Whole genome analysis reveals new insights into the molecular characteristics of Clostridioides difficile NAP1/BI/027/ST1 clinical isolates in the People’s Republic of China

References

• Zhou Y, Burnham CA, Hink T, et al. Phenotypic and genotypic analysis of Clostridium difficile isolates: a single-center study. J Clin Microbiol. 2014;52(12):4260–4266. doi:10.1128/JCM.02115-1425275005
   PubMed Web of Science ®Google Scholar
• Loo VG, Poirier L, Miller MA, et al. A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med. 2005;353(23):2442–2449. doi:10.1056/NEJMoa05163916322602
   PubMed Web of Science ®Google Scholar
• He M, Miyajima F, Roberts P, et al. Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nature Genet. 2013;45(1):109–113. doi:10.1038/ng.247823222960
   PubMed Web of Science ®Google Scholar
• He M, Sebaihia M, Lawley TD, et al. Evolutionary dynamics of Clostridium difficile over short and long time scales. Proc Natl Acad Sci U S A. 2010;107(16):7527–7532. doi:10.1073/pnas.091432210720368420
   PubMed Web of Science ®Google Scholar
• Brazier JS. Typing of Clostridium difficile. Clin Microbiol Infect. 2001;7(8):428–431.11591206
   PubMed Web of Science ®Google Scholar
• Munoz M, Rios-Chaparro DI, Patarroyo MA, Ramirez JD. Determining Clostridium difficile intra-taxa diversity by mining multilocus sequence typing databases. BMC Microbiol. 2017;17(1):62. doi:10.1186/s12866-017-0969-728288567
   PubMed Web of Science ®Google Scholar
• Eyre DW, Cule ML, Wilson DJ, et al. Diverse sources of C. difficile infection identified on whole-genome sequencing. N Engl J Med. 2013;369(13):1195–1205. doi:10.1056/NEJMoa121606424066741
   PubMed Web of Science ®Google Scholar
• Didelot X, Eyre DW, Cule M, et al. Microevolutionary analysis of Clostridium difficile genomes to investigate transmission. Genome Biol. 2012;13(12):R118. doi:10.1186/gb-2012-13-12-r11823259504
   PubMed Web of Science ®Google Scholar
• Sebaihia M, Wren BW, Mullany P, et al. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet. 2006;38(7):779–786. doi:10.1038/ng183016804543
   PubMed Web of Science ®Google Scholar
• Eyre DW, Golubchik T, Gordon NC, et al. A pilot study of rapid benchtop sequencing of Staphylococcus aureus and Clostridium difficile for outbreak detection and surveillance. BMJ Open. 2012;2:3. doi:10.1136/bmjopen-2012-001124
   Web of Science ®Google Scholar
• Didelot X, Bowden R, Wilson DJ, Peto TEA, Crook DW. Transforming clinical microbiology with bacterial genome sequencing. Nature Rev Genet. 2012;13(9):601–612. doi:10.1038/nrg322622868263
   PubMed Web of Science ®Google Scholar
• Wang P, Zhou Y, Wang Z, et al. Identification of Clostridium difficile ribotype 027 for the first time in Mainland China. Infect Control Hosp Epidemiol. 2014;35(1):95–98. doi:10.1086/67440524334809
   PubMed Web of Science ®Google Scholar
• Cheng JW, Xiao M, Kudinha T, et al. The first two Clostridium difficile ribotype 027/ST1 isolates identified in Beijing, China – an emerging problem or a neglected threat? Sci Rep. 2016;6:18834.26740150
   PubMed Web of Science ®Google Scholar
• Jia H, Du P, Yang H, et al. Nosocomial transmission of Clostridium difficile ribotype 027 in a Chinese hospital, 2012-2014, traced by whole genome sequencing. BMC Genomics. 2016;17:405. doi:10.1186/s12864-016-3328-427411304
   PubMed Web of Science ®Google Scholar
• Wang R, Suo L, Chen HX, Song LJ, Shen YY, Luo YP. Molecular epidemiology and antimicrobial susceptibility of Clostridium difficile isolated from the Chinese People’s Liberation Army General Hospital in China. Int J Infect Dis. 2018;67:86–91. doi:10.1016/j.ijid.2017.07.01028736259
   PubMed Web of Science ®Google Scholar
• Gao Q, Wu S, Huang H, et al. Toxin profiles, PCR ribotypes and resistance patterns of Clostridium difficile: a multicentre study in China, 2012-2013. Int J Antimicrob Agents. 2016;48(6):736–739. doi:10.1016/j.ijantimicag.2016.09.00927793509
