Genomic epidemiology of a protracted hospital outbreak caused by a toxin a-negative clostridium difficile sublineage PCR ribotype 017 strain in London, England

Journal of Clinical Microbiology

Volumn 53, Issue 10, 2015, Pages 3141-3147

  Cairns, M D ^a,b,c   Preston, M D ^a   Lawley, T D ^d   Clark, T G ^a   Stabler, R A ^a   Wren, B W ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c ROYAL LONDON HOSPITAL   (United Kingdom)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIUM DIFFICILE TOXIN A; CLOSTRIDIUM DIFFICILE TOXIN B; BACTERIAL TOXIN; ENTEROTOXIN; TCDA PROTEIN, CLOSTRIDIUM DIFFICILE;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CLONAL VARIATION; CLOSTRIDIUM DIFFICILE INFECTION; CONTROLLED STUDY; EPIDEMIC; GENE CLUSTER; GENE FREQUENCY; GENE LOCUS; GENE SEQUENCE; GENETIC EPIDEMIOLOGY; GENOME ANALYSIS; HAPLOTYPE; HUMAN; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PEPTOCLOSTRIDIUM DIFFICILE; PHYLOGENY; POLYMERASE CHAIN REACTION; PREVALENCE; PRIORITY JOURNAL; RIBOTYPING; SINGLE NUCLEOTIDE POLYMORPHISM; STRAIN DIFFERENCE; STRAIN IDENTIFICATION; TOXIN ANALYSIS; TRANSPOSON; UNITED KINGDOM; UNIVERSITY HOSPITAL; WARD; CLASSIFICATION; CLOSTRIDIUM INFECTIONS; CLUSTER ANALYSIS; CROSS INFECTION; DEFICIENCY; DIARRHEA; DNA SEQUENCE; ENGLAND; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EPIDEMIOLOGY;

BACTERIAL TOXINS; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; CLUSTER ANALYSIS; CROSS INFECTION; DIARRHEA; DISEASE OUTBREAKS; ENTEROTOXINS; GENOME, BACTERIAL; HUMANS; LONDON; MOLECULAR EPIDEMIOLOGY; PHYLOGENY; POLYMERASE CHAIN REACTION; POLYMORPHISM, SINGLE NUCLEOTIDE; RIBOTYPING; SEQUENCE ANALYSIS, DNA;

EID: 84941950035     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.00648-15     Document Type: Article

References (40)

