Incorporating Whole-Genome Sequencing into Public Health Surveillance: Lessons from Prospective Sequencing of Salmonella Typhimurium in Australia
Publication: Foodborne Pathogens and Disease
Volume 15, Issue Number 3
Abstract
In Australia, the incidence of Salmonella Typhimurium has increased dramatically over the past decade. Whole-genome sequencing (WGS) is transforming public health microbiology, but poses challenges for surveillance. To compare WGS-based approaches with conventional typing for Salmonella surveillance, we performed concurrent WGS and multilocus variable-number tandem-repeat analysis (MLVA) of Salmonella Typhimurium isolates from the Australian Capital Territory (ACT) for a period of 5 months. We exchanged data via a central shared virtual machine and performed comparative genomic analyses. Epidemiological evidence was integrated with WGS-derived data to identify related isolates and sources of infection, and we compared WGS data for surveillance with findings from MLVA typing. We found that WGS data combined with epidemiological data linked an additional 9% of isolates to at least one other isolate in the study in contrast to MLVA and epidemiological data, and 19% more isolates than epidemiological data alone. Analysis of risk factors showed that in one WGS-defined cluster, human cases had higher odds of purchasing a single egg brand. While WGS was more sensitive and specific than conventional typing methods, we identified barriers to uptake of genomic surveillance around complexity of reporting of WGS results, timeliness, acceptability, and stability. In conclusion, WGS offers higher resolution of Salmonella Typhimurium laboratory surveillance than existing methods and can provide further evidence on sources of infection in case and outbreak investigations for public health action. However, there are several challenges that need to be addressed for effective implementation of genomic surveillance in Australia.
Get full access to this article
View all available purchase options and get full access to this article.
References
Allard MW, Strain E, Melka D, Bunning K, Musser SM, Brown EW, Timme R. The practical value of foodborne pathogen traceability through building a whole genome sequencing network and database. J Clin Microbiol 2016;54:1975–1983.
Angelo KM, Chu A, Anand M, Nguyen TA, Bottichio L, Wise M, Williams I, Seelman S, Bell R, Fatica M, Lance S, Baldwin D, Shannon K, Lee H, Trees E, Strain E, Gieraltowski L; Centers for Disease Control and Prevention (CDC). Outbreak of Salmonella Newport infections linked to cucumbers—United States, 2014. MMWR Morb Wkly Rep 2015;64:144–147.
Ashton PM, Nair S, Peters TM, Bale JA, Powell DG, Paintset A, Tewold R, Schaefer U, Jenkins C, Dallman TJ, de Pinna EM, Grant KA; Salmonella Whole Genome Sequencing Implementation Group. Identification of Salmonella for public health surveillance using whole genome sequencing. PeerJ 2016;4:e1752.
Ashton PM, Peters T, Ameh L, McAleer R, Petrie S, Nair S, Muscat I, de Pinna E, Dallman T. Whole genome sequencing for the retrospective investigation of an outbreak of Salmonella Typhimurium DT 8. PLoS Curr 2015;7:pii:.
Byrne L, Fisher I, Peters T, Mather A, Thomson N, Rosner B, Bernard H, McKeown P, Cormican M, Cowden J, Aiyedun V, Lane C; International Outbreak Control Team. A multi-country outbreak of Salmonella Newport gastroenteritis in Europe associated with watermelon from Brazil, confirmed by whole genome sequencing: October 2011 to January 2012. Euro Surveill 2014;19:6–13.
den Bakker HC, Allard MW, Bopp D, Brown EW, Fontana J, Igbal Z, Kinney A, Limberger R, Musser KA, Shudt M, Strain E, Wiedmann M, Wolfgang WJ. Rapid whole-genome sequencing for surveillance of Salmonella enterica serovar Enteritidis. Emerg Infect Dis 2014;20:1306–1341.
Deng X, den Bakker HC, Hendriksen RS. Genomic epidemiology: Whole-genome-sequencing-powered surveillance and outbreak investigation of foodborne bacterial pathogens. Annu Rev Food Sci Technol 2016;7:353–374.
Ford L, Glass K, Veitch M, Wardell R, Polkinghorne B, Dobbins T, Lal A, Kirk MD. Increasing incidence of Salmonella in Australia, 2000–2013. PLoS One 2016;11:e0163989.
Ford L, Wang Q, Stafford R, Ressler KA, Norton S, Shadbolt C, Hope K, Franklin N, Krsteski R, Carswell A, Carter GP, Seemann T, Howard P, Valcanis M, Castillo CFS, Bates J, Glass K, Williamson DA, Sintchenko V, Howden BP, Kirk MD. Seven Salmonella Typhimurium MLVA type 03-26-13-08-523 outbreaks in Australia linked by trace-back and whole genome sequencing. (in press).
German RR, Lee LM, Horan JM, Milstein RL, Pertowski CA, Waller MN; Guidelines Working Group Centers for Disease Control and Prevention (CDC). Updated guidelines for evaluating public health surveillance systems: Recommendations from the Guidelines Working Group. MMWR Recomm Rep 2001;50:1–35.
Hoffmann M, Luo Y, Monday SR, Gonzalez-Escalona N, Ottesen AR, Muruvanda T, Wang C, Kastansis G, Keys C, Janies D, Senturk IF, Catalyurek UV, Wang H, Hammack TS, Wolfgang WJ, Schoonmaker-Bopp D, Chu A, Myers R, Haendiges J, Evans PS, Meng J, Strain EA, Allard MW, Brown EW. Tracing origins of the Salmonella Bareilly strain causing a food-borne outbreak in the United States. J Infect Dis 2016;213:502–508.
