University of Oklahoma Graduate College
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UNIVERSITY OF OKLAHOMA GRADUATE COLLEGE EARTH OBSERVATION AND MOSQUITO-BORNE DISEASES: ASSESSING ENVIRONMENTAL RISK FACTORS FOR DISEASE TRANSMISSION VIA REMOTE SENSING DATA A DISSERTATION SUBMITTED TO THE GRADUATE FACULTY In partial fulfillment of the requirements for the Degree of DOCTOR OF PHILOSOPHY By ANDREA MCMAHON Norman, Oklahoma 2021 EARTH OBSERVATION AND MOSQUITO-BORNE DISEASES: ASSESSING ENVIRONMENTAL RISK FACTORS FOR DISEASE TRANSMISSION VIA REMOTE SENSING DATA A DISSERTATION APPROVED FOR THE DEPARTMENT OF GEOGRAPHY AND ENVIRONMENTAL SUSTAINABILITY BY THE COMMITTEE CONSISTING OF Dr. Michael C. Wimberly, Chair Dr. Kirsten de Beurs Dr. John S. Greene Dr. Katherine Hirschfeld © Copyright by ANDREA MCMAHON 2021 All Rights Reserved. To all the women who have come before me and have trodden the path on which I now walk. iv Acknowledgements Over the course of the last five years, I have received tremendous support from so many people, and I want to express my deepest gratitude to all of them. First and foremost, I would like to thank my advisor Dr. Michael Wimberly. They say an advisor can make or break the PhD experience. I sincerely want to thank you for giving me the opportunity to do this exciting research, and for your patience and ongoing support without which I would not have made it to this point. I would also like to thank my committee members, each of whom has supported me on different segments of my PhD journey. I would like to thank Dr. Geoffrey Henebry and Dr. Michael Hildreth who served on my committee during my time at South Dakota State University and who have been supporting in framing my research ideas. I would also like to thank all of my committee members at the University of Oklahoma: Drs. Kirsten de Beurs, Katherine Hirschfeld, Scott Greene, Hernan Moreno, and Matthew Miller. I thank you all for your time, your support, and your insightful advice. Special shout out to those who served on my committee during my last year. Writing a dissertation is hard and writing one during a global pandemic is even harder. I am tremendously grateful for how flexible and supportive you all were during this time. Any of this work in this dissertation would have been impossible without all those who were involved as co-authors in each of the case studies, and I wholeheartedly want to thank them as well. This includes Dr. Justin Davis who always had an open ear for questions of a statistical nature, Dr. Caio França who helped me learn how to identify mosquitoes, and v our colleagues in Ethiopia who made our malaria research possible: Dr. Abere Mihretie, Adem Agmas Ahmed, Mastewal Lake, and Worku Awoke. A very big thank you also goes to past and present EcoGRAPH Lab members who gave valuable feedback during lab meetings and were always there when I needed help. Special thanks go to Dr. Dawn Nekorchuk who has been endlessly supportive and has become a dear friend. And since I transferred half-way through my studies, I would like to thank everybody at the Geospatial Sciences Center of Excellence at SDSU and at the Department of Geography and Environmental Sustainability at OU. This goes to faculty members for teaching such interesting classes, to department staff who relentlessly help with every problem graduate students come up with, and to fellow students who have become great friends along the way. Last but not least, I want to thank my biggest champions: my parents who are always there for me even when I’m far away, my PhD support puppy Hazel whose cold snout is what gets me up in the morning, and of course my husband Kenny who quit his job to be with me while I worked on my degree and who was crazy enough to marry me during a pandemic. vi Contents Acknowledgements ........................................................................................................... v List of Tables ..................................................................................................................... x List of Figures ................................................................................................................... xi Abstract ........................................................................................................................... xiv 1 Introduction................................................................................................................ 1 1.1 Challenges in combatting mosquito-borne diseases............................................. 2 1.2 Ecology of mosquito-borne diseases on a landscape scale .................................. 4 1.3 The use of satellite data to study mosquito-borne diseases .................................. 7 1.4 Research overview ............................................................................................... 9 2 Remote sensing of environmental risk factors for malaria in different geographic contexts ................................................................................................. 11 2.1 Introduction ........................................................................................................ 12 2.2 Methods .............................................................................................................. 16 2.2.1 Study area.................................................................................................... 16 2.2.2 Malaria data ................................................................................................ 19 2.2.3 Environmental variables ............................................................................. 21 2.2.4 Statistical analysis ....................................................................................... 26 2.3 Results ................................................................................................................ 27 2.3.1 Spatio-temporal patterns in malaria cases................................................... 27 2.3.2 Association between malaria and environmental variables ........................ 32 2.4 Discussion .......................................................................................................... 34 2.5 Conclusion .......................................................................................................... 40 vii 2.6 Supplemental material ........................................................................................ 41 3 Identifying environmental risk factors and mapping the distribution of West Nile virus in an endemic region of North America ..................................... 45 3.1 Introduction ........................................................................................................ 47 3.2 Methods .............................................................................................................. 51 3.2.1 West Nile virus case and control data ......................................................... 52 3.2.2 Exploratory analysis.................................................................................... 53 3.2.3 Environmental variables ............................................................................. 54 3.2.4 Statistical modelling.................................................................................... 58 3.3 Results ................................................................................................................ 63 3.3.1 Spatial patterns ............................................................................................ 63 3.3.2 Environmental data analysis ....................................................................... 67 3.4 Discussion .......................................................................................................... 69 3.5 Acknowledgments .............................................................................................. 74 4 Comparing satellite data and in-situ measurements in studying vector mosquito habitats in an urban environment ......................................................... 75 4.1 Introduction ........................................................................................................ 77 4.2 Materials and Methods ....................................................................................... 79 4.2.1 Study area.................................................................................................... 79 4.2.2 Mosquito trapping and processing .............................................................. 81 4.2.3 Environmental data collection .................................................................... 81 4.2.4 Analysis....................................................................................................... 88 viii 4.3 Results ................................................................................................................ 89 4.4 Discussion .......................................................................................................... 98 5 Synthesis ................................................................................................................. 104 5.1 Summary .......................................................................................................... 104 5.2 General considerations ..................................................................................... 107 5.2.1 Remotely-sensed variables influencing disease risk ................................. 108 5.2.2 The importance of landscape context ....................................................... 110 5.2.3 The case for remote sensing