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Molecular Epidemiology and Genetic Analysis of Staphylococcus Species in Companion Animal Medicine

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Molecular Epidemiology and Genetic Analysis of Staphylococcus Species in Companion Animal Medicine Molecular Epidemiology and Genetic Analysis of Staphylococcus species in Companion Animal Medicine by Dubraska Vanessa Diaz-Campos A dissertation submitted to the Graduate Faculty of Auburn University in partial fulfillment of the requirements for the Degree of Doctor of Philosophy Auburn, Alabama August 4, 2012 Keywords: Staphylococcus species, SCCmec, equine, canine, antimicrobial resistance, penicillin-binding proteins. Copyright 2012 by Dubraska Vanessa Diaz Campos Approved by Kenny V. Brock, Chair, Professor of Pathobiology Stuart B. Price, Associate Professor of Pathobiology Frederic Hoerr, Professor of Pathobiology Dawn M. Boothe, Professor of Anatomy, Physiology and Pharmacology James M. Barbaree, Professor of Biological Sciences Abstract In human medicine, methicillin-resistant Staphylococcus aureus (MRSA) is one of the leading causes of bacterial infections in the United States (191). In veterinary medicine, an increased number of multidrug-resistant Staphylococcus spp. in dogs, horses, and swine have been reported (36, 220, 295). Methicillin-resistance in S. aureus is determined by the addition of the penicillin-binding protein 2a (PBP2a) encoded by the mecA gene (216, 217). The gene is carried on a large heterologous mobile element called the staphylococcal cassette chromosome mec (SCCmec) (114). To date, eleven SCCmec types have been identified in human MRSA clones, and several in staphylococci from animal origin (266). In horses and dogs, MRSA is frequently reported. Additionally, methicillin-resistant strains of Staphylococcus pseudintermedius (MRSP) are frequently diagnosed in dogs (220, 271, 295). The epidemiology of methicillin-resistant staphylococci from animal origin requires more investigation because of its zoonotic potential and to optimize preventative measures (14, 66, 87, 151). Using traditional microbiological methods and molecular techniques, an investigation of methicillin resistant Staphylococci sp isolated from equine and canine species was undertaken. Special emphasis was given to determining the most sensitive diagnostic method for recognition of methicillin- resistance (MR) in canine isolates due to the differing response of methicillin-resistant strains of S. schleiferi subspecies coagulans (MRSC) and S. pseudintermedius (MRSP) to cefoxitin (FOX) as compared to MRSA. From this investigation, it was hypothesized that the differences in the reaction of MRSP and MRSC to cefoxitin, when compared with MRSA, were based on ii variations in their penicillin-binding proteins. Thus, an analysis of the PBPs from S. pseudintermedius and S. schleiferi subsp coagulans was performed. Additionally, molecular epidemiology typing methods were used and the presence of three genes associated with virulence factors (S. intermedius exfoliative toxin [SIET], LUK-I and panton-valentine leukocidin [PVL]) were investigated in canine Staphylococcus sp). Results from the pulse field gel electrophoresis of the equine MRSA indicated a highly clonal population, with a predominance of the clone USA500, followed by USA100. Typing using multiplex PCR identified a preponderance of SCCmec type-IV, though the SCCmec type-II was also detected. In comparison, the type-V cassette was present in 66% (113/171) of the canine isolates, followed by type IV at 13% (22/171). Interestingly, 11% (18/171) of the MRSC were SCCmec type-V and all the MRSA isolates were type II. While comparing diagnostic methods, the sensitivity and specificity of oxacillin for the detection of MR strains was 83% and 93%, respectively. However, using FOX, the sensitivity was 20% and the susceptibility was 100%. By the means of PCR, the genes that encode PVL were detected in 4% of the canine MRSA, but were not detected in S. pseudintermedius or S. schleiferi subsp coagulans. In contrast, the SIET and LUK-I genes were detected in the three staphylococci, S. aureus, S. pseudintermedius and S. schleiferi subsp coagulans. Using sodium-dodecyl-sulfate polyacrylamide gel electrophoresis (SDS-PAGE), a different pattern of PBPs was found in S. pseudintermedius (5 proteins) and S. schleiferi subspecies coagulans (3 - 4 proteins), when compared with S. aureus (4 – 5 proteins). A competitive binding assay demonstrated a decreased affinity of cefoxitin towards the PBPs of MRSP as compared to MRSA. From the results of these summarized studies, it is clear that more investigation directed towards understanding the different mechanisms of resistance against iii antimicrobial drugs by staphylococci from animal origin are required to address the epidemiology of Staphylococcus sp in veterinary medicine. iv Acknowledgments The author would like to express sincere