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Brucellosis in Humans and Livestock in Rural Uganda: Epidemiology and Tools for Resource-Limited Settings

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Brucellosis in Humans and Livestock in Rural Uganda: Epidemiology and Tools for Resource-Limited Settings BRUCELLOSIS IN HUMANS AND LIVESTOCK IN RURAL UGANDA: EPIDEMIOLOGY AND TOOLS FOR RESOURCE-LIMITED SETTINGS By RoseAnn Miller A DISSERTATION Submitted to Michigan State University in partial fulfillment of the requirements for the degree of Large Animal Clinical Sciences – Doctor of Philosophy 2016 ABSTRACT BRUCELLOSIS IN HUMANS AND LIVESTOCK IN RURAL UGANDA: EPIDEMIOLOGY AND TOOLS FOR RESOURCE-LIMITED SETTINGS By RoseAnn Miller Objectives: A cross-sectional study was undertaken to describe the epidemiology of zoonotic brucellosis in dairy farms in rural southwestern Uganda, and to evaluate the use of tools to address challenges to disease surveillance programs faced in rural sub-Saharan Africa and other resource-limited settings. Methods: Blood samples were collected from cattle, goats and humans, and milk samples were collected from cows on 70 dairy farms in two sites in Uganda. Samples of blood and milk from livestock were collected and dried on laboratory-grade filter paper. Data describing each animal and human subject were recorded during sample collection, and herd-level risk factor data were collected by questionnaires on livestock health and management, human health and practices associated with increased brucellosis risk. Livestock blood and milk samples were tested using the Rose Bengal (RBT) and milk ring (MRT) tests. Human blood was tested using an immunochromatographic lateral flow assay (LFA). A qualitative real-time PCR (q-PCR) and nested PCR (n-PCR) were used to detect Brucella in DNA extracted from human, cattle and goat blood clots, cow milk, and human sera, and q-PCR was used to test DNA extracted from cattle and goat dried blood and milk samples. Multivariable regression was used to test associations between positive test results with subject characteristics and brucellosis risk factors. Results: Tests for brucellosis were positive in 14% of 768 cattle sera, 29% of 635 bovine milk, 17% of 315 goat sera, and 11% of 236 human serum samples. Both q-PCR and n-PCR detected B. abortus DNA in cattle, q-PCR detected B. abortus in humans and goats, and n-PCR detected B. melitensis in cattle blood and milk, and evidence of B. melitensis in human blood. DNA was successfully extracted from blood and milk samples stored on filter papers after four years of storage at room temperature. Both B. abortus and B. melitensis DNA were detected in dried samples, and agreement was seen between results of screening tests with q-PCR results from dried samples. Increasing seroprevalences in goats was significantly (p < 0.05) associated with seropositivity in cattle (OR = 1.2, 95% CI = 1.1 – 1.3) and seropositivity in humans (OR = 1.2, 95% CI = 1.0 – 1.5). Improvements in farm biosecurity and hygiene decreased risk for positive MRT, positive RBT in goats, and positive LFA results in humans. Tick control in cattle reduced the risk of brucellosis (OR = 0.4, 95% CI = 0.2 – 0.7). Human seropositivity was associated with brucellosis in goats (OR = 1.2, 95% CI = 1.0 – 1.5), goat slaughtering (OR = 14. 2, 95% CI = 1.8 – 110.0), and acquiring goats from neighbors (OR = 5.1, 95% CI = 1.9 – 14.0). Conclusions: Brucellosis is present in cattle, goats and humans on farms in southwestern Uganda. Although cattle are the focus of brucellosis control in Uganda, brucellosis in goats may be an important contributor to the epidemiology of the disease, and goats may be an important reservoir of Brucella. The associations between livestock brucellosis with wildlife contact, and tick control measures suggests that wildlife and arthropod vectors may play roles in the epidemiology of brucellosis on these farms. The LFA for human brucellosis, and dried sample storage on filter paper, met WHO criteria for use in resource-limited settings, and have potential for use in brucellosis surveillance and research. ACKNOWLEDGEMENTS This body of work is the culmination of years of support from academics, researchers, friends, and family, without whom it would not have been possible to complete. My first and most wholehearted thanks go to my advisor Dr. John B. Kaneene; my committee members Dr. Martha Mulks, Dr. Robert Tempelman, and Dr. Jean Tsao; and the faculty of the College of Veterinary Medicine and Department of Large Animal Clinical Sciences for their support. I also thank Dr. Steve Olsen from the USDA National Veterinary Services Laboratory (NVSL), who served as my external examiner and made arrangements for conducting work at their laboratories; Drs. Rebekah Tiller, Marta Guerra, and Robyn Stoddard at the Centers for Disease Control and Prevention, for their expertise and in conducting the qualitative PCR for the DNA from