Emergence of Fluoroquinolone-Resistant Campylobacter jejuni and Campylobacter coli among Australian Chickens in the Absence of Fluoroquinolone Use

Abstract

In a structured survey of all major chicken-meat producers in Australia, we investigated the antimicrobial resistance (AMR) and genomic characteristics of Campylobacter jejuni (n = 108) and C. coli (n = 96) from cecal samples of chickens at slaughter (n = 200). The majority of the C. jejuni (63%) and C. coli (86.5%) samples were susceptible to all antimicrobials. Fluoroquinolone resistance was detected among both C. jejuni (14.8%) and C. coli (5.2%), although this only included three sequence types (STs) and one ST, respectively. Multidrug resistance among strains of C. jejuni (0.9%) and C. coli (4.1%) was rare, and fluoroquinolone resistance, when present, was never accompanied by resistance to any other agent. Comparative genome analysis demonstrated that Australian isolates were found dispersed on different branches/clusters within the international collection. The major fluoroquinolone-resistant STs of C. jejuni (ST7323, ST2083, and ST2343) and C. coli (ST860) present in Australian chickens were similar to those of international isolates and have been reported previously in humans and animals overseas. The detection of a subpopulation of Campylobacter isolates exclusively resistant to fluoroquinolone was unexpected since most critically important antimicrobials such as fluoroquinolones are excluded from use in Australian livestock. A number of factors, including the low level of resistance to other antimicrobials, the absence of fluoroquinolone use, the adoption of measures for preventing spread of contagion between flocks, and particularly the genomic identities of isolates, all point to humans, pest species, or wild birds as being the most plausible source of organisms. This study also demonstrates the need for vigilance in the form of surveillance for AMR based on robust sampling to manage AMR risks in the food chain. IMPORTANCE Campylobacter is one of the most common causes of gastroenteritis in humans, with infections frequently resulting from exposure to undercooked poultry products. Although human illness is typically self-limiting, a minority of cases do require antimicrobial therapy. Ensuring that Campylobacter originating from meat chickens does not acquire resistance to fluoroquinolones is therefore a valuable outcome for public health. Australia has never legalized the use of fluoroquinolones in commercial chickens and until now fluoroquinolone-resistant Campylobacter has not been detected in the Australian poultry. This structured survey of meat chickens derived from all major Australian producers describes the unexpected emergence of fluoroquinolone resistance in Campylobacter jejuni and C. coli. Genetic characterization suggests that these isolates may have evolved outside the Australian poultry sector and were introduced into poultry by humans, pest species, or wild birds. The findings dramatically underline the critical role of biosecurity in the overall fight against antimicrobial resistance.

Risk of multi-drug resistant Campylobacter spp. and residual antimicrobials at poultry farms and live bird markets in Bangladesh

“…10,000,000 people may die in 2050 if no action is taken [14]. Unwise antimicrobial use in poultry farms, and also their interactive environmental and industrial sources, e.g., agriculture and farmed or reared animals, and human populations, are inducing selective pressure to develop drug resistance among the zoonotic pathogens, including campylobacters [15]. Increasing occurrence of MDR pathogens, including Campylobacter spp., has been an alarming global issue for 'One Health', which consider the health of humans, animals, and the environment in a holistic manner [14,16,17].…”

Antibiotic Resistance in Recreational Waters: State of the Science

“…The animal supply chain also includes slaughter, rendering, and carcass disposal steps of the animal husbandry process, and bacteria from these sources are known to enter ambient waters. AMR of Campylobacter jejuni and Campylobacter coli was assessed in a survey of 200 cecal samples of chickens ready for slaughter from 20 major producers in Australia [169]. Of the 108 C. jejuni isolates, the most commonly detected resistance was to tetracycline (n = 24) followed by resistance to the quinolones, ciprofloxacin (n = 16) and nalidixic acid (n = 16) [169].…”

“…AMR of Campylobacter jejuni and Campylobacter coli was assessed in a survey of 200 cecal samples of chickens ready for slaughter from 20 major producers in Australia [169]. Of the 108 C. jejuni isolates, the most commonly detected resistance was to tetracycline (n = 24) followed by resistance to the quinolones, ciprofloxacin (n = 16) and nalidixic acid (n = 16) [169]. C. coli isolates exhibited less overall AMR.…”

“…C. coli isolates exhibited less overall AMR. However, 5 of the 96 isolates were resistant to ciprofloxacin, nalidixic acid, azithromycin, erythromycin, and clindamycin, respectively, 4 isolates were resistant to telithromycin, and 3 isolates were resistant to tetracycline [169]. Additionally, several studies have found AMR bacteria in untreated wastewater released directly to surface waters from slaughterhouse and animal/meat processing plants, which has led researchers to conclude that these are significant local sources of AMR bacteria [170][171][172][173][174].…”

Characterization of Sunflower Oil Extracts from the Lichen Usnea barbata

“…Among the most important MDR bacteria, the “ESKAPE” group encompassing Enterococcus faecium , Staphylococcus aureus , Klebsiella pneumoniae , Acinetobacter baumannii , Pseudomonas aeruginosa , and Enterobacter strains can escape the biocidal action of most antimicrobial agents [ 10 ]. In the poultry industry, a steadily increasing level of MDR bacteria has also been reported, for example of Escherichia coli [ 11 ], Campylobacter [ 12 , 13 , 14 ], Salmonella [ 15 , 16 ], and methicillin-resistant S. aureus (MRSA) [ 17 , 18 ].…”