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The Epidemiology of Salmonella Transmission in Chicken Meat

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The Epidemiology of Salmonella Transmission in Chicken Meat The Epidemiology of Salmonella Transmission in Chicken Meat Helen Kathleen Crabb March 2018 ORCID: 0000-0001-5550-3834 Submitted in total fulfilment of the requirements of the degree Doctor of Philosophy Melbourne Veterinary School Faculty of Agriculture and Veterinary Sciences University of Melbourne i Abstract longitudinal study was conducted between January 2013 and cluster with the human cases, and the large number of isolates used A September 2014 in a vertically integrated chicken meat enter- for comparison strongly support these findings. Bovine and non- prise under commercial farming conditions. Using methods routine- study poultry isolates were more tightly clustered with the human ly used for Salmonella surveillance in poultry production systems, en- cases, but the remaining non-human data was so sparse that fur- vironmental sampling was conducted in two generations (parent and ther resolution for source attribution was lost due to small sample broiler) at multiple locations within the production system. Data was size and the necessary aggregation of isolates from multiple sourc- collected on all product movements during the study period and so- es. These results highlight the extreme limitations of using passive cial network analysis was used to describe product movements and surveillance data to make conclusions on source attribution in the identify locations for the potential introduction and dissemination absence of strong epidemiological evidence. of Salmonella and targets for enhanced surveillance and intervention. In conclusion, this study identified that the structure of a vertically Of the 4,219 samples collected thirty six percent were positive for integrated enterprise enhanced the transmission of Salmonella be- Salmonella. Sixty-five percent of the isolates were identified as S. Ty- tween poultry generations and locations, even at very low preva- phimurium and of these isolates, 8 phage types (PT), 41 multi-lo- lence, and that the hatchery is a critical point of amplification. The cus variable-number tandem-repeats analysis (MLVA) profiles and use of phenotyping (phage typing) and genotyping (MLVA) tools 62 PT/MLVA combinations were detected. There was no difference are not sufficient in the absence of good sampling (methodology between locations in the variant assemblage of these isolates and all or intensity) or epidemiological evidence to determine the source were detected at the parent generation prior to detection in subse- of introduction or dissemination within a complex environment. quent locations or generations indicating the parent site was the most Whole genome sequencing allowed the genetic relatedness of the S. likely point of introduction and dissemination to the rest of the en- Typhimurium isolates to be elucidated and confirmed that transmis- terprise. Phenotyping (serotyping and phage typing) and genotyp- sion was occurring between generations within the enterprise with ing using MLVA profiling indicated that the introduction of at least little to no change. 13 different S. Typhimurium isolates may have occurred during the Finally, diversity and cluster analysis findings suggest that these sal- study but the genetic relatedness of the variants remained unknown. monellae were not a significant source of infection to the human Whole genome sequencing identified two major lineages of S. Typh- population during the study period. Further analysis of human and imurium that were clonally disseminated between each generation non-human isolates via whole genome sequencing is warranted to and location within the study under purifying selection. Both lineag- confirm these findings. es entered the enterprise at the same time and were present for the duration of the study. Single isolates of three unique S. Typhimuri- um genomes were also identified. Phenotyping failed to differentiate these isolates from the two major lineages; rather than 13 introduc- tions, 5 introductions had occurred during the study. Of critical importance is understanding if the Salmonella transmitted between generations within the poultry operation contributed to hu- man infection for the concurrent period. De-identified human and Next: Declaration non-human S. Typhimurium case submitted to the National Enteric It is all mine, I promise Pathogen Surveillance Scheme (NEPSS) database for the period of the longitudinal study were obtained for comparative analysis. It was identified that, phage type and MLVA profile were poorly correlated particularly for the major phage types, which comprised greater than 90% of all isolates. The isolates from this study did not significantly ii iii Declaration This is to certify that: i. This