Whole genome sequencing of ESBL-producing Escherichia coli isolated from patients, farm waste and canals in Thailand

Genome Medicine

Volumn 9, Issue 1, 2017, Pages

  Runcharoen, Chakkaphan ^a   Raven, Kathy E ^b   Reuter, Sandra ^b   Kallonen, Teemu ^d   Paksanont, Suporn ^a   Thammachote, Jeeranan ^c   Anun, Suthatip ^c   Blane, Beth ^b   Parkhill, Julian ^d   Peacock, Sharon J ^a,b,d,e   Chantratita, Narisara ^a  

^a MAHIDOL UNIVERSITY   (Thailand)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c Bhuddhasothon Hospital   (Thailand)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

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

Author keywords

ESBL; Escherichia coli; Genome; Phylogeny; Sequence

Indexed keywords

BETA LACTAMASE CTX M; BETA LACTAMASE SHV; BETA LACTAMASE SHV 12; CARBAPENEM; CIPROFLOXACIN; COLISTIN; GENTAMICIN; TOBRAMYCIN; TRIMETHOPRIM; UNCLASSIFIED DRUG; BETA LACTAMASE; WASTE WATER;

AGRICULTURAL WASTE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM ISOLATE; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ESCHERICHIA COLI; HUMAN; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; SEWER; SINGLE NUCLEOTIDE POLYMORPHISM; THAILAND; WASTE WATER; WHOLE GENOME SEQUENCING; AGRICULTURAL LAND; DNA SEQUENCE; ENZYMOLOGY; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; GENETICS; HOSPITAL; ISOLATION AND PURIFICATION; MICROBIOLOGY; MULTIDRUG RESISTANCE; PATHOPHYSIOLOGY; PHYSIOLOGY;

BETA-LACTAM RESISTANCE; BETA-LACTAMASES; DRUG RESISTANCE, MULTIPLE; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FARMS; HOSPITALS; HUMANS; SEQUENCE ANALYSIS, DNA; THAILAND; WASTE WATER;

EID: 85028945128     PISSN: None     EISSN: 1756994X     Source Type: Journal    
DOI: 10.1186/s13073-017-0471-8     Document Type: Article

References (63)

