Beyond serial passages: New methods for predicting the emergence of resistance to novel antibiotics

Current Opinion in Pharmacology

Volumn 11, Issue 5, 2011, Pages 439-445

  Martínez, José Luis ^a   Baquero, Fernando ^b   Andersson, Dan I ^c  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b HOSPITAL RAMÓN Y CAJAL   (Spain)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; ASSAY; BACTERIAL MUTATION; BACTERIAL TRANSMISSION; BACTERIUM CULTURE; DNA SEQUENCE; GENETIC PARAMETERS; HOST; IN VITRO COMPETITION ASSAY; MOBILE GENETIC ELEMENT; NONHUMAN; PLASMID; PREDICTION; PRIORITY JOURNAL;

EID: 80053124273     PISSN: 14714892     EISSN: 14714973     Source Type: Journal    
DOI: 10.1016/j.coph.2011.07.005     Document Type: Review

References (83)

1. J.L. Martinez, and F. Baquero Mutation frequencies and antibiotic resistance Antimicrob Agents Chemother 44 2000 1771 1777 (Pubitemid 30422923)
2. J.L. Martinez, F. Baquero, and D.I. Andersson Predicting antibiotic resistance Nat Rev Microbiol 5 2007 958 965 (Pubitemid 350138975)
3. N. van de Sande-Bruinsma, H. Grundmann, D. Verloo, E. Tiemersma, J. Monen, H. Goossens, and M. Ferech Antimicrobial drug use and resistance in Europe Emerg Infect Dis 14 2008 1722 1730
4. M. Bergman, S.T. Nyberg, P. Huovinen, P. Paakkari, and A.J. Hakan Association between antimicrobial consumption and resistance in Escherichia coli Antimicrob Agents Chemother 53 2009 912 917
5. H. Goossens Antibiotic consumption and link to resistance Clin Microbiol Infect 15 Suppl. 3 2009 12 15
6. F.M. Aarestrup, A.M. Seyfarth, H.D. Emborg, K. Pedersen, R.S. Hendriksen, and F. Bager 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 Antimicrob Agents Chemother 45 2001 2054 2059 (Pubitemid 32591697)
7. D.I. Andersson, and D. Hughes Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol 8 2010 260 271
8. B.R. Lev Models for the spread of resistant pathogens Neth J Med 60 2002 58 64
9. B.R Levin Minimizing potential resistance: a population dynamics view Clin Infect Dis 33 Suppl. 3 2001 S161 S169
10. B.R. Levin, V. Perrot, and N. Walker Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria Genetics 154 2000 985 997 (Pubitemid 30140690)
11. D.I. Andersson, and B.R. Levin The biological cost of antibiotic resistance Curr Opin Microbiol 2 1999 489 493 (Pubitemid 29477174)
12. A.I. Nilsson, O.G. Berg, O. Aspevall, G. Kahlmeter, and D.I. Andersson Biological costs and mechanisms of fosfomycin resistance in Escherichia coli Antimicrob Agents Chemother 47 2003 2850 2858 (Pubitemid 37040258)
13. L. Sandegren, A. Lindqvist, G. Kahlmeter, and D.I. Andersson Nitrofurantoin resistance mechanism and fitness cost in Escherichia coli J Antimicrob Chemother 62 2008 495 503
14. J.L. Martinez, A. Fajardo, L. Garmendia, A. Hernandez, J.F. Linares, L. Martinez-Solano, and M.B. Sanchez A global view of antibiotic resistance FEMS Microbiol Rev 33 2009 44 65
15. A.J. O'Neill, and I. Chopra Use of mutator strains for characterization of novel antimicrobial agents Antimicrob Agents Chemother 45 2001 1599 1600 (Pubitemid 32374146)
16. F. Baquero Low-level antibiotic resistance D. Hughes, D.I. Andersson, Antibiotics Development and Resistance 2001 Taylor & Francis Books Ltd. London 117 136