thesis comprises only my original work towards the PhD except where indicated in the Preface, ii. Due acknowledgement has been made in the text to all other material used. iii. This thesis is fewer than 100,000 words in length, exclusive of tables, maps, bibliographies and appendices. Signature: Helen K Crabb Next: Preface Information on publications and papers in progress. Conference atten- dences and talks about the content of this thesis. iv v Preface PUBLICATIONS (PUBLISHED/SUBMITTED/IN PROGRESS) International One Health Congress, Saskatoon, 22-25 June 2018, Canada Crabb, H. K., Allen, J. L., Devlin, J. M., Firestone, S. M., Steven- son, M. A., Gilkerson, J. R. (2018). The use of social network analysis Crabb, H. K., Allen, J. L., Devlin, J. M., Gilkerson, J. R. The more to examine the transmission of Salmonella spp. within a vertically inte- we do the less we know: Intensive sampling fails to identify clonal disse- grated broiler enterprise. Food Microbiology, 71 (5) , 73-81. Chap- mination of antibiotic resistance genes in poultry. Antimicrobials 2018. ter 3 22-24 February 2018, Brisbane, Australia Crabb, H. K., Allen, J. L., Devlin, J. M., Firestone, S. M., Wilks, C. Crabb, H. K. Understanding Salmonella transmission in poultry using R., Gilkerson, J. R. Salmonella spp. transmission in a vertically inte- whole genome sequencing. Australian Veterinary Association Confe- grated poultry operation: Clustering and diversity analysis using pheno- rence. 13-18 May 2018, Brisbane, Australia. typing (phage typing) and genotyping (MLVA). PlosONE. Accepted for publication. Chapter 4 Crabb H. K., Allen, J. L., Devlin, J. M., Firestone, S., Holt, K, Gilker- son. J. R. Comparing phenotyping and whole genome sequencing UNPUBLISHED MATERIAL in understanding the epidemiology of Salmonella spp. transmission in a vertically integrated broiler operation. International Symposium on Crabb, H. K., Allen, J. L., Devlin, J. M., Wilks, C. R., Gilkerson, J. Salmonella and Salmonellosis. 06 - 08 June 2016. St Malo, France. R. The effectiveness of sampling in colony cage environments; envi- ronmental factors affecting Sslmonella detection. In preparation for Crabb, H. K., Allen, J. L., Devlin, J. M., Firestone, S. M., Stevenson, submission to Applied Environmental Microbiology: Chapter 5 M. A., Gilkerson. J. R. The use of social network analysis to examine the transmission of Salmonella spp. within a vertically integrated broiler Crabb, H. K., Devlin, J. M., Wilks, C. R., Gilkerson, J. R. Diver- production system. International Symposium Salmonella and Salmo- sity analysis of Salmonella spp. isolates by location. In preparation nellosis. 06 - 08 June 2016. St Malo, France. for submission to Applied Environmental Microbiology: Chapter 6 Crabb, H. K., Firestone, S. M., Allen, J. L., Devlin, J. M., Valca- Crabb, H. K., Allen, J. L., Devlin, J. M., Wilks, C. R., Holt, K., nis, M., Holt, K., Gilkerson. J. R. A comparison of serotyping, phage Gilkerson, J. R. Comparison of Salmonella Typhimurium isola- typing, MLVA and whole genome sequencing for describing relationships tes using bioinformatics tools: poultry isolates. In Preparation for between Salmonella isolates of human and poultry origin in the food submission: Chapter 7 chain. Australasian Veterinary Poultry Association Meeting, 11 – 14 October 2015, Queenstown, New Zealand. Crabb, H. K., Allen, J. L., Devlin, J. M., Firestone, S. M., Steven- son, M. A., Wilks, C. R, Gilkerson, J. R. A comparison of Salmonella Crabb, H. K., Firestone, S. M., Allen, J. L., Devlin, J. M., Valca- Typhimurium isolates using diversity analysis: human and non-hu- nis, Ms., Holt, K., Gilkerson. J. R. A comparison of serotyping, phage man isolates. In preparation for submission to Emerging Infectious typing, MLVA and whole genome sequencing for describing relationships Diseases: Chapter 8 between Salmonella isolates of human and poultry origin in the food chain. 3rd International One Health Congress, 15 - 18 March 2015. Lead author was responsible for concept, study design, field and Amsterdam, Netherlands. laboratory sample collection and processing, methodology, data collection and analysis, and writing of the manuscript(s). Co-au- Crabb, H. K., Devlin, J. M., Firestone, S. M., Allen, J. L., Gilker- thors were responsible for sourcing funding, supervision, and revi- son. J. R. Pilot Study: Comparison of different sampling methods for sion of the draft manuscript(s). the detection of Salmonella spp. in poultry sheds. Australian Associa- tion of Veterinary Laboratory Diagnosticians Meeting. 28 Novem- Next: Acknowledgements ber 2013. Geelong, Australia. Special thanks to all my supervisors CONFERENCE PRESENTATIONS (ACCEPTED/PRESENTED) and people that helped on the jour- FUNDING SOURCES ney to completion. Abstract text for all conference presentations in Appendix B. This work was supported by
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