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Review article: Biomedical intelligence

Vol. 148 No. 4950 (2018)

Improving the quality and workflow of bacterial genome sequencing and analysis: paving the way for a Switzerland-wide molecular epidemiological surveillance platform

  • Adrian Egli
  • Dominique S. Blanc
  • Gilbert Greub
  • Peter M. Keller
  • Vladimir Lazarevic
  • Aitana Lebrand
  • Stephen Leib
  • Richard A. Neher
  • Vincent Perreten
  • Alban Ramette
  • Jacques Schrenzel
  • Roger Stephan
  • Karoline Wagner
  • Daniel Wüthrich
  • Ioannis Xenarios
DOI
https://doi.org/10.4414/smw.2018.14693
Cite this as:
Swiss Med Wkly. 2018;148:w14693
Published
04.01.2019

Summary

Facing multidrug resistant (MDR) bacterial pathogens is one of the most important challenges for our society. The spread of highly virulent and resistant pathogens can be described using molecular typing technologies; in particular, whole genome sequencing (WGS) data can be used for molecular typing purposes with high resolution. WGS data analysis can explain the spatiotemporal patterns of pathogen transmission. However, the transmission between compartments (human, animal, food, environment) is very complex. Interoperable and curated metadata are a key requirement for fully understanding this complexity. In addition, high quality sequence data are a key element between centres using WGS data for diagnostic and epidemiological applications. We aim to describe steps to improve WGS data analysis and to implement a molecular surveillance platform allowing integration of high resolution WGS typing data and epidemiological data.

References

  1. O’Neill J, et al. Tackling drug-resistant infections globally: Final report and recommendations. London: Wellcome Trust, HM government; 2016.
  2. Grundmann H, Glasner C, Albiger B, Aanensen DM, Tomlinson CT, Andrasević AT, et al.; European Survey of Carbapenemase-Producing Enterobacteriaceae (EuSCAPE) Working Group. Occurrence of carbapenemase-producing Klebsiella pneumoniae and Escherichia coli in the European survey of carbapenemase-producing Enterobacteriaceae (EuSCAPE): a prospective, multinational study. Lancet Infect Dis. 2017;17(2):153–63. doi:.https://doi.org/10.1016/S1473-3099(16)30257-2
  3. Albiger B, Glasner C, Struelens MJ, Grundmann H, Monnet DL ; European Survey of Carbapenemase-Producing Enterobacteriaceae (EuSCAPE) working group. Carbapenemase-producing Enterobacteriaceae in Europe: assessment by national experts from 38 countries, May 2015. Euro Surveill. 2015;20(45):30062. doi:.https://doi.org/10.2807/1560-7917.ES.2015.20.45.30062
  4. Aramburu C, Harbarth S, Liassine N, Girard M, Gervaix A, Scherenzel J, et al. Community-acquired methicillin-resistant Staphylococcus aureus in Switzerland: first surveillance report. Euro Surveill. 2006;11(1):42–3. doi:.https://doi.org/10.2807/esm.11.01.00594-en
  5. Boyce JM. Methicillin-resistant Staphylococcus aureus. Detection, epidemiology, and control measures. Infect Dis Clin North Am. 1989;3(4):901–13.
  6. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, Carey RB, et al.; EMERGEncy ID Net Study Group. Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med. 2006;355(7):666–74. doi:.https://doi.org/10.1056/NEJMoa055356
  7. Gijón M, Bellusci M, Petraitiene B, Noguera-Julian A, Zilinskaite V, Sanchez Moreno P, et al. Factors associated with severity in invasive community-acquired Staphylococcus aureus infections in children: a prospective European multicentre study. Clin Microbiol Infect. 2016;22(7):643.e1–6. doi:.https://doi.org/10.1016/j.cmi.2016.04.004
  8. Maeda M, Shoji H, Shirakura T, Takuma T, Ugajin K, Fukuchi K, et al. Analysis of Staphylococcal Toxins and Clinical Outcomes of Methicillin-Resistant Staphylococcus aureus Bacteremia. Biol Pharm Bull. 2016;39(7):1195–200. doi:.https://doi.org/10.1248/bpb.b16-00255
  9. Rossi F, Diaz L, Wollam A, Panesso D, Zhou Y, Rincon S, et al. Transferable vancomycin resistance in a community-associated MRSA lineage. N Engl J Med. 2014;370(16):1524–31. doi:.https://doi.org/10.1056/NEJMoa1303359
  10. Britt NS, Patel N, Shireman TI, El Atrouni WI, Horvat RT, Steed ME. Relationship between vancomycin tolerance and clinical outcomes in Staphylococcus aureus bacteraemia. J Antimicrob Chemother. 2017;72(2):535–42. doi:.https://doi.org/10.1093/jac/dkw453
  11. World Health Organization. Global action plan on antimicrobial resistance. Geneva: WHO Library Cataloguing-in-Publication Data; 2015.
