Ther. 6, 725-732. doi: 10.1586/14787210.6.5.725
104. Patel, S. N., Memari, N., Shahinas, D., Toye, B., Jamieson, F. B., and Farrell, D. J. (2013). Linezolid resistance in Enterococcus faecium isolated in Ontario, Canada. Diagn. Microbiol. Infect. Dis. 77, 350-353. doi: 10.1016/j.diagmicrobio.2013.08.012
105. Pesapane, R., Ponder, M., and Alexander, K. A. (2013). Tracking pathogen transmission at the human-wildlife interface: banded mongoose and Escherichia coli. Ecohealth 10, 115-128. doi: 10.1007/s10393-013-0838-2
106. Picard, B., Garcia, J. S., Gouriou, S., Duriez, P., Brahimi, N., Bingen, E., et al. (1999). The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect. Immun. 67, 546-553.
107. Picard, B., and Goullet, P. (1989). Correlation between electrophoretic types B1 and B2 of carboxylesterase B and sex of patients in Escherichia coli urinary tract infections. Epidemiol. Infect. 103, 97-103. doi: 10.1017/S0950268800030399
108. Pinto, L., Radhouani, H., Coelho, C., Martins da Costa, P., Simoes, R., Brandao, R. M., et al. (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, 4118-4120. doi: 10.1128/AEM.02761-09
109. Poeta, P., Costa, D., Igrejas, G., Rodrigues, J., and Torres, C. (2007a). Phenotypic and genotypic characterization of antimicrobial resistance in faecal enterococci from wild boars (Sus scrofa). Vet. Microbiol. 125, 368-374. doi: 10.1016/j.vetmic.2007.06.003
110. Poeta, P., Costa, D., Igrejas, G., Rojo-Bezares, B., Saenz, Y., Zarazaga, M., et al. (2007b). Characterization of vanA-containing Enterococcus faecium isolates carrying Tn5397-like and Tn916/Tn1545-like transposons in wild boars (Sus Scrofa). Microb. Drug Resist. 13, 151-156. doi: 10.1089/mdr.2007.759
111. Poeta, P., Radhouani, H., Igrejas, G., Goncalves, A., Carvalho, C., Rodrigues, J., et al. (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, 7439-7441. doi: 10.1128/AEM.00949-08
112. Poeta, P., Radhouani, H., Pinto, L., Martinho, A., Rego, V., Rodrigues, R., et al. (2009). Wild boars as reservoirs of extended-spectrum beta-lactamase (ESBL) producing Escherichia coli of different phylogenetic groups. J. Basic Microbiol. 49, 584-588. doi: 10.1002/jobm.200900066
113. Porrero, M. C., Mentaberre, G., Sanchez, S., Fernandez-Llario, P., Gomez-Barrero, S., Navarro-Gonzalez, N., et al. (2013). Methicillin resistant Staphylococcus aureus (MRSA) carriage in different free-living wild animal species in Spain. Vet. J. 198, 127-130. doi: 10.1016/j.tvjl.2013.06.004
114. Prakash, V. P., Rao, S. R., and Parija, S. C. (2005). Emergence of unusual species of enterococci causing infections, South India. BMC Infect. Dis. 5:14. doi: 10.1186/1471-2334-5-14
115. Pupo, G. M., Karaolis, D. K., Lan, R., and Reeves, P. R. (1997). Evolutionary relationships among pathogenic and nonpathogenic Escherichia coli strains inferred from multilocus enzyme electrophoresis and mdh sequence studies. Infect. Immun. 65, 2685-2692.
