Biofilms and Antimicrobial Resistance in Companion Animals

  • Thomas W. MaddoxEmail author
Part of the Springer Series on Biofilms book series (BIOFILMS, volume 6)


Bacterial resistance to antimicrobials is a complex interaction of bacterial populations, resistance mechanisms, resistance genes and antimicrobial agents. Although comparatively little research has focused on bacteria from companion animals, many of the mechanisms conferring resistance identified in bacteria originating from humans have also been recognised in bacterial isolates from dogs, cats and horses. In addition to these well documented resistance mechanisms, it has recently been acknowledged that biofilm formation can contribute to the resistance encountered in some bacterial populations. Biofilm-associated resistance appears to be multifactorial, with interaction of specific biofilm resistance mechanisms and potentially other classical antimicrobial resistance mechanisms. Currently, there is incomplete understanding of this complex situation, but work continues to better characterise the processes involved.


Companion Animal Antimicrobial Molecule Trimethoprim Resistance ampC Gene DHFR Enzyme 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Aarestrup FM (2005) Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic Clin Pharmacol Toxicol 96:271–281PubMedGoogle Scholar
  2. Abraham EP, Chain E (1988) An enzyme from bacteria able to destroy Penicillin (Reprinted From Nature, Vol 146, Pg 837, 1940). Rev Infect Dis 10:677–678PubMedGoogle Scholar
  3. Adair CG, Gorman SP, Feron BM, Byers LM, Jones DS, Goldsmith CE, Moore JE, Kerr JR, Curran MD, Hogg G, Webb CH, McCarthy GJ, Milligan KR (1999) Implications of endotracheal tube biofilm for ventilator-associated pneumonia. Intensive Care Med 25:1072–1076PubMedGoogle Scholar
  4. Ahern BJ, Richardson DW, Boston RC, Schaer TP (2010) Orthopedic infections in equine long bone fractures and arthrodeses treated by internal fixation: 192 cases (1990–2006). Vet Surg 39:588–593PubMedGoogle Scholar
  5. Albihn A, Baverud V, Magnusson U (2003) Uterine microbiology and antimicrobial susceptibility in isolated bacteria from mares with fertility problems. Acta Vet Scand 44:121–129PubMedGoogle Scholar
  6. Anderl JN, Franklin MJ, Stewart PS (2000) Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 44:1818–1824PubMedGoogle Scholar
  7. Anderson GG, O’Toole GA (2008) Innate and induced resistance mechanisms of bacterial biofilms. Curr Top Microbiol Immunol 322:85–105PubMedGoogle Scholar
  8. Andersson DI, Hughes D (2010) Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol 8:260–271PubMedGoogle Scholar
  9. Ando T, Itakura S, Uchii K, Sobue R, Maeda S (2009) Horizontal transfer of non-conjugative plasmid in colony biofilm of Escherichia coli on food-based media. World J Microbiol Biotechnol 25:1865–1869Google Scholar
  10. Arpin C, Quentin C, Grobost F, Cambau E, Robert J, Dubois V, Coulange L, Andre C, Sci Comm O (2009) Nationwide survey of extended-spectrum beta-lactamase-producing Enterobacteriaceae in the French community setting. J Antimicrob Chemother 63:1205–1214PubMedGoogle Scholar
  11. Arthur M, Molinas C, Depardieu F, Courvalin P (1993) Characterization of Tn1546, a Tn3-related transposon conferring glycopeptide resistance by synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J Bacteriol 175:117–127PubMedGoogle Scholar
  12. Arthur M, Reynolds P, Courvalin P (1996a) Glycopeptide resistance in enterococci. Trends Microbiol 4:401–407PubMedGoogle Scholar
  13. Arthur M, Reynolds PE, Depardieu F, Evers S, DutkaMalen S, Quintiliani R, Courvalin P (1996b) Mechanisms of glycopeptide resistance in enterococci. J Infect 32:11–16PubMedGoogle Scholar
  14. Bagcigil FA, Moodley A, Baptiste KE, Jensen VF, Guardabassi L (2007) Occurrence, species distribution, antimicrobial resistance and clonality of methicillin- and erythromycin-resistant staphylococci in the nasal cavity of domestic animals. Vet Microbiol 121:307–315PubMedGoogle Scholar
  15. Bagge N, Ciofu O, Skovgaard LT, Hoiby N (2000) Rapid development in vitro and in vivo of resistance to ceftazidime in biofilm-growing Pseudomonas aeruginosa due to chromosomal beta-lactamase. APMIS 108:589–600PubMedGoogle Scholar
  16. Bagge N, Schuster M, Hentzer M, Ciofu O, Givskov M, Greenberg EP, Hoiby N (2004) Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and beta-lactamase and alginate production. Antimicrob Agents Chemother 48:1175–1187PubMedGoogle Scholar
  17. Baptiste KE, Williams K, Willams NJ, Wattret A, Clegg PD, Dawson S, Corkill J, O’Neill T, Hart CA (2005) Methicillin resistant staphylococci in companion animals. Emerg Infect Dis 11:1942–1944PubMedGoogle Scholar
  18. Bauernfeind A, Grimm H, Schweighart S (1990) A new plasmidic cefotaximase in a clinical isolate of Escherichia coli. Infection 18:294–298PubMedGoogle Scholar
  19. Baverud V, Gustafsson A, Franklin A, Aspan A, Gunnarsson A (2003) Clostridium difficile: prevalence in horses and environment, and antimicrobial susceptibility. Equine Vet J 35:465–471PubMedGoogle Scholar
  20. Blahna MT, Zalewski CA, Reuer J, Kahlmeter G, Foxman B, Marrs CF (2006) The role of horizontal gene transfer in the spread of trimethoprim-sulfamethoxazole resistance among uropathogenic Escherichia coli in Europe and Canada. J Antimicrob Chemother 57:666–672PubMedGoogle Scholar
