Phylogeographic analysis reveals multiple international transmission events have driven the global emergence of Escherichia coli O157:H7

Authors: FRANZ, EELCO - National Institute For Public Health And The Environment (RIVM); ROTARIU, OVIDIU - University Of Aberdeen; LOPES, BRUNO - National Institute For Public Health And The Environment (RIVM); MACRAE, MARION - University Of Aberdeen; Bono, James - Jim; LAING, CHAD - Public Health Agency Of Canada; GANNON, VICTOR - Public Health Agency Of Canada; SODERLUND, ROBERT - Swedish University Of Agricultural Sciences; VAN HOEK, ANGELA H.A.M. - National Institute For Public Health And The Environment (RIVM); FRIESEMA, INGRID - National Institute For Public Health And The Environment (RIVM); FRENCH, NIGEL - Massey University; GEORGE, TESSY - Massey University; BIGGS, PATRICK - Massey University; JAROS, PATRICIA - Massey University; RIVAS, MARTA - National Laboratories And Institutes Of Health (ANLIS); CHINEN, ISABEL - National Laboratories And Institutes Of Health (ANLIS); CAMPOS, JOSEFINA - National Laboratories And Institutes Of Health (ANLIS); JERNBERG, CECILIA - The Public Health Agency Of Sweden; GOBIUS, KARI - Commonwealth Scientific And Industrial Research Organisation (CSIRO); MELLOR, GLEN - Commonwealth Scientific And Industrial Research Organisation (CSIRO); CHANDRY, P SCOTT - Commonwealth Scientific And Industrial Research Organisation (CSIRO); PEREZ-RECHE, FRANCISCO - University Of Aberdeen; FORBES, KEN - University Of Aberdeen; STRACHAN, NORVAL J C - University Of Aberdeen

Submitted to: Clinical Infectious Diseases
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/3/2018
Publication Date: 8/1/2019
Citation: Franz, E., Rotariu, O., Lopes, B.S., MacRae, M., Bono, J.L., Laing, C., Gannon, V., Söderlund, R., van Hoek, A., Friesema, I., French, N.P., George, T., Biggs, P.J., Jaros, P., Rivas, M., Chinen, I., Campos, J., Jernberg, C., Gobius, K., Mellor, G.E., Chandry, P., Perez-Reche, F., Forbes, K.J., Strachan, N. 2019. Phylogeographic analysis reveals multiple international transmission events have driven the global emergence of Escherichia coli O157:H7. Clinical Infectious Diseases. 69(3):428-437. https://doi.org/10.1093/cid/ciy919.
DOI: https://doi.org/10.1093/cid/ciy919

Interpretive Summary: Shiga toxin-containing Escherichia coli O157:H7 is a zoonotic pathogen which has caused numerous food and waterborne disease outbreaks worldwide. It is globally distributed but how it spread geographical is unknown. To answer this question, the genomes from 757 isolates from four continents were used in computer simulations to identify the country of origin and subsequent spread. The common ancestor originated from The Netherlands and was transmitted to other countries including Australia, the United States of America, and Canada. The most likely route of transmission is by intercontinental shipping of cattle. This information will provide a model for disease emergence and subsequent transmission of zoonotic pathogens to help identify high risk countries in the current global economy.

Technical Abstract: Background. Shiga toxin–producing Escherchia coli (STEC) O157:H7 is a zoonotic pathogen that causes numerous food and waterborne disease outbreaks. It is globally distributed, but its origin and the temporal sequence of its geographical spread are unknown. Methods. We analyzed whole-genome sequencing data of 757 isolates from 4 continents, and performed a pan-genome analysis to identify the core genome and, from this, extracted single-nucleotide polymorphisms. A timed phylogeographic analysis was performed on a subset of the isolates to investigate its worldwide spread. Results. The common ancestor of this set of isolates occurred around 1890 (1845–1925) and originated from the Netherlands. Phylogeographic analysis identified 34 major transmission events. The earliest were predominantly intercontinental, moving from Europe to Australia around 1937 (1909–1958), to the United States in 1941 (1921–1962), to Canada in 1960 (1943–1979), and from Australia to New Zealand in 1966 (1943–1982). This pre-dates the first reported human case of E. coli O157:H7, which was in 1975 from the United States. Conclusions. Inter- and intra-continental transmission events have resulted in the current international distribution of E. coli O157:H7, and it is likely that these events were facilitated by animal movements (eg, Holstein Friesian cattle). These findings will inform policy on action that is crucial to reduce the further spread of E. coli O157:H7 and other (emerging) STEC strains globally.