Globetrotting strangles: the unbridled national and international transmission of Streptococcus equi between horses

Hayley Wilson (1, 2) , Catriona Mitchell (1) , Karen Steward (1, 3) , Amelia Charbonneau (1, 4) , Saoirse Walsh (1, 5) , John Timoney (6) , Ulli Wernery (7) , Marina Joseph (7) , David Craig (8) , Kees van Maanen (9) , Annelies Hoogkamer-van Gennep (9) , Albertine Léon (10, 11) , Lucjan Witkowski (12) , Magdalena Rzewuska (12) , Ilona Stefańska (12) , Gunther van Loon (13) , Ray Cursons (14) , Olivia Patty (14) , Els Acke (15) , James Gilkerson (16) , Charles El-Hage (16) , Joanne Allen (17) , Hiroshi Bannai (17) , Yuta Kinoshita (17) , Hidekazu Niwa (17) , Teótimo Becú (18) , John Pringle (19) , Bengt Guss (19) , Reinhard Böse (20) , Yvonne Abbott (21) , Lisa Katz (21) , Bernadette Leggett (21) , Tom Buckley (22) , Shlomo Blum (23) , Fátima Cruz López (24) , Ana Fernández Ros (25) , Maria Cristina Marotti Campi (26) , Silvia Preziuso (27) , Carl Robinson (1) , J. Richard Newton (1) , Ellen Schofield (1, 2) , Ben Brooke (1) , Mike Boursnell (1) , Nicolas de Brauwere (28) , Roxane Kirton (28, 29) , Charlotte Barton (30) , Khalil Abudahab (31, 32) , Ben Taylor (31, 32) , Corin Yeats (31, 32) , Richard Goater (31, 32) , David Aanensen (31, 32) , Simon Harris (31, 33) , Julian Parkhill (2) , Matthew Holden (31, 34) , Andrew Waller (1, 35, 19)

1 AHT - Animal Health Trust
2 CAM - University of Cambridge [UK]
3 Technology Networks
4 Xampla
5 FU - Free University of Berlin
6 Department of Veterinary Science, Gluck Equine Research Center
7 CVRL - Central Veterinary Research Laboratory
8 Emirates Racing Authority
9 Animal Health Service (GD)
10 LABÉO - LABÉO, Pôle d’analyses et de recherche de Normandie
11 U2RM - Unité de Recherche Risques Microbiens
12 Institute of Veterinary Medicine
13 UGENT - Universiteit Gent = Ghent University
14 University of Waikato [Hamilton]
15 Massey University
16 University of Melbourne
17 Japan Racing Association
18 Clinica Equina Buenos Aires
19 Department of Biomedical Sciences and Veterinary Public Health
20 Labor Dr Böse GmbH
21 UCD - University College Dublin [Dublin]
22 IEC - Irish Equine Centre
23 KVI - Kimron Veterinary Institute
24 Facultad de Veterinaria, Universidad Complutense
25 Exopol Zaragoza
26 Al Khalediah Equine Hospital
27 UNICAM - Università degli Studi di Camerino = University of Camerino
28 Redwings Horse Sanctuary
29 Royal Society for the Prevention of Cruelty to Animals
30 Weatherford Equine Medical Centre
31 Centre for Genomic Pathogen Surveillance
32 Big Data Institute - Nuffield Department of Medicine [Oxford, UK]
33 Microbiotica Limited
34 University of St Andrews [Scotland]
35 Intervacc AB

Background: Streptococcus equi subspecies equi (S.equi) is the cause of the highly contagious equine respiratory disease ‘strangles’. Approximately 10% of recovered animals can persistently carry the bacteria and transmit it to naïve animals. The global movement of horses is an ideal mechanism for widespread transmission to geographically distant locations.Objectives: Utilise whole-genome sequence data to disentangle the transmission of S. equi and subsequent outbreaks of strangles.Study design: In vitro analysis of micro-organisms.Methods: Isolates (n = 670) of S. equi were recovered from clinical samples submitted to multiple collaborating clinics and institutions globally. Following species confirmation, isolates underwent whole-genome sequencing using Illumina technology. Sequence reads passing quality control measures were assembled and uploaded to Pathogenwatch, which assigned a phylogeny based upon sequences of core genome alleles. Population structure was inferred using the population mixture analysis in BAPS.Results: BAPS clustered the isolates into six different clusters (BAPS 1-6) and showed dominant lineages in different geographical areas but also global transmission within the clusters. Sub-groups within the clusters highlighted multiple outbreaks at local, national and international scales and highlighted population structures and transmission dynamics within single locations. For example, four different strains collected over just seven months were identified in a single location. Sequence data also identified a statistically significant decline in BAPS-5 since 2010.Main limitations: Pathogenwatch has shown its utility in investigating S. equi transmission and population structure. However, it is based upon a curated set of 1286 core genome loci. Further investigations will need to be conducted using the full spectrum of data available from whole-genome sequencing.Conclusions: Pathogenwatch was used as a tool to rapidly identify and visualise the whole-genome sequence data of a large S. equi dataset. The data demonstrate widespread transmission of multiple S. equi lineages and provide strong evidence that asymptomatic carrier horses are perpetuating this dissemination.

Keywords: Streptococcus equi; genome diversity; pandemic; strangles; transmission

Domains: Life Sciences [q-bio]; Animal biology; Veterinary medicine and animal Health

Hayley Wilson, Catriona Mitchell, Karen Steward, Amelia Charbonneau, Saoirse Walsh, et al.. Globetrotting strangles: the unbridled national and international transmission of Streptococcus equi between horses. 11th International Equine Infectious Diseases Conference, Sep 2021, Online, France. pp.20-21, ⟨10.1111/evj.17_13495⟩. ⟨hal-03375144⟩