  21. Blumberg HM, Rimland D, Carroll DJ, Terry P, Wachsmuth IK (1991) Rapid development of ciprofloxacin resistance in methicillin-susceptible and methicillin-resistant Staphylococcus aureus. J Infect Dis 163:1279–1285PubMedGoogle Scholar
  22. Boost MV, O’Donoghue MM, James A (2008) Prevalence of Staphylococcus aureus carriage among dogs and their owners. Epidemiol Infect 136:953–964PubMedGoogle Scholar
  23. Boothe JH, Morton J, Petisi JP, Wilkinson RG, Williams JH (1953) Tetracycline. J Am Chem Soc 75:4621Google Scholar
  24. Bradford PA (2001) Extended-spectrum beta-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev 14:933–951PubMedGoogle Scholar
  25. Bradford PA, Urban C, Mariano N, Projan SJ, Rahal JJ, Bush K (1997) Imipenem resistance in Klebsiella pneumoniae is associated with the combination of ACT-1, a plasmid-mediated AmpC beta-lactamase, and the loss of an outer membrane protein. Antimicrob Agents Chemother 41:563–569PubMedGoogle Scholar
  26. Brinas L, Zarazaga M, Saenz Y, Ruiz-Larrea F, Torres C (2002) Beta-lactamases in ampicillin-resistant Escherichia coli isolates from foods, humans, and healthy animals. Antimicrob Agents Chemother 46:3156–3163PubMedGoogle Scholar
  27. Briñas L, Moreno MA, Teshager T, Zarazaga M, Sáenz Y, Porrero C, Dominguez L, Torres T (2003) Beta-lactamase characterization in Escherichia coli isolates with diminished susceptibility or resistance to extended-spectrum cephalosporins recovered from sick animals in Spain. Microb Drug Resist 9:201–209PubMedGoogle Scholar
  28. Brooun A, Liu SH, Lewis K (2000) A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 44:640–646PubMedGoogle Scholar
  29. Brown DFJ, Reynolds PE (1980) Intrinsic resistance to beta-lactam antibiotics in Staphylococcus aureus. FEBS Lett 122:275–278PubMedGoogle Scholar
  30. Bryan A, Shapir N, Sadowsky MJ (2004) Frequency and distribution of tetracycline resistance genes in genetically diverse, nonselected, and nonclinical Escherichia coli strains, isolated from diverse human and animal sources. Appl Environ Microbiol 70:2503–2507PubMedGoogle Scholar
  31. Bucknell DG, Gasser RB, Irving A, Whithear K (1997) Antimicrobial resistance in Salmonella and Escherichia coli isolated from horses. Aust Vet J 75:355–356PubMedGoogle Scholar
  32. Carattoli A (2008) Animal reservoirs for extended spectrum beta-lactamase producers. Clin Microbiol Infect 14:117–123PubMedGoogle Scholar
  33. Cavaco LM, Hansen DS, Friis-Moller A, Aarestrup FM, Hasman H, Frimodt-Moller N (2007) First detection of plasmid-mediated quinolone resistance (qnrA and qnrS) in Escherichia coli strains isolated from humans in Scandinavia. J Antimicrob Chemother 59:804–805PubMedGoogle Scholar
  34. Cavaco LM, Hasman H, Xia S, Aarestrup FM (2009) qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica Serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother 53:603–608PubMedGoogle Scholar
  35. Chen L, Chen ZL, Liu JH, Zeng ZL, Ma JY, Jiang HX (2007) Emergence of RmtB methylase-producing Escherichia coli and Enterobacter cloacae isolates from pigs in China. J Antimicrob Chemother 59:880–885PubMedGoogle Scholar
  36. Chopra I, Roberts M (2001) Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232PubMedGoogle Scholar
  37. Corkill JE, Anson JJ, Hart CA (2005) High prevalence of the plasmid-mediated quinolone resistance determinant qnrA in multidrug-resistant Enterobacteriaceae from blood cultures in Liverpool, UK. J Antimicrob Chemother 56:1115–1117PubMedGoogle Scholar
  38. Cormio L, VuopioVarkila J, Siitonen A, Talja M, Ruutu M (1996) Bacterial adhesion and biofilm formation on various double-J stents in vivo and in vitro. Scand J Urol Nephrol 30:19–24PubMedGoogle Scholar
  39. Corrente M, D’Abramo M, Latronico F, Greco MF, Bellacicco AL, Greco G, Martella V, Buonavoglia D (2009) Methicillin-resistant coagulase negative staphylococci isolated from horses. New Microbiol 32:311–314PubMedGoogle Scholar
  40. D’Costa VM, Griffiths E, Wright GD (2007) Expanding the soil antibiotic resistome: exploring environmental diversity. Curr Opin Microbiol 10:481–489PubMedGoogle Scholar
  41. Das JR, Bhakoo M, Jones MV, Gilbert P (1998) Changes in the biocide susceptibility of Staphylococcus epidermidis and Escherichia coli cells associated with rapid attachment to plastic surfaces. J Appl Microbiol 84:852–858PubMedGoogle Scholar
  42. Datta N, Kontomichalou P (1965) Penicillinase synthesis controlled by infectious R factors in Enterobacteriaceae. Nature 208:239PubMedGoogle Scholar
  43. Datta N, Nugent M, Amyes SGB, McNeilly P (1979) Multiple mechanisms of trimethoprim resistance in strains of Escherichia coli from a patient treated with long-term co-trimoxazole. J Antimicrob Chemother 5:399–406PubMedGoogle Scholar
  44. Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2:114–122PubMedGoogle Scholar
  45. de Beer D, Stoodley P, Roe F, Lewandowski Z (1994) Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol Bioeng 43:1131–1138PubMedGoogle Scholar
  46. De Kievit TR, Parkins MD, Gillis RJ, Srikumar R, Ceri H, Poole K, Iglewski BH, Storey DG (2001) Multidrug efflux pumps: expression patterns and contribution to antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 45:1761–1770PubMedGoogle Scholar
  47. Dejonge BLM, Chang YS, Gage D, Tomasz A (1992) Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain – the role of penicillin binding protein-2a. J Biol Chem 267:11248–11254Google Scholar
  48. Devriese LA, Ieven M, Goossens H, Vandamme P, Pot B, Hommez J, Haesebrouck F (1996) Presence of vancomycin-resistant enterococci in farm and pet animals. Antimicrob Agents Chemother 40:2285–2287PubMedGoogle Scholar
