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25 Apr 2023
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The distribution, phenology, host range and pathogen prevalence of Ixodes ricinus in France: a systematic map and narrative review

An extensive review of Ixodes ricinus in European France

Recommended by based on reviews by Ana Palomar and 1 anonymous reviewer

Ticks are obligate, bloodsucking, nonpermanent ectoparasitic arthropods. Among them, Ixodes ricinus is a classic example of an extreme generalist tick, presenting a highly permissive feeding behavior using different groups of vertebrates as hosts, such as mammalian (including humans), avian and reptilian species (Hoogstraal & Aeschlimann, 1982; Dantas-Torresa & Otranto, 2013). This ecological adaptation can account for the broad geographical distribution of I. ricinus populations, which extends from the western end of the European continent to the Ural Mountains in Russia, and from northern Norway to the Mediterranean basin, including the North African countries - Morocco, Algeria and Tunisia (https://ecdc.europa.eu/en/disease-vectors/surveillance-and-disease-data/tick-maps). The contact with different hosts also promotes the exposure/acquisition and transmission of various pathogenic agents (viruses, bacteriae, protists and nematodes) of veterinary and medical relevance (Aeschlimann et al., 1979). As one of the prime ticks found on humans, this species is implicated in diseases such as Lyme borreliosis, Spotted Fever Group rickettsiosis, Human Anaplasmosis, Human Babesiosis and Tick-borne Encephalitis (Velez et al., 2023). 

The climate change projections drawn for I. ricinus, in the scenario of global warming, point for the expansion/increase activity in both latitude and altitude (Medlock et al., 2013). The adequacy of vector modeling is relaying in the proper characterization of complex biological systems. Thus, it is essential to increase knowledge on I. ricinus, focusing on aspects such as genetic background, ecology and eco-epidemiology on a microscale but also at a country and region level, due to possible local adaptations of tick populations and genetic drift. 

In the present systematic revision, Perez et al. (2023) combine old and recently published data (mostly up to 2020) regarding I. ricinus distribution, phenology, host range and pathogen association in continental France and Corsica Island. Based on a keyword search of peer-reviewed papers on seven databases, as well as other sources of grey literature (mostly, thesis), the authors have synthesized information on: 1) Host parasitism to detect potential differences in host use comparing to other areas in Europe; 2) The spatiotemporal distribution of I. ricinus, to identify possible geographic trends in tick density, variation in activity patterns and the influence of environmental factors; 3) Tick-borne pathogens detected in this species, to better assess their spatial distribution and variation in exposure risk. 

As pointed out by both reviewers, this work clearly summarizes the information regarding I. ricinus and associated microorganisms from European France. This review also identifies remaining knowledge gaps, providing a comparable basis to orient future research. This is why I chose to recommend Perez et al (2023)'s preprint for Peer Community Infections. 

REFERENCES

Aeschlimann, A., Burgdorfer, W., Matile, H., Peter, O., Wyler, R. (1979) Aspects nouveaux du rôle de vecteur joué par Ixodes ricinus L. en Suisse. Acta Tropica, 36, 181-191.

Dantas-Torresa, F., Otranto, D. (2013) Seasonal dynamics of Ixodes ricinus on ground level and higher vegetation in a preserved wooded area in southern Europe. Veterinary Parasitology, 192, 253- 258.
https://doi.org/10.1016/j.vetpar.2012.09.034

Hoogstraal, H., Aeschlimann, A. (1982) Tick-host specificity. Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 55, 5-32.

