Fitness of antimicrobial-resistant Campylobacter and Salmonella

Microbes and Infection

Volumn 8, Issue 7, 2006, Pages 1972-1978

  Zhang, Qijing ^a   Sahin, Orhan ^b   McDermott, Patrick F ^c   Payot, Sophie ^d  

^a IOWA STATE UNIVERSITY   (United States)

^b MUSTAFA KEMAL UNIVERSITY   (Turkey)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^d CEMAGREF   (France)

Author keywords

Adaptation; Antimicrobial resistance; Campylobacter; Fitness; Fluoroquinolone; Salmonella

Indexed keywords

ANTIBIOTIC AGENT; CLARITHROMYCIN; FUSIDIC ACID; MACROLIDE; NALIDIXIC ACID; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFAMPICIN; STREPTOMYCIN; TETRACYCLINE DERIVATIVE;

ADAPTATION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; CAMPYLOBACTER; COST; DIARRHEA; ENVIRONMENTAL FACTOR; EVOLUTION; FOOD POISONING; GENE MUTATION; GRAM NEGATIVE INFECTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PUBLIC HEALTH; SALMONELLA; SALMONELLOSIS; SHORT SURVEY;

ANIMALS; CAMPYLOBACTER; CAMPYLOBACTER INFECTIONS; DRUG RESISTANCE, BACTERIAL; HUMANS; MUTATION; SALMONELLA; SALMONELLA INFECTIONS;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER; SALMONELLA;

EID: 33746614060     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2005.12.031     Document Type: Short Survey

References (69)