  49. Domagk G (1935) A new class of disinfectant. Dtsch Med Wochenschr 61:829–832Google Scholar
  50. Donelli G (2006) Vascular catheter-related infection and sepsis. Surg Infect (Larchmt) 7(Suppl 2):S25–S27Google Scholar
  51. Driffield K, Miller K, Bostock JM, O’Neill AJ, Chopra I (2008) Increased mutability of Pseudomonas aeruginosa in biofilms. J Antimicrob Chemother 61:1053–1056PubMedGoogle Scholar
  52. Drlica K, Zhao X (1997) DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61:377–392PubMedGoogle Scholar
  53. Dunowska M, Morley PS, Traub-Dargatz JL, Hyatt DR, Dargatz DA (2006) Impact of hospitalization and antimicrobial drug administration on antimicrobial susceptibility patterns of commensal Escherichia coli isolated from the feces of horses. J Am Vet Med Assoc 228:1909–1917PubMedGoogle Scholar
  54. Ewers C, Grobbel M, Stamm I, Kopp PA, Diehl I, Semmler T, Fruth A, Beutlich J, Guerra B, Wieler LH, Guenther S (2010) Emergence of human pandemic O25:H4-ST131 CTX-M-15 extended-spectrum-beta-lactamase-producing Escherichia coli among companion animals. J Antimicrob Chemother 65:651–660PubMedGoogle Scholar
  55. Fine DM, Tobias AH (2007) Cardiovascular device infections in dogs: report of 8 cases and review of the literature. J Vet Intern Med 21:1265–1271PubMedGoogle Scholar
  56. Fleming A (1932) On the specific antibacterial properties of penicillin and potassium tellurite – incorporating a method of demonstrating some bacterial antiagonisms. J Pathol Bacteriol 35:831–842Google Scholar
  57. Fluit AC, Wielders CLC, Verhoef J, Schmitz FJ (2001) Epidemiology and susceptibility of 3,051 Staphylococcus aureus isolates from 25 university hospitals participating in the European SENTRY study. J Clin Microbiol 39:3727–3732PubMedGoogle Scholar
  58. Fux CA, Stoodley P, Hall-Stoodley L, Costerton JW (2003) Bacterial biofilms: a diagnostic and therapeutic challenge. Expert Rev Anti Infect Ther 1:667–683PubMedGoogle Scholar
  59. Gal Z, Kovacs P, Hernadi F, Barabas G, Kiss L, Igloi A, Szabo I (2001) Investigation of oxacillin-hydrolyzing beta-lactamase in borderline methicillin-resistant clinical isolates of Staphylococcus aureus. Chemotherapy 47:233–238PubMedGoogle Scholar
  60. Galimand M, Courvalin P, Lambert T (2003) Plasmid-mediated high-level resistance to aminoglycosides in Enterobacteriaceae due to 16S rRNA methylation. Antimicrob Agents Chemother 47:2565–2571PubMedGoogle Scholar
  61. Gaynor M, Mankin AS (2003) Macrolide antibiotics: binding site, mechanism of action, resistance. Curr Top Med Chem 3:949–960PubMedGoogle Scholar
  62. Georgopapadakou NH, Smith SA, Bonner DP (1982) Penicillin-binding proteins in a Staphylococcus aureus strain resistant to specific beta-lactam antibiotics. Antimicrob Agents Chemother 22:172–175PubMedGoogle Scholar
  63. Gibson JS, Cobbold RN, Heisig P, Sidjabat HE, Kyaw-Tanner MT, Trott DJ (2010a) Identification of Qnr and AAC(6′)-1b-cr plasmid-mediated fluoroquinolone resistance determinants in multidrug-resistant Enterobacter spp. isolated from extraintestinal infections in companion animals. Vet Microbiol 143:329–336PubMedGoogle Scholar
  64. Gibson JS, Cobbold RN, Trott DJ (2010b) Characterization of multidrug-resistant Escherichia coli isolated from extraintestinal clinical infections in animals. J Med Microbiol 59:592–598PubMedGoogle Scholar
  65. Gilbert P, Collier PJ, Brown MR (1990) Influence of growth rate on susceptibility to antimicrobial agents: biofilms, cell cycle, dormancy, and stringent response. Antimicrob Agents Chemother 34:1865–1868PubMedGoogle Scholar
  66. Gonzalez-Zorn B, Teshager T, Casas M, Porrero MC, Moreno MA, Courvalin P, Dominguez L (2005) armA and aminoglycoside resistance in Escherichia coli. Emerg Infect Dis 11:954–956PubMedGoogle Scholar
  67. Goto T, Nakame Y, Nishida M, Ohi Y (1999) In vitro bactericidal activities of beta-lactamases, amikacin, and fluoroquinolones against Pseudomonas aeruginosa biofilm in artificial urine. Urology 53:1058–1062PubMedGoogle Scholar
  68. Gristina AG, Oga M, Webb LX, Hobgood CD (1985) Adherent bacterial colonization in the pathogenesis of osteomyelitis. Science 228:990–993PubMedGoogle Scholar
  69. Grobbel M, Lubke-Becker A, Alesik E, Schwarz S, Wallmann J, Werckenthin C, Wieler LH (2007) Antimicrobial susceptibility of Escherichia coli from swine, horses, dogs and cats as determined in the BfT-GermVet monitoring program 2004–2006. Berl Münch Tierärztl Wochenschr 120:391–401PubMedGoogle Scholar
  70. Hall RM, Collis CM (1995) Mobile gene cassettes and integrons – capture and spread of genes by site-specific recombination. Mol Microbiol 15:593–600PubMedGoogle Scholar
  71. Hall LMC, Henderson-Begg SK (2006) Hypermutable bacteria isolated from humans – a critical analysis. Microbiology 152:2505–2514PubMedGoogle Scholar
  72. Hansen SK, Rainey PB, Haagensen JAJ, Molin S (2007) Evolution of species interactions in a biofilm community. Nature 445:533–536PubMedGoogle Scholar
  73. Hanssen AM, Sollid JUE (2006) SCCmec in staphylococci: genes on the move. FEMS Immunol Med Microbiol 46:8–20PubMedGoogle Scholar
  74. Harihara H, Barnum DA (1973) Drug resistance among pathogenic Enterobacteriaceae from animals in Ontario. Can J Public Health 64:69Google Scholar