1. Pitout JD, Laupland KB. Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis. 2008;8(3):159-66.
2. Schwaber MJ, Navon-Venezia S, Kaye KS, Ben-Ami R, Schwartz D, Carmeli Y. Clinical and economic impact of bacteremia with extended-spectrum beta-lactamase-producing Enterobacteriaceae. Antimicrob Agents Chemother. 2006;50(4):1257-62.
3. Nordmann P, Naas T, Poirel L. Global spread of carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis. 2011;17(10):1791-8.
4. Schwarz S, Johnson AP. Transferable resistance to colistin: a new but old threat. J Antimicrob Chemother. 2016;71(8):2066-70.
5. Xavier BB, Lammens C, Ruhal R, Kumar-Singh S, Butaye P, Goossens H, Malhotra-Kumar S. Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Euro Surveill. 2016;21(27):30280.
6. Oh S, Buddenborg S, Yoder-Himes DR, Tiedje JM, Konstantinidis KT. Genomic diversity of Escherichia isolates from diverse habitats. PLoS One. 2012;7(10):e47005.
7. Boonyasiri A, Tangkoskul T, Seenama C, Saiyarin J, Tiengrim S, Thamlikitkul V. Prevalence of antibiotic resistant bacteria in healthy adults, foods, food animals, and the environment in selected areas in Thailand. Pathog Glob Health. 2014;108(5):235-45.
8. Ma J, Liu JH, Lv L, Zong Z, Sun Y, Zheng H, Chen Z, Zeng ZL. Characterization of extended-spectrum beta-lactamase genes found among Escherichia coli isolates from duck and environmental samples obtained on a duck farm. Appl Environ Microbiol. 2012;78(10):3668-73.
9. Tian GB, Wang HN, Zhang AY, Zhang Y, Fan WQ, Xu CW, Zeng B, Guan ZB, Zou LK. Detection of clinically important beta-lactamases in commensal Escherichia coli of human and swine origin in western China. J Med Microbiol. 2012;61(Pt 2):233-8.
10. Tamang MD, Nam HM, Gurung M, Jang GC, Kim SR, Jung SC, Park YH, Lim SK. Molecular characterization of CTX-M beta-lactamase and associated addiction systems in Escherichia coli circulating among cattle, farm workers, and the farm environment. Appl Environ Microbiol. 2013;79(13):3898-905.
11. Blaak H, van Hoek AH, Hamidjaja RA, van der Plaats RQ, Kerkhof-de Heer L, de Roda Husman AM, Schets FM. Distribution, numbers, and diversity of ESBL-producing E. coli in the poultry farm environment. PLoS One. 2015;10(8):e0135402.
12. Diab M, Hamze M, Madec JY, Haenni M. High prevalence of non-ST131 CTX-M-15-producing Escherichia coli in healthy cattle in Lebanon. Microb Drug Resist. 2016;23(2):261-6.
13. Seiffert SN, Hilty M, Perreten V, Endimiani A. Extended-spectrum cephalosporin-resistant Gram-negative organisms in livestock: an emerging problem for human health? Drug Resist Updat. 2013;16(1-2):22-45.
14. Hartmann A, Locatelli A, Amoureux L, Depret G, Jolivet C, Gueneau E, Neuwirth C. Occurrence of CTX-M producing Escherichia coli in soils, cattle, and farm environment in France (Burgundy Region). Front Microbiol. 2012;3:83.
15. Xi C, Zhang Y, Marrs CF, Ye W, Simon C, Foxman B, Nriagu J. Prevalence of antibiotic resistance in drinking water treatment and distribution systems. Appl Environ Microbiol. 2009;75(17):5714-8.
16. Koser CU, Ellington MJ, Peacock SJ. Whole-genome sequencing to control antimicrobial resistance. Trends Genet. 2014;30(9):401-7.
17. Luo C, Walk ST, Gordon DM, Feldgarden M, Tiedje JM, Konstantinidis KT. Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc Natl Acad Sci U S A. 2011;108(17):7200-5.
18. Price LB, Johnson JR, Aziz M, Clabots C, Johnston B, Tchesnokova V, Nordstrom L, Billig M, Chattopadhyay S, Stegger M, et al. The epidemic of extended-spectrum beta-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. mBio. 2013;4(6):e00377-13.
19. Petty NK, Ben Zakour NL, Stanton-Cook M, Skippington E, Totsika M, Forde BM, Phan MD, Gomes Moriel D, Peters KM, Davies M, et al. Global dissemination of a multidrug resistant Escherichia coli clone. Proc Natl Acad Sci U S A. 2014;111(15):5694-9.
20. Matsumura Y, Pitout JD, Gomi R, Matsuda T, Noguchi T, Yamamoto M, Peirano G, DeVinney R, Bradford PA, Motyl MR, et al. Global Escherichia coli sequence type 131 clade with blaCTX-M-27 gene. Emerg Infect Dis. 2016;22(11):1900-7.
21. Trongjit S, Angkittitrakul S, Chuanchuen R. Occurrence and molecular characteristics of antimicrobial resistance of Escherichia coli from broilers, pigs and meat products in Thailand and Cambodia provinces. Microbiol Immunol. 2016;60(9):575-85.
22. Runcharoen C, Moradigaravand D, Blane B, Paksanont S, Thammachote J, Anun S, Parkhill J, Chantratita N, Peacock SJ. Whole genome sequencing reveals high-resolution epidemiological links between clinical and environmental Klebsiella pneumoniae. Genome Med. 2017;9(1):6.
