Molecular epidemiology and antimicrobial resistance mechanisms of Campylobacter coli from diarrheal patients and broiler carcasses in Belgium

Authors: ELHADIDY, MOHAMED - Mansoura University; Miller, William - Bill; ARGUELLO, HECTOR - Universidad De Cordoba; ÁLVAREZ-ORDÓÑEZ, AVELINO - University Of Leon; DIERICK, KATELIJNE - Scientific Institute Of Public Health; BOTTELDOORN, NADINE - Scientific Institute Of Public Health

Submitted to: Transboundary and Emerging Diseases
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/12/2018
Publication Date: 10/22/2018
Citation: Elhadidy, M., Miller, W.G., Arguello, H., Álvarez-Ordóñez, A., Dierick, K., Botteldoorn, N. 2018. Molecular epidemiology and antimicrobial resistance mechanisms of Campylobacter coli from diarrheal patients and broiler carcasses in Belgium. Transboundary and Emerging Diseases. 66:463-475. https://doi.org/10.1111/tbed.13046.
DOI: https://doi.org/10.1111/tbed.13046

Interpretive Summary: The food-borne pathogen Campylobacter is a natural contaminant of most birds and livestock, with poultry meat the major vehicle for Campylobacter-associated illness in humans. Although the majority of Campylobacter-caused cases of human gastroenteritis are associated with Campylobacter jejuni, a substantial proportion is associated with the related organism Campylobacter coli. This study characterized 59 C. coli strains recovered from both chicken broiler carcasses and human diarrheal samples. Four different molecular typing methods were used: all demonstrated significant discriminatory power in identifying different strain types with the number of identified strain types increasing upon combination of typing methods. Campylobacter coli are also distinguished by a high rate of antimicrobial resistance within the species. Resistance to the antibiotics ciprofloxacin, nalidixic acid, streptomycin, tetracycline, erythromycin, chloramphenicol and gentamicin was tested. All 59 strains were sensitive to gentamicin but the strain set demonstrated different degrees of resistance to the remaining antibiotics; >75% of the strains were resistant to either tetracycline or the quinolone antibiotics ciprofloxacin and nalidixic acid, while only 5% were resistant to chloramphenicol. Multidrug resistance, that is, resistance to three or more classes of antibiotics, was identified in ~40% of the strains. The genetic basis of resistance was characterized among the resistant isolates. All of the resistant strains contained genes or mutations previously associated with antimicrobial resistance. The data generated from this study will help to address food security and public health challenges resulting from C. coli infection.

Technical Abstract: The aim of this study was to better understand the molecular epidemiology of Campylobacter coli isolated from multiple sources in Belgium, by studying the genotypic diversity and antimicrobial resistance phenotypes and resistance mechanisms of 59 C. coli isolates. Isolates from broiler carcasses and human cases were genotyped using multilocus sequence typing (MLST), porA typing, flagellin gene A restriction fragment length polymorphism (flaA–RFLP) typing and by PCR binary typing (P-BIT). Thirty-two MLST sequence types, 24 flaA types, 31 porA alleles and 29 P-BIT types were identified among the screened isolates. Some types and alleles were shared among strains recovered from both broiler carcasses and diarrheal patients. Both porA typing and MLST revealed a similar discriminatory power (0.969), which was the highest discriminatory power when compared to other methods. Minimum inhibitory concentrations against seven different antibiotics (ciprofloxacin, chloramphenicol, nalidixic acid, streptomycin, tetracycline, gentamicin, and erythromycin) were analysed. Strains were most frequently-resistant to tetracycline (83.1%), followed by: ciprofloxacin and nalidixic acid (76.3%); streptomycin (33.9%); erythromycin (27.1%); and chloramphenicol (5.1%). All isolates were sensitive to gentamicin. Multidrug resistance was observed in 23 of 59 C. coli isolates (39%). Molecular screening of antimicrobial resistance mechanisms revealed the predominance of the GyrA T86I substitution among ciprofloxacin- and nalidixic acid-resistant isolates, the tet(O) gene among tetracycline-resistant isolates and the 23S rRNA A2074G mutation among erythromycin- resistant isolates. Furthermore, some erythromycin-resistant isolates harbored a diverse array of resistance mechanisms, including the presence of ermB and point mutations in the 23S rRNA genes, the rplD and rplV ribosomal genes, and the cmeABC multidrug efflux pump genes.