Dissemination of Cephalosporin Resistance Genes between Strains from Farm Animals and Humans by Specific Plasmid Lineages

English version České info

The rapid global rise of infections caused by Escherichia coli that are resistant to clinically relevant antimicrobials, including third-generation cephalosporins, is cause for concern. The intestinal tract of livestock, in particular poultry, is an important reservoir for drug resistant E. coli, but it is unknown to what extent these bacteria can spread to humans. Food is thought to be an important source because drug-resistant E. coli have been detected in animals raised for meat consumption and in meat products. Previous studies that used traditional, low-resolution, genetic typing methods found that drug resistant E. coli present in humans and poultry were indistinguishable from each other, suggesting dissemination of these bacteria through the food-chain to humans. However, by applying high-resolution, whole-genome sequencing methods, we did not find evidence for such transmission of bacteria through the food-chain. Instead, by employing a novel approach for the reconstruction of mobile genetic elements from whole-genome sequence data, we discovered that genetically unrelated E. coli isolates from both humans and animal sources carried nearly identical plasmids that encode third-generation cephalosporin resistance determinants. Our data suggest that cephalosporin resistance is mainly disseminated via the transfer of mobile genetic elements between animals and humans.

Vyšlo v časopise: Dissemination of Cephalosporin Resistance Genes between Strains from Farm Animals and Humans by Specific Plasmid Lineages. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004776
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004776

Souhrn

Zdroje

1. De KrakerMEA, DaveyPG, GrundmannH on behalf of the BURDEN study group (2011) Mortality and Hospital Stay Associated with Resistant Staphylococcus aureus and Escherichia coli Bacteremia: Estimating the Burden of Antibiotic Resistance in Europe. PLoS Med 8: e1001104 doi:10.1371/journal.pmed.1001104

2. MauldinPD, SalgadoCD, HansenIS, DurupDT, BossoJA (2010) Attributable Hospital Cost and Length of Stay Associated with Health Care-Associated Infections Caused by Antibiotic-Resistant Gram-Negative Bacteria. Antimicrob Agents Chemother 54 : 109–115 doi:10.1128/AAC.01041-09

3. CoqueTM, BaqueroF, CantónR (2008) Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Euro Surveill 13: pii: 19044.

4. HawkeyPM, JonesAM (2009) The changing epidemiology of resistance. J Antimicrob Chemother 64: i3–i10 doi:10.1093/jac/dkp256

5. DuboisV, BarbeyracBD, RoguesA-M, ArpinC, CoulangeL, et al. (2010) CTX-M-producing Escherichia coli in a maternity ward: a likely community importation and evidence of mother-to-neonate transmission. J Antimicrob Chemother 65 : 1368–1371 doi:10.1093/jac/dkq153

6. ValverdeA, CoqueTM, Sánchez-MorenoMP, RollánA, BaqueroF, et al. (2004) Dramatic Increase in Prevalence of Fecal Carriage of Extended-Spectrum β-Lactamase-Producing Enterobacteriaceae during Nonoutbreak Situations in Spain. J Clin Microbiol 42 : 4769–4775 doi:10.1128/JCM.42.10.4769-4775.2004

7. KaperJB, NataroJP, MobleyHLT (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2 : 123–140 doi:10.1038/nrmicro818

8. SmetA, MartelA, PersoonsD, DewulfJ, HeyndrickxM, et al. (2008) Diversity of Extended-Spectrum β-Lactamases and Class C β-Lactamases among Cloacal Escherichia coli Isolates in Belgian Broiler Farms. Antimicrob Agents Chemother 52 : 1238–1243 doi:10.1128/AAC.01285-07

9. MachadoE, CoqueTM, CantónR, SousaJC, PeixeL (2008) Antibiotic resistance integrons and extended-spectrum β-lactamases among Enterobacteriaceae isolates recovered from chickens and swine in Portugal. J Antimicrob Chemother 62 : 296–302 doi:10.1093/jac/dkn179

10. DoiY, PatersonDL, EgeaP, PascualA, López-CereroL, et al. (2010) Extended-spectrum and CMY-type β-lactamase-producing Escherichia coli in clinical samples and retail meat from Pittsburgh, USA and Seville, Spain. Clin Microbiol Infect 16 : 33–38 doi:10.1111/j.1469-0691.2009.03001.x

11. CollignonP, AarestrupFM, IrwinR, McEwenS (2013) Human deaths and third-generation cephalosporin use in poultry, Europe. Emerg Infect Dis 19 : 1339–1340 doi:10.3201/eid.1908.120681

12. Van de Sande-BruinsmaN, GrundmannH, VerlooD, TiemersmaE, MonenJ, et al. (2008) Antimicrobial drug use and resistance in Europe. Emerg Infect Dis 14 : 1722–1730 doi:10.3201/eid1411.070467

13. GraveK, GrekoC, KvaaleMK, Torren-EdoJ, MackayD, et al. (2012) Sales of veterinary antibacterial agents in nine European countries during 2005–09: trends and patterns. J Antimicrob Chemother 67 : 3001–3008 doi:10.1093/jac/dks298

