Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-27T11:49:19.289Z Has data issue: false hasContentIssue false

Antimicrobial resistance: its emergence and transmission

Published online by Cambridge University Press:  22 December 2008

Patrick Boerlin*
Affiliation:
Department of Pathobiology, Ontario Veterinary College, Guelph, ON, N1G 2W1, Canada Laboratory for Foodborne Zoonoses, Public Health Agency of Canada, 110 Stone Road West, Guelph, ON, N1G 3W4, Canada
Richard J. Reid-Smith
Affiliation:
Department of Pathobiology, Ontario Veterinary College, Guelph, ON, N1G 2W1, Canada Laboratory for Foodborne Zoonoses, Public Health Agency of Canada, 110 Stone Road West, Guelph, ON, N1G 3W4, Canada Department of Population Medicine, Ontario Veterinary College, Guelph, ON, N1G 2W1, Canada
*
*Corresponding author. E-mail: pboerlin@uoguelph.ca

Abstract

New concepts have emerged in the past few years that help us to better understand the emergence and spread of antimicrobial resistance (AMR). These include, among others, the discovery of the mutator state and the concept of mutant selection window for resistances emerging primarily through mutations in existing genes. Our understanding of horizontal gene transfer has also evolved significantly in the past few years, and important new mechanisms of AMR transfer have been discovered, including, among others, integrative conjugative elements and ISCR (insertion sequences with common regions) elements. Simultaneously, large-scale studies have helped us to start comprehending the immense and yet untapped reservoir of both AMR genes and mobile genetic elements present in the environment. Finally, new PCR- and DNA sequencing-based techniques are being developed that will allow us to better understand the epidemiology of classical vectors of AMR genes, such as plasmids, and to monitor them in a more global and systematic way.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aarestrup, FM, Seyfarth, AM, Emborg, HD, Pederson, K, Hendriksen, RS and Bager, F (2001). Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrobial Agents and Chemotherapy 45: 20543059.CrossRefGoogle ScholarPubMed
Aarestrup, FM (2006). The origin, evolution, and local and global dissemination of antimicrobial resistance. In: Aarestrup, FM (ed) Antimicrobial Resistance in Bacteria of Animal Origin. Washington, DC: ASM Press, pp. 339359.Google Scholar
Adesiyun, A, Offiah, N, Seepersadsingh, N, Rodrigo, S, Lashley, V and Musai, L (2007). Antimicrobial resistance of Salmonella spp. and Escherichia coli isolated from table eggs. Food Control 18: 306311.CrossRefGoogle Scholar
Almeida, D, Nuermberger, E, Tyagi, S, Bishai, WR and Grosset, J (2007). In vivo validation of the mutant selection window hypothesis with moxifloxacin in a murine model of tuberculosis. Antimicrobial Agents and Chemotherapy 51: 42614266.CrossRefGoogle Scholar
Anderson, JF, Parrish, TD, 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. Applied and Environmental Microbiology 74: 17261730.CrossRefGoogle ScholarPubMed
Antunes, P, Machado, J and Peixe, L (2007). Dissemination of sul3-containing elements linked to class 1 integrons with an unusual 3′ conserved sequence region among Salmonella isolates. Antimicrobial Agents and Chemotherapy 51: 15451548.CrossRefGoogle ScholarPubMed
Bannoehr, J, Ben Zakour, NL, Waller, AS, Guardabassi, L, Thoday, KL, van den Broek, AH and Fitzgerald, JR (2007). Population genetic structure of the Staphylococcus intermedius group: insights into agr diversification and the emergence of methicillin-resistant strains. Journal of Bacteriology 189: 86858692.CrossRefGoogle ScholarPubMed
Baquero, MR, Galan, JC, del Carmen Turrientes, M, Canton, R, Coque, TM, Martinez, JL and Baquero, F (2005). Increased mutation frequencies in Escherichia coli isolates harboring extended-spectrum beta-lactamases. Antimicrobial Agents and Chemotherapy 49: 47544756.CrossRefGoogle ScholarPubMed
Baurenfeind, A, Stemplinger, I, Jungwirth, R and Giamarellou, H (1996). Characterization of the plasmidic β-lactamase CMY-2, which is responsible for cephamycin resistance. Antimicrobial Agents and Chemotherapy 40: 221224.CrossRefGoogle Scholar