23. Raven KE, Reuter S, Gouliouris T, Reynolds R, Russell JE, Brown NM, Torok ME, Parkhill J, Peacock SJ. Genome-based characterization of hospital-adapted Enterococcus faecalis lineages. Nat Microbiol. 2016;1(3):15033.
24. Page AJ, De Silva N, Hunt M, Quail MA, Parkhill J, Harris SR, Otto TD, Keane JA. Robust high-throughput prokaryote de novo assembly and improvement pipeline for Illumina data. Microb Genom. 2016;2(8):1-7.
25. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, Fookes M, Falush D, Keane JA, Parkhill J. Roary: rapid large-scale prokaryote pan-genome analysis. Bioinformatics. 2015;31(22):3691-3.
26. de Been M, Lanza VF, de Toro M, Scharringa J, Dohmen W, Du Y, Hu J, Lei Y, Li N, Tooming-Klunderud A, et al. Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages. PLoS Genet. 2014;10(12):e1004776.
27. von Mentzer A, Connor TR, Wieler LH, Semmler T, Iguchi A, Thomson NR, Rasko DA, Joffre E, Corander J, Pickard D, et al. Identification of enterotoxigenic Escherichia coli (ETEC) clades with long-term global distribution. Nat Genet. 2014;46(12):1321-6.
28. Stoesser N, Sheppard AE, Moore CE, Golubchik T, Parry CM, Nget P, Saroeun M, Day NP, Giess A, Johnson JR, et al. Extensive within-host diversity in fecally carried extended-spectrum beta-lactamase producing Escherichia coli isolates: implications for transmission Analyses. J Clin Microbiol. 2015;53(7):2122-31.
29. Stoesser N, Sheppard AE, Pankhurst L, De Maio N, Moore CE, Sebra R, Turner P, Anson LW, Kasarskis A, Batty EM, et al. Evolutionary history of the global emergence of the Escherichia coli epidemic clone ST131. mBio. 2016;7(2):e02162.
30. Brodrick HJ, Kathy RE, Kallonen T, Jamrozy D, Blane B, Brown NM, Martin V, Torok ME, Parkhill J, Peacock SJ. Longitudinal genomic surveillance of multidrug-resistant Escherichia coli carriage in a longterm care facility in the United Kingdom. Genome Med. 2017;9(1):70.
31. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, Parkhill J, Harris SR. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2015;43(3):e15.
32. Price LB, Johnson JR, Aziz M, Clabots C, Johnston B, Tchesnokova V, Nordstrom L, Billig M, Chattopadhyay S, Stegger M et al. The epidemic of extended-spectrum beta-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. mBio. 2013;4(6):e00377-13.
33. Stoesser N, Sheppard AE, Pankhurst L, De Maio N, Moore CE, Sebra R, Turner P, Anson LW, Kasarskis A, Batty EM et al. Evolutionary history of the global emergence of the Escherichia coli epidemic clone ST131. mBio. 2016;7(2):e02162.
34. Weissman SJ, Johnson JR, Tchesnokova V, Billig M, Dykhuizen D, Riddell K, Rogers P, Qin X, Butler-Wu S, Cookson BT, et al. High-resolution two-locus clonal typing of extraintestinal pathogenic Escherichia coli. Appl Environ Microbiol. 2012;78(5):1353-60.
35. Paul S, Linardopoulou EV, Billig M, Tchesnokova V, Price LB, Johnson JR, Chattopadhyay S, Sokurenko EV. Role of homologous recombination in adaptive diversification of extraintestinal Escherichia coli. J Bacteriol. 2013;195(2):231-42.
36. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67(11):2640-4.
37. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis. 2016;16(2):161-8.
38. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One. 2010;5(3):e9490.
39. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268-81.
40. Wang Y, Zhang R, Li J, Wu Z, Yin W, Schwarz S, Tyrrell JM, Zheng Y, Wang S, Shen Z, et al. Comprehensive resistome analysis reveals the prevalence of NDM and MCR-1 in Chinese poultry production. Nat Microbiol. 2017;2:16260.
41. Netikul T, Sidjabat HE, Paterson DL, Kamolvit W, Tantisiriwat W, Steen JA, Kiratisin P. Characterization of an IncN2-type blaNDM-(1)-carrying plasmid in Escherichia coli ST131 and Klebsiella pneumoniae ST11 and ST15 isolates in Thailand. J Antimicrob Chemother. 2014;69(11):3161-3.
42. Cho SY, Huh HJ, Baek JY, Chung NY, Ryu JG, Ki CS, Chung DR, Lee NY, Song JH. Klebsiella pneumoniae co-producing NDM-5 and OXA-181 carbapenemases. South Korea Emerg Infect Dis. 2015;21(6):1088-9.
43. Johnson JR, Porter SB, Zhanel G, Kuskowski MA, Denamur E. Virulence of Escherichia coli clinical isolates in a murine sepsis model in relation to sequence type ST131 status, fluoroquinolone resistance, and virulence genotype. Infect Immun. 2012;80(4):1554-62.
44. Johnson JR, Urban C, Weissman SJ, Jorgensen JH. Lewis 2nd JS, Hansen G, Edelstein PH, Robicsek A, Cleary T, Adachi J, et al. Molecular epidemiological analysis of Escherichia coli sequence type ST131 (O25:H4) and blaCTX-M-15 among extended-spectrum beta-lactamase producing E. coli from the United States, 2000 to 2009. Antimicrob Agents Chemother. 2012;56(5):2364-70.
