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Frank Eric Tatsing Foka Assessment of feedlots cattle in the development and spread of Vancomycin resistant Enterococci Frank Eric Tatsing Foka Orcid ID: 0000-0001-6577-2827 Thesis submitted in fulfilment of requirements for the degree of Doctor of Philosophy in Biology at the North-West University Promoter: Professor C.N. Ateba Examination: December 2019 Student number: 28035348 SUMMARY Enterococci are commensals of the gastrointestinal tract of warm-blooded animals. They have been incriminated in a wide range of community-aquired infections and nosocomial diseases, especially in immunocompromised individuals and stressed animals. If enterococci have been able to survive and thrive in different ecological niches to date, it is due mainly to their outstanding capability to adapt to these various environmental settings by incorporating into their genetic constitution, resistance genes to many currently used antimicrobials. The widespread use of antibiotics in industrial animal husbandry has contributed significantly to the emergence of resistant isolates, such as vancomycin-resistant enterococci (VREs) worldwide and in South Africa, specifically. Despite the fact that Avoparcin, which is a glycopeptide and analogue of vancomycin, was identified as the source of the emergence of VREs and was forbidden worldwide in industrial animal farming decades ago, VREs are regularly screened in environmental samples in the North West Province, South Africa. This study, therefore, sheds some light on the various reasons why VREs are continuously detected in environmental samples in the North West Province of South Africa. Very few studies in South Africa have focused on the involvement of cattle feedlots in the spread and dissemination of such strains in the environment. In this regard, we aseptically collected 384 faecal samples, 24 drinking troughs water and 24 soil/liter samples from six registered feedlots of the North West Province, South Africa. Thereafter, we used biochemical and molecular methods to identify and categorise the isolated enterococci. Furthermore, we determined their antibiotic resistance and their virulence profiles with phenotypic and genotypic methods as well as Next Generation Sequencing platforms. Five humdred and twenty-seven (527) presumptive isolates were recovered, while two hundred and eighty-nine (289) isolates were confirmed as members of the genus Enterococcus. Species specific PCR protocols were used to identify them as E. faecalis (9%), E. faecium (10%), E. durans (69%), E. gallinarum (6%), E. casseliflavus (2%), 2 E. mundtii (2%) and E. avium (2%). Vancomycin resistance genes were detected through PCR assays in 176 isolates, precisely vanA (62%), vanB (17%) and vanC (21%). Moreover, four Tetracycline efflux pump genetic determinants were also detected through PCR methods in 138 of the screened VREs and these included tetK (26), tetL (57), msrA/B (111) and mefA (9). All the VREs of this study were multidrug resistant and four antibiotic resistance profiles were identified. Furthermore, cylA, hyl, esp, gelE and asa1 virulence genes were detected in 86 VREs, with some harbouring more than one virulence gene. The cluster analysis of the VREs of this study was based on the diameters of the antibiotic inhibition zones and revealed a similar exposure history to the antibiotics tested. Data on antimicrobials currently used in the feedlots under investigation, either for prophylactic purposes or for therapeutic purposes as well as for growth promoting purposes, was collected. Data was assessed along with the bioinformatical analysis of the whole genome sequences of VR E. durans strain NWUTAL1 and VR E. gallinarum strain S52016, isolated from feedlot cattle faeces and feedlot soil/liter samples respectively. The data derived from these analyses revealed that some of the antibiotics used in the feedlots, were responsible for the resurgence of VREs. Specifically, plasmids with resistance genes to Tetracycline, Tylosin and Erythromycin were detected in these VREs. These antibiotics wield a sort of selective pressure on their specific antibiotic resistance genetic determinants that are co-selected with Vancomycin resistance genes. The fact that potentially pathogenic multidrug resistant VREs were detected in this study, demonstrates that practices such as the extensive usage of antibiotics in industrial animal husbandry, have a significant impact on the environment and its ecological niches. This may, consequently, affect humans and other living organisms since it enhances the availability of antimicrobial resistance genes in the environment, which is taken up and exchanged among commensals that were not initially harmful. Since such commensals find their way through direct and indirect contacts into the 3 food chain, issues of this nature cannot be undermined, especially in the context of South Africa, where the occurrence of AIDS/HIV and diabetes is high. 4 DECLARATION I, the undersigned, declare that the thesis hereby submitted to the North-West University, Mafikeng Campus, for the degree of Doctor of Philisophy (PhD) in Biology and the work contained herein, is my own original work in design and execution. I further declare that the thesis has not previously, in its entirety or in part, been submitted to any other institution for an academic qualification. All materials used in the study have been duly acknowledged. Signed at .......................................... on this .............................. Day of ....................................... 2019 ________________ F. E. Tatsing Foka (Student) Signed at .......................................... on this................................ Day of ..................................... 2019 _______________ Professor C.N. Ateba (Supervisor) 5 DEDICATION I dedicate this study to my parents, Mr and Mrs Foka, who, against all odds, gave me the headstart I needed in life by providing and teaching me the importance of education. Your unconditional love, care and support throughout every single step of my life, made me stronger as I faced every challenge. Without you, I would not have realised this endeavour. 6 ACKNOWLEDGEMENTS I wish to thank the Heavenly Father, for my life and most especially, my studies; you stood firm and next to me and never failed me. You are worthy my Lord to receive Glory for you are above all living beings and your power is beyond any other power. All things shall pass but you were, you are and you will forever be. I would like to express my gratitude to my supervisor, Professor C.N. Ateba, for giving me the opportunity to do a PhD in his research group, for his constant support, patience and encouragement throughout my studies. It has truly been inspiring and uplifting working with him throughout these years. Institutionally, I would like to acknowledge the financial support provided by the North-West University Institutional Bursary and the North-West University merit bursary. Moreover, I acknowledge all the members of staff of the School of Biological Sciences, North-West University, Mafikeng Campus. I appreciate their support in the realisation of this project. The assistance offered by Dr Ayanbgero Ayansina, Mr Peter Montso, Mr Alayande Kazeem, Mr Akinola Stephen, Mr Christ Donald Kaptchouang and my colleagues of the Molecular Microbiology laboratory is fully appreciated. I would also like to acknowledge Professor Noutchie Okouomi Suarez Clovis and Dr Yah S. Clarence, for their kind assistance and support during this journey. I am eternally grateful to Professor Carlos Bezendehout, Dr Charlotte Minnie and Mr Rudolph of the North-West University, Potchefstroom Campus, for the guidance and support provided in the 16S rRNA and NGS analysis of my isolates. I also deeply appreciate Dr K. S. Bet, Department of Geography, North-West University, for providing a map of my sampling points and the Cameroonian community in Mafikeng, for their constant words of encouragement. Finally, I thank my parents and my sisters, for their prayers, love and unending support throughout this journey. I would also like to express my appreciation to Mr and Mrs Chongang, 7 for their support and prayers throughout these years. To my wife and my children, I know how hard it must have been for you to bear my absence throughout these years, without your love and your support, I would not have made it. 8 TABLE OF CONTENTS .......................................................................................................................................... 1 SUMMARY ...................................................................................................................... 2 DECLARATION ............................................................................................................... 5 DEDICATION .................................................................................................................. 6 ACKNOWLEDGEMENTS ............................................................................................... 7 TABLE OF CONTENTS ................................................................................................... 9 LIST OF TABLES .......................................................................................................... 15 LIST OF FIGURES ......................................................................................................... 16 CHAPTER 1.................................................................................................................... 18 General introduction and problem statement ...................................................................
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