  75. Hata M, Suzuki M, Matsumoto M, Takahashi M, Sato K, Ibe S, Sakae K (2005) Cloning of a novel gene for quinolone resistance from a transferable plasmid in Shigella flexneri 2b. Antimicrob Agents Chemother 49:801–803PubMedGoogle Scholar
  76. Heikkila E, Renkonen OV, Sunila R, Uurasmaa P, Huovinen P (1990) The emergence and mechanisms of trimethoprim resistance in Escherichia coli isolated from outpatients in Finland. J Antimicrob Chemother 25:275–283PubMedGoogle Scholar
  77. Hopkins KL, Batchelor MJ, Liebana E, Deheer-Graham AP, Threlfalla EJ (2006) Characterisation of CTX-M and AmpC genes in human isolates of Escherichia coli identified between 1995 and 2003 in England and Wales. Int J Antimicrob Agents 28:180–192PubMedGoogle Scholar
  78. Huovinen P, Sundstrom L, Swedberg G, Skold O (1995) Trimethoprim and sulfonamide resistance. Antimicrob Agents Chemother 39:279–289PubMedGoogle Scholar
  79. Huys G, D’Haene K, Collard JM, Swings J (2004) Prevalence and molecular characterization of tetracycline resistance in Enterococcus isolates from food. Appl Environ Microbiol 70:1555–1562PubMedGoogle Scholar
  80. Irina F, Misic D, Ruzica A (2007) Investigation of the presence of extended spectrum beta-lactamases (ESBL) in multiresistant strains of E. coli and Salmonella species originated from domestic animals. Acta Vet Beograd 57:369–379Google Scholar
  81. Ishida H, Ishida Y, Kurosaka Y, Otani T, Sato K, Kobayashi H (1998) In vitro and in vivo activities of levofloxacin against biofilm-producing Pseudomonas aeruginosa. Antimicrob Agents Chemother 42:1641–1645PubMedGoogle Scholar
  82. Jacoby GA, Han P (1996) Detection of extended-spectrum beta-lactamases in clinical isolates of Klebsiella pneumoniae and Escherichia coli. J Clin Microbiol 34:908–911PubMedGoogle Scholar
  83. Jacoby GA, Walsh KE, Mills DM, Walker VJ, Oh H, Robicsek A, Hooper DC (2006) qnrB, another plasmid-mediated gene for quinolone resistance. Antimicrob Agents Chemother 50:1178–1182PubMedGoogle Scholar
  84. Jang SS, Hansen LM, Breher JE, Riley DA, Magdesian KG, Madigan JE, Tang YJ, Silva J, Hirsh DC (1997) Antimicrobial susceptibilities of equine isolates of Clostridium difficile and molecular characterization of metronidazole-resistant strains. Clin Infect Dis 25:S266–S267PubMedGoogle Scholar
  85. Jevons MP, Rolinson GN, Knox R (1961) Celbenin-resistant staphylococci. Br Med J 1:124Google Scholar
  86. Jiang Y, Zhou ZH, Qian Y, Wei ZQ, Yu YS, Hu SN, Li LJ (2008) Plasmid-mediated quinolone resistance determinants qnr and aac(6′)-Ib-cr in extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in China. J Antimicrob Chemother 61:1003–1006PubMedGoogle Scholar
  87. Kajiura T, Wada H, Ito K, Anzai Y, Kato F (2006) Conjugative plasmid transfer in the biofilm formed by Enterococcus faecalis. J Health Sci 52:358–367Google Scholar
  88. Karisik E, Ellington MJ, Pike R, Warren RE, Livermore DM, Woodford N (2006) Molecular characterization of plasmids encoding CTX-M-15 beta-lactamases from Escherichia coli strains in the United Kingdom. J Antimicrob Chemother 58:665–668PubMedGoogle Scholar
  89. Kather EJ, Marks SL, Foley JE (2006) Determination of the prevalence of antimicrobial resistance genes in canine Clostridium perfringens isolates. Vet Microbiol 113:97–101PubMedGoogle Scholar
  90. Kim J, Jeong JH, Cha HY, Jin JS, Lee JC, Lee YC, Seol SY, Cho DT (2007) Detection of diverse SCCmec variants in methicillin-resistant Staphylococcus aureus and comparison of SCCmec typing methods. Clin Microbiol Infect 13:1128–1130PubMedGoogle Scholar
  91. Kizerwetter-Swida M, Chrobak D, Rzewuska M, Binek M (2009) Antibiotic resistance patterns and occurrence of mecA gene in Staphylococcus intermedius strains of canine origin. Pol J Vet Sci 12:9–13PubMedGoogle Scholar
  92. Klevens RM, Edwards JR, Tenover FC, McDonald LC, Horan T, Gaynes R (2006) Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992–2003. Clin Infect Dis 42:389–391PubMedGoogle Scholar
  93. Kliebe C, Nies BA, Meyer JF, Tolxdorffneutzling RM, Wiedemann B (1985) Evolution of plasmid-coded resistance to broad-spectrum cephalosporins. Antimicrob Agents Chemother 28:302–307PubMedGoogle Scholar
  94. Kotra LP, Haddad J, Mobashery S (2000) Aminoglycosides: perspectives on mechanisms of action and resistance and strategies to counter resistance. Antimicrob Agents Chemother 44:3249–3256PubMedGoogle Scholar
  95. Kuhl SA, Pattee PA, Baldwin JN (1978) Chromosomal map location of methicillin resistance determinant in Staphylococcus aureus. J Bacteriol 135:460–465PubMedGoogle Scholar
  96. Kuo HC, Chou CC, Tu C, Gong SR, Han CL, Liao JW, Chang SK (2009) Characterization of plasmid-mediated quinolone resistance by the qnrS gene in Escherichia coli isolated from healthy chickens and pigs. Vet Med 54:473–482Google Scholar
  97. Kvist M, Hancock V, Klemm P (2008) Inactivation of efflux pumps abolishes bacterial biofilm formation. Appl Environ Microbiol 74:7376–7382PubMedGoogle Scholar
  98. Lavigne JP, Marchandin H, Delmas J, Bouziges N, Lecaillon E, Cavalie L, Jean-Pierre H, Bonnet R, Sotto A (2006) qnrA in CTX-M-producing Escherichia coli isolates from France. Antimicrob Agents Chemother 50:4224–4228PubMedGoogle Scholar
  99. Leclercq R, Courvalin P (1991) Bacterial resistance to macrolide, lincosamide, and streptogramin antibiotics by target modification. Antimicrob Agents Chemother 35:1267–1272PubMedGoogle Scholar
  100. Leclercq R, Derlot E, Duval J, Courvalin P (1988) Plasmid-mediated resistance to vancomycin and teicoplanin in Enterococcus faecium. N Engl J Med 319:157–161PubMedGoogle Scholar
