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      Whole genome analysis and antimicrobial resistance of Neisseria gonorrhoeae isolates from Ghana

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          Abstract

          Introduction

          Gonorrhoea is a major public health concern. With the global emergence and spread of resistance to last-line antibiotic treatment options, gonorrhoea threatens to be untreatable in the future. Therefore, this study performed whole genome characterization of Neisseria gonorrhoeae collected in Ghana to identify lineages of circulating strains as well as their phenotypic and genotypic antimicrobial resistance (AMR) profiles.

          Methods

          Whole genome sequencing (WGS) was performed on 56 isolates using both the Oxford Nanopore MinION and Illumina MiSeq sequencing platforms. The Comprehensive Antimicrobial Resistance Database (CARD) and PUBMLST.org/neisseria databases were used to catalogue chromosomal and plasmid genes implicated in AMR. The core genome multi-locus sequence typing (cgMLST) approach was used for comparative genomics analysis.

          Results and Discussion

          In vitro resistance measured by the E-test method revealed 100%, 91.0% and 85.7% resistance to tetracycline, penicillin and ciprofloxacin, respectively. A total of 22 sequence types (STs) were identified by multilocus sequence typing (MLST), with ST-14422 ( n = 10), ST-1927 ( n = 8) and ST-11210 ( n = 7) being the most prevalent. Six novel STs were also identified (ST-15634, 15636-15639 and 15641). All isolates harboured chromosomal AMR determinants that confer resistance to beta-lactam antimicrobials and tetracycline. A single cefixime-resistant strain, that belongs to N. gonorrhoeae multiantigen sequence type (NG-MAST) ST1407, a type associated with widespread cephalosporin resistance was identified. Neisseria gonorrhoeae Sequence Typing for Antimicrobial Resistance (NG-STAR), identified 29 unique sequence types, with ST-464 ( n = 8) and the novel ST-3366 ( n = 8) being the most prevalent. Notably, 20 of the 29 STs were novel, indicative of the unique nature of molecular AMR determinants in the Ghanaian strains. Plasmids were highly prevalent: pTetM and p blaTEM were found in 96% and 92% of isolates, respectively. The TEM-135 allele, which is an amino acid change away from producing a stable extended-spectrum β-lactamase that could result in complete cephalosporin resistance, was identified in 28.5% of the isolates. Using WGS, we characterized N. gonorrhoeae strains from Ghana, giving a snapshot of the current state of gonococcal AMR in the country and highlighting the need for constant genomic surveillance.

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          Most cited references49

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          Chlamydia, gonorrhoea, trichomoniasis and syphilis: global prevalence and incidence estimates, 2016

          Abstract Objective To generate estimates of the global prevalence and incidence of urogenital infection with chlamydia, gonorrhoea, trichomoniasis and syphilis in women and men, aged 15–49 years, in 2016. Methods For chlamydia, gonorrhoea and trichomoniasis, we systematically searched for studies conducted between 2009 and 2016 reporting prevalence. We also consulted regional experts. To generate estimates, we used Bayesian meta-analysis. For syphilis, we aggregated the national estimates generated by using Spectrum-STI. Findings For chlamydia, gonorrhoea and/or trichomoniasis, 130 studies were eligible. For syphilis, the Spectrum-STI database contained 978 data points for the same period. The 2016 global prevalence estimates in women were: chlamydia 3.8% (95% uncertainty interval, UI: 3.3–4.5); gonorrhoea 0.9% (95% UI: 0.7–1.1); trichomoniasis 5.3% (95% UI:4.0–7.2); and syphilis 0.5% (95% UI: 0.4–0.6). In men prevalence estimates were: chlamydia 2.7% (95% UI: 1.9–3.7); gonorrhoea 0.7% (95% UI: 0.5–1.1); trichomoniasis 0.6% (95% UI: 0.4–0.9); and syphilis 0.5% (95% UI: 0.4–0.6). Total estimated incident cases were 376.4 million: 127.2 million (95% UI: 95.1–165.9 million) chlamydia cases; 86.9 million (95% UI: 58.6–123.4 million) gonorrhoea cases; 156.0 million (95% UI: 103.4–231.2 million) trichomoniasis cases; and 6.3 million (95% UI: 5.5–7.1 million) syphilis cases. Conclusion Global estimates of prevalence and incidence of these four curable sexually transmitted infections remain high. The study highlights the need to expand data collection efforts at country level and provides an initial baseline for monitoring progress of the World Health Organization global health sector strategy on sexually transmitted infections 2016–2021.
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            Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future.

