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

Eelco Franz; Ovidiu Rotariu; Bruno S. Lopes; Marion Macrae; James L. Bono; Chad Laing; Victor Gannon; Robert Söderlund; Angela H.A.M. Van Hoek; Ingrid Friesema; Nigel P. French; Tessy George; Patrick J. Biggs; Patricia Jaros; Marta Rivas; Isabel Chinen; Josefina Campos; Cecilia Jernberg; Kari Gobius; Glen E. Mellor; P. Scott Chandry; Francisco Perez-Reche; Ken J. Forbes; Norval J.C. Strachan

doi:10.1093/cid/ciy919

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

Eelco Franz, Ovidiu Rotariu, Bruno S. Lopes, Marion Macrae, James L. Bono, Chad Laing, Victor Gannon, Robert Söderlund, Angela H.A.M. Van Hoek, Ingrid Friesema, Nigel P. French, Tessy George, Patrick J. Biggs, Patricia Jaros, Marta Rivas, Isabel Chinen, Josefina Campos, Cecilia Jernberg, Kari Gobius, Glen E. MellorP. Scott Chandry, Francisco Perez-Reche, Ken J. Forbes, Norval J.C. Strachan^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

18 Citations (Scopus)

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Abstract

Background
Shiga toxin-producing Escherchia coli O157:H7 is a zoonotic pathogen which causes numerous food and waterborne disease outbreaks. It is globally distributed but its origin and temporal sequence of geographical spread is unknown.

Methods
We analysed 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. Timed phylogeographic analysis was performed on a subset of the isolates to investigate it’s 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 from Europe to Australia around 1937 (1909-1958), to USA 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 in 1975 from the USA.

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 (e.g. Holstein Friesian cattle). These findings will inform policy on action that is crucial to reduce further spread of E. coli O157:H7 and other (emerging) STEC strains globally.

Original language	English
Pages (from-to)	428-437
Number of pages	10
Journal	Clinical Infectious Diseases
Volume	69
Issue number	3
Early online date	29 Oct 2018
DOIs	https://doi.org/10.1093/cid/ciy919
Publication status	Published - 1 Aug 2019

Keywords

infectious diseases
STEC
whole genome sequencing
phylogeography
E. coli O157
whole-genome sequencing
CATTLE
SPREAD
HISTORY

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1093/cid/ciy919Licence: Unspecified

Accepted Manuscript
This is a pre-copyedited, author-produced version of an article accepted for publication in Clinical Infectious Diseases following peer review. The version of record Eelco Franz, Ovidiu Rotariu, Bruno S Lopes, Marion MacRae, James L Bono, Chad Laing, Victor Gannon, Robert Söderlund, Angela H A M van Hoek, Ingrid Friesema, Nigel P French, Tessy George, Patrick J Biggs, Patricia Jaros, Marta Rivas, Isabel Chinen, Josefina Campos, Cecilia Jernberg, Kari Gobius, Glen E Mellor, P Scott Chandry, Francisco Perez-Reche, Ken J Forbes, Norval J C Strachan, Phylogeographic Analysis Reveals Multiple International transmission Events Have Driven the Global Emergence of Escherichia coli O157:H7, Clinical Infectious Diseases, Volume 69, Issue 3, 1 August 2019, Pages 428–437, is available online at: https://academic.oup.com/cid/article/69/3/428/5146342
Accepted author manuscript, 1.19 MBLicence: Other

Cite this

Franz, E., Rotariu, O., Lopes, B. S., Macrae, M., Bono, J. L., Laing, C., Gannon, V., Söderlund, R., Van Hoek, A. H. A. M., Friesema, I., French, N. P., George, T., Biggs, P. J., Jaros, P., Rivas, M., Chinen, I., Campos, J., Jernberg, C., Gobius, K., ... Strachan, N. J. C. (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

Franz, E, Rotariu, O, Lopes, BS, Macrae, M, Bono, JL, Laing, C, Gannon, V, Söderlund, R, Van Hoek, AHAM, Friesema, I, French, NP, George, T, Biggs, PJ, Jaros, P, Rivas, M, Chinen, I, Campos, J, Jernberg, C, Gobius, K, Mellor, GE, Chandry, PS, Perez-Reche, F, Forbes, KJ & Strachan, NJC 2019, 'Phylogeographic analysis reveals multiple international transmission events have driven the global emergence of Escherichia coli O157:H7', Clinical Infectious Diseases, vol. 69, no. 3, pp. 428-437. https://doi.org/10.1093/cid/ciy919