Bennett, PM (2008). Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. British Journal of Pharmacology 153 (suppl. 1): S347S357.CrossRefGoogle ScholarPubMed
Bischoff, KM, White, DG, Hume, ME, Poole, TL and Nisbet, DJ (2005). The chloramphenicol resistance gene cmlA is disseminated on transferable plasmids that confer multiple-drug resistance in swine Escherichia coli. FEMS Microbiology Letters 243: 285291.CrossRefGoogle ScholarPubMed
Blazquez, J (2003). Hypermutation as a factor contributing to the acquisition of antimicrobial resistance. Clinical Infectious Diseases 37: 12011209.Google Scholar
Boucher, HW and Corey, GR (2008). Epidemiology of methicillin-resistant Staphylococcus aureus. Clinical Infectious Diseases 46 (suppl. 5): S344S349.CrossRefGoogle ScholarPubMed
Boucher, Y, Labbate, M, Koenig, JE and Stokes, HW (2007). Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends in Microbiology 15: 301309.CrossRefGoogle ScholarPubMed
Boyd, D, Peters, GA, Cloeckaert, A, Boumedine, KS, Chaslus-Dancla, E, Imberechts, H and Mulvey, MR (2001). Complete nucleotide sequence of a 43-kilobase genomic island associated with the multidrug resistance region of Salmonella enterica serovar Typhimurium DT104 and its identification in phage type DT120 and serovar Agona. Journal of Bacteriology 183: 57255732.CrossRefGoogle ScholarPubMed
Briggs, CE and Fratamico, PM (1999). Molecular characterization of an antibiotic resistance gene cluster of Salmonella typhimurium DT104. Antimicrobial Agents and Chemotherapy 43: 846849.CrossRefGoogle ScholarPubMed
Burrus, V and Waldor, MK (2004). Shaping bacterial genomes with integrative and conjugative elements. Research in Microbiology 155: 376386.CrossRefGoogle ScholarPubMed
Burrus, V, Pavlovic, G, Decaris, B and Guedon, G (2002). Conjugative transposons: the tip of the iceberg. Molecular Microbiology 46: 601610.CrossRefGoogle ScholarPubMed
Cantón, R and Coque, TM (2006). The CTX-M β-lactamase pandemic. Current Opinions in Microbiology 9: 466–465.CrossRefGoogle ScholarPubMed
Carattoli, A, Tosini, F, Giles, WP, Rupp, ME, Hinrichs, SH, Angulo, FJ, Barrett, TJ and Fey, PD (2002). Characterization of plasmids carrying CMY-2 from expanded-spectrum cephalosporin-resistant Salmonella strains isolated in the United States between 1996 and 1998. Antimicrobial Agents and Chemotherapy 46: 12691272.CrossRefGoogle ScholarPubMed
Carattoli, A, Bertini, A, Villa, L, Falbo, V, Hopkins, KL and Threlfall, EJ (2005). Identification of plasmids by PCR-based replicon typing. Journal of Microbiological Methods 63: 219228.CrossRefGoogle ScholarPubMed
Carattoli, A, Miriagou, V, Bertini, A, Loli, A, Colinon, C, Villa, L, Whichard, JM and Rossolini, GM (2006). Replicon typing of plasmids encoding resistance to newer beta-lactams. Emerging Infectious Diseases 12: 11451148.CrossRefGoogle ScholarPubMed
Chopra, I, O'Neill, AJ and Miller, K (2003). The role of mutators in the emergence of antibiotic-resistant bacteria. Drug Resistance Updates 6: 137145.CrossRefGoogle ScholarPubMed
Cirz, RT, Chin, JK, Andes, DR, de Crecy-Lagard, V, Craig, WA and Romesberg, FE (2005). Inhibition of mutation and combating the evolution of antibiotic resistance. PLoS Biology 3: e176.CrossRefGoogle ScholarPubMed
Couturier, M, Bex, F, Bergquist, PL and Maas, WK (1988). Identification and classification of bacterial plasmids. Microbiological Reviews 52: 375395.CrossRefGoogle ScholarPubMed
Croisier, D, Etienne, M, Bergoin, E, Charles, PE, Lequeu, C, Piroth, L, Portier, H and Chavanet, P (2004). Mutant selection window in levofloxacin and moxifloxacin treatments of experimental pneumococcal pneumonia in a rabbit model of human therapy. Antimicrobial Agents and Chemotherapy 48: 16991707.CrossRefGoogle Scholar
Cui, J, Liu, Y, Wang, R, Tong, W, Drlica, K and Zhao, X (2006). The mutant selection window in rabbits infected with Staphylococcus aureus. Journal of Infectious Diseases 194: 16011608.CrossRefGoogle ScholarPubMed
