Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter-and intracontinental transmission events

Nature Genetics

Volumn 47, Issue 6, 2015, Pages 632-639

  Wong, Vanessa K ^a,b   Baker, Stephen ^c,d,e   Pickard, Derek J ^a   Parkhill, Julian ^a   Page, Andrew J ^a   Feasey, Nicholas A ^f   Kingsley, Robert A ^a,g   Thomson, Nicholas R ^a,e   Keane, Jacqueline A ^a   Weill, François Xavier ^h   Edwards, David J ⁱ   Hawkey, Jane ^i,j   Harris, Simon R ^a   Mather, Alison E ^a   Cain, Amy K ^a   Hadfield, James ^a   Hart, Peter J ^k   Thieu, Nga Tran Vu ^c   Klemm, Elizabeth J ^a   Glinos, Dafni A ^a   Breiman, Robert F ^l,m,n   Watson, Conall H ^e   Kariuki, Samuel ^a,l   Gordon, Melita A ^o   Heyderman, Robert S ^p   Okoro, Chinyere ^a   Jacobs, Jan ^q,r   Lunguya, Octavie ^s,t   Edmunds, W John ^e   Msefula, Chisomo ^p   Chabalgoity, Jose A ^u   Kama, Mike ^v   Jenkins, Kylie ^w   Dutta, Shanta ^x   Marks, Florian ^y   Campos, Josefina ^z   Thompson, Corinne ^c,d   Obaro, Stephen ^aa,ab,ac   Maclennan, Calman A ^a,k,ad   Dolecek, Christiane ^d   Keddy, Karen H ^ae   Smith, Anthony M ^ae   Parry, Christopher M ^e,af   Karkey, Abhilasha ^c   Mulholland, E Kim ^e,ag   Campbell, James I ^c,d   Dongol, Sabina ^c   Basnyat, Buddha ^c   Dufour, Muriel ^ah   Bandaranayake, Don ^ah   Naseri, Take Toleafoa ^ai   Singh, Shalini Pravin ^aj   Hatta, Mochammad ^ak   Newton, Paul ^d,al   Onsare, Robert S ^l   Isaia, Lupeoletalalei ^am   Dance, David ^d,al   Davong, Viengmon ^al   Thwaites, Guy ^c,d   Wijedoru, Lalith ^an,ao   Crump, John A ^ap   De Pinna, Elizabeth ^aq   Nair, Satheesh ^aq   Nilles, Eric J ^aj   Thanh, Duy Pham ^c   Turner, Paul ^d,an,ar   Soeng, Sona ^ar   Valcanis, Mary ^as   Powling, Joan ^as   Dimovski, Karolina ^as   Hogg, Geoff ^as   Farrar, Jeremy ^c,d   Holt, Kathryn E ⁱ   Dougan, Gordon ^a   more..

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

^c OXFORD UNIVERSITY CLINICAL RESEARCH UNIT   (Viet Nam)

^d UNIVERSITY OF OXFORD   (United Kingdom)

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

^f LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^g INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^h INSTITUT PASTEUR   (France)

ⁱ UNIVERSITY OF MELBOURNE   (Australia)

^j UNIVERSITY OF MELBOURNE   (Australia)

^k UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^l KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^m CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

ⁿ EMORY UNIVERSITY   (United States)

^o UNIVERSITY OF LIVERPOOL   (United Kingdom)

^p UNIVERSITY OF MALAWI   (Malawi)

^q INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^r UNIVERSITY OF LEUVEN   (Belgium)

^s National Institute for Biomedical Research   (Congo)

^t University of Kinshasa Hospital   (Congo)

^u Universidad de la Republica Instituto de Higiene   (Uruguay)

^v Ministry of Health   (Fiji)

^w Fiji Health Sector Support Programme   (Fiji)

^x NATIONAL INSTITUTE OF CHOLERA AND ENTERIC DISEASES   (India)

^y International Vaccine Institute   (South Korea)

^z Administracion Nacional de Laboratorios E Institutos de Salud Dr Carlos G Malbran   (Argentina)

^aa UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^ab UNIVERSITY OF ABUJA   (Nigeria)

^ac BINGHAM UNIVERSITY   (Nigeria)

^ad NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^ae UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^af NAGASAKI UNIVERSITY   (Japan)

^ag MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^ah INSTITUTE OF ENVIRONMENTAL SCIENCE AND RESEARCH   (New Zealand)

^ai Samoa Ministry of Health   (Samoa)

^aj WORLD HEALTH ORGANIZATION   (Switzerland)

^ak HASANUDDIN UNIVERSITY   (Indonesia)

^al MAHOSOT HOSPITAL   (Laos)

