Novel gentamicin resistance genes in <i>Campylobacter</i> isolated from humans and retail meats in the USA

Zhao, Shaohua; Mukherjee, Sampa; Chen, Yuansha; Liu, Cong; Young, Shenia; Warren, Melissa J.; Abbott, Jason; Friedman, Sharon; Kabera, Claudine; Karlsson, Maria; McDermott, Patrick F.

doi:10.1093/jac/dkv001

Cited by 55 publications

(55 citation statements)

References 31 publications

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“…We identified seven GEN r genes, but only aph(2Љ)-If and aph(2Љ)-Ig were shared in isolates recovered from humans, poultry, and poultry meats. Our recent study showed that the genetically diverse APH(2Љ) family was a major contributor to GEN r in Campylobacter, with amino acid identity between the subfamilies ranging from 26% to 52% (23). Using this new knowledge, we were able to successfully correlate resistance genotypes and phenotypes for the vast majority of isolates.…”

Section: Discussionmentioning

confidence: 97%

Whole-Genome Sequencing Analysis Accurately Predicts Antimicrobial Resistance Phenotypes in Campylobacter spp

Zhao

Tyson

Chen

et al. 2016

Appl Environ Microbiol

220

189

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The objectives of this study were to identify antimicrobial resistance genotypes for Campylobacter and to evaluate the correlation between resistance phenotypes and genotypes using in vitro antimicrobial susceptibility testing and whole-genome sequencing (WGS). A total of 114 Campylobacter species isolates (82 C. coli and 32 C. jejuni) obtained from 2000 to 2013 from humans, retail meats, and cecal samples from food production animals in the United States as part of the National Antimicrobial Resistance Monitoring System were selected for study. Resistance phenotypes were determined using broth microdilution of nine antimicrobials. Genomic DNA was sequenced using the Illumina MiSeq platform, and resistance genotypes were identified using assembled WGS sequences through blastx analysis. Eighteen resistance genes, including tet ( There was a high degree of correlation between phenotypic resistance to a given drug and the presence of one or more corresponding resistance genes. Phenotypic and genotypic correlation was 100% for tetracycline, ciprofloxacin/nalidixic acid, and erythromycin, and correlations ranged from 95.4% to 98.7% for gentamicin, azithromycin, clindamycin, and telithromycin. All isolates were susceptible to florfenicol, and no genes associated with florfenicol resistance were detected. There was a strong correlation (99.2%) between resistance genotypes and phenotypes, suggesting that WGS is a reliable indicator of resistance to the nine antimicrobial agents assayed in this study. WGS has the potential to be a powerful tool for antimicrobial resistance surveillance programs. W hole-genome sequencing (WGS) technology has become a fast and affordable tool that is revolutionizing research in the fields of genetics, microbiology, and ecology, as well as public health surveillance and response. Recent studies have shown that WGS analysis can potentially be a single, rapid, and cost-effective approach to define resistance genotypes and predict resistance phenotypes of bacteria with great sensitivity and specificity (1-4).Current laboratory methods, such as broth microdilution, measure antimicrobial susceptibility based on the growth response of bacteria following exposure to the drugs. These methods are advantageous in that they help us understand the concentration of drug necessary to prevent growth of the organism, a measure that is directly related to the clinical success of antimicrobial therapy. However, such phenotypic testing can be costly and timeconsuming, especially for bacteria such Campylobacter that require special growth conditions. Several antimicrobial susceptibility testing methods have been developed for Campylobacter, including agar dilution, disk diffusion, Etest, and broth microdilution (5-7). Each of these methods can test only a limited number of antimicrobials. Reproducibility between laboratories also can be problematic, even when published guidelines are followed, due to variations in medium, incubation conditions, inoculum density, and antimicrobial stability (1,8). Several studi...

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Section: Discussionmentioning

confidence: 97%

Whole-Genome Sequencing Analysis Accurately Predicts Antimicrobial Resistance Phenotypes in Campylobacter spp

Zhao

Tyson

Chen

et al. 2016

Appl Environ Microbiol

220

189

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“…An increase in gentamicin resistance in C. coli from retail chicken the USA has recently been observed (FDA, 2011), with most isolates originating from the western region of the USA and apparently related to the clonal expansion of a particular C. coli lineage. The resistance gene aph(2'')-Ig was responsible for conferring gentamicin resistance in these USA retail chicken C. coli isolates and was colocated on a plasmid which also carried tet(O) resistance (Zhao et al, 2015). Gentamicin resistance was detected in C. jejuni from broilers and turkeys, and C. coli from broilers in EU MSs in 2014, although whether clonal expansion of strains is also playing any role in the occurrence of gentamicin resistance in these Campylobacter isolates is not known.…”