1. Gillespie S.H. Antibiotic resistance in the absence of selective pressure. Int. J. Antimicrob. Agents 17 (2001) 171-176
2. Maisnier-Patin S., and Andersson D.I. Adaptation to the deleterious effects of antimicrobial drug resistance mutations by compensatory evolution. Res. Microbiol. 155 (2004) 360-369
3. Normark B.H., and Normark S. Evolution and spread of antibiotic resistance. J. Intern. Med. 252 (2002) 91-106
4. Andersson D.I., and Levin B.R. The biological cost of antibiotic resistance. Curr. Opin. Microbiol. 2 (1999) 489-493
5. Levin B.R., Perrot V., and Walker N. Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154 (2000) 985-997
6. Bjorkman J., and Andersson D.I. The cost of antibiotic resistance from a bacterial perspective. Drug Resist. Updat. 3 (2000) 237-245
7. Andersson D.I. Persistence of antibiotic resistant bacteria. Curr. Opin. Microbiol. 6 (2003) 452-456
8. Kanai K., Shibayama K., Suzuki S., Wachino J., and Arakawa Y. Growth competition of macrolide-resistant and -susceptible Helicobacter pylori strains. Microbiol. Immunol. 48 (2004) 977-980
9. Folkesson A., Eriksson S., Andersson M., Park J.T., and Normark S. Components of the peptidoglycan-recycling pathway modulate invasion and intracellular survival of Salmonella enterica serovar Typhimurium. Cell. Microbiol. 7 (2005) 147-155
10. Mariam D.H., Mengistu Y., Hoffner S.E., and Andersson D.I. Effect of rpoB mutations conferring rifampin resistance on fitness of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 48 (2004) 1289-1294
11. Hossain A., Reisbig M.D., and Hanson N.D. Plasmid-encoded functions compensate for the biological cost of AmpC overexpression in a clinical isolate of Salmonella typhimurium. J. Antimicrob. Chemother. 53 (2004) 964-970
12. Engberg J., Neimann J., Nielsen E.M., Aerestrup F.M., and Fussing V. Quinolone-resistant Campylobacter infections: risk factors and clinical consequences. Emerg. Infect. Dis. 10 (2004) 1056-1063
13. Bjorkman J., Hughes D., and Andersson D.I. Virulence of antibiotic-resistant Salmonella typhimurium. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 3949-3953
14. Enne V.I., Delsol A.A., Roe J.M., and Bennett P.M. Rifampicin resistance and its fitness cost in Enterococcus faecium. J. Antimicrob. Chemother. 53 (2004) 203-207
15. Kugelberg E., Lofmark S., Wretlind B., and Andersson D.I. Reduction of the fitness burden of quinolone resistance in Pseudomonas aeruginosa. J. Antimicrob. Chemother. 55 (2005) 22-30
16. Pym A.S., Saint-Joanis B., and Cole S.T. Effect of katG mutations on the virulence of Mycobacterium tuberculosis and the implication for transmission in humans. Infect. Immun. 70 (2002) 4955-4960
17. Nagaev I., Bjorkman J., Andersson D.I., and Hughes D. Biological cost and compensatory evolution in fusidic acid-resistant Staphylococcus aureus. Mol. Microbiol. 40 (2001) 433-439
18. Hurdle J.G., O'Neill A.J., Ingham E., Fishwick C., and Chopra I. Analysis of mupirocin resistance and fitness in Staphylococcus aureus by molecular genetic and structural modeling techniques. Antimicrob. Agents Chemother. 48 (2004) 4366-4376
19. Sander P., Springer B., Prammananan T., Sturmfels A., Kappler M., Pletschette M., and Bottger E.C. Fitness cost of chromosomal drug resistance-conferring mutations. Antimicrob. Agents Chemother. 46 (2002) 1204-1211
20. Bottger E.C., Springer B., Pletschette M., and Sander P. Fitness of antibiotic-resistant microorganisms and compensatory mutations. Nat. Med. 4 (1998) 1343-1344
21. Gillespie S.H., Voelker L.L., and Dickens A. Evolutionary barriers to quinolone resistance in Streptococcus pneumonia. Microb. Drug Resist. 8 (2002) 79-84
22. Gustafsson I., Cars O., and Andersson D.I. Fitness of antibiotic resistant Staphylococcus epidermidis assessed by competition on the skin of human volunteers. J. Antimicrob. Chemother. 52 (2003) 258-263
23. Luo N., Pereira S., Sahin O., Lin J., Huang S., Michel L., and Zhang Q. Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 541-546
24. Lipsitch M. The rise and fall of antimicrobial resistance. Trends Microbiol. 9 (2001) 438-444
25. Schrag S.J., Perrot V., and Levin B.R. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc. Biol. Sci. 264 (1997) 1287-1291
26. Wray C., and Davies R.H. The epidemiology and ecology of Salmonella in meat-producing animals. In: Torrence M.E., and Isaacson R.E. (Eds). Microbial Food Safety in Animal Agriculture: Current Topics (2003), Iowa State Press, Ames, Iowa 73-82