1. Kuehne SA, Collery MM, Kelly ML, Cartman ST, Cockayne A, Minton NP. 2014. Importance of toxin A, toxin B, and CDT in virulence of an epidemic Clostridium difficile strain. J Infect Dis 209:83-86. http://dx. doi . org/10. 1093/infdis/jit426.
2. He M, Miyajima F, Roberts P, Ellison L, Pickard DJ, Martin MJ, Connor TR, Harris SR, Fairley D, Bamford KB, D'Arc S, Brazier J, Brown D, Coia JE, Douce G, Gerding D, Kim HJ, Koh TH, Kato H, Senoh M, Louie T, Michell S, Butt E, Peacock SJ, Brown NM, Riley T, Songer G, Wilcox M, Pirmohamed M, Kuijper E, Hawkey P, Wren BW, Dougan G, Parkhill J, Lawley TD. 2013. Emergence and global spread of epidemic healthcareassociated Clostridium difficile. Nat Genet 45:109-113. http://dx. doi. org /10. 1038/ng. 2478.
3. Valiente E, Cairns MD, Wren BW. 2014. The Clostridium difficile PCR ribotype 027 lineage: a pathogen on the move. Clin Microbiol Infect 20: 396-404. http://dx. doi. org/10. 1111/1469-0691. 12619.
4. Health Protection Agency. 2012. Clostridium difficile Ribotyping Network (CDRN) for England and Northern Ireland 2010-2011 annual report. Health Protection Agency, London, United Kingdom.
5. Wren MW, Kinson R, Sivapalan M, Shemko M, Shetty NR. 2009. Detection of Clostridium difficile infection: a suggested laboratory diagnostic algorithm. Br J Biomed Sci 66:175-179.
6. Shin BM, Kuak EY, Yoo SJ, Shin WC, Yoo HM. 2008. Emerging toxin A-B- variant strain of Clostridium difficile responsible for pseudomembranous colitis at a tertiary care hospital in Korea. Diagn Microbiol Infect Dis 60:333-337. http://dx. doi. org/10. 1016/j. diagmicrobio. 2007. 10. 022.
7. Walker AS, Eyre DW, Wyllie DH, Dingle KE, Griffiths D, Shine B, Oakley S, O'Connor L, Finney J, Vaughan A, Crook DW, Wilcox MH, Peto TE, Infections in Oxfordshire Research Database. 2013. Relationship between bacterial strain type, host biomarkers, and mortality in Clostridium difficile infection. Clin Infect Dis 56:1589-1600. http://dx. doi. org /10. 1093/cid/cit127.
8. Stabler RA, Dawson LF, Valiente E, Cairns MD, Martin MJ, Donahue EH, Riley TV, Songer JG, Kuijper EJ, Dingle KE, Wren BW. 2012. Macro and micro diversity of Clostridium difficile isolates from diverse sources and geographical locations. PLoS One 7:e31559. http://dx. doi. org /10. 1371/journal. pone. 0031559.
9. Stabler RA, He M, Dawson L, Martin M, Valiente E, Corton C, Lawley TD, Sebaihia M, Quail MA, Rose G, Gerding DN, Gibert M, Popoff MR, Parkhill J, Dougan G, Wren BW. 2009. Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium. Genome Biol 10:R102. http://dx. doi. org/10. 1186/gb-2009-10-9-r102.
10. Valiente E, Dawson LF, Cairns MD, Stabler RA, Wren BW. 2012. Emergence of new PCR ribotypes from the hypervirulent Clostridium difficile 027 lineage. J Med Microbiol 61:49-56. http://dx. doi. org/10. 1099 /jmm. 0. 036194-0.
11. Cairns MD, Stabler RA, Shetty N, Wren BW. 2012. The continually evolving Clostridium difficile species. Future Microbiol 7:945-957. http: //dx. doi. org/10. 2217/fmb. 12. 73.
12. Gerding DN, Johnson S, Rupnik M, Aktories K. 2014. Clostridium difficile binary toxin CDT: mechanism, epidemiology, and potential clinical importance. Gut Microbes 5:15-27. http://dx. doi. org/10. 4161/gmic . 26854.
13. Drudy D, Harnedy N, Fanning S, O'Mahony R, Kyne L. 2007. Isolation and characterisation of toxin A-negative, toxin B-positive Clostridium difficile in Dublin, Ireland. Clin Microbiol Infect 13:298-304. http://dx. doi . org/10. 1111/j. 1469-0691. 2006. 01634. x.
14. Drudy D, Harnedy N, Fanning S, Hannan M, Kyne L. 2007. Emergence and control of fluoroquinolone-resistant, toxin A-negative, toxin B-positive Clostridium difficile. Infect Control Hosp Epidemiol 28:932-940. http: //dx. doi. org/10. 1086/519181.
15. Elliott B, Squire MM, Thean S, Chang BJ, Brazier JS, Rupnik M, Riley TV. 2011. New types of toxin A-negative, toxin B-positive strains among clinical isolates of Clostridium difficile in Australia. J Med Microbiol 60: 1108-1111. http://dx. doi. org/10. 1099/jmm. 0. 031062-0.
16. Collins DA, Hawkey PM, Riley TV. 2013. Epidemiology of Clostridium difficile infection in Asia. Antimicrob Resist Infect Control 2:21. http://dx . doi. org/10. 1186/2047-2994-2-21.
17. Kuijper EJ, de Weerdt J, Kato H, Kato N, van Dam AP, van der Vorm ER, Weel J, van Rheenen C, Dankert J. 2001. Nosocomial outbreak of Clostridium difficile-associated diarrhoea due to a clindamycin-resistant enterotoxin A-negative strain. Eur J Clin Microbiol Infect Dis 20:528-534. http://dx. doi. org/10. 1007/s100960100550.
18. Pituch H, van den Braak N, van Leeuwen W, van Belkum A, Martirosian G, Obuch-Woszczatynski P, Luczak M, Meisel-Mikolajczyk F. 2001. Clonal dissemination of a toxin-A-negative/toxin-B-positive Clostridium difficile strain from patients with antibiotic-associated diarrhea in Poland. Clin Microbiol Infect 7:442-446. http://dx. doi. org/10. 1046/j . 1198-743x. 2001. 00312. x.
19. Huang H, Weintraub A, Fang H, Wu S, Zhang Y, Nord CE. 2010. Antimicrobial susceptibility and heteroresistance in Chinese Clostridium difficile strains. Anaerobe 16:633-635. http://dx. doi. org/10. 1016/j . anaerobe. 2010. 09. 002.
