Rapid geographical source attribution of Salmonella enterica serovar Enteritidis genomes using hierarchical machine learning

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Abstract

Salmonella enterica serovar Enteritidis is one of the most frequent causes of Salmonellosis globally and is commonly transmitted from animals to humans by the consumption of contaminated foodstuffs. In the UK and many other countries in the Global North, a significant proportion of cases are caused by consumption of imported food products or contracted during foreign travel, therefore making the rapid identification of the geographical source of new infections a requirement for robust public health outbreak investigations. Herein, we detail the development and application of a hierarchical machine learning model to rapidly identify and trace the geographical source of S. Enteritidis infections from whole genome sequencing data. 2,313 S. Enteritidis genomes, collected by the UKHSA between 2014-2019, were used to train a 'local classifier per node' hierarchical classifier to attribute isolates to 4 continents, 11 sub-regions and 38 countries (53 classes). The highest classification accuracy was achieved at the continental level followed by the sub-regional and country levels (macro F1: 0.954, 0.718, 0.661 respectively). A number of countries commonly visited by UK travellers were predicted with high accuracy (hF1: >0.9). Longitudinal analysis and validation with publicly accessible international samples indicated that predictions were robust to prospective external datasets. The hierarchical machine learning framework provided granular geographical source prediction directly from sequencing reads in <4 minutes per sample, facilitating rapid outbreak resolution and real-time genomic epidemiology. The results suggest additional application to a broader range of pathogens and other geographically structured problems, such as antimicrobial resistance prediction, is warranted.

Data availability

The final optimised hierarchical model as well as a pipeline for pre-processing raw read data to unitigs/patterns for input and paper data is available from https://github.com/SionBayliss/HierarchicalML with a short description and tutorial for ease of use. This end-to-end process, from FASTQ to prediction, is open access and available to users under GNU GPL licence . This depository also includes the preprocessed unitig datasets and resulting predictions. Short read sequencing data is available from the Sequence Read Archive (Bioproject: PRJNA248792). Please not that the sequence data has been previously deposited/published in the Sequence Read Archive by PHE/UKHSA and was not generated for this project.

The following previously published data sets were used

1. UKHSA
(2018) Public Health England - Salmonella
NCBI SRA: PRJNA248792.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA248792
(2018) Retrospective genome-wide comparisons of Salmonella enterica serovar Enteritidis from suspected outbreaks in Singapore
NCBI SRA: PRJNA434621.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA434621
1. Smith AM
2. Tau NP
3. Ngomane HM
4. Sekwadi P
5. Ramalwa N
6. Moodley K
7. Govind C
8. Khan S
9. Archary M
10. Thomas J.
(2020) Whole-genome sequencing to investigate two concurrent outbreaks of Salmonella Enteritidis in South Africa, 2018
NCBI SRA: PRJNA646325.

https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA646325

Article and author information

Author details

Sion C Bayliss

Bristol Veterinary School, University of Bristol, Bristol, United Kingdom

For correspondence
s.bayliss@bristol.ac.uk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5997-2002
Rebecca K Locke

Life Sciences Department, University of Bath, Bath, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Claire Jenkins

Gastrointestinal Reference Services, UK Health Security Agency, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Marie Anne Chattaway

Gastrointestinal Reference Services, UK Health Security Agency, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Timothy J Dallman

Institute for Risk Assessment Sciences, Utrecht University, Utrecht, Netherlands

Competing interests
The authors declare that no competing interests exist.
Lauren A Cowley

Life Sciences Department, University of Bath, Bath, United Kingdom

Competing interests
The authors declare that no competing interests exist.

Funding

Academy of Medical Sciences (SBF005\1089)

Lauren A Cowley

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.