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A Pilot Study at the Tick/Human Interface in Thailand

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A Pilot Study at the Tick/Human Interface in Thailand Monitoring Silent Spillovers Before Emergence: A Pilot Study at the Tick/Human Interface in Thailand Sarah Temmam, Delphine Chrétien, Thomas Bigot, Evelyne Dufour, Stéphane Petres, Marc Desquesnes, Elodie Devillers, Marine Dumarest, Léna Yousfi, Sathaporn Jittapalapong, et al. To cite this version: Sarah Temmam, Delphine Chrétien, Thomas Bigot, Evelyne Dufour, Stéphane Petres, et al.. Moni- toring Silent Spillovers Before Emergence: A Pilot Study at the Tick/Human Interface in Thailand. Frontiers in Microbiology, Frontiers Media, 2019, 10, pp.2315. 10.3389/fmicb.2019.02315. pasteur- 02318851 HAL Id: pasteur-02318851 https://hal-pasteur.archives-ouvertes.fr/pasteur-02318851 Submitted on 17 Oct 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License ORIGINAL RESEARCH published: 17 October 2019 doi: 10.3389/fmicb.2019.02315 Monitoring Silent Spillovers Before Emergence: A Pilot Study at the Tick/Human Interface in Thailand Sarah Temmam 1, Delphine Chrétien 1, Thomas Bigot 1,2, Evelyne Dufour 3, Stéphane Petres 3, Marc Desquesnes 4,5,6, Elodie Devillers 7, Marine Dumarest 1, Léna Yousfi 7, Sathaporn Jittapalapong 8, Anamika Karnchanabanthoeng 8, Kittipong Chaisiri 9, Léa Gagnieur 1, Jean-François Cosson 7, Muriel Vayssier-Taussat 7, Serge Morand 10,11, Sara Moutailler 7 and Marc Eloit 1,12* 1 Institut Pasteur, Biology of Infection Unit, Inserm U1117, Pathogen Discovery Laboratory, Paris, France, 2 Institut Pasteur – Bioinformatics and Biostatistics Hub – Computational Biology Department, Institut Pasteur, USR 3756 CNRS, Paris, France, 3 Institut Pasteur, Production and Purification of Recombinant Proteins Technological Platform – C2RT, Paris, France, 4 Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), UMR InterTryp, Bangkok, Thailand, 5 InterTryp, Institut de Recherche pour le Développement (IRD), CIRAD, University of Montpellier, Montpellier, 6 7 Edited by: France, Department of Parasitology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand, UMR BIPAR, Erna Geessien Kroon, Animal Health Laboratory, ANSES, INRA, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, Maisons-Alfort, France, 8 9 Federal University of Minas Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand, Faculty of Tropical Medicine, Mahidol University, 10 Gerais, Brazil Bangkok, Thailand, Institut des Sciences de l’Evolution, CNRS, CC065, Université Montpellier, Montpellier, France, 11 CIRAD ASTRE, Faculty of Veterinary Technology, Kasetsart University, Bangkok, Thailand, 12 National Veterinary School of Reviewed by: Alfort, Paris-Est University, Maisons-Alfort, France Rafal Tokarz, Columbia University, United States Nicholas Johnson, Emerging zoonoses caused by previously unknown agents are one of the most important Animal and Plant Health Agency, challenges for human health because of their inherent inability to be predictable, United Kingdom conversely to emergences caused by previously known agents that could be targeted *Correspondence: Marc Eloit by routine surveillance programs. Emerging zoonotic infections either originate from [email protected] increasing contacts between wildlife and human populations, or from the geographical expansion of hematophagous arthropods that act as vectors, this latter being more Specialty section: This article was submitted to capable to impact large-scale human populations. While characterizing the viral Virology, communities from candidate vectors in high-risk geographical areas is a necessary initial a section of the journal Frontiers in Microbiology step, the need to identify which viruses are able to spill over and those restricted to Received: 17 July 2019 their hosts has recently emerged. We hypothesized that currently unknown tick-borne Accepted: 23 September 2019 arboviruses could silently circulate in specific biotopes where mammals are highly Published: 17 October 2019 exposed to tick bites, and implemented a strategy that combined high-throughput Citation: sequencing with broad-range serological techniques to both identify novel arboviruses Temmam S, Chrétien D, Bigot T, Dufour E, Petres S, Desquesnes M, and tick-specific viruses in a ticks/mammals interface in Thailand. The virome of Devillers E, Dumarest M, Yousfi L, Thai ticks belonging to the Rhipicephalus, Amblyomma, Dermacentor, Hyalomma, Jittapalapong S, Karnchanabanthoeng A, Chaisiri K, and Haemaphysalis genera identified numerous viruses, among which several viruses Gagnieur L, Cosson J-F, could be candidates for future emergence as regards to their phylogenetic relatedness Vayssier-Taussat M, Morand S, with known tick-borne arboviruses. Luciferase immunoprecipitation system targeting Moutailler S and Eloit M (2019) Monitoring Silent Spillovers Before external viral proteins of viruses identified among the Orthomyxoviridae, Phenuiviridae, Emergence: A Pilot Study at the Flaviviridae, Rhabdoviridae, and Chuviridae families was used to screen human and Tick/Human Interface in Thailand. Front. Microbiol. 