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Intercontinental dissemination of azithromycin-resistant shigellosis through sexual transmission: a cross-sectional study.
Lancet Infect Dis. 2015 Aug; 15(8):913-21.LI

Abstract

BACKGROUND

Shigellosis is an acute, severe bacterial colitis that, in high-income countries, is typically associated with travel to high-risk regions (Africa, Asia, and Latin America). Since the 1970s, shigellosis has also been reported as a sexually transmitted infection in men who have sex with men (MSM), in whom transmission is an important component of shigellosis epidemiology in high-income nations. We aimed to use sophisticated subtyping and international sampling to determine factors driving shigellosis emergence in MSM linked to an outbreak in the UK.

METHODS

We did a large-scale, cross-sectional genomic epidemiological study of shigellosis cases collected from 29 countries between December, 1995, and June 8, 2014. Focusing on an ongoing epidemic in the UK, we collected and whole-genome sequenced clinical isolates of Shigella flexneri serotype 3a from high-risk and low-risk regions, including cases associated with travel and sex between men. We examined relationships between geographical, demographic, and clinical patient data with the isolate antimicrobial susceptibility, genetic data, and inferred evolutionary relationships.

FINDINGS

We obtained 331 clinical isolates of S flexneri serotype 3a, including 275 from low-risk regions (44 from individuals who travelled to high-risk regions), 52 from high-risk regions, and four outgroup samples (ie, closely related, but genetically distinct isolates used to determine the root of the phylogenetic tree). We identified a recently emerged lineage of S flexneri 3a that has spread intercontinentally in less than 20 years throughout regions traditionally at low risk for shigellosis via sexual transmission in MSM. The lineage had acquired multiple antimicrobial resistance determinants, and prevailing sublineages were strongly associated with resistance to the macrolide azithromycin. Eight (4%) of 206 isolates from the MSM-associated lineage were obtained from patients who had previously provided an isolate; these serial isolations indicated atypical infection patterns (eg, reinfection).

INTERPRETATION

We identified transmission-facilitating behaviours and atypical course(s) of infection as precipitating factors in shigellosis-affected MSM. The intercontinental spread of antimicrobial-resistant shigella through established transmission routes emphasises the need for new approaches to tackle the public health challenge of sexually transmitted infections in MSM.

FUNDING

Wellcome Trust (grant number 098051).

Authors+Show Affiliations

Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, UK.Gastrointestinal Bacteria Reference Unit, Public Health England, London, UK.Gastrointestinal Bacteria Reference Unit, Public Health England, London, UK.Gastrointestinal Bacteria Reference Unit, Public Health England, London, UK.Department of HIV and STIs, Centre for Infectious Disease Surveillance and Control, Public Health England, London, UK.Field Epidemiology Services, Public Health England, London, UK.Department of HIV and STIs, Centre for Infectious Disease Surveillance and Control, Public Health England, London, UK.Public Health Ontario Laboratories, Toronto, ON, Canada.Public Health Ontario Laboratories, Toronto, ON, Canada.Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Parkville, VIC, Australia; Infectious Diseases Department, Austin Health, Heidelberg, VIC, Australia; Department of Microbiology, Monash University, Clayton, VIC, Australia.Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Parkville, VIC, Australia.Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Parkville, VIC, Australia.Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, UK.Cardiff School of Biosciences, Sir Martin Evans Building, Museum Avenue, Cardiff, UK.Marie Bashir Institute for Infectious Diseases and Biosecurity and Sydney Medical School, The University of Sydney, Sydney, NSW, Australia; Centre for Infectious Diseases and Microbiology-Public Health, Institute of Clinical Pathology and Medical Research-Pathology West, Westmead Hospital, Sydney, NSW, Australia; NSW Enteric Reference Laboratory, Centre for Infectious Diseases and Microbiology Laboratory Services, Institute of Clinical Pathology and Medical Research-Pathology West, Sydney, NSW, Australia.Centre for Infectious Diseases and Microbiology-Public Health, Institute of Clinical Pathology and Medical Research-Pathology West, Westmead Hospital, Sydney, NSW, Australia; NSW Enteric Reference Laboratory, Centre for Infectious Diseases and Microbiology Laboratory Services, Institute of Clinical Pathology and Medical Research-Pathology West, Sydney, NSW, Australia.NSW Enteric Reference Laboratory, Centre for Infectious Diseases and Microbiology Laboratory Services, Institute of Clinical Pathology and Medical Research-Pathology West, Sydney, NSW, Australia.The ithree institute, University of Technology Sydney, Sydney, NSW, Australia.Institut Pasteur, Unité des Bactéries Pathogènes Entériques, Paris, France.Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam.Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa; Centre for Enteric Diseases, National Institute for Communicable Diseases, Johannesburg, South Africa.Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa; Centre for Enteric Diseases, National Institute for Communicable Diseases, Johannesburg, South Africa.International Centre for Diarrhoeal Disease Research Bangladesh, Dhaka, Bangladesh.International Centre for Diarrhoeal Disease Research Bangladesh, Dhaka, Bangladesh.Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, UK.Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam; The Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme and Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, Oxford University, Oxford, UK; The London School of Hygiene & Tropical Medicine, London, UK.Institut Pasteur, Unité des Bactéries Pathogènes Entériques, Paris, France.Gastrointestinal Bacteria Reference Unit, Public Health England, London, UK.Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, UK; The London School of Hygiene & Tropical Medicine, London, UK. Electronic address: nrt@sanger.ac.uk.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

