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Article

From the Farms to the Dining Table: The Distribution and Molecular Characteristics of Antibiotic-Resistant Enterococcus spp. in Intensive Pig Farming in South Africa

1
Antimicrobial Research Unit, College of Health Sciences, University of KwaZulu-Natal, Durban 4000, South Africa
2
Biomedical Resource Unit, College of Health Sciences, University of KwaZulu-Natal, Durban 4000, South Africa
3
Centre for Respiratory Diseases and Meningitis, National Institute for Communicable Diseases, Johannesburg 2131, South Africa
4
Epidemiology Section, KwaZulu-Natal Agriculture & Rural Development-Veterinary Service, Pietermaritzburg 3201, South Africa
*
Author to whom correspondence should be addressed.
Academic Editors: Jens André Hammerl and Cinzia Lucia Randazzo
Microorganisms 2021, 9(5), 882; https://doi.org/10.3390/microorganisms9050882
Received: 1 March 2021 / Revised: 18 March 2021 / Accepted: 1 April 2021 / Published: 21 April 2021
(This article belongs to the Special Issue Antimicrobial Resistance and Molecular Tracing of Foodborne Pathogens)
Foodborne pathogens, including antibiotic-resistant species, constitute a severe menace to food safety globally, especially food animals. Identifying points of concern that need immediate mitigation measures to prevent these bacteria from reaching households requires a broad understanding of these pathogens’ spread along the food production chain. We investigated the distribution, antibiotic susceptibility, molecular characterization and clonality of Enterococcus spp. in an intensive pig production continuum in South Africa, using the farm-to-fork approach. Enterococcus spp. were isolated from 452 samples obtained along the pig farm-to-fork continuum (farm, transport, abattoir, and retail meat) using the IDEXX Enterolert®/Quanti-Tray® 2000 system. Pure colonies were obtained on selective media and confirmed by real-time PCR, targeting genus- and species-specific genes. The susceptibility to antibiotics was determined by the Kirby–Bauer disk diffusion method against 16 antibiotics recommended by the WHO-AGISAR using EUCAST guidelines. Selected antibiotic resistance and virulence genes were detected by real-time PCR. Clonal relatedness between isolates across the continuum was evaluated by REP-PCR. A total of 284 isolates, consisting of 79.2% E. faecalis, 6.7% E. faecium, 2.5% E. casseliflavus, 0.4% E. gallinarum, and 11.2% other Enterococcus spp., were collected along the farm-to-fork continuum. The isolates were most resistant to sulfamethoxazole-trimethoprim (78.8%) and least resistant to levofloxacin (5.6%). No resistance was observed to vancomycin, teicoplanin, tigecycline and linezolid. E. faecium displayed 44.4% resistance to quinupristin-dalfopristin. Also, 78% of the isolates were multidrug-resistant. Phenotypic resistance to tetracycline, aminoglycosides, and macrolides was corroborated by the presence of the tetM, aph(3′)-IIIa, and ermB genes in 99.1%, 96.1%, and 88.3% of the isolates, respectively. The most detected virulence gene was gelE. Clonality revealed that E. faecalis isolates belonged to diverse clones along the continuum with major REP-types, mainly isolates from the same sampling source but different sampling rounds (on the farm). E. faecium isolates revealed a less diverse profile. The results suggest that intensive pig farming could serve as a reservoir of antibiotic-resistant bacteria that could be transmitted to occupationally exposed workers via direct contact with animals or consumers through animal products/food. This highlights the need for more robust guidelines for antibiotic use in intensive farming practices and the necessity of including Enterococcus spp. as an indicator in antibiotic resistance surveillance systems in food animals. View Full-Text
Keywords: antibiotic resistance; Enterococcus spp.; multidrug resistance; farm-to-fork; intensive pig farming; public health; biosecurity; food safety; virulence genes; one health antibiotic resistance; Enterococcus spp.; multidrug resistance; farm-to-fork; intensive pig farming; public health; biosecurity; food safety; virulence genes; one health
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MDPI and ACS Style

Badul, S.; Abia, A.L.K.; Amoako, D.G.; Perrett, K.; Bester, L.A.; Essack, S.Y. From the Farms to the Dining Table: The Distribution and Molecular Characteristics of Antibiotic-Resistant Enterococcus spp. in Intensive Pig Farming in South Africa. Microorganisms 2021, 9, 882. https://doi.org/10.3390/microorganisms9050882

AMA Style

Badul S, Abia ALK, Amoako DG, Perrett K, Bester LA, Essack SY. From the Farms to the Dining Table: The Distribution and Molecular Characteristics of Antibiotic-Resistant Enterococcus spp. in Intensive Pig Farming in South Africa. Microorganisms. 2021; 9(5):882. https://doi.org/10.3390/microorganisms9050882

Chicago/Turabian Style

Badul, Sasha, Akebe L.K. Abia, Daniel G. Amoako, Keith Perrett, Linda A. Bester, and Sabiha Y. Essack. 2021. "From the Farms to the Dining Table: The Distribution and Molecular Characteristics of Antibiotic-Resistant Enterococcus spp. in Intensive Pig Farming in South Africa" Microorganisms 9, no. 5: 882. https://doi.org/10.3390/microorganisms9050882

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