Co-circulation of Multidrug-resistant Shigella Among Men Who Have Sex With Men in Australia

Danielle J. Ingle, Marion Easton, Mary Valcanis, Torsten Seemann, Jason C Kwong, Nicola Stephens, Glen P. Carter, Anders Goncalves da Silva, James Adamopoulos, Sarah L Baines, Kathryn E. Holt, Eric P.F. Chow, Christopher Fairley, Marcus Chen, Martyn Kirk, Ben Howden, Deborah A. Williamson

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Background: In urban Australia, the burden of shigellosis is either in returning travelers from shigellosis-endemic regions or in men who have sex with men (MSM). Here, we combine genomic data with comprehensive epidemiological data on sexual exposure and travel to describe the spread of multidrug-resistant Shigella lineages.

Methods: A population-level study of all cultured Shigella isolates in the state of Victoria, Australia, was undertaken from 1 January 2016 through 31 March 2018. Antimicrobial susceptibility testing, whole-genome sequencing, and bioinformatic analyses of 545 Shigella isolates were performed at the Microbiological Diagnostic Unit Public Health Laboratory. Risk factor data on travel and sexual exposure were collected through enhanced surveillance forms or by interviews.

Results: Rates of antimicrobial resistance were high, with 17.6% (95/541) and 50.6% (274/541) resistance to ciprofloxacin and azithromycin, respectively. There were strong associations between antimicrobial resistance, phylogeny, and epidemiology. Specifically, 2 major MSM-associated lineages were identified: a Shigellasonnei lineage (n = 159) and a Shigella flexneri 2a lineage (n = 105). Of concern, 147/159 (92.4%) of isolates within the S. sonnei MSM-associated lineage harbored mutations associated with reduced susceptibility to recommended oral antimicrobials: namely, azithromycin, trimethoprim-sulfamethoxazole, and ciprofloxacin. Long-read sequencing demonstrated global dissemination of multidrug-resistant plasmids across Shigella species and lineages, but predominantly associated with MSM isolates.

Conclusions: Our contemporary data highlight the ongoing public health threat posed by resistant Shigella, both in Australia and globally. Urgent multidisciplinary public health measures are required to interrupt transmission and prevent infection.
Original languageEnglish
Pages (from-to)1-10
Number of pages10
JournalClinical Infectious Diseases
DOIs
Publication statusAccepted/In press - 2019

Cite this

Ingle, D. J., Easton, M., Valcanis, M., Seemann, T., Kwong, J. C., Stephens, N., ... Williamson, D. A. (Accepted/In press). Co-circulation of Multidrug-resistant Shigella Among Men Who Have Sex With Men in Australia. Clinical Infectious Diseases, 1-10. https://doi.org/10.1093/cid/ciz005
Ingle, Danielle J. ; Easton, Marion ; Valcanis, Mary ; Seemann, Torsten ; Kwong, Jason C ; Stephens, Nicola ; Carter, Glen P. ; Goncalves da Silva, Anders ; Adamopoulos, James ; Baines, Sarah L ; Holt, Kathryn E. ; Chow, Eric P.F. ; Fairley, Christopher ; Chen, Marcus ; Kirk, Martyn ; Howden, Ben ; Williamson, Deborah A. / Co-circulation of Multidrug-resistant Shigella Among Men Who Have Sex With Men in Australia. In: Clinical Infectious Diseases. 2019 ; pp. 1-10.
@article{e429a8b9b3954958a74521394e80e720,
title = "Co-circulation of Multidrug-resistant Shigella Among Men Who Have Sex With Men in Australia",
abstract = "Background: In urban Australia, the burden of shigellosis is either in returning travelers from shigellosis-endemic regions or in men who have sex with men (MSM). Here, we combine genomic data with comprehensive epidemiological data on sexual exposure and travel to describe the spread of multidrug-resistant Shigella lineages.Methods: A population-level study of all cultured Shigella isolates in the state of Victoria, Australia, was undertaken from 1 January 2016 through 31 March 2018. Antimicrobial susceptibility testing, whole-genome sequencing, and bioinformatic analyses of 545 Shigella isolates were performed at the Microbiological Diagnostic Unit Public Health Laboratory. Risk factor data on travel and sexual exposure were collected through enhanced surveillance forms or by interviews.Results: Rates of antimicrobial resistance were high, with 17.6{\%} (95/541) and 50.6{\%} (274/541) resistance to ciprofloxacin and azithromycin, respectively. There were strong associations between antimicrobial resistance, phylogeny, and epidemiology. Specifically, 2 major MSM-associated lineages were identified: a Shigellasonnei lineage (n = 159) and a Shigella flexneri 2a lineage (n = 105). Of concern, 147/159 (92.4{\%}) of isolates within the S. sonnei MSM-associated lineage harbored mutations associated with reduced susceptibility to recommended oral antimicrobials: namely, azithromycin, trimethoprim-sulfamethoxazole, and ciprofloxacin. Long-read sequencing demonstrated global dissemination of multidrug-resistant plasmids across Shigella species and lineages, but predominantly associated with MSM isolates.Conclusions: Our contemporary data highlight the ongoing public health threat posed by resistant Shigella, both in Australia and globally. Urgent multidisciplinary public health measures are required to interrupt transmission and prevent infection.",
author = "Ingle, {Danielle J.} and Marion Easton and Mary Valcanis and Torsten Seemann and Kwong, {Jason C} and Nicola Stephens and Carter, {Glen P.} and {Goncalves da Silva}, Anders and James Adamopoulos and Baines, {Sarah L} and Holt, {Kathryn E.} and Chow, {Eric P.F.} and Christopher Fairley and Marcus Chen and Martyn Kirk and Ben Howden and Williamson, {Deborah A.}",
year = "2019",
doi = "10.1093/cid/ciz005",
language = "English",
pages = "1--10",
journal = "Clinical Infectious Diseases",
issn = "1058-4838",
publisher = "Oxford University Press",