  101. Lederberg J, Lederberg EM (1952) Replica plating and indirect selection of bacterial mutants. J Bacteriol 63:399–406PubMedGoogle Scholar
  102. Leiros HKS, Kozielski-Stuhrmann S, Kapp U, Terradot L, Leonard GA, McSweeney SM (2004) Structural basis of 5-nitroimidazole antibiotic resistance – the crystal structure of NimA from Deinococcus radiodurans. J Biol Chem 279:55840–55849PubMedGoogle Scholar
  103. Leverstein-van Hall MA, Blok HEM, Donders ART, Paauw A, Fluit AC, Verhoef J (2003) Multidrug resistance among Enterobacteriaceae is strongly associated with the presence of integrons and is independent of species or isolate origin. J Infect Dis 187:251–259PubMedGoogle Scholar
  104. Lewis K (2001) Riddle of biofilm resistance. Antimicrob Agents Chemother 45:999–1007PubMedGoogle Scholar
  105. Liebana E, Gibbs M, Clouting C, Barker L, Clifton-Hadley FA, Pleydell E, Abdalhamid B, Hanson ND, Martin L, Poppe C, Davies RH (2004) Characterization of beta-lactamases responsible for resistance to extended-spectrum cephalosporins in Escherichia coli and Salmonella enterica strains from food-producing animals in the United Kingdom. Microb Drug Resist 10:1–9PubMedGoogle Scholar
  106. Liebana E, Batchelor M, Hopkins KL, Clifton-Hadley FA, Teale CJ, Foster A, Barker L, Threlfall EJ, Davies RH (2006) Longitudinal farm study of extended-spectrum beta-lactamase-mediated resistance. J Clin Microbiol 44:1630–1634PubMedGoogle Scholar
  107. Livermore DM (2003) Bacterial resistance: origins, epidemiology, and impact. Clin Infect Dis 36:S11–S23PubMedGoogle Scholar
  108. Loeffler A, Boag AK, Sung J, Lindsay JA, Guardabassi L, Dalsgaard A, Smith H, Stevens KB, Lloyd DH (2005) Prevalence of methicillin-resistant Staphylococcus aureus among staff and pets in a small animal referral hospital in the UK. J Antimicrob Chemother 56:692–697PubMedGoogle Scholar
  109. Luethje P, Schwarz S (2007) Molecular basis of resistance to macrolides and lincosamides among staphylococci and streptococci from various animal sources collected in the resistance monitoring program Bff-GermVet. Int J Antimicrob Agents 29:528–535Google Scholar
  110. Machado E, Coque TM, Canton R, Baquero F, Sousa JC, Peixe L, Portuguese Resistance Study Group (2006) Dissemination in Portugal of CTX-M-15-, OYA-1-, and TEM-1-producing Enterobacteriaceae strains containing the aac(6′)-Ib-cr gene, which encodes an aminoglycoside- and fluoroquinolone-modifying enzyme. Antimicrob Agents Chemother 50:3220–3220PubMedGoogle Scholar
  111. Malik S, Christensen H, Peng H, Barton MD (2007) Presence and diversity of the beta-lactamase gene in cat and dog staphylococci. Vet Microbiol 123:162–168PubMedGoogle Scholar
  112. Mangalappalli-Illathu AK, Lawrence JR, Swerhone GDW, Korber DR (2008) Architectural adaptation and protein expression patterns of Salmonella enterica serovar Enteritidis biofilms under laminar flow conditions. Int J Food Microbiol 123:109–120PubMedGoogle Scholar
  113. Martinez-Martinez L, Pascual A, Jacoby GA (1998) Quinolone resistance from a transferable plasmid. Lancet 351:797–799PubMedGoogle Scholar
  114. Martínez-Martínez L, Pascual A, García I, Tran JH, Jacoby GA (2003) Interaction of plasmid and host quinolone resistance. J Antimicrob Chemother 51:1037–1039PubMedGoogle Scholar
  115. Matsumoto Y, Ikeda F, Kamimura T, Yokota Y, Mine Y (1988) Novel plasmid-mediated 3-lactamase from Escherichia coli that inactivates oxyimino-cephalosporins. Antimicrob Agents Chemother 32:1243–1246PubMedGoogle Scholar
  116. Matthews DA, Bolin JT, Burridge JM, Filman DJ, Volz KW, Kraut J (1985) Dihydrofolate reductase. The stereochemistry of inhibitor selectivity. J Biol Chem 260:392–399PubMedGoogle Scholar
  117. May T, Ito A, Okabe S (2009) Induction of multidrug resistance mechanism in Escherichia coli biofilms by interplay between tetracycline and ampicillin resistance genes. Antimicrob Agents Chemother 53:4628–4639PubMedGoogle Scholar
  118. McKay KA, Ruhnke HL, Barnum DA (1965) The results of sensitivity tests on animal pathogens conducted over the period 1956–1963. Can Vet J 6:103–111PubMedGoogle Scholar
  119. Monzon M, Oteiza C, Leiva J, Lamata M, Amorena B (2002) Biofilm testing of Staphylococcus epidermidis clinical isolates: low performance of vancomycin in relation to other antibiotics. Diagn Microbiol Infect Dis 44:319–324PubMedGoogle Scholar
  120. Moura I, Radhouani H, Torres C, Poeta P, Igrejas G (2010) Detection and genetic characterisation of vanA-containing Enterococcus strains in healthy Lusitano horses. Equine Vet J 42:181–183PubMedGoogle Scholar
  121. Naseer U, Haldorsen B, Tofteland S, Hegstad K, Scheutz F, Simonsen GS, Sundsfjord A, Norwegian ESG (2009) Molecular characterization of CTX-M-15-producing clinical isolates of Escherichia coli reveals the spread of multidrug-resistant ST131 (O25:H4) and ST964 (O102:H6) strains in Norway. APMIS 117:526–536PubMedGoogle Scholar
  122. Nicolas-Chanoine MH, Blanco J, Leflon-Guibout V, Demarty R, Alonso MP, Canica MM, Park YJ, Lavigne JP, Pitout J, Johnson JR (2008) Intercontinental emergence of Escherichia coli clone O25: H4-ST131 producing CTX-M-15. J Antimicrob Chemother 61:273–281PubMedGoogle Scholar
  123. Nordmann P, Poirel L (2005) Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemother 56:463–469PubMedGoogle Scholar
  124. Ogeer-Gyles JS, Mathews KA, Boerlin P (2006) Nosocomial infections and antimicrobial resistance in critical care medicine. J Vet Emerg Crit Care 16:1–18Google Scholar