Section: Antimicrobial Resistance In Campylobacter In Poultry and Meamentioning

confidence: 99%

The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2014

2016

EFS2

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The data on antimicrobial resistance in zoonotic and indicator bacteria in 2014, submitted by 28 EU Member States (MSs), were jointly analysed by EFSA and ECDC. Resistance in zoonotic Salmonella and Campylobacter species from humans, animals and food, and resistance in indicator Escherichia coli as well as meticillin‐resistant Staphylococcus aureus in animals and food was assessed. ‘Microbiological’ resistance was assessed using epidemiological cut‐off (ECOFF) values; for some countries, quantitative data on human isolates were interpreted in a way which corresponds closely to the ECOFF‐defined ‘microbiological’ resistance. In Salmonella from humans, high proportions of isolates were resistant to ampicillin, sulfonamides and tetracyclines, whereas resistance to third‐generation cephalosporins and to fluoroquinolones remained generally low, although it was markedly higher in some serovars commonly associated with broilers and turkeys. In Salmonella and Escherichia coli isolates from broilers, fattening turkeys and meat thereof, resistance to ampicillin, (fluoro)quinolones, tetracyclines and sulfonamides was frequently detected, whereas resistance to third‐generation cephalosporins was uncommon. For the first time, presumptive extended spectrum beta‐lactamase (ESBL)‐/AmpC‐/carbapenemase production in Salmonella and Escherichia coli was monitored in poultry. The occurrence of ESBL‐/AmpC‐producers was low, and carbapenemase‐producers were not detected. Resistance to colistin was observed at low levels in Salmonella and Escherichia coli from poultry and meat thereof. In Campylobacter from humans, a high to very high proportion of isolates were resistant to ciprofloxacin and tetracyclines, whereas resistance to erythromycin was low to moderate. Resistance to fluoroquinolones in some MSs was extremely high; in such settings, the effective treatment options for human enteric Campylobacter infection may be significantly reduced. High resistance to ciprofloxacin and tetracyclines was observed in Campylobacter isolates from broilers and broiler meat, whereas much lower levels were recorded for erythromycin. Co‐resistance to critically important antimicrobials in both human and animal isolates was generally uncommon, but very high to extremely high MDR levels were observed in some Salmonella serovars. A minority of Salmonella isolates from animals belonging to a few serovars (notably Kentucky and Infantis) exhibited high‐level resistance to ciprofloxacin.

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“…In the United States, gentamicin resistance in Campylobacter was rarely reported before 2007 according to National Antimicrobial Resistance Monitoring System (NARMS) studies; however, an increasing trend of resis-tance to aminoglycosides was observed in recent years (9). In 2011, 12.2% of human isolates and 18.1% of retail isolates showed resistance to aminoglycosides (9). In China, the gentamicin resistance rate in Campylobacter has been at a much higher level than in other countries (10)(11)(12).…”

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confidence: 99%

“…The aacA/aphD gene encoding a bifunctional enzyme was associated with gentamicin resistance (16). Very recently, several variants of 2Љ-phosphotransferase accounting for gentamicin resistance were identified in Campylobacter in the United States (9,17).…”

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confidence: 99%

High Prevalence and Predominance of the aph(2″)-If Gene Conferring Aminoglycoside Resistance in Campylobacter

Yao

Liu

Wang

et al. 2017

Antimicrob Agents Chemother

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Campylobacter is a major foodborne pathogen, and previous studies revealed that Campylobacter isolates from food-producing animals are increasingly resistant to gentamicin in China. The molecular epidemiology and genetic mechanisms responsible for gentamicin resistance in China have not been well understood. In this study, 607 Campylobacter isolates of chicken and swine origins collected in 2014 were analyzed, revealing that 15.6% (25/160) of the Campylobacter jejuni isolates and 79.9% (357/447) of the Campylobacter coli isolates were resistant to gentamicin. PCR detection of the gentamicin resistance genes indicated that aph(2Љ)-If was more prevalent than the previously identified aacA/aphD gene and has become the dominant gentamicin resistance determinant in Campylobacter. Transformation and wholegenome sequencing as well as long-range PCR discovered that aph(2Љ)-If was located on a chromosomal segment inserted between two conserved genes, Cj0299 and panB. Cloning of aph(2Љ)-If into gentamicin-susceptible C. jejuni NCTC 11168 confirmed its function in conferring high-level resistance to gentamicin and kanamycin. Molecular typing by pulsed-field gel electrophoresis suggested that both regional expansion of a particular clone and horizontal transmission were involved in the dissemination of the aph(2Љ)-If gene in Campylobacter. To our knowledge, this is the first report describing the high prevalence of a chromosomally encoded aph(2Љ)-If gene in Campylobacter. The high prevalence and predominance of this gene might be driven by the use of aminoglycoside antibiotics in food animal production in China and potentially compromise the usefulness of gentamicin as a therapeutic agent for Campylobacter-associated systemic infection.

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Novel gentamicin resistance genes in Campylobacter isolated from humans and retail meats in the USA

Cited by 55 publications

References 31 publications

Whole-Genome Sequencing Analysis Accurately Predicts Antimicrobial Resistance Phenotypes in Campylobacter spp

Whole-Genome Sequencing Analysis Accurately Predicts Antimicrobial Resistance Phenotypes in Campylobacter spp

The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2014

High Prevalence and Predominance of the aph(2″)-If Gene Conferring Aminoglycoside Resistance in Campylobacter

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