}

Ingle, DJ, Easton, M, Valcanis, M, Seemann, T, Kwong, JC, Stephens, N, Carter, GP, Goncalves da Silva, A, Adamopoulos, J, Baines, SL, Holt, KE, Chow, EPF, Fairley, C, Chen, M, Kirk, M, Howden, B & Williamson, DA 2019, 'Co-circulation of Multidrug-resistant Shigella Among Men Who Have Sex With Men in Australia' Clinical Infectious Diseases, pp. 1-10. https://doi.org/10.1093/cid/ciz005

Co-circulation of Multidrug-resistant Shigella Among Men Who Have Sex With Men in Australia. / Ingle, Danielle J.; Easton, Marion; Valcanis, Mary; Seemann, Torsten; Kwong, Jason C; Stephens, Nicola; Carter, Glen P.; Goncalves da Silva, Anders; Adamopoulos, James ; Baines, Sarah L; Holt, Kathryn E.; Chow, Eric P.F.; Fairley, Christopher; Chen, Marcus; Kirk, Martyn; Howden, Ben; Williamson, Deborah A.

In: Clinical Infectious Diseases, 2019, p. 1-10.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Co-circulation of Multidrug-resistant Shigella Among Men Who Have Sex With Men in Australia

AU - Ingle, Danielle J.

AU - Easton, Marion

AU - Valcanis, Mary

AU - Seemann, Torsten

AU - Kwong, Jason C

AU - Stephens, Nicola

AU - Carter, Glen P.

AU - Goncalves da Silva, Anders

AU - Adamopoulos, James

AU - Baines, Sarah L

AU - Holt, Kathryn E.

AU - Chow, Eric P.F.

AU - Fairley, Christopher

AU - Chen, Marcus

AU - Kirk, Martyn

AU - Howden, Ben

AU - Williamson, Deborah A.

PY - 2019

Y1 - 2019

N2 - Background: In urban Australia, the burden of shigellosis is either in returning travelers from shigellosis-endemic regions or in men who have sex with men (MSM). Here, we combine genomic data with comprehensive epidemiological data on sexual exposure and travel to describe the spread of multidrug-resistant Shigella lineages.Methods: A population-level study of all cultured Shigella isolates in the state of Victoria, Australia, was undertaken from 1 January 2016 through 31 March 2018. Antimicrobial susceptibility testing, whole-genome sequencing, and bioinformatic analyses of 545 Shigella isolates were performed at the Microbiological Diagnostic Unit Public Health Laboratory. Risk factor data on travel and sexual exposure were collected through enhanced surveillance forms or by interviews.Results: Rates of antimicrobial resistance were high, with 17.6% (95/541) and 50.6% (274/541) resistance to ciprofloxacin and azithromycin, respectively. There were strong associations between antimicrobial resistance, phylogeny, and epidemiology. Specifically, 2 major MSM-associated lineages were identified: a Shigellasonnei lineage (n = 159) and a Shigella flexneri 2a lineage (n = 105). Of concern, 147/159 (92.4%) of isolates within the S. sonnei MSM-associated lineage harbored mutations associated with reduced susceptibility to recommended oral antimicrobials: namely, azithromycin, trimethoprim-sulfamethoxazole, and ciprofloxacin. Long-read sequencing demonstrated global dissemination of multidrug-resistant plasmids across Shigella species and lineages, but predominantly associated with MSM isolates.Conclusions: Our contemporary data highlight the ongoing public health threat posed by resistant Shigella, both in Australia and globally. Urgent multidisciplinary public health measures are required to interrupt transmission and prevent infection.

AB - Background: In urban Australia, the burden of shigellosis is either in returning travelers from shigellosis-endemic regions or in men who have sex with men (MSM). Here, we combine genomic data with comprehensive epidemiological data on sexual exposure and travel to describe the spread of multidrug-resistant Shigella lineages.Methods: A population-level study of all cultured Shigella isolates in the state of Victoria, Australia, was undertaken from 1 January 2016 through 31 March 2018. Antimicrobial susceptibility testing, whole-genome sequencing, and bioinformatic analyses of 545 Shigella isolates were performed at the Microbiological Diagnostic Unit Public Health Laboratory. Risk factor data on travel and sexual exposure were collected through enhanced surveillance forms or by interviews.Results: Rates of antimicrobial resistance were high, with 17.6% (95/541) and 50.6% (274/541) resistance to ciprofloxacin and azithromycin, respectively. There were strong associations between antimicrobial resistance, phylogeny, and epidemiology. Specifically, 2 major MSM-associated lineages were identified: a Shigellasonnei lineage (n = 159) and a Shigella flexneri 2a lineage (n = 105). Of concern, 147/159 (92.4%) of isolates within the S. sonnei MSM-associated lineage harbored mutations associated with reduced susceptibility to recommended oral antimicrobials: namely, azithromycin, trimethoprim-sulfamethoxazole, and ciprofloxacin. Long-read sequencing demonstrated global dissemination of multidrug-resistant plasmids across Shigella species and lineages, but predominantly associated with MSM isolates.Conclusions: Our contemporary data highlight the ongoing public health threat posed by resistant Shigella, both in Australia and globally. Urgent multidisciplinary public health measures are required to interrupt transmission and prevent infection.

U2 - 10.1093/cid/ciz005

DO - 10.1093/cid/ciz005

M3 - Article

SP - 1

EP - 10

JO - Clinical Infectious Diseases

JF - Clinical Infectious Diseases

SN - 1058-4838

ER -