10:2315. cattle Thai populations highly exposed to tick bites. Although no positive serum was doi: 10.3389/fmicb.2019.02315 detected for any of the six viruses selected, suggesting that these viruses are not infecting Frontiers in Microbiology | www.frontiersin.org 1 October 2019 | Volume 10 | Article 2315 Temmam et al. LIPS-TICKS Thailand these vertebrates, or at very low prevalence (upper estimate 0.017% and 0.047% in humans and cattle, respectively), the virome of Thai ticks presents an extremely rich viral diversity, among which novel tick-borne arboviruses are probably hidden and could pose a public health concern if they emerge. The strategy developed in this pilot study, starting from the inventory of viral communities of hematophagous arthropods to end by the identification of viruses able (or likely unable) to infect vertebrates, is the first step in the prediction of putative new emergences and could easily be transposed to other reservoirs/vectors/susceptible hosts interfaces. Keywords: virome, tick, emergence, spillover, LIPS INTRODUCTION tick-borne viruses, belonging either to known or completely new viral families, for which the potential zoonotic risk for humans Among the list of human-infecting pathogens, two-thirds are or domestic animals is still unknown (Tokarz et al., 2014a, 2018; zoonotic agents (Woolhouse et al., 2012). With increasing Xia et al., 2015; Moutailler et al., 2016; Shi et al., 2016; Pettersson contacts between humans, wildlife, and their associated et al., 2017). For example, among the Phenuiviridae, known arthropods (due to changes in land use, global climate warming, to contain tick-borne pathogens such as the severe fever with or urbanization), the frequency of human infections with animal thrombocytopenia syndrome phlebovirus (SFTS virus) (Silvas viruses is expected to increase (Cutler et al., 2010). Wolfe et al. and Aguilar, 2017), recent bisegmented phleboviruses have been noted that the emergence of a pathogen of vertebrate into a described, such as Lihan tick phlebovirus (LTPV) primarily new susceptible vertebrate population goes through four main identified in Rhipicephalus microplus ticks from China, Brazil, steps: (1) spillover of a pathogen from its animal reservoir to and Trinidad and Tobago (Li C. X. et al., 2015; Souza et al., 2018; sporadic human cases, (2) limited interhuman transmission ofa Sameroff et al., 2019) and further detected in Turkish Hyalomma zoonotic pathogen, (3) large-scale spread of a zoonotic pathogen marginatum (Dinçer et al., 2017) and Rhipicephalus sanguineus through interhuman transmissions, and (4) adaptation of the ticks (Brinkmann et al., 2018). Flaviviridae-related tick-borne pathogen to humans (Wolfe et al., 2007). This is not the case viruses (e.g., Bole tick virus 4, BLTV4) were primarily associated for arboviruses: arbovirus emergence is linked to the spread of with Hyalomma asiaticum and Rh. sanguineus ticks (Shi et al., infected arthropods (directly or via the geographical expansion 2015; Sameroff et al., 2019). This virus presents a genome of their vertebrate host, as for ticks) into new areas or to the 1.5 times larger than other Flaviviridae tick-borne viruses and incursion of humans in new biotopes. Most recent epidemics could constitute, with other related flaviviruses that present that emerged were linked to arboviruses that were already known large genomes, at least a new genus among the Flaviviridae but described in limited areas, as the recent example of Zika family. In complement to known rhabdoviruses transmitted virus rapid expansion (Liu et al., 2019). by ticks (Labuda and Nuttall, 2004) [including several viruses Ticks are major hematophagous arthropod vectors that harbor pathogenic for humans (Menghani et al., 2012)], novel single- multiple infectious agents. Some of these agents are known stranded RNA (ssRNA) negative-strand viruses belonging to to infect humans, leading to several tick-borne diseases such the
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