Spatial Risk Assessment of Mosquito-Borne Viral Diseases – Research at the Intersection of Ecology and Epidemiology
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Spatial Risk Assessment of Mosquito-Borne Viral Diseases – Research at the Intersection of Ecology and Epidemiology. Dissertation zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.) an der Fakultät für Biologie, Chemie und Geowissenschaften der Universität Bayreuth vorgelegt von Nils Benjamin Tjaden geboren in Meschede Bayreuth, 2020 “Chikungunya is a specifically tropical disease. It is relatively uncommon and poorly documented” — Pialoux et al. (2007) ii This doctoral thesis was prepared at the department of Biogeography at the University of Bayreuth from January 2013 until June 2020 and was supervised by Prof. Dr. Carl Beierkuhnlein. This is a full reprint of the thesis submitted to obtain the academic degree of Doctor of Natural Sciences (Dr. rer. nat.) and approved by the Faculty of Biology, Chemistry and Geosciences of the University of Bayreuth. Date of submission: June 23rd 2020 Date of defence: October 22nd 2020 Acting dean: Prof. Dr. Matthias Breuning Doctoral committee: Prof. Dr. Carl Beierkuhnlein (reviewer) Prof. Dr. Jonas Schmidt-Chanasit (reviewer) Prof. Dr. Cyrus Samimi (chairman) Prof. Dr. Heike Feldhaar iii iv Contents Contents .......................................................................................................................................... v Summary......................................................................................................................................... 1 Zusammenfassung ...................................................................................................................... 5 Introduction .................................................................................................................................. 9 Author’s note ...................................................................................................................... 9 Mosquito-Borne Viral Diseases ................................................................................... 9 Overview ......................................................................................................................... 9 A short history of mosquito-borne diseases................................................... 10 Transmission cycle ................................................................................................... 12 Diseases covered in this dissertation ..................................................................... 14 Dengue ........................................................................................................................... 14 Chikungunya ............................................................................................................... 17 Usutu .............................................................................................................................. 19 Climatic effects on Mosquito-Borne Viral Diseases .......................................... 23 Impacts on vector distributions and populations ........................................ 23 Impacts on disease dynamics ............................................................................... 24 Climate- and weather-based models for MBVD risk mapping ..................... 27 Risk and risk maps .................................................................................................... 27 Ecological Niche Models of species’ distributions ........................................ 30 Epidemiological disease transmission models .............................................. 33 Synopsis of the following manuscripts .................................................................. 39 Summarizing discussion and emerging research challenges ....................... 43 MBVD risk assessment based on Ecological Niche Models ....................... 43 MBVD risk assessment based on Epidemiological Models ....................... 44 Concluding remarks ................................................................................................. 46 List of manuscripts and declaration of own contribution ............................. 49 Declaration of changes made to the manuscripts ............................................. 51 References of Introduction ........................................................................................ 53 Manuscript 1: Modelling the effects of global climate change on chikungunya transmission in the 21st century ................................................................................... 77 v Manuscript 2: Areas with high hazard potential for autochthonous transmission of Aedes albopictus-associated arboviruses in Germany .................................. 143 Manuscript 3: Extrinsic incubation period of dengue: knowledge, backlog, and applications of temperature dependence .............................................................. 177 Manuscript 4: Evaluating the risk for Usutu virus circulation in Europe: comparison of environmental niche models and epidemiological models197 Manuscript 5: Mosquito-borne diseases: Advances in Modelling Climate-Change impacts ................................................................................................................................. 241 Appendix ................................................................................................................................... 283 List of abbreviations and acronyms ..................................................................... 283 Glossary .......................................................................................................................... 285 List of publications and manuscripts not included in this thesis ............. 291 Other academic activities ......................................................................................... 293 Reviewer activcities .............................................................................................. 295 Acknowledgements .............................................................................................................. 297 Declarations ............................................................................................................................. 299 vi Summary Mosquito-borne viral diseases pose an increasing threat to human and ani- mal health on a global level. Over the past few decades, competent vector spe- cies like the Asian tiger mosquito (Aedes albopictus) or the Asian bush mosquito (Aedes japonicus) have spread vigorously across the globe and far beyond their native distribution. During the same time, large outbreaks of diseases that are being transmitted by these and other mosquito species (such as chikungunya, Zika, West-Nile fever and Usutu) have been recorded. Diseases that were formerly considered purely tropical by many, such as dengue and chikungunya, showed repeated outbreaks along the coast of the Mediterranean Sea – far away from the tropics. Usutu virus (which was largely neglected in the past as long as it was spatially limited to Africa) emerged in Europe, causing mass extinction events among blackbird populations. Evidence suggests that increasing temperatures due to climate change will facilitate future spread. Clearly, there is an increasing need for spatial risk assessment of these diseases. In this thesis, I use two established approaches, Ecological Niche Models and Epidemiological Models, to assess the spatial risk arising from different mosquito-borne viral diseases. Building models for chikungunya and Usutu viruses as well as the mosquito vector Ae. albopictus, I produce risk maps at global, continental, national and local scales. I explore the strengths and weaknesses of the different approaches and make suggestions for future improvements. All models in this thesis suggest a potential for a continued increase in mosquito-borne viral disease occurrence in large parts of the respective study area. On a global scale, chikungunya is expected to increase its presence on all continents except for Antarctica as well as some areas in Australia and northern India (where climate change will lead to conditions that may prohibit vector survival). On a continental scale, two fundamentally different models for Usutu 1 suggest that large parts of Europe offer favorable environmental conditions for transmission of the disease. However, they differ considerably at the local scale. At the national scale, large parts of western Germany are projected to become climatically suitable for the establishment of Ae. albopictus in the near future due to climate change. Most of these areas (including those that are already highly suitable today) also showed elevated incidence rates of travel-related dengue and chikungunya infections, suggesting an elevated risk for virus transmission. Risk maps are an important tool that can be used by field entomologists and epidemiologists for more targeted surveillance and monitoring. And they can help to communicate essential information to politicians and decision makers in order to facilitate the establishment of the infrastructure that is necessary for these endeavors. Both Epidemiological Models and Ecological Niche Models suffer from a lack of essential data. For Epidemiological Models, laboratory studies and field data about the underlying mechanisms of transmission are severely lacking for many diseases. This is demonstrated in this thesis using the extrinsic incubation period (EIP) of dengue as an example. It has long been known that the duration of the EIP inside the mosquito vector