116. Radhouani, H., Igrejas, G., Carvalho, C., Pinto, L., Goncalves, A., Lopez, M., et al. (2011a). Clonal lineages, antibiotic resistance and virulence factors in vancomycin-resistant enterococci isolated from fecal samples of red foxes (Vulpes vulpes). J. Wildl. Dis. 47, 769-773. doi: 10.7589/0090-3558-47.3.769
117. Radhouani, H., Igrejas, G., Pinto, L., Goncalves, A., Coelho, C., Rodrigues, J., et al. (2011b). Molecular characterization of antibiotic resistance in enterococci recovered from seagulls (Larus cachinnans) representing an environmental health problem. J. Environ. Monit. 13, 2227-2233. doi: 10.1039/c0em00682c
118. Radhouani, H., Poeta, P., Pinto, L., Miranda, J., Coelho, C., Carvalho, C., et al. (2010c). Proteomic characterization of vanA-containing Enterococcus recovered from Seagulls at the Berlengas Natural Reserve, W Portugal. Proteome Sci. 8, 48. doi: 10.1186/1477-5956-8-48
119. Radhouani, H., Igrejas, G., Gonçalves, A., Estepa, V., Sargo, R., Torres, C., et al. (2012a). Molecular characterization of extended-spectrum-beta-lactamase-producing Escherichia coli isolates from red foxes in Portugal. Arch. Microbiol. 195, 141-144. doi: 10.1007/s00203-012-0853-7
120. Radhouani, H., Poeta, P., Goncalves, A., Pacheco, R., Sargo, R., and Igrejas, G. (2012b). Wild birds as biological indicators of environmental pollution: antimicrobial resistance patterns of Escherichia coli and enterococci isolated from common buzzards (Buteo buteo). J. Med. Microbiol. 61, 837-843. doi: 10.1099/jmm.0.038364-0
121. Radhouani, H., Igrejas, G., Goncalves, A., Pacheco, R., Monteiro, R., Sargo, R., et al. (2013). Antimicrobial resistance and virulence genes in Escherichia coli and enterococci from red foxes (Vulpes vulpes). Anaerobe 23, 82-86. doi: 10.1016/j.anaerobe.2013.06.013
122. Radhouani, H., Pinto, L., Coelho, C., Goncalves, A., Sargo, R., Torres, C., et al. (2010a). Detection of Escherichia coli harbouring extended-spectrum β-lactamases of the CTX-M classes in faecal samples of common buzzards (Buteo buteo). J. Antimicrob. Chemother. 65, 171-173. doi: 10.1093/jac/dkp403
123. Radhouani, H., Pinto, L., Coelho, C., Sargo, R., Araujo, C., Lopez, M., et al. (2010b). MLST and a genetic study of antibiotic resistance and virulence factors in vanA-containing Enterococcus from buzzards (Buteo buteo). Lett. Appl. Microbiol. 50, 537-541. doi: 10.1111/j.1472-765X.2010.02807.x
124. Radhouani, H., Poeta, P., Igrejas, G., Goncalves, A., Vinue, L., and Torres, C. (2009). Antimicrobial resistance and phylogenetic groups in isolates of Escherichia coli from seagulls at the Berlengas nature reserve. Vet. Rec. 165, 138-142. doi: 10.1136/vr.165.5.138
125. Rankin, D. J., Rocha, E. P., and Brown, S. P. (2011). What traits are carried on mobile genetic elements, and why? Heredity (Edinb.) 106, 1-10. doi: 10.1038/hdy.2010.24
126. Reid, A., and Buckley, M. (2011). Microbial Evolution. Washington, DC: American Academy of Microbiology
127. Ruiz-Garbajosa, P., Bonten, M. J., Robinson, D. A., Top, J., Nallapareddy, S. R., Torres, C., et al. (2006). Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of recombination. J. Clin. Microbiol. 44, 2220-2228. doi: 10.1128/JCM.02596-05
128. Santagati, M., Campanile, F., and Stefani, S. (2012). Genomic diversification of enterococci in hosts: the role of the mobilome. Front. Microbiol. 3:95. doi: 10.3389/fmicb.2012.00095
129. Santos, T., Silva, N., Igrejas, G., Rodrigues, P., Micael, J., Rodrigues, T., et al. (2013). Dissemination of antibiotic resistant Enterococcus spp. and Escherichia coli from wild birds of Azores Archipelago. Anaerobe 24, 25-31. doi: 10.1016/j.anaerobe.2013.09.004
130. Sato, G., Oka, C., Asagi, M., and Ishiguro, N. (1978). Detection of conjugative R plasmids conferring chloramphenicol resistance in Escherichia coli isolated from domestic and feral pigeons and crows. Zentralbl. Bakteriol. Orig. A 241, 407-417.
