The evolution and international spread of extensively drug resistant Shigella sonnei

Lewis C.E. Mason; David R. Greig; Lauren A. Cowley; Sally R. Partridge; Elena Martinez; Grace A. Blackwell; Charlotte E. Chong; P. Malaka De Silva; Rebecca J. Bengtsson; Jenny L. Draper; Andrew N. Ginn; Indy Sandaradura; Eby M. Sim; Jonathan R. Iredell; Vitali Sintchenko; Danielle J. Ingle; Benjamin P. Howden; Sophie Lefèvre; Elisabeth Njampeko; François Xavier Weill; Pieter Jan Ceyssens; Claire Jenkins; Kate S. Baker

doi:10.1038/s41467-023-37672-w

The evolution and international spread of extensively drug resistant Shigella sonnei

Lewis C.E. Mason, David R. Greig, Lauren A. Cowley, Sally R. Partridge, Elena Martinez, Grace A. Blackwell, Charlotte E. Chong, P. Malaka De Silva, Rebecca J. Bengtsson, Jenny L. Draper, Andrew N. Ginn, Indy Sandaradura, Eby M. Sim, Jonathan R. Iredell, Vitali Sintchenko, Danielle J. Ingle, Benjamin P. Howden, Sophie Lefèvre, Elisabeth Njampeko, François Xavier WeillPieter Jan Ceyssens, Claire Jenkins, Kate S. Baker

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18 Citations (SciVal)

Abstract

Shigella sonnei causes shigellosis, a severe gastrointestinal illness that is sexually transmissible among men who have sex with men (MSM). Multidrug resistance in S. sonnei is common including against World Health Organisation recommended treatment options, azithromycin, and ciprofloxacin. Recently, an MSM-associated outbreak of extended-spectrum β-lactamase producing, extensively drug resistant S. sonnei was reported in the United Kingdom. Here, we aimed to identify the genetic basis, evolutionary history, and international dissemination of the outbreak strain. Our genomic epidemiological analyses of 3,304 isolates from the United Kingdom, Australia, Belgium, France, and the United States of America revealed an internationally connected outbreak with a most recent common ancestor in 2018 carrying a low-fitness cost resistance plasmid, previously observed in travel associated sublineages of S. flexneri. Our results highlight the persistent threat of horizontally transmitted antimicrobial resistance and the value of continuing to work towards early and open international sharing of genomic surveillance data.

Original language	English
Article number	1983
Number of pages	1
Journal	Nature Communications
Volume	14
Issue number	1
Early online date	8 Apr 2023
DOIs	https://doi.org/10.1038/s41467-023-37672-w
Publication status	Published - 30 Apr 2023

Bibliographical note

Data availability
Sequence data relating to all isolates has been deposited in the Sequence Read Archive under BioProject numbers PRJNA315192 (United Kingdom), PRJEB44801 (France), PRJEB40097 (Belgium), and PRJNA613115 (Australia, New South Wales). Individual isolate accession numbers and isolate metadata are available in the Supplementary Data 1 as indicated in the text. Correspondence regarding isolates from the United Kingdom and the overall study should be directed to Dr. Claire Jenkins and Professor Kate Baker. Correspondence regarding isolates: from France should be directed to Professor François-Xavier Weill; from Belgium should be directed to Pieter-Jan Ceyssens; from the United States of America should be directed to Kaitlin Tagg or PulseNet; and from Australia to Ben Howden and Danielle Ingle (Victoria) or Elena Martinez or Jonathan Iredell (New South Wales).

This study was funded by the National Institute for Health and Care Research (NIHR) Health Protection Research Unit in Gastrointestinal Infections, a partnership between the UK Health Security Agency, the University of Liverpool, and the University of Warwick. The views expressed are those of the author(s) and not necessarily those of the NIHR, the UK Health Security Agency or the Department of Health and Social Care. The authors thank Hattie Webb, Kaitlin Tagg, Jason Folster, Jean Whichard, and other staff at the United States Centres for Disease Control for helpful discussions to guide access to genome data from PulseNet. The authors are also grateful to pathology laboratories that provided isolates for genomic surveillance. This work was also supported by MRC and BBSRC grants held by KSB (MR/R020787/1 and BB/V009184/1, respectively).