17. A. Alonso, E. Campanario, and J.L. Martinez Emergence of multidrug-resistant mutants is increased under antibiotic selective pressure in Pseudomonas aeruginosa Microbiology 145 Pt 10 1999 2857 2862 (Pubitemid 29485900)
18. M.C. Negri, M. Lipsitch, J. Blazquez, B.R. Levin, and F. Baquero Concentration-dependent selection of small phenotypic differences in TEM beta-lactamase-mediated antibiotic resistance Antimicrob Agents Chemother 44 2000 2485 2491 (Pubitemid 30650899)
19. F. Baquero, and M.C. Negri Selective compartments for resistant microorganisms in antibiotic gradients Bioessays 19 1997 731 736 (Pubitemid 27354094)
20. K. Drlica The mutant selection window and antimicrobial resistance J Antimicrob Chemother 52 2003 11 17 (Pubitemid 36850078)
21. A. Liu, L. Tran, E. Becket, K. Lee, L. Chinn, E. Park, K. Tran, and J.H. Miller Antibiotic sensitivity profiles determined with an Escherichia coli gene knockout collection: generating an antibiotic bar code Antimicrob Agents Chemother 54 2010 1393 1403
22. C. Alvarez-Ortega, I. Weigand, J. Olivares, R.E. Hancock, and J.L. Martinez The intrinsic resistome of Pseudomonas aeruginosa to beta-lactams Virulence 2 2011 144 146
23. A. Fajardo, N. Martinez-Martin, M. Mercadillo, J.C. Galan, B. Ghysels, S. Matthijs, P. Cornelis, L. Wiehlmann, B. Tummler, F. Baquero, and J.L. Martinez The neglected intrinsic resistome of bacterial pathogens PLoS ONE 3 2008 e1619
24. B. Bjorkholm, M. Sjolund, P.G. Falk, O.G. Berg, L. Engstrand, and D.I. Andersson Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori Proc Natl Acad Sci USA 98 2001 14607 14612 (Pubitemid 33121439)
25. J. Bjorkman, I. Nagaev, O.G. Berg, D. Hughes, and D.I. Andersson Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance Science 287 2000 1479 1482 (Pubitemid 30127140)
26. I. Nagaev, J. Bjorkman, D.I. Andersson, and D. Hughes Biological cost and compensatory evolution in fusidic acid-resistant Staphylococcus aureus Mol Microbiol 40 2001 433 439 (Pubitemid 32391637)
27. L.L. Marcusson, N. Frimodt-Moller, and D. Hughes Interplay in the selection of fluoroquinolone resistance and bacterial fitness PLoS Pathog 5 2009 e1000541
28. A.I. Nilsson, A. Zorzet, A. Kanth, S. Dahlstrom, O.G. Berg, and D.I. Andersson Reducing the fitness cost of antibiotic resistance by amplification of initiator tRNA genes Proc Natl Acad Sci USA 103 2006 6976 6981
29. D. Shcherbakov, R. Akbergenov, T. Matt, P. Sander, D.I. Andersson, and E.C. Bottger Directed mutagenesis of Mycobacterium smegmatis 16S rRNA to reconstruct the in-vivo evolution of aminoglycoside resistance in Mycobacterium tuberculosis Mol Microbiol 77 2010 830 840
30. D.R. Sherman, K. Mdluli, M.J. Hickey, T.M. Arain, S.L. Morris, C.E. Barry, and C.K. Stover 3rd Compensatory ahpC gene expression in isoniazid-resistant Mycobacterium tuberculosis Science 272 1996 1641 1643 (Pubitemid 26200020)
31. D.I. Andersson Persistence of antibiotic resistant bacteria Curr Opin Microbiol 6 2003 452 456 (Pubitemid 37345409)
32. D.I. Andersson The biological cost of mutational antibiotic resistance: any practical conclusions? Curr Opin Microbiol 9 2006 461 465 (Pubitemid 44397630)
33. S. Maisnier-Patin, O.G. Berg, L. Liljas, and D.I. Andersson Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium Mol Microbiol 46 2002 355 366 (Pubitemid 35340949)
