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THE ORIENTAL RAT FLEA in NORTHERN UGANDA Submitte DISSERTATION DDT AND PYRETHROID RESISTANCE IN XENOPSYLLA CHEOPIS (ROTHSCHILD), THE ORIENTAL RAT FLEA IN NORTHERN UGANDA Submitted by Abbe D. Ames Department of Microbiology, Immunology, and Pathology In partial fulfillment of the requirements For the Degree of Doctor of Philosophy Colorado State University Fort Collins, Colorado Fall 2011 Doctoral Committee: Advisor: William C. Black IV Kenneth L. Gage Janet C. McAllister Boris C. Kondratieff Patricia A. Cole Copyright by Abbe D. Ames 2011 All Rights Reserved ABSTRACT DDT AND PYRETHROID RESISTANCE IN XENOPSYLLA CHEOPIS (ROTHSCHILD), THE ORIENTAL RAT FLEA IN NORTHERN UGANDA Development of insecticide resistance by vectors of disease is a well-recognized and continuous concern for public health officials. Monitoring insects for development of resistance to the chosen toxicants is part of effective management philosophy. Several programs to control mosquito vectors of malaria utilize insecticides with similar modes of action targeting the insect. Fleas can vector plague and in many areas inhabit the same environment that is the focus of mosquito management. Non-target insect development of resistance is a phenomenon most commonly associated with agriculture, but can also apply to insect vectors that threaten public health. Rapid and effective methods of monitoring for the possible development of insecticide resistance in fleas are important measures taken to prevent or suppress a plague outbreak. This study describes the development and application of a new field assay for evaluating phenotypic demonstration of insecticide resistance in fleas, results of biochemical analyses performed to evaluate possible development of metabolic detoxification pathways, and the subsequent elucidation of the para voltage gated sodium channel gene in Xenopsylla cheopis (Rothschild) with concurrent analyses of the prevalence and effects of knockdown (kdr) mutations in the gene. ii The field assay used a glass Petri dish coated with a dose of a chosen insecticide and a time mortality assay that was performed for 60 minutes. Discriminating concentrations, established on colony reared fleas, was tested on field collected fleas in northern Uganda. Fleas from villages with a history of indoor residual spraying (IRS) of DDT and /or pyrethroid were tested with those insecticides and significant increased survival was demonstrated. Phenotypic resistance to DDT was demonstrated with an 81.8% survivorship. Lambda-cyhalothrin tested fleas from three villages demonstrated phenotypic resistance of levels of 57.7%, 60.5%, and 58% survivorship. Enzyme profiles indicated increased levels of expression of α-esterase and β- esterase in field caught fleas compared to colony-reared fleas. Fleas potentially exposed to DDT and/or pyrethroids had higher levels than did unexposed fleas. An increase in insensitive acetylcholinesterase was found in fleas from villages with no known history of IRS. No increase in glutathione S-transferase was noted in any population. The para voltage gated sodium channel gene for X. cheopis was amplified and sequences for colony and Ugandan fleas were analyzed with emphasis on knockdown resistance (kdr) evolution in the fleas. Extensive evidences of selective pressures influencing genetic profiles of kdr development faster than expected for random mutation or recombination were found. The phenylalanine allele, associated with kdr, was found at an average of 95.1% frequency in villages with an IRS history. Field caught fleas with no known insecticide exposure had an allele frequency of 13.3% All three studies clearly indicate resistance is developing quickly in Ugandan flea populations and should be addressed with surveillance and management. iii ACKNOWLEDGEMENTS I would like to acknowledge the thought-provoking guidance all my committee members provided to me. I have discovered that not only are they subject matter experts in their respective fields of science, they are the products of many years of experience in regulatory and political arenas and have taken the time to make sure I emerge as a freshly minted PhD with less dogma and more forward thinking. I am eternally grateful for the sincere efforts Bill, Ken, Janet, Boris and Pat put forth to guide my intellectual growth. If I started to mention by name all the individuals who contributed to the success of my projects, I would be frightened I would accidentally forget someone and hurt them because the list is extensive! Nearly the entire 4th floor of the Centers for Disease Control and Prevention in Fort Collins either voluntarily helped me or was buttonholed for any helpful information I thought I might glean. Janae Stovall was probably just as happy as I was when sequencing was a fait accompli because that meant