Characterization of a Novel Neisseria gonorrhoeae Penicillinase-Producing Plasmid Isolated in Australia in 2012

Trembizki, Ella; Buckley, Cameron; Lawrence, Andrew J; Lahra, Monica M; Whiley, David M.

doi:10.1128/aac.02993-14

Cited by 27 publications

(28 citation statements)

References 17 publications

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“…Overall, the African plasmid type was most common, comprising 237/ 327 isolates (72.5%), followed by the Rio/Toronto (n ϭ 47; 14.4%) and the Asian (n ϭ 43; 13.1%) plasmids. (It should be noted that the 47 Rio/Toronto plasmids included a single isolate with the recently described "Australian plasmid"-a variant of the Rio/Toronto plasmid that we described in our preliminary investigations [7]. The plasmid typing method does not differentiate such variants.…”

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“…A total of 351 PPNG clinical isolates were included in this study (Table 1). These were all PPNG isolates identified as part of a broader investigation of N. gonorrhoeae isolates (n ϭ 2,455) that were collected from throughout Australia in the first half of the year 2012 (7,15). The isolates were initially determined to be PPNG on the basis of acidometric and nitrocefin disc testing and subsequently by real-time PCR (7).…”

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Penicillinase-Producing Plasmid Types in Neisseria gonorrhoeae Clinical Isolates from Australia

Whiley

Trembizki

Buckley

et al. 2014

Antimicrob Agents Chemother

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h Penicillinase-producing Neisseria gonorrhoeae (PPNG) carrying the bla TEM-135 gene is of particular concern, as it is considered a stepping stone toward resistance to extended-spectrum cephalosporins. Here, we sought to characterize plasmid types and the occurrence of the bla TEM-135 gene for N. gonorrhoeae clinical isolates from Australia. We found that bla TEM-135 was prevalent in Australian PPNG and was detected on all three major plasmid types. High-level resistance to penicillin in Neisseria gonorrhoeae is conferred by plasmid-mediated penicillinase production. To date, seven different penicillinase-harboring gonococcal plasmid types have been described and comprise three main plasmid types (Asian, African, and Rio/Toronto plasmids) and four less common variants (Nimes, New Zealand, Johannesburg, and Australian plasmids) (1-7). There are two different penicillinase genes that may be carried by these plasmids, including the classical bla TEM-1 gene and the more recently described gonococcal bla TEM-135 gene (8). The bla gene is of concern as it is considered to be an intermediate between a penicillinase and an extended-spectrum ␤-lactamase (9) and is therefore considered a potential future threat to the effectiveness of N. gonorrhoeae treatment. The bla TEM-135 gene was first described in an isolate from Thailand (8) and has since been reported in various countries, including Canada (10), China (11), Japan (12), and Switzerland (13). However, there are now more recent data showing that bla has been present in gonococci since at least 1984, suggesting that the gene is not, as originally thought, a recent evolutionary event driven by selective pressure through the use of extended-spectrum cephalosporins (14).Data on the rate at which penicillinase-producing N. gonorrhoeae (PPNG) isolates carry the bla TEM-135 gene are limited, ranging from 9.4% (9/96 PPNG isolates) in Thailand (9) and 20% (2/10 PPNG isolates) in Japan (12) to 58% (66/114 PPNG isolates) in China (11). These studies also highlighted that bla TEM-135 may occur in distinct genetic backgrounds and suggested that the gene has continued to be shared among gonococci via horizontal genetic exchange, having been found on the Asian and Rio/Toronto plasmid types and across various multilocus sequence types (MLST) and N. gonorrhoeae multiantigen sequence types (NG-MAST) (8,11,12,14).In this study, we sought to characterize plasmid types and the occurrence of the bla TEM-135 gene in N. gonorrhoeae clinical isolates from Australia. A total of 351 PPNG clinical isolates were included in this study (Table 1). These were all PPNG isolates identified as part of a broader investigation of N. gonorrhoeae isolates (n ϭ 2,455) that were collected from throughout Australia in the first half of the year 2012 (7, 15). The isolates were initially determined to be PPNG on the basis of acidometric and nitrocefin disc testing and subsequently by real-time PCR (7). The DNA used for the real-time PCR testing was stored at Ϫ80°C until further investigation. Here, the DNA ...

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Penicillinase-Producing Plasmid Types in Neisseria gonorrhoeae Clinical Isolates from Australia

Whiley

Trembizki

Buckley

et al. 2014

Antimicrob Agents Chemother

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“…With regard to gonorrhea, MDR was defined as acquired non-susceptibility to at least one agent in three or more antimicrobial categories (26). Additionally, Trembizki et al (27) reported that N. gonorrhoeae isolates harbored a gene encoding for penicillinase production resulting in the spread of penicillin resistance among gonococci through horizontal gene transfer. In the present case report, production of β-lactamase by the test pathogen was confirmed and this might be contributed to the development of penicillin- and cephalosporin-resistance.…”

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Case Report of Urethritis in a Male Patient Infected with Two Different Isolates of Multiple Drug-Resistant Neisseria gonorrhoeae

Al-Madboly

Gheida

2017

Front. Med.

