Abstract
The increasing resistance of Campylobacter to clinically important antibiotics, such as fluoroquinolones and macrolides, is a serious public health problem. The objective of this study is to investigate synergistic anti-Campylobacter jejuni activity of fluoroquinolones and macrolides in combination with phenolic compounds. Synergistic antimicrobial activity was measured by performing a checkerboard assay with ciprofloxacin and erythromycin in the presence of 21 phenolic compounds. Membrane permeability changes in C. jejuni by phenolic compounds were determined by measuring the level of intracellular uptake of 1-N-phenylnaphthylamine (NPN). Antibiotic accumulation assays were performed to evaluate the level of ciprofloxacin accumulation in C. jejuni. Six phenolic compounds, including p-coumaric acid, sinapic acid, caffeic acid, vanillic acid, gallic acid, and taxifolin, significantly increased the susceptibility to ciprofloxacin and erythromycin in several human and poultry isolates. The synergistic antimicrobial effect was also observed in ciprofloxacin- and erythromycin-resistant C. jejuni strains. The phenolic compounds also substantially increased membrane permeability and antibiotic accumulation in C. jejuni. Interestingly, some phenolic compounds, such as gallic acid and taxifolin, significantly reduced the expression of the CmeABC multidrug efflux pump. Phenolic compounds increased the NPN accumulation in the cmeB mutant, indicating phenolic compounds may affect the membrane permeability. In this study, we successfully demonstrated that combinational treatment of C. jejuni with antibiotics and phenolic compounds synergistically inhibits C. jejuni by impacting both antimicrobial influx and efflux.
Highlights
Campylobacter jejuni is one of the leading bacterial causes of human gastroenteritis worldwide (Butzler, 2004)
8 μg ml−1 of the six phenolic compounds resulted in approximately 4–32-fold reduction in the MICs of ciprofloxacin and erythromycin in five different C. jejuni strains, including three human isolates (NCTC 11168, HCJ 4132, and HCJ 2316) and two poultry isolates (P1 and P2; Table 1 and Supplementary Tables S3–S7)
By screening 21 phenolic compounds, in this study, we identified six phenolic compounds that substantially increased the antimicrobial activity of ciprofloxacin and erythromycin against several C. jejuni strains from humans and poultry (Table 1 and Supplementary Tables S1–S7), including strains with antibiotic resistance (Table 1 and Supplementary Table S8)
Summary
Campylobacter jejuni is one of the leading bacterial causes of human gastroenteritis worldwide (Butzler, 2004). It is estimated that Campylobacter accounts for approximately 400–500 million infection cases worldwide per year (Ruiz-Palacios, 2007). C. jejuni inhabits the gastrointestinal tracts of poultry as a commensal microorganism; the consumption of undercooked poultry is the most frequent cause of human infections with C. jejuni (Ruiz-Palacios, 2007). C. jejuni can spread by cross-contamination and during inadequate storage (Cogan et al, 1999; Luber et al, 2006). The dissemination of foodborne pathogens via hands and food-contact surfaces of food processing equipment has been well documented by a number of researchers (Kusumaningrum et al, 2003; Van Asselt et al, 2008).
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