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Epidemiology of Dengue, Chikungunya and Zika in a Naïve Population in St Epidemiology of Dengue, Chikungunya and Zika in a Naïve Population in St. Kitts, West Indies. Iñaki Deza-Cruz DVM MCRVS Thesis submitted for the qualification of Doctor of Philosophy School of Natural and Environment Sciences, Newcastle University and Ross University of School of Veterinary Medicine September 2018 (This page is left intentionally blank) Page 1 of 275 Abstract Arboviruses such as dengue (DENV), chikungunya (CHIKV) and Zika (ZIKV) are of increasing global health concern and have caused recent rapid outbreaks in the Americas. However, studies focusing on behavioural risk that would assist with the understanding of transmission factors are scarce. This prospective study followed immunologically naïve adults in an arbovirus endemic environment to investigate disease detection, transmission and associated risk factors. University students from non-endemic areas studying in St. Kitts and Nevis were recruited as volunteers in three cohorts of sentinels between September 2014 and May 2015 (n = 224). Plasma was collected at enrolment and every 4 months subsequently until September 2016 and assayed for anti-DENV and anti-CHIKV IgM and IgG ELISA antibodies. Additionally, specimens collected from suspected cases of acute arboviral infection within the wider island population and mosquitoes captured in neighbourhoods were analysed for DENV, CHIKV and ZIKV by RT-PCR. Epidemiological data gathered at each sampling were investigated using mixed effect models, generalised estimating equations, Bayesian techniques and Cox proportional hazards survival analysis. Evidence of dengue infection was found in all (100%) the suspected cases born in St. Kitts but proof of recent infection was elusive. Chikungunya prevalence in sentinels was 12.7% (95% PI: 8.2-18.4%), whereas prevalence in suspected cases born in St. Kitts was 69.6% (95% CI: 47.1-86.8%). Zika prevalence was 39.1% (95% CI: 25.1- 54.6%) and evidence of infection and vertical transmission were also found in Ae. aegypti mosquitoes. Climatic variables were significantly associated with transmission followed by socio-economic conditions, frequency of mosquito bites and exposure to Ae. aegypti. Data suggested that arbovirus transmission in St. Kitts are epidemic and expire when climatic conditions become unfavourable for mosquito transmission or herd immunity reaches a critical threshold. These findings increase the understanding of arboviral transmission in small islands and can assist in more efficient outbreak response. Page 2 of 275 ‘Less is more’ (Browning, 1855) Dedication To my wife for her support and her love, to my parents and to my little brother for our mutual admiration. Page 3 of 275 Acknowledgements I would like to acknowledge and thank those who have assisted me with this study. In particular, my supervisors for their advice and support in the distance and their assistance, even with their blood if necessary. Prof. Stephen Rushton Dr. Aileen Mill Prof. Patrick Kelly Dr. Michel Vandenplas To the research lab team for their help during the countless hours pipetting, trapping and counting mosquitoes. Silvia Marchi, Stewart James Dr. Ximena Valderrama Kirsty Hill To the SKN Vector Control Office at the Environmental Health Department, the Health Information Unit at the Ministry of Health, the Department of Physical Planning and Environment at the Ministry of Sustainable Development, and Meteorological Services for their information. Mr. Jermaine Lake, Deputy Chief Environmental Health Officer Dr. Rafael Rosales, National Epidemiologist Mr. Meshach Alford Msc, Bsc, Senior Physical Planner Vincia Brown, Meteorological Officer And to many others for their help in this endeavour over many years, not forgetting: Dr. Ricardo Parreira Dr. Isabelle Dusfour Page 4 of 275 Table of Contents Abstract ....................................................................................................................... 2 Acknowledgements ..................................................................................................... 4 - List of abbreviations .............................................................................................. 9 - List of Tables ...................................................................................................... 11 - List of Figures ..................................................................................................... 13 Chapter 1. Introduction ......................................................................................... 16 1.1. Relevance of dengue, chikungunya and Zika in a global and regional context 16 1.2. Arbovirus: ..................................................................................................... 19 1.2.1. Structure and classification of principal human arboviruses ........................................ 19 1.2.2. Epidemiology, methods of transmission and clinical symptoms ................................... 21 1.3. Vector: .......................................................................................................... 29 1.3.1. Main arboviral vectors .................................................................................................. 29 1.3.2. Aedes aegypti morphology and classification ............................................................... 32 1.3.3. Aedes aegypti ecology and vectorial capacity ............................................................... 33 1.4. Saint Kitts and Nevis .................................................................................... 40 1.4.1. Island ecosystems and weather. ................................................................................... 40 1.4.2. Socio-economic factors ................................................................................................. 42 1.4.3. Population ..................................................................................................................... 43 1.4.4. Presence of arboviruses on St. Kitts. ............................................................................. 44 1.5. Gaps in existing knowledge. ........................................................................ 47 1.6. Characteristics of St. Kitts for the study of arboviruses. ............................... 49 1.7. Main hypothesis and structure of the thesis ................................................. 50 Chapter 2. Analysis of the study population ......................................................... 52 2.1. Introduction .................................................................................................. 52 2.2. Methods of sentinel recruitment, collection of samples and collection of epidemiological data. ............................................................................................. 54 2.2.1. Recruitment of sentinels ............................................................................................... 54 2.2.2. Collection of samples .................................................................................................... 55 2.2.3. Collection of epidemiological data ................................................................................ 56 2.2.4. Methods of analysis of sentinel behaviours, dropouts and missing data. .................... 58 2.3. Results ......................................................................................................... 58 2.3.1. Results: Dropout analysis and missing data analysis ..................................................... 59 2.3.2. Sentinels characteristics ................................................................................................ 63 2.3.3. Behavioural risk factors and exposure to the Aedes aegypti vector. ............................ 69 2.3.4. Frequency of mosquito bites. ........................................................................................ 74 Page 5 of 275 2.3.5. Suspected cases ............................................................................................................. 75 2.4. Discussion. ................................................................................................... 77 2.5. Concluding remarks ...................................................................................... 81 Chapter 3. Laboratory tests .................................................................................. 82 3.1. Introduction ................................................................................................... 82 3.1.1. Existing diagnostic methods for arboviroses ................................................................. 84 3.1.2. Challenges in Flavivirus serologic diagnosis .................................................................. 86 3.1.3. Characteristics of diagnostic tests and determination of test characteristics ............... 87 3.2. Methods: ....................................................................................................... 89 3.2.1. Laboratory tests: Serologic diagnostic methods. .......................................................... 89 3.2.2. Laboratory tests: Molecular diagnostic methods. ........................................................ 91 3.2.3. Methods: validation of plasma as sample specimen in ELISA protocols. ...................... 93 3.2.4. Methods: anti-DENV IgG ELISA performance and selection of optimal thresholds. ..... 94 3.3. Results .......................................................................................................... 96 3.3.1. Results: analysis of plasma as sample
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