20. Kim H, Jeong SH, Roh KH, Hong SG, Kim JW, Shin MG, Kim MN, Shin HB, Uh Y, Lee H, Lee K. 2010. Investigation of toxin gene diversity, molecular epidemiology, and antimicrobial resistance of Clostridium difficile isolated from 12 hospitals in South Korea. Korean J Lab Med 30:491-497. http://dx. doi. org/10. 3343/kjlm. 2010. 30. 5. 491.
21. Kim H, Riley TV, Kim M, Kim CK, Yong D, Lee K, Chong Y, Park JW. 2008. Increasing prevalence of toxin A-negative, toxin B-positive isolates of Clostridium difficile in Korea: impact on laboratory diagnosis. J Clin Microbiol 46:1116-1117. http://dx. doi. org/10. 1128/JCM. 01188-07.
22. Kim SJ, Kim H, Seo Y, Yong D, Jeong SH, Chong Y, Lee K. 2010. Molecular characterization of toxin A-negative, toxin B-positive variant strains of Clostridium difficile isolated in Korea. Diagn Microbiol Infect Dis 67:198-201. http://dx. doi. org/10. 1016/j. diagmicrobio. 2010. 01. 007.
23. Goorhuis A, Legaria MC, van den Berg RJ, Harmanus C, Klaassen CH, Brazier JS, Lumelsky G, Kuijper EJ. 2009. Application of multiple-locus variable-number tandem-repeat analysis to determine clonal spread of toxin A-negative Clostridium difficile in a general hospital in Buenos Aires, Argentina. Clin Microbiol Infect 15:1080-1086. http://dx. doi. org/10 . 1111/j. 1469-0691. 2009. 02759. x.
24. Samra Z, Talmor S, Bahar J. 2002. High prevalence of toxin A-negative toxin B-positive Clostridium difficile in hospitalized patients with gastrointestinal disease. Diagn Microbiol Infect Dis 43:189-192. http://dx. doi . org/10. 1016/S0732-8893(02)00400-5.
25. Komatsu M, Kato H, Aihara M, Shimakawa K, Iwasaki M, Nagasaka Y, Fukuda S, Matsuo S, Arakawa Y, Watanabe M, Iwatani Y. 2003. High frequency of antibiotic-associated diarrhea due to toxin A-negative, toxin B-positive Clostridium difficile in a hospital in Japan and risk factors for infection. Eur J Clin Microbiol Infect Dis 22:525-529. http://dx. doi. org/10 . 1007/s10096-003-0992-5.
26. Griffiths D, Fawley W, Kachrimanidou M, Bowden R, Crook DW, Fung R, Golubchik T, Harding RM, Jeffery KJ, Jolley KA, Kirton R, Peto TE, Rees G, Stoesser N, Vaughan A, Walker AS, Young BC, Wilcox M, Dingle KE. 2010. Multilocus sequence typing of Clostridium difficile. J Clin Microbiol 48:770-778. http://dx. doi. org/10. 1128/JCM. 01796-09.
27. He M, Sebaihia M, Lawley TD, Stabler RA, Dawson LF, Martin MJ, Holt KE, Seth-Smith HM, Quail MA, Rance R, Brooks K, Churcher C, Harris D, Bentley SD, Burrows C, Clark L, Corton C, Murray V, Rose G, Thurston S, van Tonder A, Walker D, Wren BW, Dougan G, Parkhill J. 2010. Evolutionary dynamics of Clostridium difficile over short and long time scales. Proc Natl Acad Sci U S A 107:7527-7532. http://dx. doi. org/10 . 1073/pnas. 0914322107.
28. Parkhill J, Wren BW. 2011. Bacterial epidemiology and biology-lessons from genome sequencing. Genome Biol 12:230. http://dx. doi. org/10. 1186 /gb-2011-12-10-230.
29. Harris SR, Feil EJ, Holden MT, Quail MA, Nickerson EK, Chantratita N, Gardete S, Tavares A, Day N, Lindsay JA, Edgeworth JD, de Lencastre H, Parkhill J, Peacock SJ, Bentley SD. 2010. Evolution of MRSA during hospital transmission and intercontinental spread. Science 327: 469-474. http://dx. doi. org/10. 1126/science. 1182395.
30. Preston MD, Assefa SA, Ocholla H, Sutherland CJ, Borrmann S, Nzila A, Michon P, Hien TT, Bousema T, Drakeley CJ, Zongo I, Ouedraogo JB, Djimde AA, Doumbo OK, Nosten F, Fairhurst RM, Conway DJ, Roper C, Clark TG. 2014. PlasmoView: a web-based resource to visualise global Plasmodium falciparum genomic variation. J Infect Dis 209:1808-1815. http://dx. doi. org/10. 1093/infdis/jit812.
31. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120. http://dx. doi . org/10. 1093/bioinformatics/btu170.
32. 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.
33. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079. http://dx. doi. org/10. 1093/bioinformatics/btp352.
34. Zerbino DR. 2010. Using the Velvet de novo assembler for short-read sequencing technologies. Curr Protoc Bioinformatics Chapter 11:unit 11. 5.
35. Seemann T, Gladman S. 2012. VelvetOptimiser. Victorian Bioinformatics Consortium. http://bioinformatics. net. au/software. velvetoptimiser. shtml.
36. The R Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
37. Assefa S, Keane TM, Otto TD, Newbold C, Berriman M. 2009. ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 25:1968-1969. http://dx. doi. org/10. 1093/bioinformatics/btp347.
38. Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068-2069. http://dx. doi. org/10. 1093/bioinformatics/btu153.
39. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313. http: //dx. doi. org/10. 1093/bioinformatics/btu033.
40. Eyre DW, Cule ML, Wilson DJ, Griffiths D, Vaughan A, O'Connor L, Ip CL, Golubchik T, Batty EM, Finney JM, Wyllie DH, Didelot X, Piazza P, Bowden R, Dingle KE, Harding RM, Crook DW, Wilcox MH, Peto TE, Walker AS. 2013. Diverse sources of C. difficile infection identified on whole-genome sequencing. N Engl J Med 369:1195-1205. http: //dx. doi. org/10. 1056/NEJMoa1216064.