Integrating whole-genome sequencing within the National Antimicrobial Resistance Surveillance Program in the Philippines.
Anti-Bacterial Agents
/ pharmacology
Bacteria
/ drug effects
Bacterial Infections
/ epidemiology
Drug Resistance, Bacterial
/ genetics
Genome, Bacterial
/ genetics
Genomics
/ methods
Humans
Microbial Sensitivity Tests
/ methods
Philippines
/ epidemiology
Surveys and Questionnaires
Whole Genome Sequencing
/ methods
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
01 06 2020
01 06 2020
Historique:
received:
06
03
2020
accepted:
25
04
2020
entrez:
3
6
2020
pubmed:
3
6
2020
medline:
18
8
2020
Statut:
epublish
Résumé
National networks of laboratory-based surveillance of antimicrobial resistance (AMR) monitor resistance trends and disseminate these data to AMR stakeholders. Whole-genome sequencing (WGS) can support surveillance by pinpointing resistance mechanisms and uncovering transmission patterns. However, genomic surveillance is rare in low- and middle-income countries. Here, we implement WGS within the established Antimicrobial Resistance Surveillance Program of the Philippines via a binational collaboration. In parallel, we characterize bacterial populations of key bug-drug combinations via a retrospective sequencing survey. By linking the resistance phenotypes to genomic data, we reveal the interplay of genetic lineages (strains), AMR mechanisms, and AMR vehicles underlying the expansion of specific resistance phenotypes that coincide with the growing carbapenem resistance rates observed since 2010. Our results enhance our understanding of the drivers of carbapenem resistance in the Philippines, while also serving as the genetic background to contextualize ongoing local prospective surveillance.
Identifiants
pubmed: 32483195
doi: 10.1038/s41467-020-16322-5
pii: 10.1038/s41467-020-16322-5
pmc: PMC7264328
doi:
Substances chimiques
Anti-Bacterial Agents
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2719Subventions
Organisme : NCRR NIH HHS
ID : R01 RR025040
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA207167
Pays : United States
Organisme : Medical Research Council
ID : MR/N019296/1
Pays : United Kingdom
Organisme : Department of Health
ID : 16_136_111
Pays : United Kingdom
Références
World Health Organization. Antimicrobial resistance: global report on surveillance http://www.who.int/iris/handle/10665/112642 (2014).
World Bank. Drug-resistant infections: a threat to our economic future http://documents.worldbank.org/curated/en/323311493396993758/pdf/114679-REVISED-v2-Drug-Resistant-Infections-Final-Report.pdf (2017).
World Health Organization. Global Action Plan on antimicrobial resistance http://www.wpro.who.int/entity/drug_resistance/resources/global_action_plan_eng.pdf (2015).
Department of Health, Republic of the Philippines. Morbidity https://www.doh.gov.ph/morbidity (2014).
Department of Health, Republic of the Philippines. Mortality https://www.doh.gov.ph/mortality (2013).
O’Brien, T. F. & Stelling, J. M. WHONET: an information system for monitoring antimicrobial resistance. Emerg. Infect. Dis. 1, 66 (1995).
pubmed: 8903165
pmcid: 2626837
doi: 10.3201/eid0102.950209
Antimicrobial Resistance Surveillance Reference Laboratory, Research Institute for Tropical Medicine. Annual reports https://arsp.com.ph/publications/ (2019).
World Health Organization. Global antimicrobial resistance surveillance system (GLASS) report: early implementation 2016–2017 https://www.who.int/glass/resources/publications/early-implementation-report/en/ (2017).