131. Schacherer, J., Shapiro, J. A., Ruderfer, D. M., and Kruglyak, L. (2009). Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458, 342-345. doi: 10.1038/nature07670
132. Schierack, P., Romer, A., Jores, J., Kaspar, H., Guenther, S., Filter, M., et al. (2009). Isolation and characterization of intestinal Escherichia coli clones from wild boars in Germany. Appl. Environ. Microbiol. 75, 695-702. doi: 10.1128/AEM.01650-08
133. Schubert, S., Darlu, P., Clermont, O., Wieser, A., Magistro, G., Hoffmann, C., et al. (2009). Role of intraspecies recombination in the spread of pathogenicity islands within the Escherichia coli species. PLoS Pathog. 5:e1000257. doi: 10.1371/journal.ppat.1000257
134. Segura, P. A., Francois, M., Gagnon, C., and Sauve, S. (2009). Review of the occurrence of anti-infectives in contaminated wastewaters and natural and drinking waters. Environ. Health Perspect. 117, 675-684. doi: 10.1289/ehp.11776
135. Selander, R. K., Caugant, D. A., Ochman, H., Musser, J. M., Gilmour, M. N., and Whittam, T. S. (1986). Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl. Environ. Microbiol. 51, 873-884.
136. Selander, R. K., Caugant, D. A., and Whittam, T. S. (1987). "Genetic structure and variation in natural populations of Escherichia coli," in Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, eds F. C. Neidhardt, J. L. Ingraham, K. B. Low, B. Magasanik, M. Schaechter, and H. E. Umbarger (Washington: American Society for Microbiology), 1625-1648.
137. Sherley, M., Gordon, D. M., and Collignon, P. J. (2000). Variations in antibiotic resistance profile in Enterobacteriaceae isolated from wild Australian mammals. Environ. Microbiol. 2, 620-631. doi: 10.1046/j.1462-2920.2000.00145.x
138. Silva, N., Igrejas, G., Figueiredo, N., Goncalves, A., Radhouani, H., Rodrigues, J., et al. (2010). Molecular characterization of antimicrobial resistance in enterococci and Escherichia coli isolates from European wild rabbit (Oryctolagus cuniculus). Sci. Total Environ. 408, 4871-4876. doi: 10.1016/j.scitotenv.2010.06.046
139. Silva, N., Igrejas, G., Rodrigues, P., Rodrigues, T., Goncalves, A., Felgar, A. C., et al. (2011a). 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, 473-479. doi: 10.1080/03079457.2011.599061
140. Silva, N., Igrejas, G., Vaz, J., Araujo, C., Cardoso, L., Rodrigues, J., et al. (2011b). Virulence factors in enterococci from partridges (Alectoris rufa) representing a food safety problem. Foodborne Pathog. Dis. 8, 831-833. doi: 10.1089/fpd.2010.0781
141. Silva, N., Igrejas, G., Felgar, A., Goncalves, A., Pacheco, R., and Poeta, P. (2012). Molecular characterization of vanA-containing Enterococcus from migratory birds: song thrush (Turdus philomelos). Braz. J. Microbiol. 43, 1026-1029. doi: 10.1590/S1517-83822012000300026
142. Simões, R. R., Poirel, L., Da Costa, P. M., and Nordmann, P. (2010). Seagulls and beaches as reservoirs for multidrug-resistant Escherichia coli. Emerg. Infect. Dis. 16, 110-112. doi: 10.3201/eid1601.090896
143. Singer, R. S., Ward, M. P., and Maldonado, G. (2006). Can landscape ecology untangle the complexity of antibiotic resistance? Nat. Rev. Microbiol. 4, 943-952. doi: 10.1038/nrmicro1553
144. Skurnik, D., Bonnet, D., Bernede-Bauduin, C., Michel, R., Guette, C., Becker, J. M., et al. (2008). Characteristics of human intestinal Escherichia coli with changing environments. Environ. Microbiol. 10, 2132-2137. doi: 10.1111/j.1462-2920.2008.01636.x
145. Skurnik, D., Le Menac'h, A., Zurakowski, D., Mazel, D., Courvalin, P., Denamur, E., et al. (2005). Integron-associated antibiotic resistance and phylogenetic grouping of Escherichia coli isolates from healthy subjects free of recent antibiotic exposure. Antimicrob. Agents Chemother. 49, 3062-3065. doi: 10.1128/AAC.49.7.3062-3065.2005
146. Skurnik, D., Ruimy, R., Andremont, A., Amorin, C., Rouquet, P., Picard, B., et al. (2006). Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J. Antimicrob. Chemother. 57, 1215-1219. doi: 10.1093/jac/dkl122
147. Smith, P. (2008). Antimicrobial resistance in aquaculture. Rev. Sci. Tech. 27, 243-264.
148. Sorum, H., and Sunde, M. (2001). Resistance to antibiotics in the normal flora of animals. Vet. Res. 32, 227-241. doi: 10.1051/vetres:2001121
149. Sousa, M., Torres, C., Barros, J., Somalo, S., Igrejas, G., and Poeta, P. (2011). Gilthead seabream (Sparus aurata) as carriers of SHV-12 and TEM-52 extended-spectrum beta-lactamases-containing Escherichia coli isolates. Foodborne Pathog. Dis. 8, 1139-1141. doi: 10.1089/fpd.2011.0866
150. Souza, V., Rocha, M., Valera, A., and Eguiarte, L. E. (1999). Genetic structure of natural populations of Escherichia coli in wild hosts on different continents. Appl. Environ. Microbiol. 65, 3373-3385.