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We report a brief description of a case suffering from bacterial urethritis, conjunctivitis, and arthritis, caused by two different isolates of multiple drug-resistant Neisseria gonorrhoeae. Initial diagnosis was dependent on the patient history, clinical findings, symptoms, and the bacteriological data. Polymerase chain reaction confirmed the identification of the pathogens. Random amplified polymorphic DNA revealed two different patterns. Susceptibility testing was performed using Kirby–Bauer disk diffusion method and the minimum inhibitory concentration was also determined. It revealed multiple drug resistance associated with β-lactamase production. Only gentamicin, rifampicin, and azithromycin were active against the test pathogens. A dual therapy was initiated using gentamicin as well as azithromycin to treat the possible co-infection with Chlamydia trachomatis. Complete recovery of the patient achieved with resolved symptoms a week later.

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“…The original evaluations of this PPNG-PCR showed 100% sensitivity and 98.7% specificity compared to bacterial culture for detecting PPNG strains in clinical specimens (5). However, a more recent evaluation of the assay revealed a variant plasmid type, now called the Australian plasmid, which was negative by PPNG-PCR (6). In brief, we tested 342 PPNG isolates from throughout Australia from the year 2012 and found one isolate that was negative by PPNG-PCR.…”

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“…U20374), which included the region targeted by the PPNG-PCR (937 to 1024 bp) and hence accounted for the false-negative result. Several different gonococcal plasmids with various different deletions and insertions have now been described and named according to the geographical location of their initial discovery; these include the Asian (7,426 bp), African (5,599 bp), Rio de Janeiro/Toronto (5,154 bp), Nimes (6,798 bp), New Zealand (9,309 bp), Johannesburg (4,865 bp), and now the Australian (3,629 bp) plasmids (6)(7)(8).…”

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Multitarget PCR Assay for Direct Detection of Penicillinase-Producing Neisseria gonorrhoeae for Enhanced Surveillance of Gonococcal Antimicrobial Resistance

et al. 2015

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A ntimicrobial resistance (AMR) in Neisseria gonorrhoeae, the causative agent of the disease gonorrhea, is a major public issue and is now recognized by the U.S. Centers for Disease Control and Prevention (CDC) as one of the top three urgent AMR threats (1). Action plans to control the impact and spread of N. gonorrhoeae AMR have been released by the World Health Organization (WHO) and CDC (2, 3), and prominent among the listed recommendations is the need to improve AMR surveillance capabilities. Conventional N. gonorrhoeae AMR surveillance is performed by bacterial culture. However, bacterial culture has several major limitations, including the need for stringent sample handling and transport systems to maintain viable organisms, which are problems in remote and resource-limited settings. In addition, nucleic acid amplification tests (NAATs) are increasingly commonplace in the diagnosis of gonococcal infections in both remote and urban settings, which in turn are seeing further reductions in the use of bacterial culture and widening gaps in AMR data. For these reasons, there has been an increasing need for the development of molecular methods to enhance AMR surveillance activity (4). We recently described a real-time PCR method to detect penicillinase-producing N. gonorrhoeae (PPNG) directly within clinical samples (5). The method acts as an indirect marker for PPNG by targeting a region of DNA on the gonococcal plasmids carrying the penicillinase gene but not the penicillinase gene itself. The original evaluations of this PPNG-PCR showed 100% sensitivity and 98.7% specificity compared to bacterial culture for detecting PPNG strains in clinical specimens (5). However, a more recent evaluation of the assay revealed a variant plasmid type, now called the Australian plasmid, which was negative by . In brief, we tested 342 PPNG isolates from throughout Australia from the year 2012 and found one isolate that was negative by PPNG-PCR. DNA sequencing revealed a novel 1,885-bp deletion (corresponding to nucleotides 502 to 2385 of the Asian plasmid type, GenBank accession no. U20374), which included the region targeted by the PPNG-PCR (937 to 1024 bp) and hence accounted for the false-negative result. Several different gonococcal plasmids with various different deletions and insertions have now been described and named according to the geographical location of their initial discovery; these include the Asian (7,426 bp), African (5,599 bp), Rio de Janeiro/Toronto (5,154 bp), Nimes (6,798 bp), New Zealand (9,309 bp), Johannesburg (4,865 bp), and now the Australian (3,629 bp) plasmids (6-8).While our initial data suggest that the Australian plasmid may be rare in local gonococci, we sought to rectify the PPNG-PCR to account for this plasmid, particularly given that the PPNG-PCR is now used as a routine tool to inform gonorrhea treatment guidelines in remote parts of Australia where penicillin-based treatments are still used (9). In doing so, we aimed to limit the potential for false-negative results caused by further unrec...

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Characterization of a Novel Neisseria gonorrhoeae Penicillinase-Producing Plasmid Isolated in Australia in 2012

Cited by 27 publications

References 17 publications

Penicillinase-Producing Plasmid Types in Neisseria gonorrhoeae Clinical Isolates from Australia

Penicillinase-Producing Plasmid Types in Neisseria gonorrhoeae Clinical Isolates from Australia

Case Report of Urethritis in a Male Patient Infected with Two Different Isolates of Multiple Drug-Resistant Neisseria gonorrhoeae

Multitarget PCR Assay for Direct Detection of Penicillinase-Producing Neisseria gonorrhoeae for Enhanced Surveillance of Gonococcal Antimicrobial Resistance

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