  12. Baier C, Ipaktchi R, Ebadi E, Limbourg A, Mett TR, Vogt PM, et al. A multimodal infection control concept in a burn intensive care unit - lessons learnt from a meticillin-resistant Staphylococcus aureus outbreak. J Hosp Infect. 2018;98(2):127–33. doi:.https://doi.org/10.1016/j.jhin.2017.07.023
  13. Olearo F, Albrich WC, Vernaz N, Harbarth S, Kronenberg A ; Swiss Centre For Antibiotic Resistance Anresis. Staphylococcus aureus and methicillin resistance in Switzerland: regional differences and trends from 2004 to 2014. Swiss Med Wkly. 2016;146:w14339. doi:.https://doi.org/10.4414/smw.2016.14339
  14. Bielicki JA, Cromwell DA, Johnson A, Planche T, Sharland M ; ARPEC project. Surveillance of Gram-negative bacteria: impact of variation in current European laboratory reporting practice on apparent multidrug resistance prevalence in paediatric bloodstream isolates. Eur J Clin Microbiol Infect Dis. 2017;36(5):839–46. doi:.https://doi.org/10.1007/s10096-016-2869-4
  15. Freeman R, Ironmonger D, Puleston R, Hopkins KL, Welfare W, Hope R, et al. Enhanced surveillance of carbapenemase-producing Gram-negative bacteria to support national and international prevention and control efforts. Clin Microbiol Infect. 2016;22(10):896–7. doi:.https://doi.org/10.1016/j.cmi.2016.07.020
  16. Egli A, Schmid H, Kuenzli E, Widmer AF, Battegay M, Plagge H, et al. Association of daptomycin use with resistance development in Enterococcus faecium bacteraemia-a 7-year individual and population-based analysis. Clin Microbiol Infect. 2017;23(2):118.e1–7. doi:.https://doi.org/10.1016/j.cmi.2016.10.003
  17. Ruppé E, Olearo F, Pires D, Baud D, Renzi G, Cherkaoui A, et al. Clonal or not clonal? Investigating hospital outbreaks of KPC-producing Klebsiella pneumoniae with whole-genome sequencing. Clin Microbiol Infect. 2017;23(7):470–5. doi:.https://doi.org/10.1016/j.cmi.2017.01.015
  18. Kraemer JG, Pires J, Kueffer M, Semaani E, Endimiani A, Hilty M, et al. Prevalence of extended-spectrum β-lactamase-producing Enterobacteriaceae and Methicillin-Resistant Staphylococcus aureus in pig farms in Switzerland. Sci Total Environ. 2017;603-604:401–5. doi:.https://doi.org/10.1016/j.scitotenv.2017.06.110
  19. 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. doi:.https://doi.org/10.1016/j.drup.2012.12.001
  20. Hindermann D, Gopinath G, Chase H, Negrete F, Althaus D, Zurfluh K, et al. Salmonella enterica serovar Infantis from Food and Human Infections, Switzerland, 2010-2015: Poultry-Related Multidrug Resistant Clones and an Emerging ESBL Producing Clonal Lineage. Front Microbiol. 2017;8:1322. doi:.https://doi.org/10.3389/fmicb.2017.01322
  21. Lahti E, Löfdahl M, Ågren J, Hansson I, Olsson Engvall E. Confirmation of a Campylobacteriosis Outbreak Associated with Chicken Liver Pâté Using PFGE and WGS. Zoonoses Public Health. 2017;64(1):14–20. doi:.https://doi.org/10.1111/zph.12272
  22. Davis GS, Waits K, Nordstrom L, Weaver B, Aziz M, Gauld L, et al. Intermingled Klebsiella pneumoniae Populations Between Retail Meats and Human Urinary Tract Infections. Clin Infect Dis. 2015;61(6):892–9. doi:.https://doi.org/10.1093/cid/civ428
  23. Paterson GK, Harrison EM, Craven EF, Petersen A, Larsen AR, Ellington MJ, et al. Incidence and characterisation of methicillin-resistant Staphylococcus aureus (MRSA) from nasal colonisation in participants attending a cattle veterinary conference in the UK. PLoS One. 2013;8(7):e68463. doi:.https://doi.org/10.1371/journal.pone.0068463