Dargatz, DA, Strohmeyer, RA, Morley, PS, Hyatt, DR and Salman, MA (2005). Characterization of Escherichia coli and Salmonella enterica from cattle feed ingredients. Foodborne Pathogens and Disease 2: 341347.CrossRefGoogle ScholarPubMed
Davies, J (1994). Inactivation of antibiotics and the dissemination of resistance genes. Science (New York) 264: 375382.CrossRefGoogle ScholarPubMed
Davies, J, Spiegelman, GB and Yim, G (2006). The world of subinhibitory antibiotic concentrations. Current Opinion in Microbiology 9: 445453.CrossRefGoogle ScholarPubMed
D'Costa, VM, Griffiths, E and Wright, GD (2007). Expanding the soil antibiotic resistome: exploring environmental diversity. Current Opinion in Microbiology 10: 481498.CrossRefGoogle ScholarPubMed
de Neeling, AJ, van den Broek, MJ, Spalburg, EC, van Santen-Verheuvel, MG, Dam-Deisz, WD, Boshuizen, HC, van de Giessen, AW, van Duijkeren, E and Huijsdens, XW (2007). High prevalence of methicillin resistant Staphylococcus aureus in pigs. Veterinary Microbiology 122: 366372.CrossRefGoogle ScholarPubMed
Denamur, E and Matic, I (2006). Evolution of mutation rates in bacteria. Molecular Microbiology 60: 820827.CrossRefGoogle ScholarPubMed
Deurenberg, RH and Stobberingh, EE (2008). The evolution of Staphylococcus aureus. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, in press.Google Scholar
Doublet, B, Boyd, D, Mulvey, MR and Cloeckaert, A (2005). The Salmonella genomic island 1 is an integrative mobilizable element. Molecular Microbiology 55: 19111924.CrossRefGoogle ScholarPubMed
Drlica, K (2003). The mutant selection window and antimicrobial resistance. The Journal of Antimicrobial Chemotherapy 52: 1117.CrossRefGoogle ScholarPubMed
Drlica, K and Zhao, X (2007). Mutant selection window hypothesis updated. Clinical Infectious Diseases 44: 681688.CrossRefGoogle ScholarPubMed
Enright, MC, Robinson, DA, Randle, G, Feil, EJ, Grundmann, H and Spratt, BG (2002). The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proceedings of the National Academy of Sciences of the United States of America 99: 76877692.CrossRefGoogle ScholarPubMed
Fajardo, A and Martinez, JL (2008). Antibiotics as signals that trigger specific bacterial responses. Current Opinion in Microbiology 11: 161167.CrossRefGoogle ScholarPubMed
Ferran, A, Dupouy, V, Toutain, PL and Bousquet-Melou, A (2007). Influence of inoculum size on the selection of resistant mutants of Escherichia coli in relation to mutant prevention concentrations of marbofloxacin. Antimicrobial Agents and Chemotherapy 51: 41634166.CrossRefGoogle ScholarPubMed
Firsov, AA, Vostrov, SN, Lubenko, IY, Drlica, K, Portnoy, YA and Zinner, SH (2003). In vitro pharmacodynamic evaluation of the mutant selection window hypothesis using four fluoroquinolones against Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 47: 16041613.CrossRefGoogle ScholarPubMed
Fluit, AC and Schmitz, FJ (2004). Resistance integrons and super-integrons. Clinical Microbiology and Infection 10: 272288.CrossRefGoogle ScholarPubMed
Foster, PL (2007). Stress-induced mutagenesis in bacteria. Critical Reviews in Biochemistry and Molecular Biology 42: 373397.CrossRefGoogle ScholarPubMed
Franke, AE and Clewell, DB (1981). Evidence for a chromosome-borne resistance transposon (Tn916) in Streptococcus faecalis that is capable of ‘conjugal’ transfer in the absence of a conjugative plasmid. Journal of Bacteriology 145: 494502.CrossRefGoogle ScholarPubMed
Garcia-Fernandez, A, Chiaretto, G, Bertini, A, Villa, L, Fortini, D, Ricci, A and Carattoli, A (2008). Multilocus sequence typing of IncI1 plasmids carrying extended-spectrum beta-lactamases in Escherichia coli and Salmonella of human and animal origin. Journal of Antimicrobial Chemotherapy 61: 12291233.CrossRefGoogle ScholarPubMed
Garnier, F, Raked, N, Gassama, A, Denis, F and Ploy, MC (2006). Genetic environment of quinolone resistance gene qnrB2 in a complex sul1-type integron in the newly described Salmonella enterica serovar Keurmassar. Antimicrobial Agents and Chemotherapy 50: 32003202.CrossRefGoogle Scholar