Medlock, J.M., Hansford, K.M., Bormane, A., Derdakova, M., Estrada-Peña, A., George, J.C., Golovljova, I., Jaenson, T.G.T., Jensen, J.K., Jensen, P.M., Kazimirova, M., Oteo, J.A., Papa, A., Pfister, K., Plantard, O., Randolph, S.E., Rizzoli, A., Santos-Silva, M.M., Sprong, H., Vial, L., Hendrickx, G., Zeller, H., Van Bortel, W. (2013) Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasites and Vectors, 6. https://doi.org/10.1186/1756-3305-6-1

Perez, G., Bournez, L., Boulanger, N., Fite, J., Livoreil, B., McCoy, K., Quillery, E., René-Martellet, M., Bonnet, S. (2023) The distribution, phenology, host range and pathogen prevalence of Ixodes ricinus in France: a systematic map and narrative review. bioRxiv, ver. 1 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2023.04.18.537315

Velez, R., De Meeûs, T., Beati, L., Younsi, H., Zhioua, E., Antunes, S., Domingos, A., Ataíde Sampaio, D., Carpinteiro, D., Moerbeck, L., Estrada-Peña, A., Santos-Silva, M.M., Santos, A.S. (2023) Development and testing of microsatellite loci for the study of population genetics of Ixodes ricinus Linnaeus, 1758 and Ixodes inopinatus Estrada-Peña, Nava & Petney, 2014 (Acari: Ixodidae) in the western Mediterranean region. Acarologia, 63, 356-372. https://doi.org/10.24349/bvem-4h49

The distribution, phenology, host range and pathogen prevalence of *Ixodes ricinus* in France: a systematic map and narrative reviewGrégoire Perez, Laure Bournez, Nathalie Boulanger, Johanna Fite, Barbara Livoreil, Karen D. McCoy, Elsa Quillery, Magalie René-Martellet, and Sarah I. Bonnet<p style="text-align: justify;">The tick <em>Ixodes ricinus</em> is the most important vector species of infectious diseases in European France. Understanding its distribution, phenology, and host species use, along with the distribution and preva...Animal diseases, Behaviour of hosts, infectious agents, or vectors, Disease Ecology/Evolution, Ecohealth, Ecology of hosts, infectious agents, or vectors, Epidemiology, Geography of infectious diseases, Interactions between hosts and infectious ag...Ana Sofia Santos2022-12-06 14:52:44 View
02 Jun 2023
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Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmission

What you eat can eliminate you: bloodmeal sources and mosquito fitness

Recommended by based on reviews by Francisco C. Ferreira and 1 anonymous reviewer

​​Diptera-borne pathogens rank among the most serious health threats to vertebrate organisms around the world, particularly in tropical areas undergoing strong human impacts – e.g., urbanization and farming –, where social unrest and poor economies exacerbate the risk (Allen et al. 2017; Robles-Fernández et al. 2022). Although scientists have acquired a detailed knowledge on the life-history of malaria parasites (Pacheco and Escalante 2023), they still do not have enough information about their insect vectors to make informed management and preventive decisions (Santiago-Alarcon 2022).

In this sense, I am pleased to recommend the study of Vantaux et al. (2023), where authors conducted an experimental and theoretical study to analyzed how the diversity of blood sources (i.e., human, cattle, sheep, and chicken) affected the fitness of the human malaria parasite – Plasmodium falciparum – and its mosquito vector – Anopheles gambiae s.l.

The study was conducted in Burkina Faso, West Africa. Interestingly, authors did not find a significant effect of blood meal source on parasite development, and a seemingly low impact on the fitness of mosquitoes that were exposed to parasites. However, mosquitoes’ feeding rate, survival, fecundity, and offspring size were negatively affected by the type of blood meal ingested. In general, chicken blood represented the worst meal source for the different measures of mosquito fitness, and sheep blood seems to be the least harmful. This result was supported by the theoretical model, where vectorial capacity was always better when mosquitoes fed on sheep blood compared to cow and chicken blood. Thus, the knowledge generated by this study provides a pathway to reduce human infection risk by managing the diversity of farm animals. For instance, transmission to humans can decrease when chickens and cows represent most of the available blood sources in a village.

