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Travel-associated lineages and unique endemic antimicrobial-susceptible lineages of Neisseria gonorrhoeae predominate in Western Australia

In Australia, gonococcal isolates are monitored for antimicrobial susceptibilities. In Western Australia (WA), gonorrhoea notification rates increased by 63 % between 2013 and 2016, with the steepest increase occurring between 2015 and 2016, before stabilizing at this higher baseline between 2017 an...

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Autores principales: Al Suwayyid, Barakat A., Haese, Ethan C., Mowlaboccus, Shakeel, Pearson, Julie C., Whiley, David M., Armstrong, Paul K., Giele, Carolien M., Mak, Donna B., Bastian, Lisa, Wise, Michael J., Coombs, Geoffrey W., Kahler, Charlene M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Microbiology Society 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10132056/
https://www.ncbi.nlm.nih.gov/pubmed/36988578
http://dx.doi.org/10.1099/mgen.0.000969
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author Al Suwayyid, Barakat A.
Haese, Ethan C.
Mowlaboccus, Shakeel
Pearson, Julie C.
Whiley, David M.
Armstrong, Paul K.
Giele, Carolien M.
Mak, Donna B.
Bastian, Lisa
Wise, Michael J.
Coombs, Geoffrey W.
Kahler, Charlene M.
author_facet Al Suwayyid, Barakat A.
Haese, Ethan C.
Mowlaboccus, Shakeel
Pearson, Julie C.
Whiley, David M.
Armstrong, Paul K.
Giele, Carolien M.
Mak, Donna B.
Bastian, Lisa
Wise, Michael J.
Coombs, Geoffrey W.
Kahler, Charlene M.
author_sort Al Suwayyid, Barakat A.
collection PubMed
description In Australia, gonococcal isolates are monitored for antimicrobial susceptibilities. In Western Australia (WA), gonorrhoea notification rates increased by 63 % between 2013 and 2016, with the steepest increase occurring between 2015 and 2016, before stabilizing at this higher baseline between 2017 and 2020. This increased prevalence was associated with antimicrobial-susceptible (AMS) lineages. To understand the provenance of these isolates causing gonorrhoea in WA, whether they were introduced or expanded from endogenous lineages, 741 isolates were collected in 2017 and characterized by both iPLEX typing and whole genome sequencing (WGS). Antibiograms and genocoding of the isolates revealed that AMS isolates were most prevalent in the remote regions, while the urban/rural regions were characterized by antimicrobial-resistant (AMR) isolates. iPLEX typing identified 78 iPLEX genotypes (WA-1 to WA-78) of which 20 accounted for over 88 % of isolates. WA-10 was the most frequently identified genotype in the urban/rural regions whilst WA-29 was the most frequently identified genotype in the remote regions. Genotypes WA-38, WA-52 and WA-13 accounted for 81 % (n=36/44) of the azithromycin-resistant N. gonorrhoeae (AziR) isolates. A representative isolate of each iPLEX genotype and AMR biotype was whole genome sequenced and analysed using MLST, NG-MAST and NG-STAR, and the novel core genome clustering Ng_cgc_400 typing scheme. Five predominant Bayesian population groups (termed BPG-1 to 5) were identified in the study collection. BPG-1 and BPG-2 were associated with AMS isolates from the remote regions. BPG-1 and BPG-2 were shown to be unique to the remote regions based on a minimum spanning tree against 4000 international isolates. AMS isolates in urban/rural regions were dominated by international lineages. AziR and Cef DS (decreased susceptibility to ceftriaxone) was concentrated in three urban/rural genomic groups (BPG-3, 4 and 5). Azithromycin minimum inhibitory concentrations (0.5–16 mg l(−1)) correlated with the accumulation of mtrR mutations or/and the fraction of 23S rRNA C2611T mutated copies. The majority of isolates in BPG-3, 4 and 5 could be correlated with known AMR lineages circulating globally and nationally. In conclusion, the surge in AMS isolates in WA in 2017 was due to importation of international AMS lineages into urban/rural regions, whilst the local AMS lineages persisted largely in the remote regions. Bridging between the urban/rural and remote regions was relatively rare, but continued surveillance is required to prevent ingress of AMR strains/lineages into the remote regions of WA.