  24. Doulgeraki AI, Di Ciccio P, Ianieri A, Nychas GE. Methicillin-resistant food-related Staphylococcus aureus: a review of current knowledge and biofilm formation for future studies and applications. Res Microbiol. 2017;168(1):1–15. doi:.https://doi.org/10.1016/j.resmic.2016.08.001
  25. Laaksonen S, Oksanen A, Julmi J, Zweifel C, Fredriksson-Ahomaa M, Stephan R. Presence of foodborne pathogens, extended-spectrum β-lactamase -producing Enterobacteriaceae, and methicillin-resistant Staphylococcus aureus in slaughtered reindeer in northern Finland and Norway. Acta Vet Scand. 2017;59(1):2. doi:.https://doi.org/10.1186/s13028-016-0272-x
  26. Osman K, Badr J, Al-Maary KS, Moussa IM, Hessain AM, Girah ZM, et al. Prevalence of the Antibiotic Resistance Genes in Coagulase-Positive-and Negative-Staphylococcus in Chicken Meat Retailed to Consumers. Front Microbiol. 2016;7:1846. doi:.https://doi.org/10.3389/fmicb.2016.01846
  27. Revez J, Espinosa L, Albiger B, Leitmeyer KC, Struelens MJ ; ECDC National Microbiology Focal Points and Experts Group. Survey on the Use of Whole-Genome Sequencing for Infectious Diseases Surveillance: Rapid Expansion of European National Capacities, 2015-2016. Front Public Health. 2017;5:347. doi:.https://doi.org/10.3389/fpubh.2017.00347
  28. Sabat AJ, Budimir A, Nashev D, Sá-Leão R, van Dijl J, Laurent F, et al.; ESCMID Study Group of Epidemiological Markers (ESGEM). Overview of molecular typing methods for outbreak detection and epidemiological surveillance. Euro Surveill. 2013;18(4):20380. doi:.https://doi.org/10.2807/ese.18.04.20380-en
  29. Crowe SJ, Bottichio L, Shade LN, Whitney BM, Corral N, Melius B, et al. Shiga Toxin-Producing E. coli Infections Associated with Flour. N Engl J Med. 2017;377(21):2036–43. doi:.https://doi.org/10.1056/NEJMoa1615910
  30. Fischer J, Hille K, Ruddat I, Mellmann A, Köck R, Kreienbrock L. Simultaneous occurrence of MRSA and ESBL-producing Enterobacteriaceae on pig farms and in nasal and stool samples from farmers. Vet Microbiol. 2017;200:107–13. doi:.https://doi.org/10.1016/j.vetmic.2016.05.021
  31. Ford L, Carter GP, Wang Q, Seemann T, Sintchenko V, Glass K, et al. Incorporating Whole-Genome Sequencing into Public Health Surveillance: Lessons from Prospective Sequencing of Salmonella Typhimurium in Australia. Foodborne Pathog Dis. 2018;15(3):161–7. doi:.https://doi.org/10.1089/fpd.2017.2352
  32. Timms VJ, Rockett R, Bachmann NL, Martinez E, Wang Q, Chen SC, et al. Genome Sequencing Links Persistent Outbreak of Legionellosis in Sydney (New South Wales, Australia) to an Emerging Clone of Legionella pneumophila Sequence Type 211. Appl Environ Microbiol. 2018;84(5):e02020-17. doi:.https://doi.org/10.1128/AEM.02020-17
  33. Waldram A, Dolan G, Ashton PM, Jenkins C, Dallman TJ. Epidemiological analysis of Salmonella clusters identified by whole genome sequencing, England and Wales 2014. Food Microbiol. 2018;71:39–45. doi:.https://doi.org/10.1016/j.fm.2017.02.012
  34. Oberle M, Wohlwend N, Jonas D, Maurer FP, Jost G, Tschudin-Sutter S, et al. The Technical and Biological Reproducibility of Matrix-Assisted Laser Desorption Ionization-Time of Flight Mass Spectrometry (MALDI-TOF MS) Based Typing: Employment of Bioinformatics in a Multicenter Study. PLoS One. 2016;11(10):e0164260. doi:.https://doi.org/10.1371/journal.pone.0164260
  35. Besser J, Carleton HA, Gerner-Smidt P, Lindsey RL, Trees E. Next-generation sequencing technologies and their application to the study and control of bacterial infections. Clin Microbiol Infect. 2018;24(4):335–41. doi:.https://doi.org/10.1016/j.cmi.2017.10.013