151. Tenaillon, O., Skurnik, D., Picard, B., and Denamur, E. (2010). The population genetics of commensal Escherichia coli. Nat. Rev. Microbiol. 8, 207-217. doi: 10.1038/nrmicro2298
152. Thaller, M. C., Migliore, L., Marquez, C., Tapia, W., Cedeno, V., Rossolini, G. M., et al. (2010). Tracking acquired antibiotic resistance in commensal bacteria of Galapagos land iguanas: no man, no resistance. PLoS ONE 5:e8989. doi: 10.1371/journal.pone.0008989
153. Thiele-Bruhn, S. (2003). Pharmaceutical antibiotic compounds in soils-a review. J. Plant Nutr. Soil Sci. 166, 145-167. doi: 10.1002/jpln.200390023
154. Touchon, M., Hoede, C., Tenaillon, O., Barbe, V., Baeriswyl, S., Bidet, P., et al. (2009). Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5:e1000344. doi: 10.1371/journal.pgen.1000344
155. van den Bogaard, A. E., and Stobberingh, E. E. (2000). Epidemiology of resistance to antibiotics. Links between animals and humans. Int. J. Antimicrob. Agents 14, 327-335. doi: 10.1016/S0924-8579(00)00145-X
156. van Schaik, W., and Willems, R. J. (2010). Genome-based insights into the evolution of enterococci. Clin. Microbiol. Infect. 16, 527-532. doi: 10.1111/j.1469-0691.2010.03201.x
157. Wagner, A. (2008). Neutralism and selectionism: a network-based reconciliation. Nat. Rev. Genet. 9, 965-974. doi: 10.1038/nrg2473
158. Walk, S. T., Alm, E. W., Calhoun, L. M., Mladonicky, J. M., and Whittam, T. S. (2007). Genetic diversity and population structure of Escherichia coli isolated from freshwater beaches. Environ. Microbiol. 9, 2274-2288. doi: 10.1111/j.1462-2920.2007.01341.x
159. Walsh, C. (2003). Antibiotics: Actions, Origins, Resistance. Washington: ASM Press.
160. Weng, P. L., Ramli, R., Shamsudin, M. N., Cheah, Y. K., and Hamat, R. A. (2013). High genetic diversity of Enterococcus faecium and Enterococcus faecalis clinical isolates by pulsed-field gel electrophoresis and multilocus sequence typing from a hospital in Malaysia. Biomed Res. Int. 2013, 938937. doi: 10.1155/2013/938937
161. Werner, G., Fleige, C., Geringer, U., van Schaik, W., Klare, I., and Witte, W. (2011). IS element IS16 as a molecular screening tool to identify hospital-associated strains of Enterococcus faecium. BMC Infect. Dis. 11:80. doi: 10.1186/1471-2334-11-80
162. Willems, R. J., Top, J., van Santen, M., Robinson, D. A., Coque, T. M., Baquero, F., et al. (2005). Global spread of vancomycin-resistant Enterococcus faecium from distinct nosocomial genetic complex. Emerg. Infect. Dis. 11, 821-828. doi: 10.3201/1106.041204
163. Willems, R. J., and van Schaik, W. (2009). Transition of Enterococcus faecium from commensal organism to nosocomial pathogen. Future Microbiol. 4, 1125-1135. doi: 10.2217/fmb.09.82
164. Wright, G. D. (2010). Antibiotic resistance in the environment: a link to the clinic? Curr. Opin. Microbiol. 13, 589-594. doi: 10.1016/j.mib.2010.08.005
165. Xavier, D. B., Rosa, A. H., Teixeira, D. S., Tomaz, C. A. B., and Titze-de-Almeida, R. (2010). Absence of intestinal colonization by vancomycin-resistant enterococci in nonhuman primates. Pesq. Vet. Bras. 30, 491-496. doi: 10.1590/S0100-736X2010000600004