she finally had a break from me pestering her for ideas. Old friends like Jenn Holmes were there for me and new ones like Sarah Billeter and Leah Colton helped whenever I asked. Cassie Scott helped me transition from small animal clinics to a laboratory. In actuality, the entire CDC Fort Collins campus from security to the Director‟s office always had enthusiastic words of encouragement for me whenever we saw each other. Karla and Karen in Bill Black‟s lab were so understanding and helpful too. My entire family and friends around the world continued to support and encourage me, especially when the 3-year deadline loomed and I had a seemingly insurmountable amount of writing to do. My wonderful, long suffering son, Talon, probably could have written the dissertation himself from hearing me ramble about iv problems and new concepts I wrestled with so much. I am forever indebted to my friend Christine Lorenz, who‟s unswerving support and belief in my purpose got me here. Thanks to the CDC for funding the research and the trip to Uganda to collect the fleas. The incredible trapping crew, headed by Joseph Tendo, were funny, skilled, and taught me all sorts of tricks to trapping rats. The Ugandan Virology Research Institute in Kampala and Arua were very generous with their assistance and were instrumental in my success in Uganda. Thanks to the United States Army Veterinary Corps for funding my PhD and for the opportunity to master new skills. v DEDICATION To my parents, Dr. Sherman and Mrs. Elizabeth Ames, and my son, Talon. They are my generational bookends that have supported me unconditionally throughout all my endeavors, especially this one. To Christine Lorenz, an exceptional person and an incredible friend. vi TABLE OF CONTENTS I. LITERATURE REVIEW ……………………………………………………………….1 A. INTRODUCTION………………………………………………………………...2 1. Global resurgence of diseases leading to more intense chemical control…..….. measures…………………………………………………..…………..………2 2. Arthropod responses to insecticidal selective pressures……....…………........3 B. INSECTICIDES………………………………………………………………......4 1. Classification……………………………………………………………….....4 2. Primary modes of action of the four major groups…………….……...………8 3. Uses/ Formulations……………………………………………………………9 C. INSECTICIDE RESISTANCE…………………………………………………..11 1. Mechanisms of resistance……………………………………………………11 2. Methods of detection………………………………………………………...14 3. Prevalence/ Importance……………………………………………………...17 D. RESISTANCE IN XENOPSYLLA CHEOPIS…………………………………...18 1. History of plague…………………………………………………………….19 2. Pathology…………………………………………………………………….20 3. Ecology and dynamics of plague…………………………………………….23 4. Transmission of plague by Xenopsylla cheopis…………...…………………25 5. Current status of insecticide resistance in fleas……………………………...26 E. RATIONALE AND OUTLINE OF DISSERTATION……………….…………28 II. A NEW INSECTICIDAL BIOASSAY TECHNIQUE FOR FLEAS………………..30 A. INTRODUCTION……………………………………………………………….31 B. MATERIALS AND METHODS……………………………...………………...35 1. Source of fleas……………………………………………………………….35 2. Description of dish assay…………………………….………………………36 3. Discriminating concentration determination...……….……………………...37 4. Field Assays in Uganda...……………………………………………………38 5. Statistical analyses…………………………………………………………...39 6. Comparisons to colony……………………………………………………....41 7. Comparisons of two samples…………...……………………………………41 C. RESULTS…………………………………………………….…………………..42 1. Discriminating concentration…………….…………………………………..42 2. Field bioassay…………………….…………………………………………..42 D. DISCUSSION…………………………………………….……………………..44 III. BIOCHEMICAL DETECTION OF INSECTICIDE RESISTANCE MECHANISMS EXPRESSED IN XENOPSYLLA CHEOPIS (ROTHSCHILD) IN NORTHERN UGANDA, AFRICA…………………………………………………………………….48 vii A. INTRODUCTION……………………………………………………………….49 B. MATERIALS AND METHODS………………………………………………...52 1. Source of fleas and study areas……………………………….……………...52 2. Microplate assay……………………………………………………………..53 3. Data analysis…………………………………………………………………55 C. RESULTS………………………….……………………………………………..57 1. Microplate assays……………………………….……………………………57 D. DISCUSSION……….…………………………………….……………………..72 IV. EVOLUTION OF KDR IN UGANDAN XENOPSYLLA CHEOPIS (ROTHSCHILD)................................................................................................................76 A. INTRODUCTION……………………………………………………………….77 B. MATERIALS AND METHODS………………………………………………...80 1. Collection methods and sites………………………………………………...80 2. Bioassay……………………………………………………………………...82 3. DNA Isolation…………………………………….………………………….83 4. PCR……………………………………………….………………………….83 5. DNA sequencing………………………………….………………………….86 6. Population and phylogenetic analyses…………….…………………………86 C. RESULTS………………………………….……………………………………..87 1. Collection methods and sites..………...…………..………………………….87 2. Bioassays…………………………………………..…...…………………….89 3. PCR………………………………………………..…...…………………….89
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