Giles, WP, Benson, AK, Olson, ME, Hutkins, RW, Whichard, JM, Winokur, PL and Fey, PD (2004). DNA sequence analysis of regions surrounding bla CMY-2 from multiple Salmonella plasmid backbones. Antimicrobial Agents and Chemotherapy 48: 28452852.CrossRefGoogle ScholarPubMed
Gillings, M, Boucher, Y, Labbate, M, Holmes, A, Krishnan, S, Holley, M and Stokes, HW (2008). The evolution of class 1 integrons and the rise of antibiotic resistance. Journal of Bacteriology 190: 50955100.CrossRefGoogle ScholarPubMed
Giraud, A, Radman, M, Matic, I and Taddei, F (2001). The rise and fall of mutator bacteria. Current Opinion in Microbiology 4: 582585.CrossRefGoogle ScholarPubMed
Goessens, WH, Mouton, JW, ten Kate, MT, Bijl, AJ, Ott, A and Bakker-Woudenberg, IA (2007). Role of ceftazidime dose regimen on the selection of resistant Enterobacter cloacae in the intestinal flora of rats treated for an experimental pulmonary infection. Journal of Antimicrobial Chemotherapy 59: 507516.CrossRefGoogle ScholarPubMed
Government of Canada (2007). Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) 2005. Guelph, ON: Public Health Agency of Canada.Google Scholar
Griffeth, GC, Morris, DO, Abraham, JL, Shofer, FS and Rankin, SC (2008). Screening for skin carriage of methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi in dogs with healthy and inflamed skin. Veterinary Dermatology 19: 142149.CrossRefGoogle ScholarPubMed
Hanssen, AM and Ericson Sollid, JU (2006). SCCmec in staphylococci: genes on the move. FEMS Immunology and Medical Microbiology 46: 820.CrossRefGoogle ScholarPubMed
Hansson, K, Sundstrom, L, Pelletier, A and Roy, PH (2002). IntI2 integron integrase in Tn7. Journal of Bacteriology 184: 17121721.CrossRefGoogle ScholarPubMed
Hochhut, B, Jahreis, K, Lengeler, JW and Schmid, K (1997). CTnscr94, a conjugative transposon found in enterobacteria. Journal of Bacteriology 179: 20972102.CrossRefGoogle ScholarPubMed
Hopkins, KL, Davies, RH and Threlfall, EJ (2005). Mechanisms of quinolone resistance in Escherichia coli and Salmonella: recent developments. International Journal of Antimicrobial Agents 25: 358373.CrossRefGoogle ScholarPubMed
Hopkins, KL, Liebana, E, Villa, L, Batchelor, M, Threlfall, EJ and Carattoli, A (2006). Replicon typing of plasmids carrying CTX-M or CMY beta-lactamases circulating among Salmonella and Escherichia coli isolates. Antimicrobial Agents and Chemotherapy 50: 32033206.CrossRefGoogle ScholarPubMed
Horst, JP, Wu, TH and Marinus, MG (1999). Escherichia coli mutator genes. Trends in Microbiology 7: 2936.CrossRefGoogle ScholarPubMed
Huijsdens, XW, van Dijke, BJ, Spalburg, E, van Santen-Verheuvel, MG, Heck, ME, Pluister, GN, Voss, A, Wannet, WJ and de Neeling, AJ (2006). Community-acquired MRSA and pig-farming. Annals of Clinical Microbiology and Antimicrobials 5: 26.CrossRefGoogle ScholarPubMed
Irwin, R, Dutil, L, Doré, K, Finley, R, Ng, LK and Avery, B (2008). Salmonella Heidelberg: ceftiofur-related resistance in human and retail chicken isolates in Canada (Speaker Abstract S5:2). Proceedings of the American Society of Microbiology Conference: Antimicrobial Resistance in Zoonotic Bacteria and Foodborne Pathogens. June 15–18, 2008, Copenhagen, Denmark. American Society for Microbiology, Washington DC, p. 16.Google Scholar
Jevons, MP, Coe, AW and Parker, MT (1963). Methicillin resistance in staphylococci. Lancet 1: 904907.CrossRefGoogle ScholarPubMed
Katayama, Y, Ito, T and Hiramatsu, K (2000). A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 44: 15491555.CrossRefGoogle ScholarPubMed
Khanna, T, Friendship, R, Dewey, C and Weese, JS (2008). Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Veterinary Microbiology 128: 298303.CrossRefGoogle ScholarPubMed
Klevens, RM, Morrison, MA, Nadle, J, Petit, S, Gershman, K, Ray, S, Harrison, LH, Lynfield, R, Dumyati, G, Townes, JM, Craig, AS, Zell, ER, Fosheim, GE, McDougal, LK, Carey, RB and Fridkin, SK (2007). Invasive methicillin-resistant Staphylococcus aureus infections in the United States. Journal of the American Medical Association 298: 17631771.CrossRefGoogle ScholarPubMed