   PubMed Web of Science ®Google Scholar
• Chen YB, Gu SL, Shen P, et al. Molecular epidemiology and antimicrobial susceptibility of Clostridium difficile isolated from hospitals during a 4-year period in China. J Med Microbiol. 2018;67(1):52–59. doi:10.1099/jmm.0.00064629160203
   PubMed Web of Science ®Google Scholar
• Bauer MP, Notermans DW, van Benthem BH, et al. Clostridium difficile infection in Europe: a hospital-based survey. Lancet. 2011;377(9759):63–73. doi:10.1016/S0140-6736(10)61266-421084111
   PubMed Web of Science ®Google Scholar
• Davies KA, Ashwin H, Longshaw CM, et al. Diversity of Clostridium difficile PCR ribotypes in Europe: results from the European, multicentre, prospective, biannual, point-prevalence study of Clostridium difficile infection in hospitalised patients with diarrhoea (EUCLID), 2012 and 2013. Euro Surveill. 2016;21(29):30294. doi:10.2807/1560-7917.ES.2016.21.29.30294
   Google Scholar
• Wilcox MH, Shetty N, Fawley WN, et al. Changing epidemiology of Clostridium difficile infection following the introduction of a national ribotyping-based surveillance scheme in England. Clin Infect Dis. 2012;55(8):1056–1063. doi:10.1093/cid/cis61422784871
   PubMed Web of Science ®Google Scholar
• McDonald LC, Coignard B, Dubberke E, Song X, Horan T, Kutty PK. Recommendations for surveillance of Clostridium difficile-associated disease. Infect Control Hosp Epidemiol. 2007;28(2):140–145. doi:10.1086/51179817265394
   PubMed Web of Science ®Google Scholar
• Kato H, Kato N, Watanabe K, et al. Identification of toxin A-negative, toxin B-positive Clostridium difficile by PCR. J Clin Microbiol. 1998;36(8):2178–2182.9665986
   PubMed Web of Science ®Google Scholar
• Stubbs S, Rupnik M, Gibert M, Brazier J, Duerden B, Popoff M. Production of actin-specific ADP-ribosyltransferase (binary toxin) by strains of Clostridium difficile. FEMS Microbiol Lett. 2000;186(2):307–312. doi:10.1111/j.1574-6968.2000.tb09122.x10802189
   PubMed Web of Science ®Google Scholar
• Cheng VC, Yam WC, Chan JF, To KK, Ho PL, Yuen KY. Clostridium difficile ribotype 027 arrives in Hong Kong. Int J Antimicrob Agents. 2009;34(5):492–493. doi:10.1016/j.ijantimicag.2009.04.00419464857
   PubMed Web of Science ®Google Scholar
• Indra A, Huhulescu S, Schneeweis M, et al. Characterization of Clostridium difficile isolates using capillary gel electrophoresis-based PCR ribotyping. J Med Microbiol. 2008;57(Pt 11):1377–1382. doi:10.1099/jmm.0.47714-018927415
   PubMed Web of Science ®Google Scholar
• Gal M, Northey G, Brazier JS. A modified pulsed-field gel electrophoresis (PFGE) protocol for subtyping previously non-PFGE typeable isolates of Clostridium difficile polymerase chain reaction ribotype 001. J Hosp Infect. 2005;61(3):231–236. doi:10.1016/j.jhin.2005.01.01716002184
   PubMed Web of Science ®Google Scholar
• Griffiths D, Fawley W, Kachrimanidou M, et al. Multilocus sequence typing of Clostridium difficile. J Clin Microbiol. 2010;48(3):770–778. doi:10.1128/JCM.01796-0920042623
   PubMed Web of Science ®Google Scholar
• Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–1760. doi:10.1093/bioinformatics/btp32419451168
   PubMed Web of Science ®Google Scholar
• McKenna A, Hanna M, Banks E, et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20(9):1297–1303. doi:10.1101/gr.107524.11020644199
   PubMed Web of Science ®Google Scholar
• Aziz RK, Bartels D, Best AA, et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics. 2008;9:75. doi:10.1186/1471-2164-9-7518261238
   PubMed Web of Science ®Google Scholar
• Clinical and Laboratory Standards Institute (CLSI). M11-A8. Methods for Antimicrobial Susceptibility Testing of Anaerobic Bacteria; Approved Standard-Eighth Edition Wayne, PA: Clinical and Laboratory Standards Institute; 2012.
