Étude Des Facteurs Environnementaux Associés À Son Établissement

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Étude Des Facteurs Environnementaux Associés À Son Établissement Université de Montréal Éco-épidémiologie de la maladie de Lyme dans le Sud-Ouest du Québec: étude des facteurs environnementaux associés à son établissement par Catherine Bouchard Département de pathologie et microbiologie Faculté de médecine vétérinaire Thèse présentée à la Faculté de médecine vétérinaire en vue de l’obtention du grade de doctorat de philosophiae doctor (Ph.D.) en sciences vétérinaires option épidémiologie Septembre, 2013 © Catherine Bouchard, 2013 Résumé Depuis les années 90, les études réalisées au Canada ont permis d’identifier de nouvelles zones endémiques de l’agent de la maladie de Lyme, Borrelia burgdorferi, ou de sa tique vectrice, Ixodes scapularis. Ces régions représentent des zones privilégiées pour étudier le cycle de transmission dans son contexte environnemental. L’objectif principal de ce projet est d’étudier les relations spirochètes – tiques - hôtes et les facteurs environnementaux impliqués dans le cycle de transmission à partir des données du vecteur et de l’agent pathogène recueilli dans le Sud-Ouest du Québec de 2007 à 2008. Tout d’abord sera décrite la saisonnalité des tiques et des associations entre le vecteur et les hôtes rongeurs capturés. En effet, l’identification de la saisonnalité spécifique à chaque stade de la tique I. scapularis permet d’établir quels seront les mois propices pour effectuer les futures collectes de tiques. La saisonnalité synchrone des tiques immatures en quête peut également être un indicateur de la nature ou des souches de B. burgdorferi retrouvées. L’association des tiques immatures à différentes espèces ou à différentes classes d’hôtes (c.-à-d. âge, sexe, statut reproductif) a également été explorée. Nos résultats montrent que les souris du genre Peromyscus, principalement les mâles adultes, contribuent significativement à la survie et au développement du complexe I. scapularis - B. burgdorferi. Les tamias et les écureuils contribuent aussi à la survie et au développement des populations de la tique I. scapularis. Ensuite les associations entre le vecteur et les hôtes cervidés ont été examinées en tenant compte des facteurs environnementaux associés à leur niveau d’infestation. Ceci a permis d’évaluer i l’utilisation des cerfs à titre de sentinelles pour le vecteur et les agents pathogènes. D’après nos résultats, bien qu’ils soient des sentinelles efficaces pour détecter Anaplasma phagocytophilum, les cerfs semblent des sentinelles inefficaces pour détecter les zones d’établissement du complexe I. scapularis-B. burgdorferi. Enfin, une analyse de l’impact de la diversité des hôtes et de l’habitat sur l’abondance de la tique I. scapularis et la prévalence de B. burgdorferi a été effectuée et ce, en tenant compte d’autres facteurs environnementaux. Ces analyses ont permis de déterminer les facteurs critiques pour l’établissement du complexe I. scapularis – B. burgdorferi et d’explorer la contribution relative de diverses espèces d’hôtes. D’après nos études, la diversité de la communauté d’hôte et la diversité de l’habitat influencent le complexe I. scapularis - B. burgdorferi. De plus, le climat (la température et les précipitations) joue un rôle significatif dans l’établissement, la survie et le développement des populations d’I. scapularis. Ce projet de recherche a permis d’explorer et d’identifier divers facteurs environnementaux biotiques et abiotiques influençant l’établissement du complexe I. scapularis - B. burgdorferi dans le Sud-Ouest du Québec. Ceux-ci pourraient être utilisés à titre d’indicateurs environnementaux du risque de la maladie de Lyme au Québec et possiblement ailleurs au Canada. Mots-clés : Maladie de Lyme, éco-épidémiologie, facteurs environnementaux, Ixodes scapularis, Borrelia burgdorferi, Anaplasma phagocytophilum, micromammifères, cerfs, Québec ii Abstract Since the 90s in Canada, studies have identified new endemic areas for the agent of Lyme disease, Borrelia burgdorferi and the tick vector, Ixodes scapularis. These newly endemic areas for complex I. scapularis - B. burgdorferi are prime areas to study the transmission cycle in its environmental context. The main objective of this project is to study the spirochete-tick-host relationships and environmental factors involved in the transmission cycle from the data of the vector and the pathogen collected in southwestern Quebec, 2007 to 2008. First, a description of the seasonality of ticks and associations between the vector and captured rodent hosts was performed. The identification of specific seasonality at each stage of the tick I. scapularis establishes months conducive to make the future collections of ticks. Synchronous seasonality of questing immature ticks may also be an indicator of the nature or