Papp-Wallace, K. M., Endimiani, A., Taracila, M. A. & Bonomo, R. A. Carbapenems: past, present, and future. Antimicrob. Agents Chemother. 55, 4943–4960 (2011).
pubmed: 21859938
pmcid: 3195018
doi: 10.1128/AAC.00296-11
Ashton, P. M. et al. Identification of Salmonella for public health surveillance using whole genome sequencing. PeerJ 4, e1752 (2016).
pubmed: 27069781
pmcid: 4824889
doi: 10.7717/peerj.1752
Deng, X., den Bakker, H. C. & Hendriksen, R. S. Genomic epidemiology: whole-genome-sequencing-powered surveillance and outbreak investigation of foodborne bacterial pathogens. Annu. Rev. Food Sci. Technol. 7, 353–374 (2016).
pubmed: 26772415
doi: 10.1146/annurev-food-041715-033259
Doumith, M. et al. Detection of the plasmid-mediated mcr-1 gene conferring colistin resistance in human and food isolates of Salmonella enterica and Escherichia coli in England and Wales. J. Antimicrob. Chemother. 71, 2300–2305 (2016).
pubmed: 27090630
doi: 10.1093/jac/dkw093
Wong, V. K. et al. Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events. Nat. Genet. 47, 632–639 (2015).
pubmed: 25961941
pmcid: 4921243
doi: 10.1038/ng.3281
Koser, C. U., Ellington, M. J. & Peacock, S. J. Whole-genome sequencing to control antimicrobial resistance. Trends Genet. 30, 401–407 (2014).
pubmed: 25096945
pmcid: 4156311
doi: 10.1016/j.tig.2014.07.003
Dadashi, M. et al. Frequency distribution, genotypes and the most prevalent sequence types of New Delhi metallo-beta-lactamase-producing Escherichia coli among clinical isolates around the world: a review. J. Glob. Antimicrob. Resist. 19, 284–293 (2019).
pubmed: 31212107
doi: 10.1016/j.jgar.2019.06.008
Diene, S. M. & Rolain, J. M. Carbapenemase genes and genetic platforms in gram-negative bacilli: Enterobacteriaceae, Pseudomonas and Acinetobacter species. Clin. Microbiol. Infect. 20, 831–838 (2014).
pubmed: 24766097
doi: 10.1111/1469-0691.12655
Liu, Y. et al. First report of OXA-181-producing Escherichia coli in China and characterization of the isolate using whole-genome sequencing. Antimicrob. Agents Chemother. 59, 5022–5025 (2015).
pubmed: 26014927
pmcid: 4505247
doi: 10.1128/AAC.00442-15
Roer, L. et al. Escherichia coli sequence type 410 is causing new international high-risk clones. mSphere 3, e00337–e00318 (2018).
pubmed: 30021879
pmcid: 6052333
doi: 10.1128/mSphere.00337-18
Falgenhauer, L. et al. Circulation of clonal populations of fluoroquinolone-resistant CTX-M-15-producing Escherichia coli ST410 in humans and animals in Germany. Int. J. Antimicrob. Agents 47, 457–465 (2016).
pubmed: 27208899
doi: 10.1016/j.ijantimicag.2016.03.019
Schaufler, K. et al. Clonal spread and interspecies transmission of clinically relevant ESBL-producing Escherichia coli of ST410–another successful pandemic clone? FEMS Microbiol. Ecol. 92, fiv155 (2016).
pubmed: 26656065
doi: 10.1093/femsec/fiv155
Dortet, L., Poirel, L., Al Yaqoubi, F. & Nordmann, P. NDM-1, OXA-48 and OXA-181 carbapenemase-producing Enterobacteriaceae in Sultanate of Oman. Clin. Microbiol. Infect. 18, E144–E148 (2012).
pubmed: 22404169
doi: 10.1111/j.1469-0691.2012.03796.x
Szekely, E. et al. First description of bla(NDM-1), bla(OXA-48), bla(OXA-181) producing Enterobacteriaceae strains in Romania. Int. J. Med. Microbiol. 303, 697–700 (2013).
pubmed: 24183483
doi: 10.1016/j.ijmm.2013.10.001
Gamal, D., Fernandez-Martinez, M., El-Defrawy, I., Ocampo-Sosa, A. A. & Martinez-Martinez, L. First identification of NDM-5 associated with OXA-181 in Escherichia coli from Egypt. Emerg. Microbes. Infect. 5, e30 (2016).