  36. van Belkum A, Tassios PT, Dijkshoorn L, Haeggman S, Cookson B, Fry NK, et al.; European Society of Clinical Microbiology and Infectious Diseases (ESCMID) Study Group on Epidemiological Markers (ESGEM). Guidelines for the validation and application of typing methods for use in bacterial epidemiology. Clin Microbiol Infect. 2007;13(Suppl 3):1–46. doi:.https://doi.org/10.1111/j.1469-0691.2007.01786.x
  37. Köser CU, Ellington MJ, Cartwright EJ, Gillespie SH, Brown NM, Farrington M, et al. Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog. 2012;8(8):e1002824. doi:.https://doi.org/10.1371/journal.ppat.1002824
  38. Reuter S, Ellington MJ, Cartwright EJ, Köser CU, Török ME, Gouliouris T, et al. Rapid bacterial whole-genome sequencing to enhance diagnostic and public health microbiology. JAMA Intern Med. 2013;173(15):1397–404. doi:.https://doi.org/10.1001/jamainternmed.2013.7734
  39. Struelens MJ, Brisse S. From molecular to genomic epidemiology: transforming surveillance and control of infectious diseases. Euro Surveill. 2013;18(4):20386. doi:.https://doi.org/10.2807/ese.18.04.20386-en
  40. Chattaway MA, Schaefer U, Tewolde R, Dallman TJ, Jenkins C. Identification of Escherichia coli and Shigella Species from Whole-Genome Sequences. J Clin Microbiol. 2017;55(2):616–23. doi:.https://doi.org/10.1128/JCM.01790-16
  41. Meinel DM, Kuehl R, Zbinden R, Boskova V, Garzoni C, Fadini D, et al. Outbreak investigation for toxigenic Corynebacterium diphtheriae wound infections in refugees from Northeast Africa and Syria in Switzerland and Germany by whole genome sequencing. Clin Microbiol Infect. 2016;22(12):1003.e1–8. doi:.https://doi.org/10.1016/j.cmi.2016.08.010
  42. Piso RJ, Käch R, Pop R, Zillig D, Schibli U, Bassetti S, et al. A Cross-Sectional Study of Colonization Rates with Methicillin-Resistant Staphylococcus aureus (MRSA) and Extended-Spectrum Beta-Lactamase (ESBL) and Carbapenemase-Producing Enterobacteriaceae in Four Swiss Refugee Centres. PLoS One. 2017;12(1):e0170251. doi:.https://doi.org/10.1371/journal.pone.0170251
  43. Sommerstein R, Führer U, Lo Priore E, Casanova C, Meinel DM, Seth-Smith HM, et al.; On Behalf Of Anresis; On Behalf Of Swissnoso. Burkholderia stabilis outbreak associated with contaminated commercially-available washing gloves, Switzerland, May 2015 to August 2016. Euro Surveill. 2017;22(49). doi:.https://doi.org/10.2807/1560-7917.ES.2017.22.49.17-00213
  44. Gargis AS, Kalman L, Bick DP, da Silva C, Dimmock DP, Funke BH, et al. Good laboratory practice for clinical next-generation sequencing informatics pipelines. Nat Biotechnol. 2015;33(7):689–93. doi:.https://doi.org/10.1038/nbt.3237
  45. Gargis AS, Kalman L, Lubin IM. Assuring the Quality of Next-Generation Sequencing in Clinical Microbiology and Public Health Laboratories. J Clin Microbiol. 2016;54(12):2857–65. doi:.https://doi.org/10.1128/JCM.00949-16
  46. McNerney R, Clark TG, Campino S, Rodrigues C, Dolinger D, Smith L, et al. Removing the bottleneck in whole genome sequencing of Mycobacterium tuberculosis for rapid drug resistance analysis: a call to action. Int J Infect Dis. 2017;56:130–5. doi:.https://doi.org/10.1016/j.ijid.2016.11.422
  47. Sjödin A, Broman T, Melefors Ö, Andersson G, Rasmusson B, Knutsson R, et al. The need for high-quality whole-genome sequence databases in microbial forensics. Biosecur Bioterror. 2013;11(S1, Suppl 1):S78–86. doi:.https://doi.org/10.1089/bsp.2013.0007
  48. Mellmann A, Bletz S, Böking T, Kipp F, Becker K, Schultes A, et al. Real-Time Genome Sequencing of Resistant Bacteria Provides Precision Infection Control in an Institutional Setting. J Clin Microbiol. 2016;54(12):2874–81. doi:.https://doi.org/10.1128/JCM.00790-16