Komp Lindgren, P, Karlsson, A and Hughes, D (2003). Mutation rate and evolution of fluoroquinolone resistance in Escherichia coli isolates from patients with urinary tract infections. Antimicrobial Agents and Chemotherapy 47: 32223232.CrossRefGoogle ScholarPubMed
Kostich, MS and Lazorchak, JM (2008). Risk to aquatic organisms posed by human pharmaceutical use. Science of the Total Environment 389: 329339.CrossRefGoogle ScholarPubMed
LeClerc, JE, Li, B, Payne, WL and Cebula, TA (1996). High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274: 12081211.CrossRefGoogle ScholarPubMed
Lefebvre, SL, Reid-Smith, R and Weese, JS (2008). Evaluation of the risks of shedding salmonellae and other potential pathogens by therapy dogs fed raw diets in Ontario and Alberta. Zoonoses and Public Health 55: 470480.CrossRefGoogle ScholarPubMed
Levy, DD, Sharma, B and Cebula, TA (2004). Single-nucleotide polymorphism mutation spectra and resistance to quinolones in Salmonella enterica serovar Enteritidis with a mutator phenotype. Antimicrobial Agents and Chemotherapy 48: 23552363.CrossRefGoogle ScholarPubMed
Liebert, CA, Hall, RM and Summers, AO (1999). Transposon Tn21, flagship of the floating genome. Microbiology and Molecular Biology Reviews 63: 507522.CrossRefGoogle ScholarPubMed
Linares, JF, Gustafsson, I, Baquero, F and Martinez, JL (2006). Antibiotics as intermicrobial signaling agents instead of weapons. Proceedings of the National Academy of Sciences of the United States of America 103: 1948419489.CrossRefGoogle ScholarPubMed
Linton, AH (1977). Antibiotic resistance: the present situation reviewed. Veterinary Record 100: 354360.CrossRefGoogle ScholarPubMed
Liu, J-H, Wei, S-Y, Ma, J-Y, Zeng, Z-L, , D-H, Yang, G-X and Chen, Z-L (2007). Detection and characterisation of CTX-M and CMY-2 β-lactamases among Escherichia coli from farm animals in Guiangdong Province of China. International Journal of Antimicrobial Agents 29: 576581.CrossRefGoogle ScholarPubMed
Loeffler, A, Linek, M, Moodley, A, Guardabassi, L, Sung, JM, Winkler, M, Weiss, R and Lloyd, DH (2007). First report of multiresistant, mecA-positive Staphylococcus intermedius in Europe: 12 cases from a veterinary dermatology referral clinic in Germany. Veterinary Dermatology 18: 412421.CrossRefGoogle ScholarPubMed
Lu, K, Asano, R and Davies, J (2004). Antimicrobial resistance gene delivery in animal feeds. Emerging Infectious Diseases 10: 679683.CrossRefGoogle ScholarPubMed
Machado, E, Coque, TM, Cantón, R, Sousa, JC and Peixe, L (2008). Antibiotic resistance integrons and extended-spectrum β-lactamases among Enterobacteriacea isolates recovered from chickens and swine in Portugal. Journal of Antimicrobial Chemotherapy 62: 296302.CrossRefGoogle ScholarPubMed
Macia, MD, Blanquer, D, Togores, B, Sauleda, J, Perez, JL and Oliver, A (2005). Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrobial Agents and Chemotherapy 49: 33823386.CrossRefGoogle ScholarPubMed
Macovei, L, Miles, B and Zurek, L (2008). Potential of houseflies to contaminate ready-to-eat food with antibiotic-resistant enterococci. Journal of Food Protection 71: 435439.CrossRefGoogle ScholarPubMed
Martinez, JL (2008). Antibiotics and antibiotic resistance genes in natural environments. Science (New York) 321: 365367.CrossRefGoogle ScholarPubMed
Matic, I, Radman, M, Taddei, F, Picard, B, Doit, C, Bingen, E, Denamur, E and Elion, J (1997). Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science (New York) 277: 18331834.CrossRefGoogle ScholarPubMed
Matsuhashi, M, Song, MD, Ishino, F, Wachi, M, Doi, M, Inoue, M, Ubukata, K, Yamashita, N and Konno, M (1986). Molecular cloning of the gene of a penicillin-binding protein supposed to cause high resistance to beta-lactam antibiotics in Staphylococcus aureus. Journal of Bacteriology 167: 975980.CrossRefGoogle ScholarPubMed
Mendiola, MV, Bernales, I and de la Cruz, F (1994). Differential roles of the transposon termini in IS91 transposition. Proceedings of the National Academy of Sciences of the United States of America 91: 19221926.CrossRefGoogle ScholarPubMed