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

abstract = "BackgroundShiga toxin-producing Escherchia coli O157:H7 is a zoonotic pathogen which causes numerous food and waterborne disease outbreaks. It is globally distributed but its origin and temporal sequence of geographical spread is unknown.MethodsWe analysed 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. Timed phylogeographic analysis was performed on a subset of the isolates to investigate it{\textquoteright}s worldwide spread.ResultsThe 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 from Europe to Australia around 1937 (1909-1958), to USA 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 in 1975 from the USA.ConclusionsInter- 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 (e.g. Holstein Friesian cattle). These findings will inform policy on action that is crucial to reduce further spread of E. coli O157:H7 and other (emerging) STEC strains globally.",

keywords = "infectious diseases, STEC, whole genome sequencing, phylogeography, E. coli O157, whole-genome sequencing, CATTLE, SPREAD, HISTORY",

author = "Eelco Franz and Ovidiu Rotariu and Lopes, {Bruno S.} and Marion Macrae and Bono, {James L.} and Chad Laing and Victor Gannon and Robert S{\"o}derlund and {Van Hoek}, {Angela H.A.M.} and Ingrid Friesema and French, {Nigel P.} and Tessy George and Biggs, {Patrick J.} and Patricia Jaros and Marta Rivas and Isabel Chinen and Josefina Campos and Cecilia Jernberg and Kari Gobius and Mellor, {Glen E.} and Chandry, {P. Scott} and Francisco Perez-Reche and Forbes, {Ken J.} and Strachan, {Norval J.C.}",

note = "This work was supported by: Scotland by Food Standards Scotland [Grant Number FS102029] and University of Aberdeen; New Zealand, Institute of Environmental Science and Research; Canada, the Public Health Agency of Canada; United States, United States Department of Agriculture",

year = "2019",

month = aug,

day = "1",

doi = "10.1093/cid/ciy919",

language = "English",

volume = "69",

pages = "428--437",

journal = "Clinical Infectious Diseases",

issn = "1058-4838",

publisher = "Oxford University Press",

number = "3",

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T1 - Phylogeographic analysis reveals multiple international transmission events have driven the global emergence of Escherichia coli O157:H7

AU - Franz, Eelco

AU - Rotariu, Ovidiu

AU - Lopes, Bruno S.

AU - Macrae, Marion

AU - Bono, James L.

AU - Laing, Chad

AU - Gannon, Victor

AU - Söderlund, Robert

AU - Van Hoek, Angela H.A.M.

AU - Friesema, Ingrid

AU - French, Nigel P.

AU - George, Tessy

AU - Biggs, Patrick J.

AU - Jaros, Patricia

AU - Rivas, Marta

AU - Chinen, Isabel

AU - Campos, Josefina

AU - Jernberg, Cecilia

AU - Gobius, Kari

AU - Mellor, Glen E.

AU - Chandry, P. Scott

AU - Perez-Reche, Francisco

AU - Forbes, Ken J.

AU - Strachan, Norval J.C.

N1 - This work was supported by: Scotland by Food Standards Scotland [Grant Number FS102029] and University of Aberdeen; New Zealand, Institute of Environmental Science and Research; Canada, the Public Health Agency of Canada; United States, United States Department of Agriculture

PY - 2019/8/1

Y1 - 2019/8/1

N2 - BackgroundShiga toxin-producing Escherchia coli O157:H7 is a zoonotic pathogen which causes numerous food and waterborne disease outbreaks. It is globally distributed but its origin and temporal sequence of geographical spread is unknown.MethodsWe analysed 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. Timed phylogeographic analysis was performed on a subset of the isolates to investigate it’s worldwide spread.ResultsThe 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 from Europe to Australia around 1937 (1909-1958), to USA 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 in 1975 from the USA.ConclusionsInter- 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 (e.g. Holstein Friesian cattle). These findings will inform policy on action that is crucial to reduce further spread of E. coli O157:H7 and other (emerging) STEC strains globally.

AB - BackgroundShiga toxin-producing Escherchia coli O157:H7 is a zoonotic pathogen which causes numerous food and waterborne disease outbreaks. It is globally distributed but its origin and temporal sequence of geographical spread is unknown.MethodsWe analysed 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. Timed phylogeographic analysis was performed on a subset of the isolates to investigate it’s worldwide spread.ResultsThe 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 from Europe to Australia around 1937 (1909-1958), to USA 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 in 1975 from the USA.ConclusionsInter- 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 (e.g. Holstein Friesian cattle). These findings will inform policy on action that is crucial to reduce further spread of E. coli O157:H7 and other (emerging) STEC strains globally.

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KW - STEC

KW - whole genome sequencing

KW - phylogeography

KW - E. coli O157

KW - whole-genome sequencing

KW - CATTLE

KW - SPREAD

KW - HISTORY

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JO - Clinical Infectious Diseases

JF - Clinical Infectious Diseases

SN - 1058-4838

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

Abstract

Keywords

UN SDGs

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Norval Strachan

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

Abstract

Keywords

UN SDGs

Access to Document

Other files and links

Fingerprint

Profiles

Norval Strachan

Cite this