  49. Struelens M, et al. (ed ECDC) 1-14 (ECDC, Stockholm, 2016).
  50. Agodi A, Auxilia F, Barchitta M, Brusaferro S, D’Errico MM, Montagna MT, et al.; SPIN-UTI network of the GISIOWorking Group of the Italian Society of Hygiene, Preventive Medicine and Public Health (SItI). Antibiotic consumption and resistance: results of the SPIN-UTI project of the GISIO-SItI. Epidemiol Prev. 2015;39(4, Suppl 1):94–8.
  51. Conceição T, Diamantino F, Coelho C, de Lencastre H, Aires-de-Sousa M. Contamination of public buses with MRSA in Lisbon, Portugal: a possible transmission route of major MRSA clones within the community. PLoS One. 2013;8(11):e77812. doi:.https://doi.org/10.1371/journal.pone.0077812
  52. Mortensen R, Christensen D, Hansen LB, Christensen JP, Andersen P, Dietrich J. Local Th17/IgA immunity correlate with protection against intranasal infection with Streptococcus pyogenes. PLoS One. 2017;12(4):e0175707. doi:.https://doi.org/10.1371/journal.pone.0175707
  53. Turner RD, Chiu C, Churchyard GJ, Esmail H, Lewinsohn DM, Gandhi NR, et al. Tuberculosis Infectiousness and Host Susceptibility. J Infect Dis. 2017;216(suppl_6):S636–43. doi:.https://doi.org/10.1093/infdis/jix361
  54. Islam MA, Islam M, Hasan R, Hossain MI, Nabi A, Rahman M, et al. Environmental Spread of New Delhi Metallo-β-Lactamase-1-Producing Multidrug-Resistant Bacteria in Dhaka, Bangladesh. Appl Environ Microbiol. 2017;83(15):e00793-17. doi:.https://doi.org/10.1128/AEM.00793-17
  55. Surette MD, Wright GD. Lessons from the Environmental Antibiotic Resistome. Annu Rev Microbiol. 2017;71(1):309–29. doi:.https://doi.org/10.1146/annurev-micro-090816-093420
  56. Furness LE, Campbell A, Zhang L, Gaze WH, McDonald RA. Wild small mammals as sentinels for the environmental transmission of antimicrobial resistance. Environ Res. 2017;154:28–34. doi:.https://doi.org/10.1016/j.envres.2016.12.014
  57. Parker D, Sniatynski MK, Mandrusiak D, Rubin JE. Extended-spectrum β-lactamase producing Escherichia coli isolated from wild birds in Saskatoon, Canada. Lett Appl Microbiol. 2016;63(1):11–5. doi:.https://doi.org/10.1111/lam.12589
  58. Marques C, Belas A, Franco A, Aboim C, Gama LT, Pomba C. Increase in antimicrobial resistance and emergence of major international high-risk clonal lineages in dogs and cats with urinary tract infection: 16 year retrospective study. J Antimicrob Chemother. 2018;73(2):377–84. doi:.https://doi.org/10.1093/jac/dkx401
  59. Afset JE, Larssen KW, Bergh K, Larkeryd A, Sjodin A, Johansson A, et al. Phylogeographical pattern of Francisella tularensis in a nationwide outbreak of tularaemia in Norway, 2011. Euro Surveill. 2015;20(19):9–14. doi:.https://doi.org/10.2807/1560-7917.ES2015.20.19.21125
  60. Stucki D, Brites D, Jeljeli L, Coscolla M, Liu Q, Trauner A, et al. Mycobacterium tuberculosis lineage 4 comprises globally distributed and geographically restricted sublineages. Nat Genet. 2016;48(12):1535–43. doi:.https://doi.org/10.1038/ng.3704
  61. Wong VK, Baker S, Pickard DJ, Parkhill J, Page AJ, Feasey NA, et al. Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events. Nat Genet. 2015;47(6):632–9. doi:.https://doi.org/10.1038/ng.3281
  62. Glaser P, Martins-Simões P, Villain A, Barbier M, Tristan A, Bouchier C, et al. Demography and Intercontinental Spread of the USA300 Community-Acquired Methicillin-Resistant Staphylococcus aureus Lineage. MBio. 2016;7(1):e02183-15. doi:.https://doi.org/10.1128/mBio.02183-15
