Time-scaled evolutionary analysis of the transmission and antibiotic resistance dynamics of Staphylococcus aureus clonal complex 398

Applied and Environmental Microbiology

Volumn 80, Issue 23, 2014, Pages 7275-7282

  Ward, M J ^a   Gibbons, C L ^a   McAdam, P R ^b   van Bunnik, B A D ^a   Girvan, E K ^c   Edwards, G F ^c   Fitzgerald, J R ^b   Woolhouse, M E J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c GLASGOW ROYAL INFIRMARY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BACTERIA; HOSPITALS;

ANTIBIOTIC RESISTANCE; EPISTATIC INTERACTIONS; HOSPITAL ENVIRONMENT; MULTIPLE TRANSMISSION; PHYLOGENETIC ANALYSIS; SOURCE POPULATION; STAPHYLOCOCCUS AUREUS; STATE-OF-THE-ART METHODS;

AGRICULTURE;

ANTIBIOTIC RESISTANCE; BACTERIUM; EPISTASIS; GENOME; PHYLOGENETICS; PHYLOGENY;

STAPHYLOCOCCUS AUREUS;

ANTIINFECTIVE AGENT;

ANIMAL; ANTIBIOTIC RESISTANCE; CLASSIFICATION; DRUG EFFECTS; DRUG UTILIZATION; EPIDEMIOLOGY; GENETIC VARIABILITY; GENETICS; GENOTYPE; HUMAN; ISOLATION AND PURIFICATION; LIVESTOCK; MICROBIOLOGY; MOLECULAR EPIDEMIOLOGY; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; TIME; TRANSMISSION; UNITED KINGDOM; VETERINARY; ZOONOSIS;

ANIMALS; ANTI-BACTERIAL AGENTS; DRUG RESISTANCE, BACTERIAL; DRUG UTILIZATION; GENETIC VARIATION; GENOTYPE; GREAT BRITAIN; HUMANS; LIVESTOCK; MOLECULAR EPIDEMIOLOGY; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TIME FACTORS; ZOONOSES;

EID: 84910109057     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01777-14     Document Type: Article

References (39)