These results along with other interesting details of this study, represent a clear example of the knowledge and understanding of insect vectors that we need to produce in the future, particularly to manage and prevent hazards and risks (sensu Hoseini et al. 2017).

REFERENCES

Allen T., et al., Global hotspots and correlates of emerging zoonotic diseases. Nat. Commun. 8, 1124. (2017). https://doi.org/10.1038/s41467-017-00923-8

Hosseini P.R., et al., Does the impact of biodiversity differ between emerging and endemic pathogens? The need to separate the concepts of hazard and risk. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160129 (2017). https://doi.org/10.1098/rstb.2016.0129

Pacheco M.A., and Escalante, A.A., Origin and diversity of malaria parasites and other Haemosporida. Trend. Parasitol. (2023) https://doi.org/10.1016/j.pt.2023.04.004

Robles-Fernández A., et al., Wildlife susceptibility to infectious diseases at global scales. PNAS 119: e2122851119. (2022). https://doi.org/10.1073/pnas.2122851119

Santiago-Alarcon D. A meta-analytic approach to investigate mosquitoes’ (Diptera: Culicidae) blood feeding preferences from non-urban to urban environments. In: Ecology and Control of Vector-borne Diseases, vol. 7 (R.G. Gutiérrez-López, J.G. Logan, Martínez-de la Puente J., Eds). Pp. 161-177. Wageningen Academic Publishers. eISBN: 978-90-8686-931-2 | ISBN: 978-90-8686-379-2 (2022).

Vantaux A. et al. Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmission. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Infections (2023). https://doi.org/10.1101/2023.02.10.527988

Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmissionAmélie Vantaux, Nicolas Moiroux, Kounbobr Roch Dabiré, Anna Cohuet, Thierry Lefèvre<p style="text-align: justify;">The transmission of malaria parasites from mosquito to human is largely determined by the dietary specialization of <em>Anopheles mosquitoes</em> to feed on humans. Few studies have explored the impact of blood meal...Ecology of hosts, infectious agents, or vectors, Parasites, VectorsDiego Santiago-Alarcon2023-02-13 11:02:58 View
08 Dec 2022
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Zoonotic emergence at the animal-environment-human interface: the forgotten urban socio-ecosystems

Zoonotic emergence and the overlooked case of cities

Recommended by based on reviews by Eric Dumonteil, Nicole L. Gottdenker and 1 anonymous reviewer

Zoonotic pathogens, those transmitted from animals to humans, constitute a major public health risk with high associated global economic costs. Diseases associated with these pathogens represent more than 60% of emerging infectious diseases and predominantly originate in wildlife (1). Over the last decades, the emergence and re-emergence of zoonotic pathogens have led to an increasing number of epidemics, as illustrated by the current Covid-19 pandemic. There is ample evidence that human impact on native ecosystems such as deforestation, agricultural development, and urbanization, is linked to spillover of pathogens from animals to humans (2). However, research and calls to action have mainly focused on the importance of surveillance and prevention of zoonotic emergences along landscape interfaces, with special emphasis on tropical forests and agroecosystems, and studies and reviews pointing out the zoonotic risk associated with cities are scarce.  Additionally, cities are sometimes wrongly seen as one homogeneous ecosystem, almost exclusively human, with a Northern hemisphere-biased perception of what a city is, which fails to take into account the ecological and socio-economic diversities that can constitute an urban area.

