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LES PESTIVIRUS À L'interface FAUNE SAUVAGE/FAUNE DOMESTIQUE : Pathogénie Chez L'isard Gestant Et Épidémiologie Dans La

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LES PESTIVIRUS À L'interface FAUNE SAUVAGE/FAUNE DOMESTIQUE : Pathogénie Chez L'isard Gestant Et Épidémiologie Dans La THESE Présentée devant L’UNIVERSITE DE NICE SOPHIA ANTIPOLIS EN COTUTELLE AVEC L’UNIVERSITE DE LIEGE pour l’obtention du DIPLOME DE DOCTORAT (arrêté du 25 avril 2002) Spécialité INTERACTIONS MOLECULAIRES Et du DIPLOME EN SCIENCES VETERINAIRES présentée et soutenue publiquement le 20 décembre 2011 par Mlle Claire MARTIN LES PESTIVIRUS À L’INTERFACE FAUNE SAUVAGE/FAUNE DOMESTIQUE : Pathogénie chez l’isard gestant et épidémiologie dans la région Provence-Alpes-Côte D’azur JURY : M. Richard THIERY, co-directeur de thèse M. Claude SAEGERMAN, co-directeur de thèse Mme Anny CUPO, co-directeur de thèse Mme Sophie ROSSI, Examinateur M. François MOUTOU, Examinateur M. Benoît DURAND, Rapporteur Mme Marie-Pierre RYSER-GEGIORGIS, Rapporteur M. Pascal HENDRIKS, Président de jury 1 2 RESUME Dans les Alpes du Sud de la France, des diminutions de populations de chamois (Rupicapra rupicapra) ont été rapportées. Or, depuis une dizaine d’année, des pestivirus ont causé de fortes mortalités dans des populations d’isards des Pyrénées (Rupicapra pyrenaica). Bien que les signes cliniques associés à cette infection aient été caractérisés chez cette espèce, la pathogénie chez les animaux gestants est peu étudiée. De plus, des transmissions inter-espèces ont régulièrement été incriminées dans l’épidémiologie des pestiviroses ; ceci particulièrement au niveau des alpages où des contacts fréquents sont décrits entre ruminants sauvages et domestiques. Les objectifs de ce travail de thèse ont donc été, dans un premier temps, d’étudier la pathogénie de l’infection à pestivirus chez des isards et plus particulièrement ses effets sur la gestation. Dans un second temps, nous avons étudié l’épidémiologie de l’infection dans différentes zones de la région Provence-Alpes-Côte d’Azur (PACA), tout d’abord chez des ruminants sauvages, puis à l’interface entre les ruminants sauvages et domestiques partageant les mêmes alpages. Trois femelles isards ont été inoculées, durant le deuxième tiers de leur gestation, avec une souche de BDV-4, préalablement isolée d’un isard sauvage dans les Pyrénées espagnoles. Un groupe témoin était constitué d’une quatrième femelle isard gestante, associée à une agnelle. Une virémie longue, de quatre jours post infection jusqu’à la mort des animaux, était associée à des profils de séroconversion variables et à des lymphopénies importantes. Bien qu’aucune gestation n’ait été menée à terme, la détection des ARN viraux dans tous les organes testés des fœtus de femelles inoculées suggéraient la naissance possible d’animaux infectés persistants immunotolérants (IPI) chez cette espèce. Par ailleurs, dans la région PACA, une première étude séro-épidémiologique, longitudinale, a été réalisée dans le département des Hautes-Alpes sur les campagnes de chasse de 2003 à 2007. Des anticorps dirigés contre les pestivirus étaient présents chez 45,9% (Intervalle de confiance à 95% [IC95%] : 40,5-51,3) des chamois et 61,1% (IC 95% : 38,6-83,6%) des mouflons (Ovis aries musimon). Une deuxième étude épidémiologique transversale, conduite à la fois chez les ruminants sauvages et domestiques lors des saisons de chasse 2009 et 2010, a montré des séroprévalences élevées, atteignant 38,8% (IC95% : 74,3 – 78,8 %) chez les chamois et 25,9% (IC95% : 9,4 – 42,4 %) chez les chevreuils (Capreolus capreolus). Tous les cheptels ovins testés (n=37) présentaient une séroprévalence positive, atteignant 76,6 % (IC95%: 74,3 – 78,8 %) pour l’ensemble des 1383 sérums analysés. Dans le département des Alpes-Maritimes, deux souches ovines de pestivirus ont été isolées et classées respectivement dans le génogroupe BDV-3 (Border Disease Virus type 3) et dans le génogroupe BDV-Tunisien. Dans le département des Alpes de Haute-Provence, deux souches ont été isolées, d’une brebis avortée et, pour la première fois, d’un chamois (souche « Rupi-05 »). Les deux souches ont été classées parmi les virus du génogroupe BDV-6. Des séroneutralisations croisées ont montré que les chamois avaient des titres en anticorps supérieurs contre la souche « Rupi-05 », alors que les moutons réagissent de façon homogène envers les différentes souches ovines locales. De plus, les ovins ont des titres en anticorps neutralisants en moyenne plus élevés que les chamois pouvant laisser suspecter une circulation plus importante chez les moutons. Des anticorps neutralisant ont été détectés chez un seul chevreuil et étaient dirigés vers une souche de BVDV-1 (Bovine Viral Diarrhea Virus type 1). En conclusion, une circulation active de pestivirus est présente dans la région PACA, chez les animaux sauvages comme domestiques. Dans les Alpes de Haute-Provence, les souches isolées des différentes espèces sont classées parmi le même génogroupe, montrant une continuité géographique dans la répartition des souches. Les résultats obtenus lors de l’infection expérimentale montrent des effets sur la gestation importants, avec une possible présence d’animaux IPI chez les chamois comme chez les ovins. Bien que nos résultats ne permettent pas d’établir de façon précise un sens de transmission entre les espèces de ruminants domestiques et sauvages, deux cycles épidémiologiques semblent être présents, caractérisés par une forte circulation intra-spécifique et connectés à des transmissions ponctuelles entre chamois et moutons. 