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

Author:

Ingle Danielle J12,Easton Marion3,Valcanis Mary1,Seemann Torsten145,Kwong Jason C5,Stephens Nicola3,Carter Glen P15,Gonçalves da Silva Anders1,Adamopoulos James3,Baines Sarah L5,Holt Kathryn E67,Chow Eric P F89,Fairley Christopher K89,Chen Marcus Y89,Kirk Martyn D2,Howden Benjamin P15,Williamson Deborah A15

Affiliation:

1. Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne

2. National Centre for Epidemiology and Population Health, The Australian National University, Canberra

3. Victorian Department of Health and Human Services, Melbourne

4. Melbourne Bioinformatics Group, Victoria, Australia

5. Doherty Applied Microbial Genomics, Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Parkville, Australia

6. Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Australia

7. London School of Hygiene and Tropical Medicine, United Kingdom

8. Melbourne Sexual Health Centre, Alfred Health, Carlton

9. Central Clinical School, Monash University, Melbourne, Australia

Abstract

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.

Funder

National Health and Medical Research Council

Career Development Fellowship

European Union’s Horizon 2020 research and innovation

Publisher

Oxford University Press (OUP)

Subject

Infectious Diseases,Microbiology (medical)

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