^am Tupua Tamasese Meaole Hospital   (Samoa)

^an MAHIDOL UNIVERSITY   (Thailand)

^ao CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

^ap UNIVERSITY OF OTAGO   (New Zealand)

^aq PUBLIC HEALTH ENGLAND   (United Kingdom)

^ar Angkor Hospital for Children   (Cambodia)

^as UNIVERSITY OF MELBOURNE   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; AZITHROMYCIN; CHLORAMPHENICOL; COTRIMOXAZOLE; QUINOLONE DERIVATIVE; STREPTOMYCIN; SULFONAMIDE; TRIMETHOPRIM; ANTIINFECTIVE AGENT; QUINOLINE; QUINOLINE DERIVATIVE;

AFRICA; ANTIBIOTIC RESISTANCE; ARTICLE; ASIA; BACTERIAL TRANSMISSION; BACTERIUM IDENTIFICATION; CLADISTICS; CONVERGENT EVOLUTION; EPIDEMIC; GENE INSERTION SEQUENCE; GENE MUTATION; HAPLOTYPE; MAXIMUM LIKELIHOOD METHOD; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYLOGEOGRAPHY; PLASMID; POPULATION STRUCTURE; PRIORITY JOURNAL; REPLICON; SALMONELLA ENTERICA SEROVAR TYPHI; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSPOSON; TYPHOID FEVER; BACTERIAL GENOME; DNA SEQUENCE; GENETICS; HUMAN; MICROBIOLOGY; MOLECULAR GENETICS; TRANSMISSION;

BACTERIA (MICROORGANISMS); SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHI; SALMONELLA TYPHI;

ANTI-BACTERIAL AGENTS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENOME, BACTERIAL; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PHYLOGEOGRAPHY; QUINOLINES; SALMONELLA TYPHI; SEQUENCE ANALYSIS, DNA; TYPHOID FEVER;

EID: 84930064392     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3281     Document Type: Article

References (73)

