Abstract
Since the 1970s, shigellosis has been reported as a sexually transmissible infection, and in recent years, genomic data have revealed the breadth of Shigella spp. transmission among global networks of men who have sex with men (MSM). In 2015, Public Health England (PHE) introduced routine whole-genome sequencing (WGS) of Shigella spp. to identify transmission clusters. However, limited behavioural information for the cases hampers interpretation. We investigated whether WGS can distinguish between clusters representing sexual transmission in MSM and clusters representing community (non-sexual) transmission to inform infection control. WGS data for Shigella flexneri from August 2015 to July 2017 were aggregated into single linkage clusters based on SNP typing using a range of SNP distances (the standard for Shigella surveillance at PHE is 10 SNPs). Clusters were classified as ‘adult male’, ‘household’, ‘travel-associated’ or ‘community’ using routine demographic data submitted alongside laboratory cultures. From August 2015 to March 2017, PHE contacted those with shigellosis as part of routine public-health follow-up and collected exposure data on a structured questionnaire, which for the first time included questions about sexual identity and behaviour. The questionnaire data were used to determine whether clusters classified as ‘adult male’ represented likely sexual transmission between men, thereby validating the use of the SNP clustering tool for informing appropriate public-health responses. Overall, 1006 S . flexneri cases were reported, of which 563 clustered with at least one other case (10-SNP threshold). Linked questionnaire data were available for 106 clustered cases, of which 84.0 % belonged to an ‘adult male’ cluster. At the 10-SNP threshold, 95.1 % [95 % confidence interval (CI) 88.0–98.1%] of MSM belonged to an ‘adult male’ cluster, while 73.2 % (95 % CI 49.1–87.5%) of non-MSM belonged to a ‘community’ or ‘travel-associated’ cluster. At the 25-SNP threshold, all MSM (95 % CI 96.0–100%) belonged to an ‘adult male’ cluster and 77.8 % (95 % CI 59.2–89.4%) of non-MSM belonged to a ‘community’ or ‘travel-associated’ cluster. Within one phylogenetic clade of S. flexneri , 9 clusters were identified (7 ‘adult male’; 2 ‘community’) using a 10-SNP threshold, while a single ‘adult male’ cluster was identified using a 25-SNP threshold. Genotypic markers of azithromycin resistance were detected in 84.5 % (294/348) of ‘adult male’ cases and 20.9 % (9/43) of cases in other clusters (10-SNP threshold), the latter of which contained gay-identifying men who reported recent same-sex sexual contact. Our study suggests that SNP clustering can be used to identify Shigella clusters representing likely sexual transmission in MSM to inform infection control. Defining clusters requires a flexible approach in terms of genetic relatedness to ensure a clear understanding of underlying transmission networks.
Highlights
Shigellosis or severe bacillary dysentery is caused by four Shigella species (Shigella flexneri, Shigella dysenteriae, Shigella sonnei and Shigella boydii) transmitted via the faecal–oral route of infection [1, 2]
The four gay- identifying men within the ‘community’ clusters belonged to the two ‘community’ clusters that were part of a larger 25-S NP ‘adult male’ cluster. This is the first time that robust data on sexual identity and behaviour have been available for a large sub-set of Shigella cases in England, and we have been able to utilize this data to validate a real-time SNP clustering algorithm
We provide evidence that SNP clustering using limited routine demographic data can distinguish clusters representing likely sexual transmission in men who have sex with men (MSM) from other clusters representing community transmission, thereby informing rapid and appropriate public-health responses
Summary
Shigellosis or severe bacillary dysentery is caused by four Shigella species (Shigella flexneri, Shigella dysenteriae, Shigella sonnei and Shigella boydii) transmitted via the faecal–oral route of infection [1, 2]. Over the last 10 years, there has been evidence of increasing transmission through sex between men [4, 5] This occurs through oral–anal sexual contact, and has been linked with specific sexual activities and drug-use behaviours among predominantly human immunodeficiency virus (HIV)-positive men who have sex with men (MSM) [6]. SNP typing is used to aggregate isolates into single linkage clusters considered to represent cases that are linked through recent transmission events. This provides a tool used for public-health decision-making in near real-time to distinguish between linked cases that might be part of an evolving UK outbreak, requiring a robust infection-control response, and cases who likely acquired their infection whilst travelling abroad [11]. Limited routine demographic data are submitted to the GBRU alongside laboratory isolates (see Methods) and are used to classify clusters, but these data lack information on sexual identity and behaviour
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