14. OverdevestI, WillemsenI, RijnsburgerM, EustaceA, XuL, et al. (2011) Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerg Infect Dis 17 : 1216–1222 doi:10.3201/eid1707.110209

15. Leverstein-van HallMA, DierikxCM, Cohen StuartJ, VoetsGM, van den MunckhofMP, et al. (2011) Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis 17 : 873–880 doi:10.1111/j.1469-0691.2011.03497.x

16. KluytmansJAJW, OverdevestITMA, WillemsenI, Kluytmans-van den BerghMFQ, van der ZwaluwK, et al. (2013) Extended-spectrum β-lactamase-producing Escherichia coli from retail chicken meat and humans: comparison of strains, plasmids, resistance genes, and virulence factors. Clin Infect Dis Off Publ Infect Dis Soc Am 56 : 478–487 doi:10.1093/cid/cis929

17. SabatAJ, BudimirA, NashevD, Sá-LeãoR, van Dijl Jm, et al. (2013) Overview of molecular typing methods for outbreak detection and epidemiological surveillance. Euro Surveill Bull Eur Sur Mal Transm Eur Commun Dis Bull 18 : 20380.

18. VoetsGM, FluitAC, ScharringaJ, SchapendonkC, van den MunckhofT, et al. (2013) Identical plasmid AmpC beta-lactamase genes and plasmid types in E. coli isolates from patients and poultry meat in the Netherlands. Int J Food Microbiol 167 : 359–362 doi:10.1016/j.ijfoodmicro.2013.10.001

19. McNallyA, ChengL, HarrisSR, CoranderJ (2013) The evolutionary path to extraintestinal pathogenic, drug-resistant Escherichia coli is marked by drastic reduction in detectable recombination within the core genome. Genome Biol Evol 5 : 699–710 doi:10.1093/gbe/evt038

20. LiL, StoeckertCJJr, RoosDS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13 : 2178–2189 doi:10.1101/gr.1224503

21. GradYH, LipsitchM, FeldgardenM, ArachchiHM, CerqueiraGC, et al. (2012) Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011. Proc Natl Acad Sci U S A 109 : 3065–3070 doi:10.1073/pnas.1121491109

22. ReevesPR, LiuB, ZhouZ, LiD, GuoD, et al. (2011) Rates of Mutation and Host Transmission for an Escherichia coli Clone over 3 Years. PLoS ONE 6: e26907 doi:10.1371/journal.pone.0026907

23. LanzaVF, de ToroM, Garcillán-BarciaMP, MoraA, BlancoJ, CoqueTM, de la CruzF Turbulent plasmid flux in Escherichia coli ST131 sublineages, analyzed by plasmid constellation network (PLACNET), a new method for plasmid reconstruction from whole genome sequences. PLoS Gen 10: e1004766.

24. SmillieC, Garcillán-BarciaMP, FranciaMV, RochaEPC, de la CruzF (2010) Mobility of plasmids. Microbiol Mol Biol Rev MMBR 74 : 434–452 doi:10.1128/MMBR.00020-10

25. Garcillán-BarciaMP, FranciaMV, de la CruzF (2009) The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev 33 : 657–687.

26. Den BakkerHC, AllardMW, BoppD, BrownEW, FontanaJ, et al. (2014) Rapid Whole-Genome Sequencing for Surveillance of Salmonella enterica Serovar Enteritidis. Emerg Infect Dis 20 : 1306–1314 doi:10.3201/eid2008.131399

27. KöserCU, HoldenMTG, EllingtonMJ, CartwrightEJP, BrownNM, et al. (2012) Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 366 : 2267–2275 doi:10.1056/NEJMoa1109910

28. RoetzerA, DielR, KohlTA, RückertC, NübelU, et al. (2013) Whole genome sequencing versus traditional genotyping for investigation of a Mycobacterium tuberculosis outbreak: a longitudinal molecular epidemiological study. PLoS Med 10: e1001387 doi:10.1371/journal.pmed.1001387

29. IshiwaA, KomanoT (2004) PilV Adhesins of Plasmid R64 Thin Pili Specifically Bind to the Lipopolysaccharides of Recipient Cells. J Mol Biol 343 : 615–625 doi:10.1016/j.jmb.2004.08.059

30. DierikxC, van der GootJ, FabriT, van Essen-ZandbergenA, SmithH, et al. (2013) Extended-spectrum-β-lactamase -⁠ and AmpC-β-lactamase-producing Escherichia coli in Dutch broilers and broiler farmers. J Antimicrob Chemother 68 : 60–67 doi:10.1093/jac/dks349

31. DierikxC, van Essen-ZandbergenA, VeldmanK, SmithH, MeviusD (2010) Increased detection of extended spectrum beta-lactamase producing Salmonella enterica and Escherichia coli isolates from poultry. Vet Microbiol 145 : 273–278 doi:10.1016/j.vetmic.2010.03.019

32. BörjessonS, JernbergC, BrolundA, EdquistP, FinnM, et al. (2013) Characterization of plasmid-mediated AmpC-producing E. coli from Swedish broilers and association with human clinical isolates. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis 19: E309–311 doi:10.1111/1469-0691.12192

33. BaudryPJ, MatasejeL, ZhanelGG, HobanDJ, MulveyMR (2009) Characterization of plasmids encoding CMY-2 AmpC beta-lactamases from Escherichia coli in Canadian intensive care units. Diagn Microbiol Infect Dis 65 : 379–383 doi:\10.1016/j.diagmicrobio.2009.08.011.\

34. VillaL, García-FernándezA, FortiniD, CarattoliA (2010) Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J Antimicrob Chemother 65 2518–2529 : 34.