  63. Faria NR, Quick J, Claro IM, Thézé J, de Jesus JG, Giovanetti M, et al. Establishment and cryptic transmission of Zika virus in Brazil and the Americas. Nature. 2017;546(7658):406–10. doi:.https://doi.org/10.1038/nature22401
  64. Grubaugh ND, Ladner JT, Kraemer MUG, Dudas G, Tan AL, Gangavarapu K, et al. Genomic epidemiology reveals multiple introductions of Zika virus into the United States. Nature. 2017;546(7658):401–5. doi:.https://doi.org/10.1038/nature22400
  65. Neher RA, Bedford T, Daniels RS, Russell CA, Shraiman BI. Prediction, dynamics, and visualization of antigenic phenotypes of seasonal influenza viruses. Proc Natl Acad Sci USA. 2016;113(12):E1701–9. doi:.https://doi.org/10.1073/pnas.1525578113
  66. Carroll MW, Matthews DA, Hiscox JA, Elmore MJ, Pollakis G, Rambaut A, et al. Temporal and spatial analysis of the 2014-2015 Ebola virus outbreak in West Africa. Nature. 2015;524(7563):97–101. doi:.https://doi.org/10.1038/nature14594
  67. Dudas G, Carvalho LM, Bedford T, Tatem AJ, Baele G, Faria NR, et al. Virus genomes reveal factors that spread and sustained the Ebola epidemic. Nature. 2017;544(7650):309–15. doi:.https://doi.org/10.1038/nature22040
  68. Hayman DT, Fooks AR, Marston DA, Garcia-R JC. The Global Phylogeography of Lyssaviruses - Challenging the ‘Out of Africa’ Hypothesis. PLoS Negl Trop Dis. 2016;10(12):e0005266. doi:.https://doi.org/10.1371/journal.pntd.0005266
  69. Argimón S, Abudahab K, Goater RJ, Fedosejev A, Bhai J, Glasner C, et al. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microb Genom. 2016;2(11):e000093. doi:.https://doi.org/10.1099/mgen.0.000093
  70. Aanensen DM, Feil EJ, Holden MT, Dordel J, Yeats CA, Fedosejev A, et al.; European SRL Working Group. Whole-Genome Sequencing for Routine Pathogen Surveillance in Public Health: a Population Snapshot of Invasive Staphylococcus aureus in Europe. MBio. 2016;7(3):e00444-16. doi:.https://doi.org/10.1128/mBio.00444-16
  71. Hadfield J, et al. Nextstrain: real-time tracking of pathogen evolution. bioRxiv. 2017. doi:.https://doi.org/10.1101/224048
  72. Neher RA, Bedford T. nextflu: real-time tracking of seasonal influenza virus evolution in humans. Bioinformatics. 2015;31(21):3546–8. doi:.https://doi.org/10.1093/bioinformatics/btv381
  73. Griffiths E, Dooley D, Graham M, Van Domselaar G, Brinkman FSL, Hsiao WWL. Context Is Everything: Harmonization of Critical Food Microbiology Descriptors and Metadata for Improved Food Safety and Surveillance. Front Microbiol. 2017;8:1068. doi:.https://doi.org/10.3389/fmicb.2017.01068
  74. Brhelova E, Antonova M, Pardy F, Kocmanova I, Mayer J, Racil Z, et al. Investigation of next-generation sequencing data of Klebsiella pneumoniae using web-based tools. J Med Microbiol. 2017;66(11):1673–83. doi:.https://doi.org/10.1099/jmm.0.000624
  75. Yin X, Jiang XT, Chai B, Li L, Yang Y, Cole JR, et al. ARGs-OAP v2.0 with an expanded SARG database and Hidden Markov Models for enhancement characterization and quantification of antibiotic resistance genes in environmental metagenomes. Bioinformatics. 2018;34(13):2263–70. doi:.https://doi.org/10.1093/bioinformatics/bty053
  76. Chen L, Zheng D, Liu B, Yang J, Jin Q. VFDB 2016: hierarchical and refined dataset for big data analysis--10 years on. Nucleic Acids Res. 2016;44(D1):D694–7. doi:.https://doi.org/10.1093/nar/gkv1239
