Occurrence, Antimicrobial Resistance and Molecular Characterization of <i>Campylobacter</i> spp. in Intensive Pig Production in South Africa

• Main Authors: Viwe Sithole, Daniel Gyamfi Amoako, Akebe Luther King Abia, Keith Perrett, Linda A. Bester, Sabiha Y. Essack
• Format: Article
• Language: English
• Published: MDPI AG 2021-04-01
• Series: Pathogens
• Subjects: molecular epidemiology; <i>Campylobacter</i> spp.; multidrug resistance; intensive pig production; foodborne pathogens; South Africa
• Online Access: https://www.mdpi.com/2076-0817/10/4/439

<i>Campylobacter</i> spp. are among the leading foodborne pathogens, causing campylobacteriosis, a zoonotic infection that results in bacterial gastroenteritis and diarrheal disease in animals and humans. This study investigated the molecular epidemiology of antibiotic-resistant <i>Campylobacter </i>spp. isolated across the farm-to-fork-continuum in an intensive pig production system in South Africa. Following ethical approval, samples were collected over sixteen weeks from selected critical points (farm, transport, abattoir, and retail) using a farm-to-fork sampling approach according to WHO-AGISAR guidelines. Overall, 520 samples were investigated for the presence of <i>Campylobacter</i> spp., which were putatively identified using selective media with identity and speciation confirmed by polymerase chain reaction (PCR) of specific genes. Resistance profiles were ascertained by the Kirby–Bauer disk diffusion method. Antibiotic resistance and virulence genes were identified using PCR and DNA sequencing. Clonal relatedness was determined using ERIC-PCR. Altogether, 378/520 (72.7%) samples were positive for <i>Campylobacter</i> spp., with <i>Campylobacter coli</i> being the predominant species (73.3%), followed by <i>Campylobacter jejuni</i> (17.7%); 8.9% of the isolates were classified as “other spp”. Relatively high resistance was observed in <i>C. coli</i> and <i>C. jejuni</i> to erythromycin (89% and 99%), streptomycin (87% and 93%), tetracycline (82% and 96%), ampicillin (69% and 85%), and ciprofloxacin (53% and 67%), respectively. Multidrug resistance (MDR) was noted in 330 of the 378 (87.3%) isolates. The antibiotic resistance genes observed were <i>tetO</i> (74.6%), <i>bla_OXA-</i>₆₁ (2.9%), and <i>cmeB</i> (11.1%), accounting for the resistance to tetracycline and ampicillin. The membrane efflux pump (<i>cmeB</i>), conferring resistance to multiple antibiotics, was also detected in most resistant isolates. Chromosomal mutations in <i>gyrA</i> (Thr-86-Ile) and <i>23S rRNA</i> (A2075G and A2074C) genes, conferring quinolone and erythromycin resistance, respectively, were also found. Of the virulence genes tested, <i>ciaB</i>, <i>dnaJ</i>, <i>pldA</i>, <i>cdtA</i>, <i>cdtB</i>, <i>cdtC</i>, and <i>cadF</i> were detected in 48.6%, 61.1%, 17.4%, 67.4%, 19.3%, 51%, and 5% of all <i>Campylobacter</i> isolates, respectively. Clonal analysis revealed that isolates along the continuum were highly diverse, with isolates from the same sampling points belonging to the same major ERIC-types. The study showed relatively high resistance to antibiotics commonly used in intensive pig production in South Africa with some evidence, albeit minimal, of transmission across the farm-to-fork continuum. This, together with the virulence profiles present in <i>Campylobacter</i> spp., presents a challenge to food safety and a potential risk to human health, necessitating routine surveillance, antibiotic stewardship, and comprehensive biosecurity in intensive pig production.