            Neisseria gonorrhoeae is evolving into a superbug with resistance to previously and currently recommended antimicrobials for treatment of gonorrhea, which is a major public health concern globally. Given the global nature of gonorrhea, the high rate of usage of antimicrobials, suboptimal control and monitoring of antimicrobial resistance (AMR) and treatment failures, slow update of treatment guidelines in most geographical settings, and the extraordinary capacity of the gonococci to develop and retain AMR, it is likely that the global problem of gonococcal AMR will worsen in the foreseeable future and that the severe complications of gonorrhea will emerge as a silent epidemic. By understanding the evolution, emergence, and spread of AMR in N. gonorrhoeae, including its molecular and phenotypic mechanisms, resistance to antimicrobials used clinically can be anticipated, future methods for genetic testing for AMR might permit region-specific and tailor-made antimicrobial therapy, and the design of novel antimicrobials to circumvent the resistance problems can be undertaken more rationally. This review focuses on the history and evolution of gonorrhea treatment regimens and emerging resistance to them, on genetic and phenotypic determinants of gonococcal resistance to previously and currently recommended antimicrobials, including biological costs or benefits; and on crucial actions and future advances necessary to detect and treat resistant gonococcal strains and, ultimately, retain gonorrhea as a treatable infection. Copyright © 2014, American Society for Microbiology. All Rights Reserved.
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              Antimicrobial resistance in Neisseria gonorrhoeae: Global surveillance and a call for international collaborative action

              In a Policy Forum, Teodora Wi and colleagues discuss the challenges of antimicrobial resistance in gonococci.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                29 June 2023
                2023
                : 14
                : 1163450
                Affiliations
                [1] 1Naval Medical Research Unit No. 3 , Accra, Ghana
                [2] 2West African Centre for Cell Biology of Infectious Pathogens, College of Basic and Applied Sciences, University of Ghana , Accra, Ghana
                [3] 3Department of Biochemistry, Cell and Molecular Biology, University of Ghana , Accra, Ghana
                [4] 4Biomedical Engineering Department, School of Engineering Sciences, University of Ghana , Accra, Ghana
                [5] 5Bacteriology Department, Noguchi Memorial Institute for Medical Research, University of Ghana , Accra, Ghana
                [6] 6Center for Bio/Molecular Science and Engineering, Naval Research Laboratory , Washington, DC, United States
                [7] 7Nebraska Medical Center , Omaha, NE, United States
                Author notes

                Edited by: Veron Ramsuran, University of KwaZulu-Natal, South Africa

                Reviewed by: Nireshni Mitchev, University of Kwa-Zulu-Natal, South Africa; Michael Benedik, Texas A&M University, United States

                Article
                10.3389/fmicb.2023.1163450
                10339232
                37455743
                5b560a9b-e72d-4afe-84b9-879876c27502
                Copyright © 2023 Agbodzi, Duodu, Dela, Kumordjie, Yeboah, Behene, Ocansey, Yanney, Boateng-Sarfo, Kwofie, Egyir, Colston, Miranda, Watters, Sanders, Fox, Letizia, Wiley and Attram.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 10 February 2023
                : 07 June 2023
                Page count
                Figures: 3, Tables: 4, Equations: 0, References: 49, Pages: 10, Words: 7429
                Categories
                Microbiology
                Original Research
                Custom metadata
                Antimicrobials, Resistance and Chemotherapy

                Microbiology & Virology
                neisseria gonorrhoeae,antimicrobial resistance,ghana,whole genome sequencing,gonorrhea,core genome mlst

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