Exploration of Potential Reservoir Hosts and Vectors Of
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EXPLORATION OF POTENTIAL RESERVOIR HOSTS AND VECTORS OF LEISHMANIA IN NICARAGUA A Dissertation by RUSSELL WAYNE RAYMOND Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY August 2008 Major Subject: Wildlife and Fisheries Sciences EXPLORATION OF POTENTIAL RESERVOIR HOSTS AND VECTORS OF LEISHMANIA IN NICARAGUA A Dissertation by RUSSELL WAYNE RAYMOND Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Approved by: Chair of Committee, Norman O. Dronen, Jr. Committee Members, Thomas M. Craig Jimmy K. Olson Markus J. Peterson Head of Department, Thomas E. Lacher, Jr. August 2008 Major Subject: Wildlife and Fisheries Sciences iii ABSTRACT Exploration of Potential Reservoir Hosts and Vectors of Leishmania in Nicaragua. (August 2008) Russell Wayne Raymond, B.S., University of the Incarnate Word; M.S., University of the Incarnate Word Chair of Advisory Committee: Dr. Norman O. Dronen, Jr. Leishmaniasis is caused by infection with protozoan parasites within the genus Leishmania and, in the New World, is transmitted by the bites of female sand flies within the genus Lutzomyia. The occurrence of leishmaniasis in rodent species, the geographic distribution of sand fly species in Nicaragua, and environmental factors associated with the distribution of human cases of typical cutaneous leishmaniasis were investigated. Three hundred ninety five rodents representing 17 species were collected from 13 localities from August 2001–March 2006 and screened for Leishmania infections. One Heteromys desmarestianus and one Peromyscus mexicanus were found to be positive for leishmanial infections by PCR. This is the first report of Leishmania infections in rodents in Nicaragua. Five hundred fifty six sand flies representing 12 species were collected from 8 localities, including Lutzomyia hartmanni, a new record for this species in Nicaragua. The predominant sand fly species captured in western Nicaragua were Lutzomyia longipalpis and Lutzomyia evansi. The predominant species captured in central and eastern Nicaragua was Lutzomyia cruciata. The geographic iv distribution of sand flies in this study provides additional support to previously- published reports of suspected vectors of Leishmania species that cause typical and atypical forms of cutaneous leishmaniasis in Nicaragua. Distribution data of human cases of typical cutaneous leishmaniasis obtained from the Nicaraguan Ministry of Health, along with GIS and remotely sensed data of elevation, precipitation, temperature, soil types and land use/cover classes, were used to develop predictive logistic regression models for the presence or absence of human cases within 151 municipalities. Mean annual precipitation and land use/cover were determined to be the best environmental variable predictors for the occurrence of typical cutaneous leishmaniasis. v ACKNOWLEDGEMENTS A great number of individuals are responsible for the success of this research and manuscript. I would like to express gratitude to my graduate studies committee: Dr. Norman O. Dronen, Jr., Chairman, and members Dr. Thomas M. Craig, Dr. Jimmy K. Olson, and Dr. Markus J. Peterson. Dr. Dronen provided guidance in navigating around the pitfalls associated with a doctoral program. He provided invaluable assistance in the development of a degree plan, the writing of a research proposal and the development of this dissertation. Thank you for taking me under your wing and providing support, encouragement and guidance along the way. Dr. Craig provided an interesting and intensive course in Veterinary Parasitology. I learned skills in his lecture and laboratory that I am certain will serve me well for years to come. Thank you for your input on my research proposal and this dissertation. Dr. Olson’s course in Medical and Veterinary Entomology was an incredible introduction to this field. Although I hope that I never have to identify mosquito larvae again; I am reasonably confident that I could. Thank you for your input and guidance along the way. I am perhaps most thankful for Dr. Olson’s ability to make me feel like one of the crew. I only spent a short time living in College Station and even though I did not receive my B.S. or M.S. from Texas A&M, he was the one that made me feel like I was an Aggie. Dr. Peterson’s class in Research Methods was an invaluable experience. It was one of the most challenging courses that I have ever taken, but I enjoyed it very much. He taught me how the entire research vi process comes together, from proposals and funding to data collection, analysis and presentation. I am indebted to my mentor Dr. Sara F. Kerr, University of the Incarnate Word. Thank you