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

Bright Agbodzi; Samuel Duodu; Helena Dela; Selassie Kumordjie; Clara Yeboah; Eric Behene; Karen Ocansey; Jennifer N Yanney; George Boateng-Sarfo; Samuel Kojo Kwofie; Beverly Egyir; Sophie M Colston; Hugo V Miranda; Chaselynn Watters; Terrel Sanders; Anne T Fox; Andrew G Letizia; Michael R Wiley; Naiki Attram

doi:10.3389/fmicb.2023.1163450

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

Front Microbiol. 2023 Jun 29:14:1163450. doi: 10.3389/fmicb.2023.1163450. eCollection 2023.

Authors

Bright Agbodzi^{1

2

3}, Samuel Duodu^{2

3}, Helena Dela¹, Selassie Kumordjie¹, Clara Yeboah¹, Eric Behene¹, Karen Ocansey¹, Jennifer N Yanney¹, George Boateng-Sarfo¹, Samuel Kojo Kwofie^{2

3

4}, Beverly Egyir⁵, Sophie M Colston⁶, Hugo V Miranda¹, Chaselynn Watters¹, Terrel Sanders¹, Anne T Fox¹, Andrew G Letizia¹, Michael R Wiley⁷, Naiki Attram¹

Affiliations

¹ Naval Medical Research Unit No. 3, Accra, Ghana.
² West African Centre for Cell Biology of Infectious Pathogens, College of Basic and Applied Sciences, University of Ghana, Accra, Ghana.
³ Department of Biochemistry, Cell and Molecular Biology, University of Ghana, Accra, Ghana.
⁴ Biomedical Engineering Department, School of Engineering Sciences, University of Ghana, Accra, Ghana.
⁵ Bacteriology Department, Noguchi Memorial Institute for Medical Research, University of Ghana, Accra, Ghana.
⁶ Center for Bio/Molecular Science and Engineering, Naval Research Laboratory, Washington, DC, United States.
⁷ Nebraska Medical Center, Omaha, NE, United States.

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 pblaTEM 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.

Keywords: Ghana; Neisseria gonorrhoeae; antimicrobial resistance; core genome MLST; gonorrhea; whole genome sequencing.