  125. Oliver A, Canton R, Campo P, Baquero F, Blazquez J (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251–1253PubMedGoogle Scholar
  126. Oliver A, Perez-Diaz JC, Coque TM, Baquero F, Canton R (2001) Nucleotide sequence and characterization of a novel cefotaxime-hydrolyzing beta-lactamase (CTX-M-10) isolated in Spain. Antimicrob Agents Chemother 45:616–620PubMedGoogle Scholar
  127. Ossiprandi MC, Bottarelli E, Cattabiani F, Bianchi E (2008) Susceptibility to vancomycin and other antibiotics of 165 Enterococcus strains isolated from dogs in Italy. Comp Immunol Microbiol Infect Dis 31:1–9PubMedGoogle Scholar
  128. Owen MR, Moores AP, Coe RJ (2004) Management of MRSA septic arthritis in a dog using a gentamicin-impregnated collagen sponge. J Small Anim Pract 45:609–612PubMedGoogle Scholar
  129. Paladino JA, Sunderlin JL, Price CS, Schentag JJ (2002) Economic consequences of antimicrobial resistance. Surg Infect (Larchmt) 3:259–267Google Scholar
  130. Papanicolaou GA, Medeiros AA, Jacoby GA (1990) Novel plasmid-mediated β-lactamase (MIR-1) conferring resistance to oxyimino- and a-methoxy β-lactams in clinical isolates of Klebsiella pneumoniae. Antimicrob Agents Chemother 34:2200–2209PubMedGoogle Scholar
  131. Perichon B, Courvalin P, Galimand M (2007) Transferable resistance to aminoglycosides by methylation of G1405 in 16S rRNA and to hydrophilic fluoroquinolones by QepA-mediated efflux in Escherichia coli. Antimicrob Agents Chemother 51:2464–2469PubMedGoogle Scholar
  132. Perreten V, Kadlec K, Schwarz S, Andersson UG, Finn M, Greko C, Moodley A, Kania SA, Frank LA, Bemis DA, Franco A, Iurescia M, Battisti A, Duim B, Wagenaar JA, van Duijkeren E, Weese JS, Fitzgerald JR, Rossano A, Guardabassi L (2010) Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: an international multicentre study. J Antimicrob Chemother 65:1145–1154PubMedGoogle Scholar
  133. Pitout JDD, Laupland KB (2008) Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 8:159–166PubMedGoogle Scholar
  134. Poeta P, Costa D, Rodrigues J, Torres C (2005) Study of faecal colonization by vanA-containing Enterococcus strains in healthy humans, pets, poultry and wild animals in Portugal. J Antimicrob Chemother 55:278–280PubMedGoogle Scholar
  135. Pomba C, da Fonseca JD, Baptista BC, Correia JD, Martinez-Martinez L (2009) Detection of the pandemic O25-ST131 human virulent Escherichia coli CTX-M-15-producing clone harboring the qnrB2 and aac(6′)-Ib-cr genes in a dog. Antimicrob Agents Chemother 53:327–328PubMedGoogle Scholar
  136. Pyorala S, Taponen S (2009) Coagulase-negative staphylococci-emerging mastitis pathogens. Vet Microbiol 134:3–8PubMedGoogle Scholar
  137. Rachid S, Ohlsen K, Witte W, Hacker J, Ziebuhr W (2000) Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrob Agents Chemother 44:3357–3363PubMedGoogle Scholar
  138. Ramsay JWA, Garnham AJ, Mulhall AB, Crow RA, Bryan JM, Eardley I, Vale JA, Whitfield HN (1989) Biofilms, bacteria and bladder catheters. A clinical study. Br J Urol 64:395–398PubMedGoogle Scholar
  139. Rankin SC, Whichard JM, Joyce K, Stephens L, O’Shea K, Aceto H, Munro DS, Benson CE (2005) Detection of a bla(SHV) extended-spectrum beta-lactamase in Salmonella enterica serovar Newport MDR-AmpC. J Clin Microbiol 43:5792–5793PubMedGoogle Scholar
  140. Reece RJ, Maxwell A, Wang JC (1991) DNA gyrase: structure and function. Crit Rev Biochem Mol Biol 26:335–375PubMedGoogle Scholar
  141. Rice EW, Boczek LA, Johnson CH, Messer JW (2003) Detection of intrinsic vancomycin resistant enterococci in animal and human feces. Diagn Microbiol Infect Dis 46:155–158PubMedGoogle Scholar
  142. Riesen A, Perreten V (2009) Antibiotic resistance and genetic diversity in Staphylococcus aureus from slaughter pigs in Switzerland. Schweiz Arch Tierheilkd 151:425–431PubMedGoogle Scholar
  143. Roberts MC (1996) Tetracycline resistance determinants: mechanisms of action, regulation of expression, genetic mobility, and distribution. FEMS Microbiol Rev 19:1–24PubMedGoogle Scholar
  144. Roberts MC (2005) Update on acquired tetracycline resistance genes. FEMS Microbiol Lett 245:195–203PubMedGoogle Scholar
  145. Roberts MC, Sutcliffe J, Courvalin P, Jensen LB, Rood J, Seppala H (1999) Nomenclature for macrolide and macrolide-lincosamide-streptogramin B resistance determinants. Antimicrob Agents Chemother 43:2823–2830PubMedGoogle Scholar
  146. Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D, Park CH, Bush K, Hooper DC (2006) Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med 12:83–88PubMedGoogle Scholar
  147. Rossolini GM, Mantengoli E, Montagnani F, Pollini S (2010) Epidemiology and clinical relevance of microbial resistance determinants versus anti-Gram-positive agents. Curr Opin Microbiol 13:582–588PubMedGoogle Scholar
  148. Roupas A, Pitton JS (1974) R factor-mediated and chromosomal resistance to ampicillin in Escherichia coli. Antimicrob Agents Chemother 5:186–191PubMedGoogle Scholar
  149. Ruiz J (2003) Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection. J Antimicrob Chemother 51:1109–1117PubMedGoogle Scholar
  150. Saenz Y, Zarazaga M, Brinas L, Lantero M, Ruiz-Larrea F, Torres C (2001) Antibiotic resistance in Escherichia coli isolates obtained from animals, foods and humans in Spain. Int J Antimicrob Agents 18:353–358PubMedGoogle Scholar