1. Parry, C.M., Hien, T.T., Dougan, G., White, N.J. & Farrar, J.J. Typhoid fever. N. Engl. J. Med. 347, 1770-1782 (2002).
2. Connor, B.A. & Schwartz, E. Typhoid and paratyphoid fever in travellers. Lancet Infect. Dis. 5, 623-628 (2005).
3. Crump, J.A. & Mintz, E.D. Global trends in typhoid and paratyphoid fever. Clin. Infect. Dis. 50, 241-246 (2010).
4. Mogasale, V. et al. Burden of typhoid fever in low-income and middle-income countries: a systematic, literature-based update with risk-factor adjustment. Lancet Glob. Health 2, e570-e580 (2014).
5. Bodhidatta, L., Taylor, D.N., Thisyakorn, U. & Echeverria, P. Control of typhoid fever in Bangkok, Thailand, by annual immunization of schoolchildren with parenteral typhoid vaccine. Rev. Infect. Dis. 9, 841-845 (1987).
6. Fraser, A., Paul, M., Goldberg, E., Acosta, C.J. & Leibovici, L. Typhoid fever vaccines: systematic review and meta-analysis of randomised controlled trials. Vaccine 25, 7848-7857 (2007).
7. Khan, M.I., Ochiai, R.L. & Clemens, J.D. Population impact of Vi capsular polysaccharide vaccine. Expert Rev. Vaccines 9, 485-496 (2010).
8. Bhutta, Z.A. Current concepts in the diagnosis and treatment of typhoid fever. Br. Med. J. 333, 78-82 (2006).
9. Olarte, J. & Galindo, E. Salmonella Typhi resistant to chloramphenicol, ampicillin, and other antimicrobial agents: strains isolated during an extensive typhoid fever epidemic in Mexico. Antimicrob. Agents Chemother. 4, 597-601 (1973).
10. Anderson, E.S. The problem and implications of chloramphenicol resistance in the typhoid bacillus. J. Hyg. (Lond.) 74, 289-299 (1975).
11. Mirza, S.H., Beeching, N.J. & Hart, C.A. Multi-drug resistant typhoid: a global problem. J. Med. Microbiol. 44, 317-319 (1996).
12. Holt, K.E. et al. Emergence of a globally dominant IncHI1 plasmid type associated with multiple drug resistant typhoid. PLoS Negl. Trop. Dis. 5, e1245 (2011).
13. Chau, T.T. et al. Antimicrobial drug resistance of Salmonella enterica serovar Typhi in Asia and molecular mechanism of reduced susceptibility to the fuoroquinolones. Antimicrob. Agents Chemother. 51, 4315-4323 (2007).
14. Kariuki, S. et al. Typhoid in Kenya is associated with a dominant multidrug-resistant Salmonella enterica serovar Typhi haplotype that is also widespread in Southeast Asia. J. Clin. Microbiol. 48, 2171-2176 (2010).
15. Chiou, C.S. et al. Antimicrobial resistance in Salmonella enterica serovar Typhi from Bangladesh, Indonesia, Taiwan and Vietnam. Antimicrob. Agents Chemother. 58, 6501-6507 (2014).
16. Hendriksen, R.S. et al. Genomic signature of multi-drug resistant Salmonella Typhi related to a massive outbreak in Zambia during 2010 and 2012. J. Clin. Microbiol. 53, 262-272 (2015).
17. Roumagnac, P. et al. Evolutionary history of Salmonella Typhi. Science 314, 1301-1304 (2006).
18. Kidgell, C. et al. Salmonella Typhi, the causative agent of typhoid fever, is approximately 50, 000 years old. Infect. Genet. Evol. 2, 39-45 (2002).
19. Holt, K.E. et al. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat. Genet. 40, 987-993 (2008).
20. Holt, K.E. et al. Pseudogene accumulation in the evolutionary histories of Salmonella enterica serovars Paratyphi A and Typhi. BMC Genomics 10, 36 (2009).
21. Baker, S. et al. High-throughput genotyping of Salmonella enterica serovar Typhi allowing geographical assignment of haplotypes and pathotypes within an urban District of Jakarta, Indonesia. J. Clin. Microbiol. 46, 1741-1746 (2008).
22. Holt, K.E. et al. High-throughput bacterial SNP typing identifes distinct clusters of Salmonella Typhi causing typhoid in Nepalese children. BMC Infect. Dis. 10, 144 (2010).
23. Phan, M.D. et al. Variation in Salmonella enterica serovar Typhi IncHI1 plasmids during the global spread of resistant typhoid fever. Antimicrob. Agents Chemother. 53, 716-727 (2009).
24. Le, T.A. et al. Clonal expansion and microevolution of quinolone-resistant Salmonella enterica serotype Typhi in Vietnam from 1996 to 2004. J. Clin. Microbiol. 45, 3485-3492 (2007).
25. Holt, K.E. et al. Temporal fuctuation of multidrug resistant Salmonella Typhi haplotypes in the Mekong River delta region of Vietnam. PLoS Negl. Trop. Dis. 5, e929 (2011).
26. Baker, S. et al. Combined high-resolution genotyping and geospatial analysis reveals modes of endemic urban typhoid fever transmission. Open Biol. 1, 110008 (2011).
27. Holt, K.E. et al. High-resolution genotyping of the endemic Salmonella Typhi population during a Vi (typhoid) vaccination trial in Kolkata. PLoS Negl. Trop. Dis. 6, e1490 (2012).
28. Lutterloh, E. et al. Multidrug-resistant typhoid fever with neurologic fndings on the Malawi-Mozambique border. Clin. Infect. Dis. 54, 1100-1106 (2012).
29. Phoba, M.F. et al. Multidrug-resistant Salmonella enterica, Democratic Republic of the Congo. Emerg. Infect. Dis. 18, 1692-1694 (2012).
30. Breiman, R.F. et al. Population-based incidence of typhoid fever in an urban informal settlement and a rural area in Kenya: implications for typhoid vaccine use in Africa. PLoS ONE 7, e29119 (2012).
31. Drummond, A.J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007).
32. Wain, J. et al. Quinolone-resistant Salmonella Typhi in Viet Nam: molecular basis of resistance and clinical response to treatment. Clin. Infect. Dis. 25, 1404-1410 (1997).
33. Holt, K.E. et al. Multidrug-resistant Salmonella enterica serovar Paratyphi A harbors IncHI1 plasmids similar to those found in serovar Typhi. J. Bacteriol. 189, 4257-4264 (2007).