field and dried samples; Dr. Betsy Bricker (USDA NVSL) for technical expertise and assistance with the nested PCR used in this study; and to Dr. Jeff Landgraf and the MSU Research Technology Support Facility Genomics Core in the extraction of DNA from dried blood and milk samples. Special thanks go to the faculty, staff and students at Makerere University that helped bring this project into being: faculty members Dr. John D. Kabasa, Dr. Jesca L. Nakavuma, Dr. Paul Ssajjakambwe, and Dr. Patrick Vudriko from the College of Veterinary Medicine, Animal Resources and Biosecurity (COVAB), and Dr. Moses Joloba from the College of Health Sciences (CHS); technical assistance from Mr. Musisi (COVAB) and Willie Ssengooba (CHS); driver Robert Lomu (COVAB); student workers Geoffrey Mukisa Aliti, Collins Atuheire, Winnie Akiteng and Tracy Kanyunyuzi (COVAB) for their assistance in sample and data collection; the School of iv Medicine Research and Ethics Committee (CHS), and the veterinary medical officers, health care technicians, and farmers from the study areas for their participation. My deepest thanks go to family and friends that supported me over this long project, particularly those that were there at the beginning but are no longer here to appreciate its end: my father Robert L. Miller, father-in-law Cesare Sansotta, ‘adopted father’ Mike Ledyard, and S. Kathy Byrd, and old and dear friend. My mother Sumiko, sister Wendy, brother Roy and brother Roberto and his family: you were all a wonderful, positive refuge when things looked bleak, that kept me going to the end, and joining the Sansotta family has been another source of strength. My friends Julie Pierce, Rhonda Oyer, Anne Akin, Sue and Steven Ledyard, Laura Zarb & family, James and Sandy Scott, and many, many others: thank you very much. I’d also like to thank my intellectual ‘role models’ Steve Muhlberger, Joe and Sandy Straubhaar, Mary Rossano, Yvette Johnson, and all of the other MSU CVM grad students I’ve met and befriended. Finally, my beloved husband Rocco deserves more thanks and praise than I could ever offer anyone, as a husband, cheerleader, handyman, cook, and as the best dad two spoilt Papillons could ever have. v TABLE OF CONTENTS LIST OF TABLES ............................................................................................................................. xi LIST OF FIGURES ......................................................................................................................... xiii KEY TO ABBREVIATIONS ............................................................................................................. xiv CHAPTER 1: Introduction ............................................................................................................... 1 Problem Statement: ................................................................................................................. 3 Study Overview: ....................................................................................................................... 5 Primary Research Questions: ................................................................................................... 6 Structure of the Dissertation: .................................................................................................. 6 Chapter 2: Review of the Literature .................................................................................. 6 Chapter 3: The Prevalence of Brucellosis in Humans, Cattle, and Goats in Uganda: a comparative study ........................................................................................... 7 Chapter 4: Detecting Human Brucellosis in Southwestern Uganda: Evaluation of a lateral flow assay for use in resource-limited settings ..................................... 7 Chapter 5: Validation of the use of dried blood and dried milk spots for detection of Brucella in cattle and goats for surveillance in resource-limited settings ....... 8 Chapter 6: Use of molecular tools to detect Brucella in cattle, goats, and humans in Ugandan dairy farms ........................................................................................ 9 Chapter 7: Summary and Conclusions ............................................................................. 10 CHAPTER 2: Review of the Literature ......................................................................................... 11 Introduction: Zoonotic Diseases ............................................................................................ 12 Brucella: a Model Zoonotic Pathogen .................................................................................... 13 Brucellosis: a brief history ................................................................................................ 14 The Brucellae ...................................................................................................................
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