25936611

Citation

Baker, Kate S., et al. "Intercontinental Dissemination of Azithromycin-resistant Shigellosis Through Sexual Transmission: a Cross-sectional Study." The Lancet. Infectious Diseases, vol. 15, no. 8, 2015, pp. 913-21.
Baker KS, Dallman TJ, Ashton PM, et al. Intercontinental dissemination of azithromycin-resistant shigellosis through sexual transmission: a cross-sectional study. Lancet Infect Dis. 2015;15(8):913-21.
Baker, K. S., Dallman, T. J., Ashton, P. M., Day, M., Hughes, G., Crook, P. D., Gilbart, V. L., Zittermann, S., Allen, V. G., Howden, B. P., Tomita, T., Valcanis, M., Harris, S. R., Connor, T. R., Sintchenko, V., Howard, P., Brown, J. D., Petty, N. K., Gouali, M., ... Thomson, N. R. (2015). Intercontinental dissemination of azithromycin-resistant shigellosis through sexual transmission: a cross-sectional study. The Lancet. Infectious Diseases, 15(8), 913-21. https://doi.org/10.1016/S1473-3099(15)00002-X
Baker KS, et al. Intercontinental Dissemination of Azithromycin-resistant Shigellosis Through Sexual Transmission: a Cross-sectional Study. Lancet Infect Dis. 2015;15(8):913-21. PubMed PMID: 25936611.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Intercontinental dissemination of azithromycin-resistant shigellosis through sexual transmission: a cross-sectional study. AU - Baker,Kate S, AU - Dallman,Timothy J, AU - Ashton,Philip M, AU - Day,Martin, AU - Hughes,Gwenda, AU - Crook,Paul D, AU - Gilbart,Victoria L, AU - Zittermann,Sandra, AU - Allen,Vanessa G, AU - Howden,Benjamin P, AU - Tomita,Takehiro, AU - Valcanis,Mary, AU - Harris,Simon R, AU - Connor,Thomas R, AU - Sintchenko,Vitali, AU - Howard,Peter, AU - Brown,Jeremy D, AU - Petty,Nicola K, AU - Gouali,Malika, AU - Thanh,Duy Pham, AU - Keddy,Karen H, AU - Smith,Anthony M, AU - Talukder,Kaisar A, AU - Faruque,Shah M, AU - Parkhill,Julian, AU - Baker,Stephen, AU - Weill,François-Xavier, AU - Jenkins,Claire, AU - Thomson,Nicholas R, Y1 - 2015/04/27/ PY - 2015/5/5/entrez PY - 2015/5/6/pubmed PY - 2015/10/31/medline SP - 913 EP - 21 JF - The Lancet. Infectious diseases JO - Lancet Infect Dis VL - 15 IS - 8 N2 - BACKGROUND: Shigellosis is an acute, severe bacterial colitis that, in high-income countries, is typically associated with travel to high-risk regions (Africa, Asia, and Latin America). Since the 1970s, shigellosis has also been reported as a sexually transmitted infection in men who have sex with men (MSM), in whom transmission is an important component of shigellosis epidemiology in high-income nations. We aimed to use sophisticated subtyping and international sampling to determine factors driving shigellosis emergence in MSM linked to an outbreak in the UK. METHODS: We did a large-scale, cross-sectional genomic epidemiological study of shigellosis cases collected from 29 countries between December, 1995, and June 8, 2014. Focusing on an ongoing epidemic in the UK, we collected and whole-genome sequenced clinical isolates of Shigella flexneri serotype 3a from high-risk and low-risk regions, including cases associated with travel and sex between men. We examined relationships between geographical, demographic, and clinical patient data with the isolate antimicrobial susceptibility, genetic data, and inferred evolutionary relationships. FINDINGS: We obtained 331 clinical isolates of S flexneri serotype 3a, including 275 from low-risk regions (44 from individuals who travelled to high-risk regions), 52 from high-risk regions, and four outgroup samples (ie, closely related, but genetically distinct isolates used to determine the root of the phylogenetic tree). We identified a recently emerged lineage of S flexneri 3a that has spread intercontinentally in less than 20 years throughout regions traditionally at low risk for shigellosis via sexual transmission in MSM. The lineage had acquired multiple antimicrobial resistance determinants, and prevailing sublineages were strongly associated with resistance to the macrolide azithromycin. Eight (4%) of 206 isolates from the MSM-associated lineage were obtained from patients who had previously provided an isolate; these serial isolations indicated atypical infection patterns (eg, reinfection). INTERPRETATION: We identified transmission-facilitating behaviours and atypical course(s) of infection as precipitating factors in shigellosis-affected MSM. The intercontinental spread of antimicrobial-resistant shigella through established transmission routes emphasises the need for new approaches to tackle the public health challenge of sexually transmitted infections in MSM. FUNDING: Wellcome Trust (grant number 098051). SN - 1474-4457 UR - https://www.unboundmedicine.com/medline/citation/25936611/full_citation L2 - https://linkinghub.elsevier.com/retrieve/pii/S1473-3099(15)00002-X DB - PRIME DP - Unbound Medicine ER -