  77. Gámez G, Castro A, Gómez-Mejia A, Gallego M, Bedoya A, Camargo M, et al. The variome of pneumococcal virulence factors and regulators. BMC Genomics. 2018;19(1):10. doi:.https://doi.org/10.1186/s12864-017-4376-0
  78. Rasmussen LH, Højholt K, Dargis R, Christensen JJ, Skovgaard O, Justesen US, et al. In silico assessment of virulence factors in strains of Streptococcus oralis and Streptococcus mitis isolated from patients with Infective Endocarditis. J Med Microbiol. 2017. doi:.https://doi.org/10.1099/jmm.0.000573
  79. Kleinheinz KA, Joensen KG, Larsen MV. Applying the ResFinder and VirulenceFinder web-services for easy identification of acquired antibiotic resistance and E. coli virulence genes in bacteriophage and prophage nucleotide sequences. Bacteriophage. 2014;4(2):e27943. doi:.https://doi.org/10.4161/bact.27943
  80. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67(11):2640–4. doi:.https://doi.org/10.1093/jac/dks261
  81. Zankari E, Allesøe R, Joensen KG, Cavaco LM, Lund O, Aarestrup FM. PointFinder: a novel web tool for WGS-based detection of antimicrobial resistance associated with chromosomal point mutations in bacterial pathogens. J Antimicrob Chemother. 2017;72(10):2764–8. doi:.https://doi.org/10.1093/jac/dkx217
  82. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 2017;45(D1):D566–73. doi:.https://doi.org/10.1093/nar/gkw1004
  83. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ, et al. The comprehensive antibiotic resistance database. Antimicrob Agents Chemother. 2013;57(7):3348–57. doi:.https://doi.org/10.1128/AAC.00419-13
  84. Ding W, Baumdicker F, Neher RA. panX: pan-genome analysis and exploration. Nucleic Acids Res. 2018;46(1):e5. doi:.https://doi.org/10.1093/nar/gkx977
  85. Leider JP, DeBruin D, Reynolds N, Koch A, Seaberg J. Ethical Guidance for Disaster Response, Specifically Around Crisis Standards of Care: A Systematic Review. Am J Public Health. 2017;107(9):e1–9. doi:.https://doi.org/10.2105/AJPH.2017.303882
  86. Smith MJ, Silva DS. Ethics for pandemics beyond influenza: Ebola, drug-resistant tuberculosis, and anticipating future ethical challenges in pandemic preparedness and response. Monash Bioeth Rev. 2015;33(2-3):130–47. doi:.https://doi.org/10.1007/s40592-015-0038-7
  87. Alirol E, Kuesel AC, Guraiib MM, de la Fuente-Núñez V, Saxena A, Gomes MF. Ethics review of studies during public health emergencies - the experience of the WHO ethics review committee during the Ebola virus disease epidemic. BMC Med Ethics. 2017;18(1):43. doi:.https://doi.org/10.1186/s12910-017-0201-1
  88. Jamrozik E, Selgelid MJ. Ethics, health policy, and Zika: From emergency to global epidemic? J Med Ethics. 2018;44(5):343–8. doi:.https://doi.org/10.1136/medethics-2017-104389
  89. Derpmann S. Ethical reasoning in pandemic preparedness plans: Southeast Asia and the Western Pacific. Bioethics. 2011;25(8):445–50. doi:.https://doi.org/10.1111/j.1467-8519.2011.01922.x
  90. Rump B, Cornelis C, Woonink F, VAN Steenbergen J, Verweij M, Hulscher M. Using typing techniques in a specific outbreak: the ethical reflection of public health professionals. Epidemiol Infect. 2017;145(7):1431–6. doi:.https://doi.org/10.1017/S0950268817000127

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