   Google Scholar
• Xu Q, Chen Y, Gu S, et al. Hospital-acquired Clostridium difficile infection in Mainland China: a seven-year (2009-2016) retrospective study in a large university hospital. Sci Rep. 2017;7(1):9645. doi:10.1038/s41598-017-09961-028852010
   PubMed Web of Science ®Google Scholar
• Drudy D, Kyne L, O’Mahony R, Fanning S. gyrA mutations in fluoroquinolone-resistant Clostridium difficile PCR-027. Emerg Infect Dis. 2007;13(3):504–505. doi:10.3201/eid1303.06077117552115
   PubMed Web of Science ®Google Scholar
• Van Boeckel TP, Gandra S, Ashok A, et al. Global antibiotic consumption 2000 to 2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis. 2014;14(8):742–750. doi:10.1016/S1473-3099(14)70780-725022435
   PubMed Web of Science ®Google Scholar
• Stabler RA, He M, Dawson L, et al. Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium. Genome Biol. 2009;10(9):R102. doi:10.1186/gb-2009-10-9-r10219781061
   PubMed Web of Science ®Google Scholar
• Spigaglia P, Carattoli A, Barbanti F, Mastrantonio P. Detection of gyrA and gyrB mutations in Clostridium difficile isolates by real-time PCR. Mol Cell Probes. 2010;24(2):61–67. doi:10.1016/j.mcp.2009.10.00219837154
   PubMed Web of Science ®Google Scholar
• Stock AM, Robinson VL, Goudreau PN. Two-component signal transduction. Annu Rev Biochem. 2000;69:183–215. doi:10.1146/annurev.biochem.69.1.18310966457
   PubMed Web of Science ®Google Scholar
• Dembek M, Barquist L, Boinett CJ, et al. High-throughput analysis of gene essentiality and sporulation in Clostridium difficile. mBio. 2015;6(2):e02383. doi:10.1128/mBio.02383-1425714712
   PubMed Web of Science ®Google Scholar
• Mullany P, Allan E, Roberts AP. Mobile genetic elements in Clostridium difficile and their role in genome function. Res Microbiol. 2015;166(4):361–367. doi:10.1016/j.resmic.2014.12.00525576774
   PubMed Web of Science ®Google Scholar
• Su YA, He P, Clewell DB. Characterization of the tet(M) determinant of Tn916: evidence for regulation by transcription attenuation. Antimicrob Agents Chemother. 1992;36(4):769–778. doi:10.1128/aac.36.4.7691323953
   PubMed Web of Science ®Google Scholar
• Roberts AP, Mullany P. A modular master on the move: the Tn916 family of mobile genetic elements. Trends Microbiol. 2009;17(6):251–258. doi:10.1016/j.tim.2009.03.00219464182
   PubMed Web of Science ®Google Scholar