Mulvey, MR, Boyd, DA, Olson, AB, Doublet, B and Cloeckaert, A (2006). The genetics of Salmonella genomic island 1. Microbes and Infection/Institut Pasteur 8: 19151922.CrossRefGoogle ScholarPubMed
Murphy, DB and Pembroke, JT (1995). Transfer of the IncJ plasmid R391 to recombination deficient Escherichia coli K12: evidence that R391 behaves as a conjugal transposon. FEMS Microbiology Letters 134: 153158.CrossRefGoogle ScholarPubMed
Nelson, JM, Chiller, TM, Powers, JH and Angulo, FJ (2007). Fluoroquinolone-resistant Campylobacter species and the withdrawal of fluoroquinolones from use in poultry: a public health success story. Clinical Infectious Diseases 44: 977980.CrossRefGoogle ScholarPubMed
Nemergut, DR, Robeson, MS, Kysela, RF, Martin, AP, Schmidt, SK and Knight, R (2008). Insights and inferences about integron evolution from genomic data. BMC Genomics 9: 261.CrossRefGoogle ScholarPubMed
Nordmann, P and Poirel, L (2005). Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. Journal of Antimicrobial Chemotherapy 56: 463469.CrossRefGoogle ScholarPubMed
Novick, RP (1987). Plasmid incompatibility. Microbiological Reviews 51: 381395.CrossRefGoogle ScholarPubMed
Olofsson, SK, Marcusson, LL, Stromback, A, Hughes, D and Cars, O (2007). Dose-related selection of fluoroquinolone-resistant Escherichia coli. Journal of Antimicrobial Chemotherapy 60: 795801.CrossRefGoogle ScholarPubMed
Orencia, MC, Yoon, JS, Ness, JE, Stemmer, WP and Stevens, RC (2001). Predicting the emergence of antibiotic resistance by directed evolution and structural analysis. Nature Structural Biology 8: 238242.CrossRefGoogle ScholarPubMed
Österblad, M, Norrdahl, K, Korpmäki, E and Huovinen, P (2001). How wild are wild mammals? Nature 409: 3738.CrossRefGoogle ScholarPubMed
Petersen, A, Andersen, JS, Kaewmak, T, Somsiri, T and Dalsgaard, A (2002). Impact of integrated fish farming on antimicrobial resistance in a pond environment. Applied and Environmental Microbiology 68: 60366042.CrossRefGoogle Scholar
Poppe, C, Smart, N, Khakhria, R, Johnson, W, Spika, J and Prescott, J (1998). Salmonella typhimurium DT104: a virulent and drug-resistant pathogen. The Canadian Veterinary Journal 39: 559565.Google ScholarPubMed
Poppe, C, Martin, LC, Gyles, CL, Reid-Smith, R, Boerlin, P, McEwen, SA, Prescott, JF and Forward, KR (2005). Acquisition of resistance to extended-spectrum cephalosporins by Salmonella Newport and Escherichia coli in the intestinal tract of turkey poults. Applied and Environmental Microbiology 71: 11841192.CrossRefGoogle Scholar
Prescott, JF (2000). Antimicrobial drug resistance and its epidemiology. In: Prescott, JF, Baggot, JD and Walker, RD (eds) Antimicrobial Therapy in Veterinary Medicine. Ames, Iowa, USA: Iowa State University Press, pp. 2749.Google Scholar
Quiroga, MP, Andres, P, Petroni, A, Soler Bistue, AJ, Guerriero, L, Vargas, LJ, Zorreguieta, A, Tokumoto, M, Quiroga, C, Tolmasky, ME, Galas, M and Centron, D (2007). Complex class 1 integrons with diverse variable regions, including aac(6′)-Ib-cr, and a novel allele, qnrB10, associated with ISCR1 in clinical enterobacterial isolates from Argentina. Antimicrobial Agents and Chemotherapy 51: 44664470.CrossRefGoogle Scholar
Rayssiguier, C, Thaler, DS and Radman, M (1989). The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342: 396401.CrossRefGoogle ScholarPubMed
Rice, LB (1998). Tn916 family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrobial Agents and Chemotherapy 42: 18711877.CrossRefGoogle ScholarPubMed
Salyers, AA, Gupta, A and Wang, Y (2004). Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends in Microbiology 12: 412416.CrossRefGoogle ScholarPubMed
Schluter, A, Szczepanowski, R, Puhler, A and Top, EM (2007). Genomics of IncP-1 antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence for a widely accessible drug resistance gene pool. FEMS Microbiology Reviews 31: 449477.CrossRefGoogle ScholarPubMed
Schmidt, H and Hensel, M (2004). Pathogenicity islands in bacterial pathogenesis. Clinical Microbiology Reviews 17: 1456.CrossRefGoogle ScholarPubMed