pubmed: 27048740
pmcid: 4820674
doi: 10.1038/emi.2016.24
Overballe-Petersen, S. et al. Complete nucleotide sequence of an Escherichia coli sequence type 410 strain carrying bla
pubmed: 29437102
pmcid: 5794949
doi: 10.1128/genomeA.01542-17
Abboud, C. S. et al. A space-time model for carbapenemase-producing Klebsiella pneumoniae (KPC) cluster quantification in a high-complexity hospital. Epidemiol. Infect. 143, 2648–2652 (2015).
pubmed: 25578301
doi: 10.1017/S0950268814003811
Park, R. et al. Statistical detection of geographic clusters of resistant Escherichia coli in a regional network with WHONET and SaTScan. Expert Rev. Anti Infect. Ther. 14, 1097–1107 (2016).
pubmed: 27530311
pmcid: 5109973
doi: 10.1080/14787210.2016.1220303
Argimon, S. et al. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Micro. Genom. 2, e000093 (2016).
Wyres, K. L. et al. Identification of Klebsiella capsule synthesis loci from whole genome data. Micro. Genom. 2, e000102 (2016).
Gwinn, M., MacCannell, D. R. & Khabbaz, R. F. Integrating advanced molecular technologies into public health. J. Clin. Microbiol. 55, 703–714 (2017).
pubmed: 28031438
pmcid: 5328438
doi: 10.1128/JCM.01967-16
Epson, E. E. et al. Carbapenem-resistant Klebsiella pneumoniae producing New Delhi metallo-beta-lactamase at an acute care hospital, Colorado, 2012. Infect. Control Hosp. Epidemiol. 35, 390–397 (2014).
pubmed: 24602944
doi: 10.1086/675607
Harris, S. R. et al. Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect. Dis. 13, 130–136 (2013).
pubmed: 23158674
pmcid: 3556525
doi: 10.1016/S1473-3099(12)70268-2
Peacock, S. J., Parkhill, J. & Brown, N. M. Changing the paradigm for hospital outbreak detection by leading with genomic surveillance of nosocomial pathogens. Microbiology 164, 1213–1219 (2018).
pubmed: 30052172
doi: 10.1099/mic.0.000700
Dymond, A. et al. Genomic surveillance of methicillin-resistant Staphylococcus aureus: a mathematical early modelling study of cost effectiveness. Clin. Infect. Dis. ciz480 https://doi.org/10.1093/cid/ciz480 (2019).
pmcid: 7145999
doi: 10.1093/cid/ciz480
Lascols, C., Peirano, G., Hackel, M., Laupland, K. B. & Pitout, J. D. Surveillance and molecular epidemiology of Klebsiella pneumoniae isolates that produce carbapenemases: first report of OXA-48-like enzymes in North America. Antimicrob. Agents Chemother. 57, 130–136 (2013).
pubmed: 23070171
pmcid: 3535978
doi: 10.1128/AAC.01686-12
Wyres, K. L. et al. Genomic surveillance for hypervirulence and multi-drug resistance in invasive Klebsiella pneumoniae from South and Southeast Asia. Genome Med 12, 11 (2020).
pubmed: 31948471
pmcid: 6966826
doi: 10.1186/s13073-019-0706-y
Baker, S., Thomson, N., Weill, F. X. & Holt, K. E. Genomic insights into the emergence and spread of antimicrobial-resistant bacterial pathogens. Science 360, 733–738 (2018).
pubmed: 29773743
pmcid: 6510332
doi: 10.1126/science.aar3777
Qin, S., Cheng, J., Wang, P., Feng, X. & Liu, H. M. Early emergence of OXA-181-producing Escherichia coli ST410 in China. J. Glob. Antimicrob. Resist. 15, 215–218 (2018).