27. Moore J.E., Corcoran D., Dooley J.S., Fanning S., Lucey B., Matsuda M., McDowell D.A., Megraud F., Millar B.C., O'Mahony R., O'Riordan L., O'Rourke M., Rao J.R., Rooney P.J., Sails A., and Whyte P. Campylobacter. Vet. Res. 36 (2005) 351-382
28. Zhang Q., Lin J., and Pereira S. Fluoroquinolone-resistant Campylobacter in animal reservoirs: dynamics of development, resistance mechanisms and ecological fitness. Anim. Health Res. Rev. 4 (2003) 63-71
29. White D.G., Zhao S., Simjee S., Wagner D.D., and McDermott P.F. Antimicrobial resistance of foodborne pathogens. Microbes Infect. 4 (2002) 405-412
30. Payot S., Bolla J.-M., Corcoran D., Fanning S., Megraud F., and Zhang Q. Mechanisms of fluoroquinolone and macrolide resistance in Campylobacter spp. Microbes Infect. 8 7 (2006) 1967-1971
31. Taylor D.E., and Tracz D.M. Mechanisms of antimicrobial resistance in Campylobacter. In: Ketley J.M., and Konkel M.E. (Eds). Campylobacter: Molecular and Cellular Biology (2005), Horizon Bioscience, Norfolk 193-204
32. Velge P., Cloeckaert A., and Barrow P. Emergence of Salmonella epidemics: the problems related to Salmonella enterica serotype Enteritidis and multiple antibiotic resistance in other major serotypes. Vet. Res. 36 (2005) 267-288
33. Maisnier-Patin S., Berg O.G., Liljas L., and Andersson D.I. Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Mol. Microbiol. 46 (2002) 355-366
34. Bjorkman J., Samuelsson P., Andersson D.I., and Hughes D. Novel ribosomal mutations affecting translational accuracy, antibiotic resistance and virulence of Salmonella typhimurium. Mol. Microbiol. 31 (1999) 53-58
35. Bjorkman J., Nagaev I., Berg O.G., Hughes D., and Andersson D.I. Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287 (2000) 1479-1482
36. Johanson U., Aevarsson A., Liljas A., and Hughes D. The dynamic structure of EF-G studied by fusidic acid resistance and internal revertants. J. Mol. Biol. 258 (1996) 420-432
37. Macvanin M., Johanson U., Ehrenberg M., and Hughes D. Fusidic acid-resistant EF-G perturbs the accumulation of ppGpp. Mol. Microbiol. 37 (2000) 98-107
38. Macvanin M., Bjorkman J., Eriksson S., Rhen M., Andersson D.I., and Hughes D. 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
39. Macvanin M., Ballagi A., and Hughes D. Fusidic acid-resistant mutants of Salmonella enterica serovar Typhimurium have low levels of heme and a reduced rate of respiration and are sensitive to oxidative stress. Antimicrob. Agents Chemother. 48 (2004) 3877-3883
40. Giraud E., Brisabois A., Martel J.L., and Chaslus-Dancla E. Comparative studies of mutations in animal isolates and experimental in vitro- and in vivo-selected mutants of Salmonella spp. suggest a counterselection of highly fluoroquinolone-resistant strains in the field. Antimicrob. Agents Chemother. 43 (1999) 2131-2137
41. Giraud E., Cloeckaert A., Baucheron S., Mouline C., and Chaslus-Dancla E. Fitness cost of fluoroquinolone resistance in Salmonella enterica serovar Typhimurium. J. Med. Microbiol. 52 (2003) 697-703
42. Morosini M.I., Ayala J.A., Baquero F., Martinez J.L., and Blazquez J. Biological cost of AmpC production for Salmonella enterica serotype Typhimurium. Antimicrob. Agents Chemother. 44 (2000) 3137-3143
43. Su L.H., Chiu C.H., Chu C., and Ou J.T. Antimicrobial resistance in nontyphoid Salmonella serotypes: a global challenge. Clin. Infect. Dis. 39 (2004) 546-551
44. Su L.H., Wu T.L., Chia J.H., Chu C., Kuo A.J., and Chiu C.H. Increasing ceftriaxone resistance in Salmonella isolates from a university hospital in Taiwan. J. Antimicrob. Chemother. 55 (2005) 846-852
45. Chen S., Zhao S., White D.G., Schroeder C.M., Lu R., Yang H., McDermott P.F., Ayers S., and Meng J. Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl. Environ. Microbiol. 70 (2004) 1-7
46. Chopra I., O'Neill A.J., and Miller K. The role of mutators in the emergence of antibiotic-resistant bacteria. Drug Resist. Updat. 6 (2003) 137-145
47. LeClerc J.E., Li B., Payne W.L., and Cebula T.A. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274 (1996) 1208-1211
48. Levy D.D., Sharma B., and Cebula T.A. Single-nucleotide polymorphism mutation spectra and resistance to quinolones in Salmonella enterica serovar Enteritidis with a mutator phenotype. Antimicrob. Agents Chemother. 48 (2004) 2355-2363
49. Molbak K., Baggesen D.L., Aarestrup F.M., Ebbesen J.M., Engberg J., Frydendahl K., Gerner-Smidt P., Petersen A.M., and Wegener H.C. An outbreak of multidrug-resistant, quinolone-resistant Salmonella enterica serotype Typhimurium DT104. N. Engl. J. Med. 341 (1999) 1420-1425