for your years of encouragement and support, without which I am certain that I would have ended my academic studies upon the completion of my B.S. I had no idea that those initial hot afternoons and early mornings spend crawling through the brush at Rothe Ranch and La Copita would lead to hot afternoons and early mornings of crawling through the jungle in Nicaragua. I take pride in explaining to people that I am a professional rat trapper. To Dr. Chad McHugh, I am well aware of the amount time and effort that you put into identification of sand flies from Nicaragua. Without your expertise in this area, the identification of insect specimens may well have taking forever. I also am appreciative of your advice on improving my writing and organizational skills. Dr. Robert Bradley and his crew at Texas Tech University provided enormous assistance with identification of rodent species from Nicaragua. Doctora Rafaela Montoya, Nicaraguan Ministry of Health, was my primary point of contact within the country. She took time from her very busy schedule at the hospital in Nueva Guinea to serve as liaison between our crew and numerous individuals and government agencies in Nicaragua. Doctora Montoya’s staff in Nueva Guinea as well as the Ministry of Health staffs in Siuna, Matagalpa, Jinotega, Bluefields, Chinendega, and Leon provided hours of help with the identification of trapping localities as well as assistance with field work. Doctora Arlette Vargas traveled with us, on many occasions, to various communities in vii order to help explain our project to local leaders and to help gather information about “hot spots” of leishmaniasis. Doctor Byron Perez provided much assistance with gaining access to trapping sites in the Matagalpa area and with navigating the paperwork required to export rodents from Nicaragua. Data on the distribution of human cutaneous leishmaniasis was provided by Dr. Juan Jose Amador, Chief Epidemiologist of the Ministry of Health, Managua, Nicaragua. The GIS maps of Nicaragua were provided by the staff at the Nicaraguan Ministerio del Ambiente y los Recursos Naturales. Diana Kruger was of enormous assistance in a number of areas associated with this project. She provided help with travel plans, reservations, arranged for drivers, graciously allowed us to store mounds of equipment at her home in Managua and provided the best lemonade that I’ve ever tasted. Most importantly, it was Diana’s phone calls to various individuals within the Nicaraguan government that help secure meetings and gain access to Ministry of Health data on the prevalence and distribution of human cases of typical cutaneous leishmaniasis. I also need to thank Reggie Romo with ESRI for showing me a more efficient way to get at the data analysis in GIS and Dr. Paul Messina for much needed assistance with statistical analysis. Many individuals assisted with the “heavy lifting” associated with specimen collection in sometimes very rugged terrain. Robert Miranda, Christina Salinas, and Sebastian Villarreal (students from the University of the Incarnate Word) made numerous treks carrying equipment into and out of research sites. Ernesto Hernandez and Ariel Hernandez from Chinandega and Waldemar Rios from Siuna provided viii countless hours of assistance in everything from specimen collection and specimen processing to driving duties and Spanish/English translation. I am very grateful to my parents, Ray and Marlene Raymond; thank you for many years of love and support. Finally and most of all, I would like to recognize my wife Carol Armata Raymond; thank you for years of love, encouragement and support. You are an inspiration to me. Without you, I would not have made it this far. ix TABLE OF CONTENTS Page ABSTRACT .............................................................................................................. iii ACKNOWLEDGEMENTS ...................................................................................... v TABLE OF CONTENTS .......................................................................................... ix LIST OF FIGURES................................................................................................... xiii LIST OF TABLES .................................................................................................... xv INTRODUCTION..................................................................................................... 1 Overview ............................................................................................................. 1 Clinical manifestations of leishmaniasis ............................................................. 2 Occurrence of clinical forms of leishmaniasis in Nicaragua..............................