pubmed: 30393155
doi: 10.1016/j.jgar.2018.06.017
Khong, W. X. et al. Tracking inter-institutional spread of NDM and identification of a novel NDM-positive plasmid, pSg1-NDM, using next-generation sequencing approaches. J. Antimicrob. Chemother. 71, 3081–3089 (2016).
pubmed: 27494913
doi: 10.1093/jac/dkw277
Baek, J. Y. et al. Plasmid analysis of Escherichia coli isolates from South Korea co-producing NDM-5 and OXA-181 carbapenemases. Plasmid 104, 102417 (2019).
pubmed: 31150689
doi: 10.1016/j.plasmid.2019.102417
Aung, M. S. et al. Prevalence of extended-spectrum beta-lactamase and carbapenemase genes in clinical isolates of Escherichia coli in Myanmar: dominance of bla
doi: 10.1089/mdr.2017.0387
Dallman, T. J. et al. Use of whole-genome sequencing for the public health surveillance of Shigella sonnei in England and Wales, 2015. J. Med. Microbiol. 65, 882–884 (2016).
pubmed: 27302408
doi: 10.1099/jmm.0.000296
Nadon, C. et al. PulseNet International: vision for the implementation of whole genome sequencing (WGS) for global food-borne disease surveillance. Eur. Surveill. 22, 23.30544 (2017).
doi: 10.2807/1560-7917.ES.2017.22.23.30544
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).
pubmed: 24145532
pmcid: 3910750
doi: 10.1128/AAC.01310-13
Jia, B. et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res 45, D566–D573 (2017).
pubmed: 27789705
doi: 10.1093/nar/gkw1004
Zankari, E. et al. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 2640–2644 (2012).
pubmed: 22782487
pmcid: 3468078
doi: 10.1093/jac/dks261
Gayeta, J. et al. Establishment of whole genome sequencing in the antimicrobial resistance surveillance program in the Philippines: assessment of whole genome sequence quality. In Applied Bioinformatics and Public Health Microbiology. (Advanced Courses and Scientific Conferences, Hinxton, Cambridge, UK, 2019).
Masim, M. A. et al. Genomic surveillance report for methicillin-resistant Staphylococcus aureus in the Philippines. In Applied Bioinformatics and Public Health Microbiology. (Advanced Courses and Scientific Conferences, Hinxton, Cambridge, UK, 2019).
Magiorakos, A. P. 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. 18, 268–281 (2012).
pubmed: 21793988
doi: 10.1111/j.1469-0691.2011.03570.x
Wood, D. E. & Salzberg, S. L. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 15, R46 (2014).
pubmed: 24580807
pmcid: 4053813
doi: 10.1186/gb-2014-15-3-r46
Pruitt, K. D., Tatusova, T., Brown, G. R. & Maglott, D. R. NCBI reference sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res. 40, D130–D135 (2012).
pubmed: 22121212
doi: 10.1093/nar/gkr1079
Page, A. J. et al. Robust high-throughput prokaryote de novo assembly and improvement pipeline for Illumina data. Micro. Genom. 2, e000083 (2016).
Gladman, S. & Seemann, T. Velvet optimiser: for automatically optimising the primary parameter options for the Velvet de novo sequence assembler. Victorian Bioinformatics Consortium https://github.com/Victorian-Bioinformatics-Consortium/VelvetOptimiser (2008).
Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821–829 (2008).
pubmed: 18349386
pmcid: 2336801
doi: 10.1101/gr.074492.107
Boetzer, M., Henkel, C. V., Jansen, H. J., Butler, D. & Pirovano, W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27, 578–579 (2011).
pubmed: 21149342
doi: 10.1093/bioinformatics/btq683
Boetzer, M. & Pirovano, W. Toward almost closed genomes with GapFiller. Genome Biol. 13, R56 (2012).
pubmed: 22731987
pmcid: 3446322
doi: 10.1186/gb-2012-13-6-r56
Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).
pubmed: 24642063
doi: 10.1093/bioinformatics/btu153
Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589–595 (2010).
pubmed: 20080505
pmcid: 2828108
doi: 10.1093/bioinformatics/btp698
Broad Institute. Picard: a set of command line tools (in Java) for manipulating high-throughput sequencing (HTS) data https://broadinstitute.github.io/picard/ (2020).