Schmieger, H and Schicklmaier, P (1999). Transduction of multiple drug resistance of Salmonella enterica serovar typhimurium DT104. FEMS Microbiology Letters 170: 251256.CrossRefGoogle ScholarPubMed
Schwarz, S, Cloeckaert, A and Roberts, MC (2006). Mechanisms and spread of bacterial resistance to antimicrobial agents. In: Aarestrup, FM(ed) Antimicrobial Resistance in Bacteria of Animal Origin. Washington, DC: ASM Press. pp. 7398.Google Scholar
Sengeløv, G, Agersø, Y, Halling-Sørensen, B, Baloda, SB, Andersen, JS and Jensen, LB (2003). Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environment International 28: 587595.CrossRefGoogle ScholarPubMed
Smith, JL, Fratamico, PM and Gunther, NW (2007). Extraintestinal pathogenic Escherichia coli. Foodborne Pathogens and Disease 4: 134161.CrossRefGoogle ScholarPubMed
Smith, KE, Besser, JM, Hedberg, CW, Leano, FT, Bender, JB, Wicklund, JH, Johnson, BP, Moore, KA, Osterholm, MT and the Investigation Team (1999). Quinolone-resistant Campylobacter infections in Minnesota, 1992–1998. New England Journal of Medicine 340: 15251532.CrossRefGoogle ScholarPubMed
Stepanova, MN, Pimkin, M, Nikulin, AA, Kozyreva, VK, Agapova, ED and Edelstein, MV (2008). Convergent in vivo and in vitro selection of ceftazidime resistance mutations at position 167 of CTX-M-3 beta-lactamase in hypermutable Escherichia coli strains. Antimicrobial Agents and Chemotherapy 52: 12971301.CrossRefGoogle ScholarPubMed
Tanaka, MM, Bergstrom, CT and Levin, BR (2003). The evolution of mutator genes in bacterial populations: the roles of environmental change and timing. Genetics 164: 843854.CrossRefGoogle ScholarPubMed
Tavakoli, N, Comanducci, A, Dodd, HM, Lett, MC, Albiger, B and Bennett, P (2000). IS1294, a DNA element that transposes by RC transposition. Plasmid 44: 6684.CrossRefGoogle ScholarPubMed
Tenaillon, O, Toupance, B, Le Nagard, H, Taddei, F and Godelle, B (1999). Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics 152: 485493.CrossRefGoogle ScholarPubMed
Threlfall, EJ (2000). Epidemic Salmonella typhimurium DT 104 – a truly international multiresistant clone. Journal of Antimicrobial Chemotherapy 46: 710.CrossRefGoogle ScholarPubMed
Threlfall, EJ (2008). Transmission of antimicrobial-resistant Salmonella from food animals to humans. Proceedings of the American Society of Microbiology Conference: Antimicrobial Resistance in Zoonotic Bacteria and Foodborne Pathogens, 15–18 June 2008, Copenhagen, Denmark.Google Scholar
Toleman, MA and Walsh, TR (2008). Evolution of the ISCR3 group of ISCR elements. Antimicrobial Agents and Chemotherapy 52: 37893791.CrossRefGoogle ScholarPubMed
Toleman, MA, Bennett, PM and Walsh, TR (2006a). Common regions e.g. orf513 and antibiotic resistance: IS91-like elements evolving complex class 1 integrons. Journal of Antimicrobial Chemotherapy 58: 16.CrossRefGoogle ScholarPubMed
Toleman, MA, Bennett, PM and Walsh, TR (2006b). ISCR elements: novel gene-capturing systems of the 21st century? Microbiology and Molecular Biology Reviews 70: 296316.CrossRefGoogle Scholar
Top, J, Willems, R and Bonten, M (2008). Emergence of CC17 Enterococcus faecium: from commensal to hospital-adapted pathogen. FEMS Immunology and Medical Microbiology 52: 297308.CrossRefGoogle ScholarPubMed
Townsend, JP, Nielsen, KM, Fisher, DS and Hartl, DL (2003). Horizontal acquisition of divergent chromosomal DNA in bacteria: effects of mutator phenotypes. Genetics 164: 1321.CrossRefGoogle ScholarPubMed
Travis, JM and Travis, ER (2002). Mutator dynamics in fluctuating environments. Proceedings of the Royal Society of London Series B – Biological Sciences 269: 591597.CrossRefGoogle ScholarPubMed
Trong, HN, Prunier, AL and Leclercq, R (2005). Hypermutable and fluoroquinolone-resistant clinical isolates of Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 49: 20982101.CrossRefGoogle ScholarPubMed
van Loo, I, Huijsdens, X, Tiemersma, E, de Neeling, A, van de Sande-Bruinsma, N, Beaujean, D, Voss, A and Kluytmans, J (2007). Emergence of methicillin-resistant Staphylococcus aureus of animal origin in humans. Emerging Infectious Diseases 13: 18341839.CrossRefGoogle ScholarPubMed
