Antibiotic resistant bacteria prevalent in livestock and wildlife species in South Africa

Van den Honert, Michaela Sannettha (2019-04)

Thesis (PhDFoodSc)--Stellenbosch University, 2019.

Thesis

ENGLISH ABSTRACT: Much research has focussed on the fate of antibiotics in clinical settings whereas research of antibiotics in natural environments has been comparatively limited. It has been hypothesised that wildlife could play a significant role in the development of antibiotic resistant bacteria in nature as a variety of wildlife species carry antibiotic resistant bacteria and cover a large territory throughout their lifespan The aim of this study was to determine whether wild ungulates, namely, African buffalo (Syncerus caffer), black wildebeest (Connochaetes gnou), blue wildebeest (Connochaetes taurinus), bontebok (Damaliscus pygargus), eland (Taurotragus oryx), fallow deer (Dama dama), impala (Aepyceros melampus) and springbok (Antidorcas marsupialis), host antibiotic resistant bacteria, specifically, Escherichia coli, Enterococcus faecalis and Staphylococcus aureus, from various South African farms. The Kirby-Bauer disk diffusion method was used according to the Clinical and Laboratory Standards Institute 2018 guidelines. Overall, antibiotic resistance among the wild ungulate species was low towards the selected antibiotics. On average, the antibiotic resistance levels were 8% E. coli (N= 353), 4% E. faecalis (N= 194) and 22% S. aureus (N= 106). The highest antibiotic resistance was towards antibiotics which are of natural origin, namely the β-lactams and streptomycin. These antibiotics are found in the soil microbiome, produced by Actinobacteria. In addition, certain resistant genes were detected using the polymerase chain reaction in isolates which showed phenotypic resistance. The resistant genes sul1 (40%), sul2 (80%), sul3 (0%), blaCMY (98%), tetA (63%), tetB (75%), tetC (0%) and aadA (98%) were detected in resistant E. coli isolates (N= 44); tetK (7%), tetL (100%), tetM (100%), blaZ (100%), vanA (95%) and vanB (10%) in resistant S. aureus (N= 5) and E. faecalis (N= 22) isolates. The results of this study indicate that wildlife can be considered a natural reservoir of antibiotic resistant genes. The wildlife were also found to be more multi-drug resistant than the livestock. Thus it is speculated that these resistant genes are picked up from the soil and the surrounding environment and are spread by the animals as well as by other natural vectors like the wind and flies. Various factors and agricultural practices were found to influence the antibiotic resistance of the bacteria harboured by the wildlife species, namely, co-grazing with livestock, the practice of wildlife supplementary feeding and farm history of antibiotic use. Bacteria isolated from game meat was frequently more antibiotic resistant than bacteria from the faeces, indicating human cross-contamination during slaughter. The level of antibiotic resistance determined in this study from the bacteria of the wildlife from pristine areas, could serve as a baseline for monitoring the influence of human activities on the development of antibiotic resistance in various environments, which this study contributed towards.

AFRIKAANSE OPSOMMING: Heelwat navorsing fokus op die lot van antibiotika in kliniese omgewings terwyl navorsing van antibiotika in natuurlike omgewings relatief beperk is. Daar word veronderstel dat wild ‘n betekenisvolle rol kan speel in die ontwikkeling van antibiotika weerstandbiedende bakterieë in die natuur aangesien verskeie wildspesies draers van antibiotika weerstandbiedende bakterieë is en tydens hul lewensduur ‘n groot area dek. Die doel van hierdie studie was om te bepaal of wilde hoefdiere, naamlik Afrika-buffel (Syncerus caffer), swart wildebees (Connochaetes gnou), blou wildebees (Connochaetes taurinus), bontebok (Damaliscus pygargus), eland (Taurotragus oryx), hert (Dama dama), rooibok (Aepyceros melampus) en springbok (Antidorcas marsupialis), antibiotika weerstandbiedende bakterieë huisves, spesifiek, Escherichia coli, Enterococcus faecalis en Staphylococcus aureus, van verskeie Suid-Afrikaanse plase. Die Kirby-Bauer skyf diffusie metode is gebruik volgens die “Clinical and Laboratory Standards Institute” 2018 riglyne. Oor die algemeen was antibiotika weerstandbiedendheid onder die wild hoefdierspesies laag in terme van die geselekteerde antibiotika. Die gemiddelde antibiotika weerstandvlakke was 8% E. coli (N= 353), 4% E. faecalis (N= 194) en 22% S. aureus (N= 106). Die hoogste antibiotika weerstandbiedendheid was teenoor antibiotika van natuurlike oorsprong, naamlik die β-laktame en streptomisien. Hierdie antibiotika word gevind in die grondmikrobioom, en word geproduseer deur Aktinobakterieë. Daarbenewens is sekere weerstandbiedende gene opgespoor met behulp van die polimerase kettingreaksie in isolate wat fenotipiese weerstand getoon het. Die weerstandbiedende gene sul1 (40%), sul2 (80%), sul3 (0%), blaCMY (98%), tetA (63%), tetB (75%), tetC (0%) en aadA (98%) is opgespoor in weerstandbiedende E. coli isolate (N= 44); tetK (7%), tetL (100%), tetM (100%), blaZ (100%), vanA (95%) en vanB (10%) in weerstandbiedende S. aureus (N= 5) en E. faecalis (N= 22) isolate. Die resultate van hierdie studie dui aan dat wild beskou kan word as ‘n natuurlike reservoir vir antibiotika weerstandbiedende gene. Daar is ook bevind dat wild meer weerstandig is teen veelsoortige antibiotika as wat vee is. Daar word dus gespekuleer dat hierdie weerstandbiedende gene opgetel word uit die grond en die omliggende omgewing en dan versprei word deur die diere sowel as ander natuurlike vektore soos die wind en vlieë. Daar is gevind dat verskeie faktore en landboupraktyke die antibiotika weerstandbiedendheid van die bakterieë wat deur die wildspesies gehuisves word beïnvloed, naamlik, mede-weiding met vee, die gebruik van aanvullende voeding vir wild en geskiedenis van antibiotika gebruik op die plaas. Bakterieë wat uit wildvleis geisoleer is, was dikwels meer weerstandbiedend teen antibiotika as bakterieë wat afkomstig is van ontlasting. Dit dui op menslike kruiskontaminasie tydens die slagproses. Die vlak van antibiotika weerstandbiedendheid wat in hierdie studie bepaal is vanaf die bakterieë van die wild van ongerepte gebiede, kan as basis dien vir die monitering van die invloed van menslike aktiwiteite op die ontwikkeling van antibiotika weerstandbiedendheid in verskeie omgewings, waartoe hierdie studie bygedra het.

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