ASJC Scopus subject areas

General Chemistry
General Biochemistry,Genetics and Molecular Biology
General
General Physics and Astronomy

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Mason, L. C. E., Greig, D. R., Cowley, L. A., Partridge, S. R., Martinez, E., Blackwell, G. A., Chong, C. E., De Silva, P. M., Bengtsson, R. J., Draper, J. L., Ginn, A. N., Sandaradura, I., Sim, E. M., Iredell, J. R., Sintchenko, V., Ingle, D. J., Howden, B. P., Lefèvre, S., Njampeko, E., ... Baker, K. S. (2023). The evolution and international spread of extensively drug resistant Shigella sonnei. Nature Communications, 14(1), Article 1983. https://doi.org/10.1038/s41467-023-37672-w

Mason, LCE, Greig, DR, Cowley, LA, Partridge, SR, Martinez, E, Blackwell, GA, Chong, CE, De Silva, PM, Bengtsson, RJ, Draper, JL, Ginn, AN, Sandaradura, I, Sim, EM, Iredell, JR, Sintchenko, V, Ingle, DJ, Howden, BP, Lefèvre, S, Njampeko, E, Weill, FX, Ceyssens, PJ, Jenkins, C & Baker, KS 2023, 'The evolution and international spread of extensively drug resistant Shigella sonnei', Nature Communications, vol. 14, no. 1, 1983. https://doi.org/10.1038/s41467-023-37672-w

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abstract = "Shigella sonnei causes shigellosis, a severe gastrointestinal illness that is sexually transmissible among men who have sex with men (MSM). Multidrug resistance in S. sonnei is common including against World Health Organisation recommended treatment options, azithromycin, and ciprofloxacin. Recently, an MSM-associated outbreak of extended-spectrum β-lactamase producing, extensively drug resistant S. sonnei was reported in the United Kingdom. Here, we aimed to identify the genetic basis, evolutionary history, and international dissemination of the outbreak strain. Our genomic epidemiological analyses of 3,304 isolates from the United Kingdom, Australia, Belgium, France, and the United States of America revealed an internationally connected outbreak with a most recent common ancestor in 2018 carrying a low-fitness cost resistance plasmid, previously observed in travel associated sublineages of S. flexneri. Our results highlight the persistent threat of horizontally transmitted antimicrobial resistance and the value of continuing to work towards early and open international sharing of genomic surveillance data.",

author = "Mason, {Lewis C.E.} and Greig, {David R.} and Cowley, {Lauren A.} and Partridge, {Sally R.} and Elena Martinez and Blackwell, {Grace A.} and Chong, {Charlotte E.} and {De Silva}, {P. Malaka} and Bengtsson, {Rebecca J.} and Draper, {Jenny L.} and Ginn, {Andrew N.} and Indy Sandaradura and Sim, {Eby M.} and Iredell, {Jonathan R.} and Vitali Sintchenko and Ingle, {Danielle J.} and Howden, {Benjamin P.} and Sophie Lef{\`e}vre and Elisabeth Njampeko and Weill, {Fran{\c c}ois Xavier} and Ceyssens, {Pieter Jan} and Claire Jenkins and Baker, {Kate S.}",

note = "Data availability Sequence data relating to all isolates has been deposited in the Sequence Read Archive under BioProject numbers PRJNA315192 (United Kingdom), PRJEB44801 (France), PRJEB40097 (Belgium), and PRJNA613115 (Australia, New South Wales). Individual isolate accession numbers and isolate metadata are available in the Supplementary Data 1 as indicated in the text. Correspondence regarding isolates from the United Kingdom and the overall study should be directed to Dr. Claire Jenkins and Professor Kate Baker. Correspondence regarding isolates: from France should be directed to Professor Fran{\c c}ois-Xavier Weill; from Belgium should be directed to Pieter-Jan Ceyssens; from the United States of America should be directed to Kaitlin Tagg or PulseNet; and from Australia to Ben Howden and Danielle Ingle (Victoria) or Elena Martinez or Jonathan Iredell (New South Wales). This study was funded by the National Institute for Health and Care Research (NIHR) Health Protection Research Unit in Gastrointestinal Infections, a partnership between the UK Health Security Agency, the University of Liverpool, and the University of Warwick. The views expressed are those of the author(s) and not necessarily those of the NIHR, the UK Health Security Agency or the Department of Health and Social Care. The authors thank Hattie Webb, Kaitlin Tagg, Jason Folster, Jean Whichard, and other staff at the United States Centres for Disease Control for helpful discussions to guide access to genome data from PulseNet. The authors are also grateful to pathology laboratories that provided isolates for genomic surveillance. This work was also supported by MRC and BBSRC grants held by KSB (MR/R020787/1 and BB/V009184/1, respectively).",

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AU - Blackwell, Grace A.

AU - Chong, Charlotte E.

AU - De Silva, P. Malaka

AU - Bengtsson, Rebecca J.

AU - Draper, Jenny L.

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The evolution and international spread of extensively drug resistant Shigella sonnei

Abstract

Bibliographical note

ASJC Scopus subject areas

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