45. Colpan A, Johnston B, Porter S, Clabots C, Anway R, Thao L, Kuskowski MA, Tchesnokova V, Sokurenko EV, Johnson JR, et al. Escherichia coli sequence type 131 (ST131) subclone H30 as an emergent multidrug-resistant pathogen among US veterans. Clin Infect Dis. 2013;57(9):1256-65.
46. Olesen B, Hansen DS, Nilsson F, Frimodt-Moller J, Leihof RF, Struve C, Scheutz F, Johnston B, Krogfelt KA, Johnson JR. Prevalence and characteristics of the epidemic multiresistant Escherichia coli ST131 clonal group among extended-spectrum beta-lactamase-producing E. coli isolates in Copenhagen, Denmark. J Clin Microbiol. 2013;51(6):1779-85.
47. Rimrang B, Chanawong A, Lulitanond A, Wilailuckana C, Charoensri N, Sribenjalux P, Phumsrikaew W, Wonglakorn L, Kerdsin A, Chetchotisakd P. Emergence of NDM-1 and IMP-14a-producing Enterobacteriaceae in Thailand. J Antimicrob Chemother. 2012;67(11):2626-30.
48. Hornsey M, Phee L, Wareham DW. A novel variant, NDM-5, of the New Delhi metallo-beta-lactamase in a multidrug-resistant Escherichia coli ST648 isolate recovered from a patient in the United Kingdom. Antimicrob Agents Chemother. 2011;55(12):5952-4.
49. Yang P, Xie Y, Feng P, Zong Z. blaNDM-5 carried by an IncX3 plasmid in Escherichia coli sequence type 167. Antimicrob Agents Chemother. 2014;58(12):7548-52.
50. Nakano R, Nakano A, Hikosaka K, Kawakami S, Matsunaga N, Asahara M, Ishigaki S, Furukawa T, Suzuki M, Shibayama K, et al. First report of metallo-beta-lactamase NDM-5-producing Escherichia coli in Japan. Antimicrob Agents Chemother. 2014;58(12):7611-2.
51. Sassi A, Loucif L, Gupta SK, Dekhil M, Chettibi H, Rolain JM. NDM-5 carbapenemase-encoding gene in multidrug-resistant clinical isolates of Escherichia coli from Algeria. Antimicrob Agents Chemother. 2014;58(9):5606-8.
52. Epstein L, Hunter JC, Arwady MA, Tsai V, Stein L, Gribogiannis M, Frias M, Guh AY, Laufer AS, Black S, et al. New Delhi metallo-beta-lactamase-producing carbapenem-resistant Escherichia coli associated with exposure to duodenoscopes. JAMA. 2014;312(14):1447-55.
53. Hammerum AM, Littauer P, Hansen F. Detection of Klebsiella pneumoniae co-producing NDM-7 and OXA-181, Escherichia coli producing NDM-5 and Acinetobacter baumannii producing OXA-23 in a single patient. Int J Antimicrob Agents. 2015;46(5):597-8.
54. Wailan AM, Paterson DL, Caffery M, Sowden D, Sidjabat HE. Draft genome sequence of NDM-5-producing Escherichia coli sequence type 648 and genetic context of blaNDM-5 in Australia. Genome Announc. 2015;3(2):e00194-15.
55. Gamal D, Fernandez-Martinez M, El-Defrawy I, Ocampo-Sosa AA, Martinez-Martinez L. First identification of NDM-5 associated with OXA-181 in Escherichia coli from Egypt. Emerg Microbes Infect. 2016;5:e30.
56. Park M, Park SD, Lee MH, Kim SH, Lim K, Lee G, Woo HJ, Kim HW, Yang JY, Eom YB, et al. The first report of NDM-5-producing uropathogenic Escherichia coli isolates in South Korea. Diagn Microbiol Infect Dis. 2016;85(2):198-9.
57. Yousfi M, Mairi A, Bakour S, Touati A, Hassissen L, Hadjadj L, Rolain JM. First report of NDM-5-producing Escherichia coli ST1284 isolated from dog in Bejaia. Algeria New Microbes New Infect. 2015;8:17-8.
58. Vourli S, Giakkoupi P, Miriagou V, Tzelepi E, Vatopoulos AC, Tzouvelekis LS. Novel GES/IBC extended-spectrum beta-lactamase variants with carbapenemase activity in clinical enterobacteria. FEMS Microbiol Lett. 2004;234(2):209-13.
59. Rogers BA, Sidjabat HE, Paterson DL. Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain. J Antimicrob Chemother. 2011;66(1):1-14.
60. Pitout JD, Campbell L, Church DL, Gregson DB, Laupland KB. Molecular characteristics of travel-related extended-spectrum beta-lactamase-producing Escherichia coli isolates from the Calgary Health Region. Antimicrob Agents Chemother. 2009;53(6):2539-43.
61. Hussain A, Ranjan A, Nandanwar N, Babbar A, Jadhav S, Ahmed N. Genotypic and phenotypic profiles of Escherichia coli isolates belonging to clinical sequence type 131 (ST131), clinical non-ST131, and fecal non-ST131 lineages from India. Antimicrob Agents Chemother. 2014;58(12):7240-9.
62. Zurfluh K, Nuesch-Inderbinen M, Morach M, Zihler Berner A, Hachler H, Stephan R. Extended-spectrum-beta-lactamase-producing Enterobacteriaceae isolated from vegetables imported from the Dominican Republic, India, Thailand, and Vietnam. Appl Environ Microbiol. 2015;81(9):3115-20.
63. Lim C, Takahashi E, Hongsuwan M, Wuthiekanun V, Thamlikitkul V, Hinjoy S, Day NP, Peacock SJ, Limmathurotsakul D. Epidemiology and burden of multidrug-resistant bacterial infection in a developing country. eLife. 2016;5:e18082.