gratitude to Dr. Kenny for believing in her and for offering the opportunity of pursuing doctoral studies together with the residency in Clinical Microbiology. Dr. Brock has provided important professional opportunities. Moreover, Dr. Brock stimulated the development of critical thinking with enthusiasm and support. The author truly had a great time working with Dr. Brock and admires him as a professional and mentor. The author acknowledges the members of her committee. Thanks to Dr. Dawn Boothe, who offered support, enthusiasm and many good ideas. Dr. Boothe’s expertise and knowledge as a clinical pharmacologist gave an invaluable contribution to this work. Thanks to Dr. Stuart Price who was an excellent resource during this process, offering guidance and support. Thanks to Dr. Frederick Hoerr, who stressed that a clinical microbiologist has to be integral, being capable of evaluating all the factors associated with a clinical syndrome. A special thanks to Terri Hathcock , who guided the author when she started working as a clinical microbiologist resident and throughout. Mrs. Hathcock’s ideas and enthusiasm, together with strict directions, were a cornerstone for the author’s achievements during all these years. Thanks to Denise Williams for her teaching and friendship. Thanks to all the members of the “Microbiology lab”, especially Brenda Bixler, who offered lots of help and support. Thanks to Abbie, Taylor, Krystina and Terri Wood. The author is indebted to her long-standing mentor, Dr. Armando Hoet and his family. The author wishes to express deep admiration for Dr. Hoet who opened a new world full of excellence, loyalty, honor, and friendship. Thanks to Dr. Palomares for his friendship and v collaboration during the good and bad. Thanks to Lis, Gigi, Barbara, Lujan, Rodri, Juaco, Vladi, and the other “Latin” friends, who are more than just friends. A special thank you is extended to the author’s family, especially her parents Mireyita, Armando y Greta: Aunt Elionora, Aunt Norma, and Uncle Roberto who were always praying and watching over her. In addition, gratitude is expressed to her brothers and sisters, Gerar, Mayra, Amira, Mario, and Ana for being cheerful and supportive throughout the all these years. Thanks to Wale, who is an inspiration in every way. Thanks also to Dore, Roger, and Joa for their love and support. The author wishes to express her heart felt gratitude to her husband, Rafael Portillo, who has been the best husband and friend though the years. Thanks to him for his support and patience. Finally, she wishes to express her gratitude to God for His blessings which includes all the wonderful people mentioned above. vi Table of Contents Abstract ........................................................................................................................................... ii Acknowledgments........................................................................................................................... v List of Tables ................................................................................................................................. ix List of Figures ................................................................................................................................ xi List of Abbreviations .................................................................................................................... xii I. Literature review .................................................................................................................. 1 Staphylococcus species and host specificity ................................................................................... 1 Most common antimicrobials used in veterinary medicine ............................................................ 7 Mechanisms of antimicrobial resistance and methicillin- resistance in Staphylococcus aureus and other Staphylococcus species ........................................................................................................ 14 MRSA SCCmec and its molecular epidemiology human, horses and dogs ................................. 20 Penicillin-Binding Proteins in Staphylococcus species ................................................................ 23 Molecular typing ........................................................................................................................... 27 Multilocus Sequence Typing: ................................................................................................... 28 Pulse field gel electrophoresis .................................................................................................. 28 Spa typing ................................................................................................................................. 29 Staphylococcal cassette chromosome typing ...........................................................................
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