34. Hooper, D.C. Quinolone mode of action-new aspects. Drugs 45 (suppl. 3), 8-14 (1993).
35. Menezes, G.A., Harish, B.N., Khan, M.A., Goessens, W.H. & Hays, J.P. Antimicrobial resistance trends in blood culture positive Salmonella Typhi isolates from Pondicherry, India, 2005-2009. Clin. Microbiol. Infect. 18, 239-245 (2012).
36. Keddy, K.H., Smith, A.M., Sooka, A., Ismail, H. & Oliver, S. Fluoroquinolone-resistant typhoid, South Africa. Emerg. Infect. Dis. 16, 879-880 (2010).
37. Thomson, N. et al. The role of prophage-like elements in the diversity of Salmonella enterica serovars. J. Mol. Biol. 339, 279-300 (2004).
38. Hensel, M. et al. Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella Pathogenicity Island 2. Mol. Microbiol. 24, 155-167 (1997).
39. Teplitski, M., Goodier, R.I. & Ahmer, B.M. Pathways leading from BarA/SirA to motility and virulence gene expression in Salmonella. J. Bacteriol. 185, 7257-7265 (2003).
40. Lawhon, S.D. et al. Global regulation by CsrA in Salmonella typhimurium. Mol. Microbiol. 48, 1633-1645 (2003).
41. Parkhill, J. et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413, 848-852 (2001).
42. Fu, Y. & Galan, J.E. A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401, 293-297 (1999).
43. Ashton, P.M. et al. MinION nanopore sequencing identifes the position and structure of a bacterial antibiotic resistance island. Nat. Biotechnol. 33, 296-300 (2015).
44. Holt, K.E. et al. Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat. Genet. 44, 1056-1059 (2012).
45. Le Hello, S. et al. The global establishment of a highly-fuoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain. Front. Microbiol. 4, 395 (2013).
46. Baker, S. et al. Fitness benefts in fuoroquinolone-resistant Salmonella Typhi in the absence of antimicrobial pressure. eLife 2, e01229 (2013).
47. Bwakura-Dangarembizi, M. et al. A randomized trial of prolonged co-trimoxazole in HIV-infected children in Africa. N. Engl. J. Med. 370, 41-53 (2014).
48. Guy, L., Kultima, J.R. & Andersson, S.G. genoPlotR: comparative gene and genome visualization in R. Bioinformatics 26, 2334-2335 (2010).
49. Croucher, N.J. et al. Rapid pneumococcal evolution in response to clinical interventions. Science 331, 430-434 (2011).
50. Chin, C.S. et al. Nonhybrid, fnished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563-569 (2013).
51. Casali, N. et al. Evolution and transmission of drug-resistant tuberculosis in a Russian population. Nat. Genet. 46, 279-286 (2014).
52. Harris, S.R. et al. Whole-genome analysis of diverse Chlamydia trachomatis strains identifes phylogenetic relationships masked by current clinical typing. Nat. Genet. 44, 413-419 (2012).
53. Harris, S.R. et al. Evolution of MRSA during hospital transmission and intercontinental spread. Science 327, 469-474 (2010).
54. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
55. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690 (2006).
56. Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127-128 (2007).
57. Letunic, I. & Bork, P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 39, W475-W478 (2011).
58. Bollback, J.P. SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 7, 88 (2006).
59. Zerbino, D.R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829 (2008).
60. Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068-2069 (2014).
61. Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).
62. Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595 (2010).
63. Zhou, Y., Liang, Y., Lynch, K.H., Dennis, J.J. & Wishart, D.S. PHAST: a fast phage search tool. Nucleic Acids Res. 39, W347-W352 (2011).
64. Inouye, M. et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med. 6, 90 (2014).
65. Gupta, S.K. et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob. Agents Chemother. 58, 212-220 (2014).
66. Eaves, D.J. et al. Prevalence of mutations within the quinolone resistance-determining region of gyrA, gyrB, parC, and parE and association with antibiotic resistance in quinolone-resistant Salmonella enterica. Antimicrob. Agents Chemother. 48, 4012-4015 (2004).
67. Baucheron, S., Chaslus-Dancla, E., Cloeckaert, A., Chiu, C.H. & Butaye, P. High-level resistance to fuoroquinolones linked to mutations in gyrA, parC, and parE in Salmonella enterica serovar Schwarzengrund isolates from humans in Taiwan. Antimicrob. Agents Chemother. 49, 862-863 (2005).
68. Song, Y. et al. A multiplex single nucleotide polymorphism typing assay for detecting mutations that result in decreased fuoroquinolone susceptibility in Salmonella enterica serovars Typhi and Paratyphi A. J. Antimicrob. Chemother. 65, 1631-1641 (2010).
69. Haanperä, M., Huovinen, P. & Jalava, J. Detection and quantifcation of macrolide resistance mutations at positions 2058 and 2059 of the 23S rRNA gene by pyrosequencing. Antimicrob. Agents Chemother. 49, 457-460 (2005).
70. Gomes, C. et al. In vitro development and analysis of Escherichia coli and Shigella boydii azithromycin-resistant mutants. Microb. Drug Resist. 19, 88-93 (2013).
71. Marvig, R.L. et al. Mutations in 23S rRNA confer resistance against azithromycin in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 56, 4519-4521 (2012).
72. Carver, T. et al. Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 24, 2672-2676 (2008).
73. Carattoli, A. et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58, 3895-3903 (2014).