34. S. Bershtein, M. Segal, R. Bekerman, N. Tokuriki, and D.S. Tawfik Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein Nature 444 2006 929 932 (Pubitemid 46025005)
35. A. Novais, I. Comas, F. Baquero, R. Canton, T.M. Coque, A. Moya, F. Gonzalez-Candelas, and J.C. Galan Evolutionary trajectories of beta-lactamase CTX-M-1 cluster enzymes: predicting antibiotic resistance PLoS Pathog 6 2010 e1000735
36. A. Novais, R. Canton, T.M. Coque, A. Moya, F. Baquero, and J.C. Galan Mutational events in cefotaximase extended-spectrum beta-lactamases of the CTX-M-1 cluster involved in ceftazidime resistance Antimicrob Agents Chemother 52 2008 2377 2382 (Pubitemid 351915665)
37. W. Paulander, A. Pennhag, D.I. Andersson, and S. Maisnier-Patin Caenorhabditis elegans as a model to determine fitness of antibiotic-resistant Salmonella enterica serovar Typhimurium Antimicrob Agents Chemother 51 2007 766 769 (Pubitemid 46185305)
38. P.A. Lind, C. Tobin, O.G. Berg, C.G. Kurland, and D.I. Andersson Compensatory gene amplification restores fitness after inter-species gene replacements Mol Microbiol 75 2010 1078 1089
39. P.A. Lind, O.G. Berg, and D.I. Andersson Mutational robustness of ribosomal protein genes Science 330 2010 825 827
40. J. Yu, J. Wu, K.P. Francis, T.F. Purchio, and J.L. Kadurugamuwa Monitoring in vivo fitness of rifampicin-resistant Staphylococcus aureus mutants in a mouse biofilm infection model J Antimicrob Chemother 55 2005 528 534 (Pubitemid 40542595)
41. P. Sanchez, J.F. Linares, B. Ruiz-Diez, E. Campanario, A. Navas, F. Baquero, and J.L. Martinez Fitness of in vitro selected Pseudomonas aeruginosa nalB and nfxB multidrug resistant mutants J Antimicrob Chemother 50 2002 657 664 (Pubitemid 35331682)
42. M. Macvanin, J. Bjorkman, S. Eriksson, M. Rhen, D.I. Andersson, and D. Hughes Fusidic acid-resistant mutants of Salmonella enterica serovar Typhimurium with low fitness in vivo are defective in RpoS induction Antimicrob Agents Chemother 47 2003 3743 3749 (Pubitemid 37484982)
43. P. Komp Lindgren, L.L. Marcusson, D. Sandvang, N. Frimodt-Moller, and D. Hughes Biological cost of single and multiple norfloxacin resistance mutations in Escherichia coli implicated in urinary tract infections Antimicrob Agents Chemother 49 2005 2343 2351 (Pubitemid 40734464)
44. B. Heym, E. Stavropoulos, N. Honore, P. Domenech, B. Saint-Joanis, T.M. Wilson, D.M. Collins, M.J. Colston, and S.T. Cole Effects of overexpression of the alkyl hydroperoxide reductase AhpC on the virulence and isoniazid resistance of Mycobacterium tuberculosis Infect Immun 65 1997 1395 1401 (Pubitemid 27146630)
45. C.N. Johnson, D.E. Briles, W.H. Benjamin Jr., S.K. Hollingshead, and K.B. Waites Relative fitness of fluoroquinolone-resistant Streptococcus pneumoniae Emerg Infect Dis 11 2005 814 820 (Pubitemid 40720840)
46. N. Luo, S. Pereira, O. Sahin, J. Lin, S. Huang, L. Michel, and Q. Zhang Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure Proc Natl Acad Sci USA 102 2005 541 546 (Pubitemid 40282701)
47. I. Gustafsson, O. Cars, and D.I. Andersson Fitness of antibiotic resistant Staphylococcus epidermidis assessed by competition on the skin of human volunteers J Antimicrob Chemother 52 2003 258 263 (Pubitemid 36986888)