3 ABSTRACT In the French South Alps, diminutions of effectives of chamois (Rupicapra rupicapra) were recently reported. Besides, Pestivirus were shown to cause high mortalities in Pyrenean chamois (Rupicapra pyrenaica). While clinical signs associated to the infection were characterized in wild populations, the pathogeny in pregnant female has not been studied yet. Moreover, interspecies transmissions were recently incriminated in the epidemiology of Pestivirus infections, especially in alpine pastures, known for their high rate contact between wild and domestic ruminants. The objectives of this doctorate were, in a first time, to study the pathogeny on pregnancy associated to the Pestivirus infection in Pyrenen chamois. Then, this survey was aimed to study the infection epidemiology in various areas of the Provence-Alpes-Côte d’Azur (PACA) region, firstly in wild ruminants and at the interface between wild and domestic ruminants sharing the same pastures. Three pregnant female Pyrenean chamois were inoculated during the second third of gestation with BDV-4 strain, previously isolated from a diseased wild Pyrenean chamois. A group control was constituted by a fourth pregnant female Pyrenean chamois and a ewe. A long-lasting viremia from four days post inoculation to the death of animals was associated to different profiles of seroconversion and important lymphopenia. All pregnancies aborted. Viral RNA were detected in all organs tested of the three inoculated females, suggesting that persistently infected animals (PI) may be born in this species. Besides, in the PACA region, a first epidemiological study was performed in the Hautes-Alpes district during the hunting seasons of 2003 to 2007. Antibodies directed to Pestivirus were found in 45,9% (95% Confidence Interval [95% CI] : 40,5-51,3%) of chamois and 61,1% (95% CI: 38,6-83,6%) of mouflons (Ovis aries musimon). A second epidemiological study, transversal, performed during the hunting seasons 2009 and 2010 showed high seroprevalences, reaching 38,8% (95% CI: 74,3 – 78,8 %) in chamois and 25,9% (95% CI : 9,4 – 42,4 %) in roe deer (Capreolus capreolus). All ovine herds tested (n=37) presented positive seroprevalence, reaching 76,6 % (95% CI: 74,3 – 78,8 %) of the 1383 sera tested. In the Alpes-Maritimes district, two ovine strains were isolated and classified in the Border Disease Virus (BDV) type 3 and the BDV-tunisian genogroups, respectively. In the Alpes de Haute- Provence district, two viral strains were isolated: one from an aborted ewe, and for the first time, from a chamois (strain named “Rupi-05”). Comparative viral neutralization tests showed that chamois had neutralizing antibodies titers higher against the “Rupi-05” strain, and sheep had homogenous titers against all local ovine strains. Besides, sheep had mean titers in neutralizing antibodies higher than chamois, suggesting a circulation more important in sheep. Neutralizing antibodies were detected in only one roe deer, and were directed against a Bovine Viral Diarrhea Virus type 1. In conclusion, an active circulation of Pestivirus is present in the PACA region, in both wild and domestic ruminants. In the Alpes de Haute-Provence district, isolated pestiviral strains from chamois and sheep clustered in the same genogroup, showing a geographical continuity in the strains repartition. Results obtained from the experimental infection showed important effects on the pregnancy, with a possible birth of PI animal in chamois and in sheep. Our results showed that two epidemiological cycles are present in chamois and sheep, respectively, characterized by an important circulation intra-species and connected by punctual transmission between animal species. 4 REMERCIEMENTS Un projet de l’ampleur d’une thèse ne peut aboutir sans l’aide de nombreuses personnes. Ces remerciements, bien que représentant les remerciements « officiels » ne pourront jamais être à la hauteur de toute la gratitude que je peux ressentir envers celles et ceux m’ayant permis de mettre en place, de surmonter les moments de doutes et de remise en questions récurrents et d’achever cette thèse dans de bonnes conditions. Tout d’abord, je tiens à remercier les membres du jury ayant accepté cette lourde tache en supplément de leurs nombreuses taches : Dr. Marie-Pierre Ryser-Degiorgis (Centre pour la Médecine des Poissons et des Animaux sauvages – FIWI, Faculté Vetsuisse, Université de Bern) et Dr. Benoît Durand (Directeur de recherche au laboratoire de l’Anses Alfort LERPAZ) pour avoir accepté d’en être rapporteur. Dr. Pascal Hendriks, Dr. François Moutou, Dr. Sophie Rossi pour avoir accepté d’en être examinateur. Prof. Anny Cupo pour avoir accepté d’être Président de Jury Je remercie mes directeurs de recherche et encadrants: Dr. Richard Thiéry, Directeur du laboratoire de l’Anses Sophia Antipolis pour m’avoir accueillie dans son laboratoire. Pr.
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