Campylobacter jejuni and other emerging Campylobacteraceae in retail beef liver – an underestimated potential source?

Abstract

Bovine by‐products, such as liver, could be an underestimated source of Campylobacter jejuni. Therefore, our aims were to evaluate the occurrence of C. jejuni and other Campylobacteraceae in retail beef liver and characterize their antibiotic resistance (ciprofloxacin, tetracycline, erythromycin and gentamicin) and potential genetic relationship by flagellin gene restriction fragment length polymorphism (flaA‐RFLP) and multilocus sequence typing with clinical strains. Seventy‐six out of 206 samples (36·9%) were positive for Campylobacter and related organisms. Arcobacter butzleri was the most frequently isolated species (21·8%), followed by C. jejuni (9·7%), C. fetus (7·8%) and C. coli (1%). The C. jejuni strains showed resistance to tetracycline (17·2%) or ciprofloxacin (6·9%), with only one strain resistant to both antibiotics. Meanwhile, 8·3% of ciprofloxacin resistance was observed in C. fetus. The other species showed no resistance. Most of the clonal complexes (CC) in which the C. jejuni genotypes were grouped (CC‐21, 42, 48 and 52), coincided with genotypes of clinical strains previously reported in Chile. As such, this study provides evidence that beef liver could be an underestimated route for resistant C. jejuni to humans. Further studies should assess whether this food could play a role in the transmission of other emerging Campylobacteraceae such as those reported here.

Genomic Characterization of Antibiotic-Resistant Campylobacterales Isolated from Chilean Poultry Meat

“…This mutation is also associated with a gain in the fitness of Campylobacter, which would imply that strains with these mutations persist over time, even when the antibiotic is discontinued [44,45]. On the other hand, Campylobacter resistance to TET was similar to what had previously been reported for clinical strains, chicken meat and bovine liver in Chile [3,19]. All strains phenotypically resistant to TET possess the tet(O) gene in their genome [46].…”

“…The C. jejuni strains were grouped into clonal complexes (CC) previously reported in clinical strains isolated in Valdivia (CC-21, CC-48, CC-257 and CC-353) and Santiago (CC-21, CC-48, CC-49, CC-257, CC-353, CC-443, CC-446 and CC-658) [17,53]. One poultry isolate corresponded to ST-3874 belonging to CC-354, which has been previously reported in a bovine liver isolate in the same geographical area (Valdivia city) and has also been isolated from clinical samples in the USA and Canada [19,75]. A total of 21% of the C. jejuni strains (4/19) clustered in CC-353, being the most prevalent CC, a genotype known to cause human infections and colonize broiler products, as well as its association with resistance to quinolones [76][77][78].…”

“…This pump has already been reported in Chile in Campylobacter spp. strains of bovine origin, as well as in clinical strains [19,53]. However, seven of the 19 C. jejuni genomes and all of C. coli (n = 14) presented mutations in the cmeR gene, which is associated with a greater expression of this multidrug efflux pump.…”

“…presented a prevalence of 40.8%, where the most isolated species was A. butzleri (37.4%), predominating even over the genus Campylobacter spp. (Table 2) [19,32,33]. This could be due to the capacity of A. butzleri to grow in a wide range of temperatures, in different atmospheres and in aquatic environments.…”

“…over the past two decades [17,18]. Likewise, resistance to CIP, TET, and Erythromycin (E) has been reported in isolates obtained from chicken and bovine meat [3,19]. Globally, it has been suggested that this increase in antimicrobial resistance is mainly due to the indiscriminate use of antibiotics in poultry and livestock production, to which is added the ability of these microorganisms to survive in these conditions and, therefore, endure over time, although there are also other potential resistance sources [20][21][22].…”