48. A. Navas, G. Cobas, M. Talavera, J.A. Ayala, J.A. Lopez, and J.L. Martinez Experimental validation of Haldane's hypothesis on the role of infection as an evolutionary force for Metazoans Proc Natl Acad Sci USA 104 2007 13728 13731 (Pubitemid 350003388)
49. B. Ruiz-Diez, P. Sanchez, F. Baquero, J.L. Martinez, and A. Navas Differential interactions within the Caenorhabditis elegans-Pseudomonas aeruginosa pathogenesis model J Theor Biol 225 2003 469 476 (Pubitemid 37393276)
50. A. Alonso, G. Morales, R. Escalante, E. Campanario, L. Sastre, and J.L. Martinez Overexpression of the multidrug efflux pump SmeDEF impairs Stenotrophomonas maltophilia physiology J Antimicrob Chemother 53 2004 432 434 (Pubitemid 38380238)
51. D.H. Mariam, Y. Mengistu, S.E. Hoffner, and D.I. Andersson Effect of rpoB mutations conferring rifampin resistance on fitness of Mycobacterium tuberculosis Antimicrob Agents Chemother 48 2004 1289 1294 (Pubitemid 38405483)
52. J.F. Linares, J.A. Lopez, E. Camafeita, J.P. Albar, F. Rojo, and J.L. Martinez Overexpression of the multidrug efflux pumps MexCD-OprJ and MexEF-OprN is associated with a reduction of type III secretion in Pseudomonas aeruginosa J Bacteriol 187 2005 1384 1391 (Pubitemid 40299463)
53. M.I. Morosini, J.A. Ayala, F. Baquero, J.L. Martinez, and J. Blazquez Biological cost of AmpC production for Salmonella enterica serotype Typhimurium Antimicrob Agents Chemother 44 2000 3137 3143
54. R.M. May, S. Gupta, and A.R. McLean Infectious disease dynamics: what characterizes a successful invader? Philos Trans R Soc Lond B Biol Sci 356 2001 901 910 (Pubitemid 32614665)
55. T. Cohen, B. Sommers, and M. Murray The effect of drug resistance on the fitness of Mycobacterium tuberculosis Lancet Infect Dis 3 2003 13 21 (Pubitemid 36041784)
56. M. Burgos, K. DeRiemer, P.M. Small, P.C. Hopewell, and C.L. Daley Effect of drug resistance on the generation of secondary cases of tuberculosis J Infect Dis 188 2003 1878 1884 (Pubitemid 38064874)
57. E.C. Bottger, M. Pletschette, and D. Andersson Drug resistance and fitness in Mycobacterium tuberculosis infection J Infect Dis 191 2005 823 824 author reply 824 (Pubitemid 40271079)
58. F. Luciani, S.A. Sisson, H. Jiang, A.R. Francis, and M.M. Tanaka The epidemiological fitness cost of drug resistance in Mycobacterium tuberculosis Proc Natl Acad Sci USA 106 2009 14711 14715
59. M.L. Foucault, F. Depardieu, P. Courvalin, and C. Grillot-Courvalin Inducible expression eliminates the fitness cost of vancomycin resistance in enterococci Proc Natl Acad Sci USA 107 2010 16964 16969
60. R.I. Aminov The role of antibiotics and antibiotic resistance in nature Environ Microbiol 11 2009 2970 2988
61. G.D. Wright The antibiotic resistome: the nexus of chemical and genetic diversity Nat Rev Microbiol 5 2007 175 186 (Pubitemid 46291277)
62. F. Baquero, C. Alvarez-Ortega, and J.L. Martinez Ecology and evolution of antibiotic resistance Environ Microbiol Rep 1 2009 469 476
63. V.M. D'Costa, K.M. McGrann, D.W. Hughes, and G.D. Wright Sampling the antibiotic resistome Science 311 2006 374 377 (Pubitemid 43132661)
64. M.O. Sommer, G. Dantas, and G.M. Church Functional characterization of the antibiotic resistance reservoir in the human microflora Science 325 2009 1128 1131