35. WoodfordN, CarattoliA, KarisikE, UnderwoodA, EllingtonMJ, et al. (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 : 4472–4482 doi:10.1128/AAC.00688-09

36. KruseH, SørumH (1994) Transfer of multiple drug resistance plasmids between bacteria of diverse origins in natural microenvironments. Appl Environ Microbiol 60 : 4015–4021.

37. WarnesSL, HighmoreCJ, KeevilCW (2012) Horizontal transfer of antibiotic resistance genes on abiotic touch surfaces: implications for public health. mBio 3 doi:10.1128/mBio.00489-12

38. CavacoLM, AbatihE, AarestrupFM, GuardabassiL (2008) Selection and persistence of CTX-M-producing Escherichia coli in the intestinal flora of pigs treated with amoxicillin, ceftiofur, or cefquinome. Antimicrob Agents Chemother 52 : 3612–3616 doi:10.1128/AAC.00354-08

39. GorenMG, CarmeliY, SchwaberMJ, ChmelnitskyI, SchechnerV, et al. (2010) Transfer of carbapenem-resistant plasmid from Klebsiella pneumoniae ST258 to Escherichia coli in patient. Emerg Infect Dis 16 : 1014–1017 doi:10.3201/eid1606.091671

40. WirthT, FalushD, LanR, CollesF, MensaP, et al. (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60 : 1136–1151 doi:10.1111/j.1365-2958.2006.05172.x

41. CarattoliA, BertiniA, VillaL, FalboV, HopkinsKL, et al. (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63 : 219–228 doi:10.1016/j.mimet.2005.03.018

42. García-FernándezA, ChiarettoG, BertiniA, VillaL, FortiniD, et al. (2008) Multilocus sequence typing of IncI1 plasmids carrying extended-spectrum beta-lactamases in Escherichia coli and Salmonella of human and animal origin. J Antimicrob Chemother 61 : 1229–1233 doi:10.1093/jac/dkn131

43. JolleyKA, MaidenMCJ (2010) BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11 : 595 doi:10.1186/1471-2105-11-595

44. Cohen StuartJ, DierikxC, Al NaiemiN, KarczmarekA, Van HoekAHAM, et al. (2010) Rapid detection of TEM, SHV and CTX-M extended-spectrum beta-lactamases in Enterobacteriaceae using ligation-mediated amplification with microarray analysis. J Antimicrob Chemother 65 : 1377–1381 doi:10.1093/jac/dkq146

45. LiY, HuY, BolundL, WangJ (2010) State of the art de novo assembly of human genomes from massively parallel sequencing data. Hum Genomics 4 : 271–277.

46. SchatzMC, PhillippyAM, SommerDD, DelcherAL, PuiuD, et al. (2013) Hawkeye and AMOS: visualizing and assessing the quality of genome assemblies. Brief Bioinform 14 : 213–224 doi:10.1093/bib/bbr074

47. AzizRK, BartelsD, BestAA, DeJonghM, DiszT, et al. (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9 : 75 doi:10.1186/1471-2164-9-75

48. TatusovRL, NataleDA, GarkavtsevIV, TatusovaTA, ShankavaramUT, et al. (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29 : 22–28.

49. de BeenM, van SchaikW, ChengL, CoranderJ, WillemsRJ (2013) Recent recombination events in the core genome are associated with adaptive evolution in Enterococcus faecium. Genome Biol Evol 5 : 1524–1535 doi:10.1093/gbe/evt111

50. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 : 1792–1797 doi:10.1093/nar/gkh340

51. Capella-GutiérrezS, Silla-MartínezJM, GabaldónT (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinforma Oxf Engl 25 : 1972–1973 doi:10.1093/bioinformatics/btp348

52. StamatakisA (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinforma Oxf Engl 22 : 2688–2690 doi:10.1093/bioinformatics/btl446

53. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28 : 2731–2739 doi:10.1093/molbev/msr121

54. LangmeadB, SalzbergSL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9 : 357–359 doi:10.1038/nmeth.1923

55. LarsenMV, CosentinoS, RasmussenS, FriisC, HasmanH, et al. (2012) Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 50 : 1355–1361 doi:10.1128/JCM.06094-11

56. KurtzS, PhillippyA, DelcherAL, SmootM, ShumwayM, et al. (2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12 doi:10.1186/gb-2004-5-2-r12

57. TekaiaF, YeramianE (2005) Genome trees from conservation profiles. PLoS Comput Biol 1: e75 doi:10.1371/journal.pcbi.0010075

58. LiW, GodzikA (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinforma Oxf Engl 22 : 1658–1659 doi:10.1093/bioinformatics/btl158