Inns T, Ashton PM, Herrera-Leon S, Lighthill J, Foulkes S, Jombart T, Rehman Y, Fox A, Dallman T, de Pinna E, Browning L, Coia JE, Edeghere O, Vivancos R. Prospective use of whole genome sequencing (WGS) detected a multi-country outbreak of Salmonella Enteritidis. Epidemiol Infect 2017;145:289–298.
Inns T, Lane C, Peters T, Dallman T, Chatt C, McFarland N, Crook P, Bishop T, Edge J, Hawker J, Elson R, Neal K, Adak GK, Cleary P; Outbreak Control Team. A multi-country Salmonella Enteritidis phage type 14b outbreak associated with eggs from a German producer: “Near real-time” application of whole genome sequencing and food chain investigations, United Kingdom, May to September 2014. Euro Surveill 2015;20:pii:.
Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, Guibourdench M, de Pinna E, Nair S, Fields PL, Weill FX. Supplement 2008–2010 (no. 48) to the White-Kauffmann-Le Minor scheme. Res Microbiol 2014;165:526–530.
Iwamoto M, Huang JY, Cronquist AB, Medus C, Hurd S, Zansky S, Dunn J, Woron AM, Oosmanally N, Griffin PM, Besser J, Henao OL; Centers for Disease Control and Prevention (CDC). Bacterial enteric infections detected by culture-independent diagnostic tests—FoodNet, United States, 2012–2014. MMWR Morb Mortal Wkly Rep 2015;64:252–257.
Jackson BR, Tarr C, Strain E, Jackson KA, Conrad A, Carleton H, Katz LS, Stroika S, Gould LH, Mody RK, Silk BJ, Beal J, Chen Y, Timme R, Doyle M, Fields A, Wise M, Tillman G, Defibaugh-Chavez S, Kucerova Z, Sabol A, Roache K, Trees E, Simmons M, Wasilenko J, Kubota K, Pouseele H, Klimke W, Besser J, Brown E, Allard M, Gerner-Smidt P. Implementation of nationwide real-time whole-genome sequencing to enhance listeriosis outbreak detection and investigation. Clin Infect Dis 2016;63:380–386.
Kirk M, Ford L, Glass K, Hall G. Foodborne illness, Australia, circa 2000 and circa 2010. Emerg Infect Dis 2014;20:1857–1864.
Leekitcharoenphon P, Nielsen EM, Kaas RS, Lund O, Aarestrup FM. Evaluation of whole genome sequencing for outbreak detection of Salmonella enterica. PLoS One 2014;9:e87991.
Lindstedt BA, Vardund T, Aas L, Kapperud G. Multiple-locus variable-number tandem-repeat analysis of Salmonella enterica subsp. enterica serovar Typhimurium using PCR multiplexing and multicolor capillary electrophoresis. J Microbiol Methods 2004;59:163–172.
Moffatt CR, Greig A, Valcanis M, Gao W, Seemann T, Howden BP, Kirk MD. A large outbreak of Campylobacter jejuni infection in a university college caused by chicken liver pate, Australia 2013. Epidemiol Infect 2016a;144:2971–2978.
Moffatt CR, Musto J, Pingault N, Miller M, Stafford R, Gregory J, Polkinghorne BG, Kirk MD. Salmonella Typhimurium and outbreaks of egg-associated disease in Australia, 2001 to 2011. Foodborne Pathog Dis 2016b;13:379–385.
OzFoodNet Working Group. Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: Annual report of the OzFoodNet network, 2011. Commun Dis Intell Q Rep 2015;39:E236–E264.
Taylor AJ, Lappi V, Wolfgang WG, Lapierre P, Palumbo MJ, Medus C, Boxrud D. Characterization of foodborne outbreaks of Salmonella enterica serovar Enteritidis with whole-genome sequencing single nucleotide polymorphism-based analysis for surveillance and outbreak detection. J Clin Microbiol 2015;53:334–3340.
Vally H, Glass K, Ford L, Hall G, Kirk MD, Shadbolt C, Veitch M, Fullerton KE, Musto J, Becker N. Proportion of illness acquired by foodborne transmission for nine enteric pathogens in Australia: An expert elicitation. Foodborne Pathog Dis 2014;11:727–733.
Wang Q, Holmes N, Martinez E, Howard P, Hill-Cawthorne G, Sintchenko V. It is not all about single nucleotide polymorphisms: Comparison of mobile genetic elements and deletions in Listeria monocytogenes genomes links cases of hospital-acquired listeriosis to the environmental source. J Clin Microbiol 2015;53:3492–3500.
Yokoyama E, Murakami K, Shiwa Y, Ishige T, Ando N, Kikuchi T, Murakami S. Phylogenetic and population genetic analysis of Salmonella enterica subsp. enterica serovar Infantis strains isolated in Japan using whole genome sequencing data. Infect Genet Evol 2014;27:62–68.
Information & Authors
Information
Published In
Foodborne Pathogens and Disease
Volume 15 • Issue Number 3 • March 2018
Pages: 161 - 167
PubMed: 29336594
Copyright
Copyright 2018, Mary Ann Liebert, Inc.
History
Published in print: March 2018
Published online: 1 March 2018
Published ahead of print: 16 January 2018
Topics
Authors
Disclosure Statement
No competing financial interests exist.
Metrics & Citations
Metrics
Citations
Export Citation
Export citation
Select the format you want to export the citations of this publication.
View Options
Get Access
Access content
To read the fulltext, please use one of the options below to sign in or purchase access.⚠ Society Access
If you are a member of a society that has access to this content please log in via your society website and then return to this publication.