50. Varma J.K., Greene K.D., Ovitt J., Barrett T.J., Medalla F., and Angulo F.J. Hospitalization and antimicrobial resistance in Salmonella outbreaks, 1984-2002. Emerg. Infect. Dis. 11 (2005) 943-946
51. Angulo F.J., Nargund V.N., and Chiller T.C. Evidence of an association between use of anti-microbial agents in food animals and anti-microbial resistance among bacteria isolated from humans and the human health consequences of such resistance. J. Vet. Med. B 51 (2004) 374-379
52. Guerra B., Soto S., Helmuth R., and Mendoza M.C. Characterization of a self-transferable plasmid from Salmonella enterica serotype Typhimurium clinical isolates carrying two integron-borne gene cassettes together with virulence and drug resistance genes. Antimicrob. Agents Chemother. 46 (2002) 2977-2981
53. Fluit A.C. Towards more virulent and antibiotic-resistant Salmonella?. FEMS Immunol. Med. Microbiol. 43 (2005) 1-11
54. Davis M.A., Hancock D.D., and Besser T.E. Multiresistant clones of Salmonella enterica: the importance of dissemination. J. Lab. Clin. Med. 140 (2002) 135-141
55. Molbak K. Spread of resistant bacteria and resistance genes from animals to humans - the public health consequences. J. Vet. Med. B 51 (2004) 364-369
56. Allen C.A., Fedorka-Cray P.J., Vazquez-Torres A., Suyemoto M., Altier C., Ryder L.R., Fang F.C., and Libby S.J. In vitro and in vivo assessment of Salmonella enterica serovar Typhimurium DT104 virulence. Infect. Immun. 69 (2001) 4673-4677
57. Luo N., Sahin O., Lin J., Michel L.O., and Zhang Q. In vivo selection of Campylobacter isolates with high levels of fluoroquinolone resistance associated with gyrA mutations and the function of the CmeABC efflux pump. Antimicrob. Agents Chemother. 47 (2003) 390-394
58. Gootz T.D., and Martin B.A. Characterization of high-level quinolone resistance in Campylobacter jejuni. Antimicrob. Agents Chemother. 35 (1991) 840-845
59. Lin J., Sahin O., Michel L.O., and Zhang Q. Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect. Immun. 71 (2003) 4250-4259
60. Price L.B., Johnson E., Vailes R., and Silbergeld E. Fluoroquinolone-resistant Campylobacter isolates from conventional and antibiotic-free chicken products. Environ. Health Perspect. 113 (2005) 557-560
61. Pedersen K., and Wedderkopp A. Resistance to quinolones in Campylobacter jejuni and Campylobacter coli from Danish broilers at farm level. J. Appl. Microbiol. 94 (2003) 111-119
62. Smith K.E., Besser J.M., Hedberg C.W., Leano F.T., Bender J.B., Wicklund J.H., Johnson B.P., Moore K.A., and Osterholm M.T. Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992-1998. N. Engl. J. Med. 340 (1999) 1525-1532
63. Helms M., Simonsen J., Olsen K.E., and Molbak K. Adverse health events associated with antimicrobial drug resistance in Campylobacter species: a registry-based cohort study. J. Infect. Dis. 191 (2005) 1050-1055
64. Parkhill J., Wren B.W., Mungall K., Ketley J.M., Churcher C., Basham D., Chillingworth T., Davies R.M., Feltwell T., Holroyd S., Jagels K., Karlyshev A.V., Moule S., Pallen M.J., Penn C.W., Quail M.A., Rajandream M.A., Rutherford K.M., van Vliet A.H., Whitehead S., and Barrell B.G. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403 (2000) 665-668
65. Fouts D.E., Mongodin E.F., Mandrell R.E., Miller W.G., Rasko D.A., Ravel J., Brinkac L.M., DeBoy R.T., Parker C.T., Daugherty S.C., Dodson R.J., Durkin A.S., Madupu R., Sullivan S.A., Shetty J.U., Ayodeji M.A., Shvartsbeyn A., Schatz M.C., Badger J.H., Fraser C.M., and Nelson K.E. Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol. 3 (2005) e15
66. Bjorkholm B., Sjolund M., Falk P.G., Berg O.G., Engstrand L., and Andersson D.I. Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 14607-14612
67. Gibreel A., Kos V.N., Keelan M., Trieber C.A., Levesque S., Michaud S., and Taylor D.E. Macrolide resistance in Campylobacter jejuni and Campylobacter coli: molecular mechanism and stability of the resistance phenotype. Antimicrob. Agents Chemother. 49 (2005) 2753-2759
68. Avrain L., Vernozy-Rozand C., and Kempf I. Evidence for natural horizontal transfer of tetO gene between Campylobacter jejuni strains in chickens. J. Appl. Microbiol. 97 (2004) 134-140
69. Sato K., Bartlett P.C., Kaneene J.B., and Downes F.P. Comparison of prevalence and antimicrobial susceptibilities of Campylobacter spp. isolates from organic and conventional dairy herds in Wisconsin. Appl. Environ. Microbiol. 70 (2004) 1442-1447