strain of B. burgdorferi found. In addition, the association of immature ticks in different species or different classes of hosts (i.e. age, sex, reproductive status) was explored. The Peromyscus mice and adult males in particular contributed significantly to the survival and development of complex I. scapularis- B. burgdorferi. Chipmunks and squirrels also contributed to the survival and development of I. scapularis populations. Second, the associations between vector and examined deer was described taking into account the environmental factors associated with the level of infestation and the use of deer as sentinels for the vector and the pathogen was evaluated. According to our results, the deer are effective sentinels to iii detect Anaplasma phagocytophilum, but seem ineffective or imprecise to detect endemic areas for complex I. scapularis-B. burgdorferi. Finally, an analysis of the impact of the host diversity and habitat on the abundance of I. scapularis and prevalence of B. burgdorferi considering other environmental factors was performed. These analyzes were used to determine the critical factors in the establishment of complex I. scapularis- B. burgorferi and explore the relative contribution of various host species. According to our studies, the diversity of the host community and habitat influences the complex I. scapularis-B. burgdorferi. On the other hand, the climate (temperature and precipitation) plays a significant role in the establishment, survival and development of the I. scapularis populations. This study allowed us to explore and identify various biotic and abiotic environmental factors influencing the establishment of complex I. scapularis-B. burgdorferi in southwestern Quebec. These environmental factors could be used as environmental indicators of the risk of Lyme disease in Quebec and possibly elsewhere in Canada. Keywords : Lyme disease, eco-epidemiology, environmental factors, Ixodes scapularis, Borrelia burgdorferi, Anaplasma phagocytophilum, rodents, deer, Quebec iv Table des matières RÉSUMÉ I ABSTRACT III TABLE DES MATIÈRES V LISTE DES TABLEAUX X LISTE DES FIGURES XII LISTE DES SIGLES ET DES ABRÉVIATIONS XIV REMERCIEMENTS XVII INTRODUCTION 1 L’émergence des maladies vectorielles 1 L’émergence de la maladie de Lyme 3 L’éco-épidémiologie de la maladie de Lyme 4 OBJECTIFS 7 RECENSION DES ÉCRITS 10 La maladie de Lyme chez l’Homme 11 Symptomatologie 11 Diagnostic, traitement et prévention 12 L’épidémiologie de la maladie de Lyme 14 v Incidence aux États-Unis 15 Incidence au Canada 15 Le spirochète 17 B. burgdorferi sensu lato 18 Génome de B. burgdorferi 19 Interactions spirochètes-tiques-hôtes 19 La tique vectrice 21 Famille Ixodidae 22 Interactions de la tique I. scapularis avec son environnement 22 I. scapularis comme vecteur de B. burgdorferi 26 Les hôtes 27 Les mammifères sauvages 28 Les oiseaux migrateurs 31 Les facteurs environnementaux 33 Facteurs biotiques et impact de la biodiversité 33 Facteurs abiotiques 36 Tableaux 38 EXPOSÉ ET ANALYSE DES RÉSULTATS 47 Article 1: Associations between Ixodes scapularis ticks and small mammal hosts in a newly-endemic zone in southeastern Canada: implications for Borrelia burgdorferi transmission 48 Abstract 49 Introduction 50 Materials and methods 51 Study areas 51 Wild small mammal trapping 52 Blood and tick collection and detection of B. burgdorferi infection. 53 Statistical analyses 54 vi Results 57 Wild small mammal trapping and tick collection 57 B. burgdorferi infection in wild small mammals and their tick ectoparasites 57 Host associations of I. scapularis 58 Analysis of the intensity of infestation on I. scapularis-positive sites 59 Discussion 61 Acknowledgements 65 References 66 Figures 71 Tables 74 Article 2: Harvested white-tailed deer as sentinel hosts for early establishing Ixodes scapularis populations and risk from vector-borne zoonoses in southeastern Canada 78 Abstract 79 Introduction 80 Materials and Methods 82 Study site 82 Deer examination and tick collection 82 Diagnostic tests for tick-associated pathogens 83 Environmental determinants 84 Data on I. scapularis tick and tick population occurrence 85 Statistical analyses of tick infestation levels of deer 87 Spatial cluster analysis 89 Results 89 Statistical analyses: Models of tick infestation levels of deer 90 Spatial cluster analysis 91 Discussion 92 Conclusion 94 vii Acknowledgements 95 References 96 Figures 103 Tables 106 Article 3: Does high biodiversity reduce the risk of Lyme disease invasion? 111 Abstract 112 Introduction 114 Methods 116 Study sites 116 Collection and sampling of ticks and captured mammals 117 Testing of tick and rodent samples for B. burgdorferi infection 118 Collection and development of explanatory variables (see Table XIX) 118 Accounting for rates of I. scapularis and B. burgdorferi immigration 121 Statistical
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