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spelling pubmed-101320562023-04-27 Travel-associated lineages and unique endemic antimicrobial-susceptible lineages of Neisseria gonorrhoeae predominate in Western Australia Al Suwayyid, Barakat A. Haese, Ethan C. Mowlaboccus, Shakeel Pearson, Julie C. Whiley, David M. Armstrong, Paul K. Giele, Carolien M. Mak, Donna B. Bastian, Lisa Wise, Michael J. Coombs, Geoffrey W. Kahler, Charlene M. Microb Genom Research Articles In Australia, gonococcal isolates are monitored for antimicrobial susceptibilities. In Western Australia (WA), gonorrhoea notification rates increased by 63 % between 2013 and 2016, with the steepest increase occurring between 2015 and 2016, before stabilizing at this higher baseline between 2017 and 2020. This increased prevalence was associated with antimicrobial-susceptible (AMS) lineages. To understand the provenance of these isolates causing gonorrhoea in WA, whether they were introduced or expanded from endogenous lineages, 741 isolates were collected in 2017 and characterized by both iPLEX typing and whole genome sequencing (WGS). Antibiograms and genocoding of the isolates revealed that AMS isolates were most prevalent in the remote regions, while the urban/rural regions were characterized by antimicrobial-resistant (AMR) isolates. iPLEX typing identified 78 iPLEX genotypes (WA-1 to WA-78) of which 20 accounted for over 88 % of isolates. WA-10 was the most frequently identified genotype in the urban/rural regions whilst WA-29 was the most frequently identified genotype in the remote regions. Genotypes WA-38, WA-52 and WA-13 accounted for 81 % (n=36/44) of the azithromycin-resistant N. gonorrhoeae (AziR) isolates. A representative isolate of each iPLEX genotype and AMR biotype was whole genome sequenced and analysed using MLST, NG-MAST and NG-STAR, and the novel core genome clustering Ng_cgc_400 typing scheme. Five predominant Bayesian population groups (termed BPG-1 to 5) were identified in the study collection. BPG-1 and BPG-2 were associated with AMS isolates from the remote regions. BPG-1 and BPG-2 were shown to be unique to the remote regions based on a minimum spanning tree against 4000 international isolates. AMS isolates in urban/rural regions were dominated by international lineages. AziR and Cef DS (decreased susceptibility to ceftriaxone) was concentrated in three urban/rural genomic groups (BPG-3, 4 and 5). Azithromycin minimum inhibitory concentrations (0.5–16 mg l(−1)) correlated with the accumulation of mtrR mutations or/and the fraction of 23S rRNA C2611T mutated copies. The majority of isolates in BPG-3, 4 and 5 could be correlated with known AMR lineages circulating globally and nationally. In conclusion, the surge in AMS isolates in WA in 2017 was due to importation of international AMS lineages into urban/rural regions, whilst the local AMS lineages persisted largely in the remote regions. Bridging between the urban/rural and remote regions was relatively rare, but continued surveillance is required to prevent ingress of AMR strains/lineages into the remote regions of WA. Microbiology Society 2023-03-29 /pmc/articles/PMC10132056/ /pubmed/36988578 http://dx.doi.org/10.1099/mgen.0.000969 Text en © 2023 The Authors https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
spellingShingle Research Articles
Al Suwayyid, Barakat A.
Haese, Ethan C.
Mowlaboccus, Shakeel
Pearson, Julie C.
Whiley, David M.
Armstrong, Paul K.
Giele, Carolien M.
Mak, Donna B.
Bastian, Lisa
Wise, Michael J.
Coombs, Geoffrey W.
Kahler, Charlene M.
Travel-associated lineages and unique endemic antimicrobial-susceptible lineages of Neisseria gonorrhoeae predominate in Western Australia
title Travel-associated lineages and unique endemic antimicrobial-susceptible lineages of Neisseria gonorrhoeae predominate in Western Australia
title_full Travel-associated lineages and unique endemic antimicrobial-susceptible lineages of Neisseria gonorrhoeae predominate in Western Australia
title_fullStr Travel-associated lineages and unique endemic antimicrobial-susceptible lineages of Neisseria gonorrhoeae predominate in Western Australia
title_full_unstemmed Travel-associated lineages and unique endemic antimicrobial-susceptible lineages of Neisseria gonorrhoeae predominate in Western Australia
title_short Travel-associated lineages and unique endemic antimicrobial-susceptible lineages of Neisseria gonorrhoeae predominate in Western Australia
title_sort travel-associated lineages and unique endemic antimicrobial-susceptible lineages of neisseria gonorrhoeae predominate in western australia
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10132056/
https://www.ncbi.nlm.nih.gov/pubmed/36988578
http://dx.doi.org/10.1099/mgen.0.000969
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