  151. Saenz Y, Brinas L, Dominguez E, Ruiz J, Zarazaga M, Vila J, Torres C (2004) Mechanisms of resistance in multiple-antibiotic-resistant Escherichia coli strains of human, animal, and food origins. Antimicrob Agents Chemother 48:3996–4001PubMedGoogle Scholar
  152. Sailer FC, Meberg BM, Young KD (2003) Beta-lactam induction of colanic acid gene expression in Escherichia coli. FEMS Microbiol Lett 226:245–249PubMedGoogle Scholar
  153. Sanders CC (1987) Chromosomal cephalosporinases responsible for multiple resistance to newer β-lactam antibiotics. Annu Rev Microbiol 41:573–593PubMedGoogle Scholar
  154. Sanders WE, Sanders CC (1988) Inducible beta-lactamases: clinical and epidemiologic implications for use of newer cephalosporins. Rev Infect Dis 10:830–838PubMedGoogle Scholar
  155. Sanders CC, Bradford PA, Ehrhardt AF, Bush K, Young KD, Henderson TA, Sanders EW (1997) Penicillin-binding proteins and induction of AmpC beta-lactamase. Antimicrob Agents Chemother 41:2013–2015PubMedGoogle Scholar
  156. Saroglou G, Cromer M, Bisno AL (1980) Methicillin-resistant Staphylococcus aureus – interstate spread of nosocomial infections with emergence of gentamicin–methicillin resistant strains. Infect Control Hosp Epidemiol 1:81–89Google Scholar
  157. Schnellmann C, Gerber V, Rossano A, Jaquier V, Panchaud Y, Doherr MG, Thomann A, Straub R, Perreten V (2006) Presence of new mecA and mph(C) variants conferring antibiotic resistance in Staphylococcus spp. isolated from the skin of horses before and after clinic admission. J Clin Microbiol 44:4444–4454PubMedGoogle Scholar
  158. Schwarz S, Kadlec K, Strommenger B (2008) Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius detected in the BfT-GermVet monitoring programme 2004–2006 in Germany. J Antimicrob Chemother 61:282–285PubMedGoogle Scholar
  159. Seo MR, Park YS, Pai H (2010) Characteristics of plasmid-mediated quinolone resistance genes in extended-spectrum cephalosporin-resistant isolates of Klebsiella pneumoniae and Escherichia coli in Korea. Chemotherapy 56:46–53PubMedGoogle Scholar
  160. Shaw KJ, Rather PN, Hare RS, Miller GH (1993) Molecular-genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol Rev 57:138–163PubMedGoogle Scholar
  161. Sheehan E, McKenna J, Mulhall KJ, Marks P, McCormack D (2004) Adhesion of Staphylococcus to orthopaedic metals, an in vivo study. J Orthop Res 22:39–43PubMedGoogle Scholar
  162. Shigeta M, Tanaka G, Komatsuzawa H, Sugai M, Suginaka H, Usui T (1997) Permeation of antimicrobial agents through Pseudomonas aeruginosa biofilms: a simple method. Chemotherapy 43:340–345PubMedGoogle Scholar
  163. Sidjabat HE, Hanson ND, Smith-Moland E, Bell JM, Gibson JS, Filippich LJ, Trott DJ (2007) Identification of plasmid-mediated extended-spectrum and AmpC beta-lactamases in Enterobacter spp. isolated from dogs. J Med Microbiol 56:426–434PubMedGoogle Scholar
  164. Singh R, Ray P, Das A, Sharma M (2010) Penetration of antibiotics through Staphylococcus aureus and Staphylococcus epidermidis biofilms. J Antimicrob Chemother 65:1955–1958PubMedGoogle Scholar
  165. Skinner S, Inglis B, Matthews PR, Stewart PR (1988) Mercury and tetracycline resistance genes and flanking repeats associated with methicillin resistance on the chromosome of Staphylococcus aureus. Mol Microbiol 2:289–292PubMedGoogle Scholar
  166. Smith MM, Vasseur PB, Saunders HM (1989) Bacterial growth associated with metallic implants in dogs. J Am Vet Med Assoc 195:765–767PubMedGoogle Scholar
  167. Sternberg C, Christensen BB, Johansen T, Toftgaard Nielsen A, Andersen JB, Givskov M, Molin S (1999) Distribution of bacterial growth activity in flow-chamber biofilms. Appl Environ Microbiol 65:4108–4117PubMedGoogle Scholar
  168. Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138PubMedGoogle Scholar
  169. Stone G, Wood P, Dixon L, Keyhan M, Matin A (2002) Tetracycline rapidly reaches all the constituent cells of uropathogenic Escherichia coli biofilms. Antimicrob Agents Chemother 46:2458–2461PubMedGoogle Scholar
  170. Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A (2009) Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 22:664-PubMedGoogle Scholar
  171. Suzuki S, Shibata N, Yamane K, Wachino J, Ito K, Arakawa Y (2009) Change in the prevalence of extended-spectrum-beta-lactamase-producing Escherichia coli in Japan by clonal spread. J Antimicrob Chemother 63:72–79PubMedGoogle Scholar
  172. Towner KJ, Brennan A, Zhang Y, Holtham CA, Brough JL, Carter GI (1994) Genetic structures associated with spread of the type IA trimethoprim-resistant dihydrofolate-reductase gene amongst Escherichia coli strains isolated in the Nottingham area of the United-Kingdom. J Antimicrob Chemother 33:25–32PubMedGoogle Scholar
  173. Tran Van Nhieu G, Bordon F, Collatz E (1992) Incidence of an aminoglycoside 6′-N-acetyltransferase, ACC(6′)-1b, in amikacin-resistant clinical isolates of Gram-negative bacilli, as determined by DNA–DNA hybridisation and immunoblotting. J Med Microbiol 36:83–88PubMedGoogle Scholar
  174. Tran JH, Jacoby GA (2002) Mechanism of plasmid-mediated quinolone resistance. Proc Natl Acad Sci USA 99:5638–5642PubMedGoogle Scholar
  175. Tran JH, Jacoby GA, Hooper DC (2005) Interaction of the plasmid-encoded quinolone resistance protein Qnr with Escherichia coli DNA gyrase. Antimicrob Agents Chemother 49:118–125PubMedGoogle Scholar
  176. Tuckman M, Petersen PJ, Howe AYM, Orlowski M, Mullen S, Chan K, Bradford PA, Jones CH (2007) Occurrence of tetracycline resistance genes among Escherichia coli isolates from the phase 3 clinical trials for tigecycline. Antimicrob Agents Chemother 51:3205–3211PubMedGoogle Scholar