65. M.F. Lartigue, L. Poirel, D. Aubert, and P. Nordmann In vitro analysis of ISEcp1B-mediated mobilization of naturally occurring beta-lactamase gene blaCTX-M of Kluyvera ascorbata Antimicrob Agents Chemother 50 2006 1282 1286
66. F. Baquero From pieces to patterns: evolutionary engineering in bacterial pathogens Nat Rev Microbiol 2 2004 510 518 (Pubitemid 39200018)
67. F. Baquero, J.L. Martinez, and R. Canton Antibiotics and antibiotic resistance in water environments Curr Opin Biotechnol 19 2008 260 265
68. R.G. Beiko, T.J. Harlow, and M.A. Ragan Highways of gene sharing in prokaryotes Proc Natl Acad Sci USA 102 2005 14332 14337 (Pubitemid 41429698)
69. M. Fondi, G. Bacci, M. Brilli, M.C. Papaleo, A. Mengoni, M. Vaneechoutte, L. Dijkshoorn, and R. Fani Exploring the evolutionary dynamics of plasmids: the Acinetobacter pan-plasmidome BMC Evol Biol 10 2010 59
70. A. Carattoli Resistance plasmid families in Enterobacteriaceae Antimicrob Agents Chemother 53 2009 2227 2238
71. T.M. Coque, F. Baquero, and R. Canton Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe Euro Surveill 13 2008
72. R. Jain, M.C. Rivera, J.E. Moore, and J.A. Lake Horizontal gene transfer accelerates genome innovation and evolution Mol Biol Evol 20 2003 1598 1602 (Pubitemid 41070820)
73. G. Werner, A.R. Freitas, T.M. Coque, J.E. Sollid, C. Lester, A.M. Hammerum, L. Garcia-Migura, L.B. Jensen, M.V. Francia, W. Witte, and R.J. Willems Host range of enterococcal vanA plasmids among Gram-positive intestinal bacteria J Antimicrob Chemother 66 2011 273 282
74. W. van Schaik, and R.J. Willems Genome-based insights into the evolution of enterococci Clin Microbiol Infect 16 2010 527 532
75. B.A. Rogers, H.E. Sidjabat, and D.L. Paterson Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain J Antimicrob Chemother 66 2011 1 14
76. N. Woodford, J.F. Turton, and D.M. Livermore Multiresistant Gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance FEMS Microbiol Rev 2011 doi:10.1111/j.1574-6976.2011.00268.x, in press
77. F. Baquero, T.M. Coque, and F. de la Cruz Ecology and evolution as targets: the need for novel eco-evo drugs and strategies to fight antibiotic resistance Antimicrob Agents Chemother 55 2011 3649 3660
78. G. Cornaglia, W. Hryniewicz, V. Jarlier, G. Kahlmeter, H. Mittermayer, L. Stratchounski, and F. Baquero European recommendations for antimicrobial resistance surveillance Clin Microbiol Infect 10 2004 349 383 (Pubitemid 38519367)
79. T.R. Walsh, M.A. Toleman, L. Poirel, and P. Nordmann Metallo-beta- lactamases: the quiet before the storm? Clin Microbiol Rev 18 2005 306 325
80. A.R. Freitas, T.M. Coque, C. Novais, A.M. Hammerum, C.H. Lester, M.J. Zervos, S. Donabedian, L.B. Jensen, M.V. Francia, F. Baquero, and L. Peixe 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 2011 925 931
81. A. Novais, F. Baquero, E. Machado, R. Canton, L. Peixe, and T.M. Coque International spread and persistence of TEM-24 is caused by the confluence of highly penetrating Enterobacteriaceae clones and an IncA/C2 plasmid containing Tn1696::Tn1 and IS5075-Tn21 Antimicrob Agents Chemother 54 2010 825 834
82. G.R. Price Selection and covariance Nature 227 1970 520 521
83. J.L. Martinez Antibiotics and antibiotic resistance genes in natural environments Science 321 2008 365 367 (Pubitemid 352029941)