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Houseflies As Potential Vectors for Antibiotic Resistant Bacteria THESIS

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Houseflies As Potential Vectors for Antibiotic Resistant Bacteria THESIS Houseflies as Potential Vectors for Antibiotic Resistant Bacteria THESIS Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in the Graduate School of The Ohio State University By Wenfei Wang Graduate Program in Food Science and Nutrition The Ohio State University 2013 Master's Examination Committee: Dr. Hua Wang, Advisor Dr. Curtis Lynn Knipe Dr. Zhongtang Yu Copyrighted by Wenfei Wang 2013 Abstract The rapid emergence of antibiotic resistant (ART) pathogens is a growing public health concern. Although the roles of antibiotics in clinical medicine and food animal production have been clearly implicated, there is a growing body of evidence that commensal bacteria, environmental factors and animal hosts are also playing important roles in the emergence, dissemination and evolution of antibiotic resistance (AR). Recently a number of insect vectors have been identified as potential carriers of ART pathogenic bacteria, suggesting that these insects may serve as an important avenue of disseminating disease-causing agents to the environment and hosts. Since horizontal gene transfer is crucial to the rapid dissemination of AR, and commensal bacteria, instead of pathogens, serve as the main avenue disseminating AR genes in microbial ecosystems, an important knowledge gap to be closed is whether the insects are also carriers of ART commensal bacteria, and whether the prevalence is correlated to the environment the insects are exposed to. Therefore, the objectives of this study were to reveal the prevalence of ART commensal bacteria from houseflies collected from agricultural and residential environments, and to analyze the genetic elements of ART commensals for an improved understanding of the risk factors associated with AR ecology. Houseflies (Musca domestica) were sampled from four different locations: indoors and outdoors at a poultry barn; and outdoors at two residential areas. The flies were captured ii using flytraps, identified, homogenized and plated on media containing different antibiotics. Conventional and quantitative PCR were used to screen for the presence of representative antibiotic resistance-encoding genes. Representative tetr, ermr, sulr encoding genes were found in up to 18.2% and 19.2% of the commensal isolates from houseflies collected at the indoor and outdoor locations at the poultry barn. Bacterial population recovered from samples from the two residential locations had a significantly lower percentage of resistant isolates (7.1% and 0.5%, respectively). Enterococcus sp., Staphylococcus sp., Providencia sp., Vagococcus sp. and Alcaligenes sp. were among the identified AR gene carriers with several isolates showing resistance to multiple antibiotics and carrying multiple resistance genes. These results suggest that houseflies may serve as potential vectors disseminating AR gene-containing bacteria in the environment and to hosts. The data also indicated a potential correlation between exposure to animal facility and the prevalence of AR-gene containing bacteria in houseflies. Results from this study will contribute to an improved understanding regarding potential community risks of AR dissemination due to insects that are exposed to various environmental conditions, which is essential for public health and targeted strategies for AR mitigation. iii Dedication Dedicated to my family and friends iv Acknowledgments I would like to thank Dr. Hua H. Wang, my advisor and true mentor, for her encouragement, guidance, and support throughout my undergraduate and graduate program. Thank you for sharing your thoughts and providing valuable advice on all aspects of my life. Your patience and dedication were priceless to me. I would also like to thank Dr. Lynn Knipe and Dr. Zhongtang Yu for serving as my committee members and providing helpful suggestions on my master’s studies and research. I would also like to show my appreciation for the help of Dr. Timothy Buckley, the initiator and co-author of this project, for his support and effort during all phases of this study. I am very grateful to Ying Huang, Lu Zhang, Xiaojing Li, Xinhui Li, Linlin Xiao, Yi Shao for their assistance and guidance during my research. I want to thank all my friends and my family for their understanding and support. I am also thankful to OARDC SEEDS Program and The Ohio State University Fellowship for providing financial support to make this research possible. v Vita 2002-2007…………………………………...Simba International School, Ndola - Zambia 2008-2011……………………………….B.S. Honors Biology, The Ohio State University 2008-2011……………….............International Buckeye Scholarship, The Ohio State University 2011-2012………………………………….Student Employee, The Ohio State University 2012-Present……………………………...Graduate Student, Department of Food Science and Technology, The Ohio State University 2012-2013…………………University Fellowship, The Ohio State University 2012-2013……………………Graduate Teaching Assistant, Department of Food Science and Technology, The Ohio State University Fields of Study Major Field: Food Science and Nutrition vi Table of Contents Abstract .............................................................................................................................. ii Dedication ......................................................................................................................... iv Acknowledgments ............................................................................................................. v Vita .................................................................................................................................... vi List of Tables .................................................................................................................. viii List of Figures ................................................................................................................... ix Chapter 1: Introduction and Literature Review........................................................... 1 Chapter 2: Houseflies as Potential Vectors for Antibiotic Resistant Bacteria .......... 40 Bibliography .................................................................................................................... 66 vii List of Tables Table 1.1. Common antibiotic classes .............................................................................. 14 Table 1.2. Hospital-acquired infections by selected resistant bacteria in the U.S. (2002). ........................................................................................................................................... 29 Table 1.3. Leading foodborne pathogens in the U.S. (2000-2008)................................... 30 Table 1.4. Sales and distribution of antimicrobial drugs for food-producing animals (2010) ................................................................................................................................ 31 Table 2.1. Primers for AR gene detection......................................................................... 58 Table 2.2. AR gene determinants and representative AR gene carriers from housefly samples .............................................................................................................................. 61 Table 2.3. Persistence of resistance within resistant isolates ............................................ 63 viii List of Figures Figure 1.1. Representative antibiotics from natural products ............................................. 6 Figure 1.2. Representative antibiotics of synthetic origin .................................................. 9 Figure 1.3. Incidences of three antibiotic resistant pathogens since 1980 ........................ 16 Figure 1.4. Main reservoirs of antibiotic resistance .......................................................... 25 Figure 1.5. Worldwide causes of death ............................................................................. 28 Figure 1.6. Housefly lifecycle: complete metamorphosis ................................................ 34 Figure 2.1. Prevalence of bacteria with phenotypic resistance to antibiotics from housefly samples .............................................................................................................................. 60 Figure 2.2. Phenotypic multidrug resistant isolates from housefly samples..................... 60 Figure 2.3. Distribution of resistant isolates carrying multiple resistance genes ............. 62 Figure 2.4. AR gene pools in housefly samples................................................................ 62 Figure 2.5. pCC1FOS™ vector map ................................................................................. 64 Figure 2.6. Agarose gel electrophoresis of Tetr sub-clones .............................................. 65 ix Chapter 1 Introduction and Literature Review 1.1 Introduction Antibiotics were initially defined as substances or compounds (secondary metabolites) produced by certain microorganisms that could kill or inhibit the growth of other microorganisms. Today, antibiotics also include many synthetic compounds with similar functions such as β-lactams, cephalosporins and carbapenems (Khardori, 2006). Since the initial discovery, antibiotics have been broadly used in human and veterinary medicine, agricultural production and food processing, and have been essential for protecting human and animal health against pathogens. Countless once-deadly bacterial infections have been effectively treated by antibiotics, greatly enhanced the life
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