  177. Tupin A, Gualtieri M, Roquet-Baneres F, Morichaud Z, Brodolin K, Leonetti JP (2010) Resistance to rifampicin: at the crossroads between ecological, genomic and medical concerns. Int J Antimicrob Agents 35:519–523PubMedGoogle Scholar
  178. Turkyilmaz S, Erdem V, Bozdogan B (2010) Investigation of antimicrobial susceptibility for enterococci isolated from cats and dogs and the determination of resistance genes by polymerase chain reaction. Turk J Vet Anim Sci 34:61–68Google Scholar
  179. Tzouvelekis LS, Tzelepi E, Tassios PT, Legakis NJ (2000) CTX-M-type beta-lactamases: an emerging group of extended-spectrum enzymes. Int J Antimicrob Agents 14:137–142PubMedGoogle Scholar
  180. van Duijkeren E, Vulto AG, Vanmiert A (1994) Trimethoprim sulfonamide combinations in the horse – a review. J Vet Pharmacol Ther 17:64–73PubMedGoogle Scholar
  181. van Duijkeren E, Moleman M, van Oldruitenborgh-Oosterbaan MMS, Multem J, Troelstra A, Fluit AC, van Wamel WJB, Houwers DJ, de Neeling AJ, Wagenaar JA (2010) Methicillin-resistant Staphylococcus aureus in horses and horse personnel: an investigation of several outbreaks. Vet Microbiol 141:96–102PubMedGoogle Scholar
  182. Vanni M, Tognetti R, Pretti C, Crema F, Soldani G, Meucci V, Intorre L (2009) Antimicrobial susceptibility of Staphylococcus intermedius and Staphylococcus schleiferi isolated from dogs. Res Vet Sci 87:192–195PubMedGoogle Scholar
  183. Vengust M, Anderson MEC, Rousseau J, Weese JS (2006) Methicillin-resistant staphylococcal colonization in clinically normal dogs and horses in the community. Lett Appl Microbiol 43:602–606PubMedGoogle Scholar
  184. VMD (2009) Sales of antimicrobial products used as veterinary medicines, growth promoters and coccidiostats in the UK in 2008., Accessed November 2010
  185. Vo ATT, van Duijkeren E, Fluit AC, Gaastra W (2007) Characteristics of extended-spectrum cephalosporin-resistant Escherichia coli and Klebsiella pneumoniae isolates from horses. Vet Microbiol 124:248–255PubMedGoogle Scholar
  186. Waksman SA, Reilly HC, Schatz A (1945) Strain specificity and production of antibiotic substances: V. Strain resistance of bacteria to antibiotic substances, especially to streptomycin. Proc Natl Acad Sci USA 31:157–164PubMedGoogle Scholar
  187. Wang MH, Guo QL, Xu XG, Wang XY, Ye XY, Wu S, Hooper DC, Wang MG (2009) New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother 53:1892–1897PubMedGoogle Scholar
  188. Weese J, van Duijkeren E (2010) Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in veterinary medicine. Vet Microbiol 140:418–429PubMedGoogle Scholar
  189. Weese JS, Rousseau J, Traub-Dargatz JL, Willey BM, McGeer AJ, Low DE (2005) Community-associated methicillin-resistant Staphylococcus aureus in horses and humans who work with horses. J Am Vet Med Assoc 226:580–583PubMedGoogle Scholar
  190. Weigel LM, Donlan RM, Shin DH, Jensen B, Clark NC, McDougal LK, Zhu WM, Musser KA, Thompson J, Kohlerschinidt D, Dumas N, Limberger RJ, Patel JB (2007) High-level vancomycin-resistant Staphylococcus aureus isolates associated with a polymicrobial biofilm. Antimicrob Agents Chemother 51:231–238PubMedGoogle Scholar
  191. Weisblum B (1995) Insights into erythromycin action from studies of its activity as inducer of resistance. Antimicrob Agents Chemother 39:797–805PubMedGoogle Scholar
  192. White PA, Rawlinson WD (2001) Current status of the aadA and dfr gene cassette families. J Antimicrob Chemother 47:495–496PubMedGoogle Scholar
  193. White PA, McIver CJ, Deng YM, Rawlinson WD (2000) Characterisation of two new gene cassettes, aadA5 and dfrA17. FEMS Microbiol Lett 182:265–269PubMedGoogle Scholar
  194. WHO (2007) Critically important antimicrobials for human medicine. In: Report of the second WHO expert meeting, Copenhagen, 29–31 May 2007Google Scholar
  195. Wimpenny J, Manz W, Szewzyk U (2000) Heterogeneity in biofilms. FEMS Microbiol Rev 24:661–671PubMedGoogle Scholar
  196. Woodford N, Johnson AP, Morrison D, Speller DCE (1995) Current perspectives on glycopeptide resistance. Clin Microbiol Rev 8:585–615PubMedGoogle Scholar
  197. Woodford N, Carattoli A, Karisik E, Underwood A, Ellington MJ, Livermore DM (2009) Complete nucleotide sequences of plasmids pEK204, pEK499, and pEK516, encoding CTX-M enzymes in three major Escherichia coli lineages from the United Kingdom, all belonging to the international O25:H4-ST131 clone. Antimicrob Agents Chemother 53:4472–4482PubMedGoogle Scholar
  198. Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175–186PubMedGoogle Scholar
  199. Yamane K, Wachino JI, Suzuki S, Kimura K, Shibata N, Kato H, Shibayama K, Konda T, Arakawa Y (2007) New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate. Antimicrob Agents Chemother 51:3354–3360PubMedGoogle Scholar
  200. Yan J, Wu J, Ko W, Tsai S, Chuang C, Wu H, Lu Y, Li J (2004) Plasmid-mediated 16S rRNA methylases conferring high-level aminoglycoside resistance in Escherichia coli and Klebsiella pneumoniae isolates from two Taiwanese hospitals. J Antimicrob Chemother 54:1007–1012PubMedGoogle Scholar
  201. Zhang L, Mah TF (2008) Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J Bacteriol 190:4447–4452PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Faculty of Health and Life Sciences, School of Veterinary ScienceUniversity of LiverpoolNestonUK

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