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 19505943
doi: 10.1093/bioinformatics/btp352
Samtools. Bcftools: utilities for variant calling and manipulating VCFs and BCFs http://samtools.github.io/bcftools/ (2020).
Croucher, N. J. et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 43, e15 (2015).
pubmed: 25414349
doi: 10.1093/nar/gku1196
Page, A. J. et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Micro. Genom. 2, e000056 (2016).
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
pubmed: 3998144
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
Hunt, M. et al. ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. Micro. Genom. 3, e000131 (2017).
David, S. et al. Epidemic of carbapenem-resistant Klebsiella pneumoniae in Europe is driven by nosocomial spread. Nat. Microbiol. 4, 1919–1929 (2019).
pubmed: 31358985
pmcid: 7244338
doi: 10.1038/s41564-019-0492-8
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).
pubmed: 24777092
pmcid: 4068535
doi: 10.1128/AAC.02412-14
Page, A. J., Taylor, B. & Keane, J. A. Multilocus sequence typing by blast from de novo assemblies against PubMLST. J. Open Source Softw. 8, 2 (2016).
Jolley, K. A., Bray, J. E. & Maiden, M. C. J. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 3, 124 (2018).
pubmed: 30345391
pmcid: 6192448
doi: 10.12688/wellcomeopenres.14826.1
Wirth, T. et al. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol. Microbiol. 60, 1136–1151 (2006).
pubmed: 16689791
pmcid: 1557465
doi: 10.1111/j.1365-2958.2006.05172.x
Bartual, S. G. et al. Development of a multilocus sequence typing scheme for characterization of clinical isolates of Acinetobacter baumannii. J. Clin. Microbiol. 43, 4382–4390 (2005).
pubmed: 16145081
pmcid: 1234098
doi: 10.1128/JCM.43.9.4382-4390.2005
Curran, B., Jonas, D., Grundmann, H., Pitt, T. & Dowson, C. G. Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J. Clin. Microbiol. 42, 5644–5649 (2004).
pubmed: 15583294
pmcid: 535286
doi: 10.1128/JCM.42.12.5644-5649.2004
Diancourt, L., Passet, V., Verhoef, J., Grimont, P. A. & Brisse, S. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J. Clin. Microbiol. 43, 4178–4182 (2005).
pubmed: 16081970
pmcid: 1233940
doi: 10.1128/JCM.43.8.4178-4182.2005
Wick, R. R., Judd, L. M., Gorrie, C. L. & Holt, K. E. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 13, e1005595 (2017).
pubmed: 28594827
pmcid: 5481147
doi: 10.1371/journal.pcbi.1005595
Wick, R. R., Schultz, M. B., Zobel, J. & Holt, K. E. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31, 3350–3352 (2015).
pubmed: 26099265
pmcid: 4595904
doi: 10.1093/bioinformatics/btv383
Hunt, M. et al. Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biol. 16, 294 (2015).
pubmed: 26714481
pmcid: 4699355
doi: 10.1186/s13059-015-0849-0
Partridge, S. R. & Tsafnat, G. Automated annotation of mobile antibiotic resistance in gram-negative bacteria: the multiple antibiotic resistance annotator (MARA) and database. J. Antimicrob. Chemother. 73, 883–890 (2018).
pubmed: 29373760
doi: 10.1093/jac/dkx513
Alikhan, N. F., Petty, N. K., Ben Zakour, N. L. & Beatson, S. A. BLAST ring image generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12, 402 (2011).
pubmed: 21824423
pmcid: 3163573
doi: 10.1186/1471-2164-12-402