Walsh, C, Duffy, G, Nally, P, O'Mahoney, R, McDowell, DA and Fanning, S (2008). Transfer of ampicillin resistance from Salmonella Typhimurium DT104 to Escherichia coli K12 in food. Letters in Applied Microbiology 46: 210215.CrossRefGoogle ScholarPubMed
Wang, M, Tran, JH, Jacoby, GA, Zhang, Y, Wang, F and Hooper, DC (2003). Plasmid-mediated quinolone resistance in clinical isolates of Escherichia coli from Shanghai, China. Antimicrobial Agents and Chemotherapy 47: 22422248.CrossRefGoogle ScholarPubMed
Webb, V and Davies, J (1993). Antibiotic preparations contain DNA: a source of drug resistance genes? Antimicrobial Agents and Chemotherapy 37: 23792384.CrossRefGoogle ScholarPubMed
Weese, JS (2004). Methicillin-resistant Staphylococcus aureus in horses and horse personnel. The Veterinary Clinics of North America: Equine Practice 20: 601613.Google ScholarPubMed
Weese, JS (2005). Methicillin-resistant Staphylococcus aureus: an emerging pathogen in small animals. Journal of the American Animal Hospital Association 41: 150157.CrossRefGoogle ScholarPubMed
White, DG, Zhao, S, Sudler, R, Ayers, S, Friedman, S, Chen, S, McDermott, PF, McDermott, S, Wagner, DD and Meng, J (2001). The isolation of antibiotic-resistant salmonella from retail ground meats. New England Journal of Medicine 345: 11471154.CrossRefGoogle ScholarPubMed
Wisplinghoff, H, Rosato, AE, Enright, MC, Noto, M, Craig, W and Archer, GL (2003). Related clones containing SCCmec type IV predominate among clinically significant Staphylococcus epidermidis isolates. Antimicrobial Agents and Chemotherapy 47: 35743579.CrossRefGoogle ScholarPubMed
Woodford, N and Ellington, MJ (2007). The emergence of antibiotic resistance by mutation. Clinical Microbiology and Infection 13: 518.CrossRefGoogle ScholarPubMed
Wu, SW, de Lencastre, H and Tomasz, A (2001). Recruitment of the mecA gene homologue of Staphylococcus sciuri into a resistance determinant and expression of the resistant phenotype in Staphylococcus aureus. Journal of Bacteriology 183: 24172424.CrossRefGoogle ScholarPubMed
Yoke-Kqueen, C, Learn-Han, L, Noorzaleha, AS, Son, R, Sabrina, S, Jiun-Horng, S and Chia-Hoon, K (2008). Characterization of multiple-antimicrobial-resistant Salmonella enterica subsp. enterica isolated from indigenous vegetables and poultry in Malaysia. Letters in Applied Microbiology 46: 318324.CrossRefGoogle ScholarPubMed
Zhao, X and Drlica, K (2001). Restricting the selection of antibiotic-resistant mutants: a general strategy derived from fluoroquinolone studies. Clinical Infectious Diseases 33 (Suppl. 3): S147S156.CrossRefGoogle ScholarPubMed
Zhang, Y and LeJeune, JT (2008). Transduction of bla(CMY-2), tet(A), and tet(B) from Salmonella enterica subspecies enterica serovar Heidelberg to S. Typhimurium. Veterinary Microbiology 129: 418425.CrossRefGoogle Scholar
Zhao, S, White, DG, McDermott, PF, Friedman, S, English, L, Ayers, S, Meng, J, Maurer, JJ, Holland, R and Walker, RD (2001). Identification and expression of cephamycinase blaCMY genes in Escherichia coli and Salmonella isolates from food animals and ground meat. Antimicrobial Agents and Chemotherapy 45: 36473650.CrossRefGoogle ScholarPubMed
Zhang, Q, Lin, J and Pereira, S (2003). Fluoroquinolone-resistant Campylobacter in animal reservoirs: dynamics of development, resistance mechanisms and ecological fitness. Animal Health Research Reviews 4: 6371.CrossRefGoogle ScholarPubMed
Zinner, SH, Gilbert, D, Lubenko, IY, Greer, K and Firsov, AA (2008). Selection of linezolid-resistant Enterococcus faecium in an in vitro dynamic model: protective effect of doxycycline. Journal of Antimicrobial Chemotherapy 61: 629635.CrossRefGoogle Scholar
Zubeir, IE, Kanbar, T, Alber, J, Lammler, C, Akineden, O, Weiss, R and Zschock, M (2007). Phenotypic and genotypic characteristics of methicillin/oxacillin-resistant Staphylococcus intermedius isolated from clinical specimens during routine veterinary microbiological examinations. Veterinary Microbiology 121: 170176.CrossRefGoogle ScholarPubMed