1. DeLeo FR, Otto M, Kreiswirth BN, Chambers HF. 2010. Communityassociated meticillin-resistant Staphylococcus aureus. Lancet 375:1557-1568. http://dx.doi.org/10.1016/S0140-6736(09)61999-1.
2. Graveland H, Wagenaar JA, Bergs K, Heesterbeek H, Heederik D. 2011. Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS One 6:e16830. http://dx.doi.org/10.1371/journal.pone.0016830.
3. Enright MC, Day NPJ, Davies CE, Peacock SJ, Spratt BG. 2000. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 38:1008-1015.
4. Bhat M, Dulmortier C, Taylor BS, Miller M, Vasquez G, Yunen J, Brudney K, Sanchez J, Rodriguez-Taveras C, Rojas R, Leon P, Lowy FD. 2009. Staphylococcus aureus ST398, New York City and Dominican Republic. Emerg. Infect. Dis. 15:285-287. http://dx.doi.org/10.3201/eid1502.080609.
5. Uhlemann AC, Dumortier C, Hafer C, Taylor BS, Sanchez J, Rodriguez-Taveras C, Leon P, Rojas R, Olive C, Lowy FD. 2012. Molecular characterization of Staphylococcus aureus from outpatients in the Caribbean reveals the presence of pandemic clones. Eur. J. Clin. Microbiol. Infect. Dis. 31:505-511. http://dx.doi.org/10.1007/s10096-011-1339-2.
6. Uhlemann AC, Porcella SF, Trivedi S, Sullivan SB, Hafer C, Kennedy AD, Barbian KD, McCarthy AJ, Street C, Hirschberg DL, Lipkin WI, Lindsay JA, DeLeo FR, Lowy FD. 2012. Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. mBio 3:e00027-12. http://dx.doi.org/10.1128/mBio.00027-12.
7. Rasigade JP, Laurent F, Hubert P, Vandenesch F, Etienne J. 2010. Lethal necrotizing pneumonia caused by an ST398 Staphylococcus aureus strain. Emerg. Infect. Dis. 16:1330. http://dx.doi.org/10.3201/eid1608.100317.
8. Fessler A, Scott C, Kadlec K, Ehricht R, Monecke S, Schwarz S. 2010. Characterization of methicillin-resistant Staphylococcus aureus ST398 from cases of bovine mastitis. J. Antimicrob. Chemother. 65:619-625. http://dx.doi.org/10.1093/jac/dkq021.
9. Weinert LA, Welch JJ, Suchard MA, Lemey P, Rambaut A, Fitzgerald JR. 2012. Molecular dating of human-to-bovid host jumps by Staphylococcus aureus reveals an association with the spread of domestication. Biol. Lett. 8:829-832. http://dx.doi.org/10.1098/rsbl.2012.0290.
10. Shepheard MA, Fleming VM, Connor TR, Corander J, Feil EJ, Fraser C, Hanage WP. 2013. Historical zoonoses and other changes in host tropism of Staphylococcus aureus, identified by phylogenetic analysis of a population dataset. PLoS One 8:e62369. http://dx.doi.org/10.1371/journal.pone.0062369.
11. McCarthy AJ, van Wamel W, Vandendriessche S, Larsen J, Denis O, Garcia-Graells C, Uhlemann AC, Lowy FD, Skov R, Lindsay JA. 2012. Staphylococcus aureus CC398 clade associated with human-to-human transmission. Appl. Environ. Microbiol. 78:8845-8848. http://dx.doi.org/10.1128/AEM.02398-12.
12. Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, Pearson T, Waters AE, Foster JT, Schupp J, Gillece J, Driebe E, Liu CM, Springer B, Zdovc I, Battisti A, Franco A, Zumudzki J, Schwarz S, Butaye P, Jouy E, Pomba C, Porrero MC, Ruimy R, Smith TC, Robinson DA, Weese JS, Arriola CS, Yu FY, Laurent F, Keim P, Skov R, Aarestrup FM. 2012. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 3:e00305-11. http://dx.doi.org/10.1128/mBio.00305-11.
13. Loeffler A, Kearns AM, Ellington MJ, Smith LJ, Unt VE, Lindsay JA, Pfeiffer DU, Lloyd DH. 2009. First isolation of MRSA ST398 from UK animals: a new challenge for infection control teams? J. Hosp. Infect. 72: 269-271. http://dx.doi.org/10.1016/j.jhin.2009.04.002.
14. Paterson GK, Larsen J, Harrison EM, Larsen AR, Morgan FJ, Peacock SJ, Parkhill J, Zadoks RN, Holmes MA. 2012. First detection of livestock-associated meticillin-resistant Staphylococcus aureus CC398 in bulk tank milk in the United Kingdom, January to July 2012. Euro Surveill. 17:5-7.
15. Department for Environment, Food, and Rural Affairs. 2013. Livestockassociated MRSA found at a farm in East Anglia. https://www.gov.uk/government/news/livestock-associated-mrsa-found-at-a-farm-in-east-anglia. Accessed 5 August 2014.
16. European Food Safety Authority. 2009. Analysis of the baseline survey on the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in holdings with breeding pigs, in the EU, 2008. Part A: MRSA prevalence estimates. EFSA J. 7:1736. http://dx.doi.org/10.2903/j.efsa.2009.1376.
17. Dancer SJ, White LF, Lamb J, Girvan EK, Robertson C. 2009. Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study. BMC Med. 7:28. http://dx.doi.org/10.1186/1741-7015-7-28.
18. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. http://dx.doi.org/10.1093/bioinformatics/btp324.
19. McAdam PR, Templeton KE, Edwards GF, Holden MTG, Feil EJ, Aanensen DM, Bargawi HJA, Spratt BG, Bentley SD, Parkhill J, Enright MC, Holmes A, Girvan EK, Godfrey PA, Feldgarden M, Kearns AM, Rambaut A, Robinson DA, Fitzgerald JR. 2012. Molecular tracing of the emergence, adaptation and transmission of hospital-associated methicillin-resistant Staphylococcus aureus. Proc. Natl. Acad. Sci. U. S. A. 109: 9107-9112. http://dx.doi.org/10.1073/pnas.1202869109.
20. Stegger M, Aziz M, Chroboczek T, Price LB, Ronco T, Kiil K, Skov RL, Laurent F, Andersen PS. 2013. Genome analysis of Staphylococcus aureus ST291, a double locus variant of ST398, reveals a distinct genetic lineage. PLoS One 8:e63008. http://dx.doi.org/10.1371/journal.pone.0063008.
21. Marttinen P, Hanage WP, Croucher NJ, Connor TR, Harris SR, Bentley SD, Corander J. 2012. Detection of recombination events in bacterial genomes from large population samples. Nucleic Acids. Res. 40:e6. http://dx.doi.org/10.1093/nar/gkr928.
22. Swofford DL. 2003. Phylogenetic analysis using parsimony (* and other methods), version 4, 4th ed. Sinauer Associates, Sunderland, MA.
23. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59:307-321. http://dx.doi.org/10.1093/sysbio/syq010.
24. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
25. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29:1969-1973. http://dx.doi.org/10.1093/molbev/mss075.
26. Lemey P, Rambaut A, Drummond AJ, Suchard MA. 2009. Bayesian phylogeography finds its roots. PLoS Comput. Biol. 5:e1000520. http://dx.doi.org/10.1371/journal.pcbi.1000520.
27. Minin VN, Suchard MA. 2008. Counting labeled transitions in continuous-time Markov models of evolution. J. Math. Biol. 56:391-412. http://dx.doi.org/10.1007/s00285-007-0120-8.
28. Minin VN, Suchard MA. 2008. Fast, accurate and simulation-free stochastic mapping. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363:3985-3995. http://dx.doi.org/10.1098/rstb.2008.0176.
29. van Wamel WJB, Rooijakkers SHM, Ruyken M, van Kessel KPM, van Strijp JAG. 2006. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J. Bacteriol. 188:1310-1315. http://dx.doi.org/10.1128/JB.188.4.1310-1315.2006.
30. Qiu YL, Lee J, Whitlock BA, Bernasconi-Quadroni F, Dombrovska O. 2001. Was the ANITA rooting of the angiosperm phylogeny affected by long-branch attraction? Mol. Biol. Evol. 18:1745-1753. http://dx.doi.org/10.1093/oxfordjournals.molbev.a003962.
31. Fitzgerald JR. 2012. Human origin for livestock-associated methicillinresistant Staphylococcus aureus. mBio 3:e00082-12. http://dx.doi.org/10.1128/mBio.00082-12.
32. Lemey P, Rambaut A, Bedford T, Faria N, Bielejec F, Baele G, Russell CA, Smith DJ, Pybus OG, Brockmann D, Suchard MA. 2014. Unifying viral genetics and human transportation data to predict the global transmission dynamics of human influenza H3N2. PLoS Pathog. 10:e1003932. http://dx.doi.org/10.1371/journal.ppat.1003932.
33. Goldberg TL. 2003. Application of phylogeny reconstruction and character-evolution analysis to inferring patterns of directional microbial transmission. Prev. Vet. Med. 61:59-70. http://dx.doi.org/10.1016/S0167-5877(03)00161-2.
34. Mather AE, Reid SWJ, Maskell DJ, Parkhill J, Fookes MC, Harris SR, Brown DJ, Coia JE, Mulvey MR, Gilmour MW, Petrovska L, de Pinna E, Kuroda M, Akiba M, Izumiya H, Connor TR, Suchard MA, Lemey P, Mellor DJ, Haydon DT, Thomson NR. 2013. Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts. Science 341:1514-1517. http://dx.doi.org/10.1126/science.1240578.
35. Hall MD, Knowles NJ, Wadsworth J, Rambaut A, Woolhouse MEJ. 2013. Reconstructing geographical movements and host species transitions of foot-and-mouth disease virus serotype SAT 2. mBio 4:e00591-13. http://dx.doi.org/10.1128/mBio.00591-13.
36. Trzcinski K, Cooper BS, Hryniewicz W, Dowson CG. 2000. Expression of resistance to tetracyclines in strains of methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother. 45:763-770. http://dx.doi.org/10.1093/jac/45.6.763.
37. Cogliani C, Goossens H, Greko C. 2011. Restricting antimicrobial use in food animals: lessons from Europe. Microbe Mag. 6:274-279. http://dx.doi.org/10.1128/microbe.6.274.1.
38. Chopra I, Roberts M. 2001. Tetracycline antibiotics: Mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev. 65:232-260. http://dx.doi.org/10.1128/MMBR.65.2.232-260.2001.
39. Woolhouse MEJ, Ward MJ. 2013. Sources of antimicrobial resistance. Science 341:1460-1461. http://dx.doi.org/10.1126/science.1243444.