Here, Dobigny and Morand (3) aim to draw attention to the importance of urban ecosystems in zoonotic risk and advocate that further attention should be paid to urban, peri-urban and suburban areas. In this well-organized and well-documented review, the authors show, using updated literature, that cities are places where massive contacts occur between wildlife, domestic animals, and human inhabitants (thus constituting spillover opportunities), and that it is even likely that human and wildlife contact in urban centers is more prevalent than in wild areas, perhaps contrary to intuition. Indeed, cities currently constitute the most important environment of human life and are places for millions of close interactions between humans and animals, including pets and domestic animals, wild animals through the intrusion of wild urban-adapted species (e.g., some bat, rodent, or bird species among others), manipulation and consumption of wildlife meat, and the existence of wildlife meat markets, which all constitute a major risk for zoonotic spillover. In cities, lab escapees of zoonotic pathogens also exist, and trends of adaptation to urban ecological conditions of many vectors of primary health importance is also a concern. The authors further argue that cities are predominant places for both epidemic amplification of human-human transmitted pathogens, because they are places with high human densities and population growth, and for dissemination of reservoirs, vectors and pathogens, as they are transport hubs. Dobigny & Morand further predict, likely correctly, that cities may be important places for pathogen evolution.  Finally, they propose actions and recommendations to limit the risk of zoonotic spillover events from urban ecosystems and future directions for research aiming at assessing this risk. 

The reviewers found the manuscript well-organized and presented, timely, and bringing novel contributions to the field of zoonotic emergence. I strongly recommend this article, which should benefit a large audience, particularly in the context of the current Covid-19 pandemics and the ongoing One Health initiatives aiming at preventing future zoonotic disease emergence (4). 

References

(1) Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature, 451, 990–993. https://doi.org/10.1038/nature06536

(2) White RJ, Razgour O (2020) Emerging zoonotic diseases originating in mammals: a systematic review of effects of anthropogenic land-use change. Mammal Review, 50, 336–352. https://doi.org/10.1111/mam.12201

(3) Dobigny G, Morand S (2022) Zoonotic emergence at the animal-environment-human interface: the forgotten urban socio-ecosystems. Zenodo, 6444776, ver. 3 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.5281/zenodo.6444776

(4) Morand S, Lajaunie C (2021) Biodiversity and COVID-19: A report and a long road ahead to avoid another pandemic. One Earth, 4, 920–923. https://doi.org/10.1016/j.oneear.2021.06.007

Zoonotic emergence at the animal-environment-human interface: the forgotten urban socio-ecosystemsDobigny, G. & Morand, S.<p style="text-align: justify;">Zoonotic emergence requires spillover from animals to humans, hence animal-human interactions. A lot has been emphasized on human intrusion into wild habitats (e.g., deforestation, hunting) and the development of ag...Disease Ecology/Evolution, Ecohealth, Ecology of hosts, infectious agents, or vectors, Evolution of hosts, infectious agents, or vectors, One Health, ZoonosesEtienne Waleckx2022-04-11 11:39:11 View
17 Jan 2024
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Assessing the dynamics of Mycobacterium bovis infection in three French badger populations

From disease surveillance to public action. Re-inforcing both epidemiological surveillance and data analysis: an illustration with Mycobacterium bovis

Recommended by based on reviews by Rowland Kao and 1 anonymous reviewer

Mycobacterium bovis, also called M. tuberculosis var. bovis, is a bacterium belonging to the M. tuberculosis complex (i.e., MTBC) and which can cause through zoonotic transmission another form of human tuberculosis (Tb). It is above all the agent of bovine tuberculosis (i.e., bTb) which affects not only cattle (wild or farmed) but also a large diversity of other wild mammals worldwide. An increasing number of infected animal cases are being discovered in many regions of the world, thus raising the problem of tuberculosis transmission, including to humans, more complex than previously thought. Efforts have been made in terms of vaccination or culling of populations of host carrier species, such as the badger for example, however leading to consequences of greater dispersion of the infectious agent. M. bovis shows a more or less significant capacity to persist outside its hosts, particularly in the environment under certain abiotic and biotic conditions. This bacillus can be transmitted and spread in many ways, including through aerosol, mucus and sputum, urine and feces, by direct contact with infected animals, their dead bodies or rather via their excreta or by inhalation of aerosols, depending on the host species concerned.

In this paper, Calenge and his collaborators (Callenge et al. 2024) benefited from a national surveillance program on M. bovis cases in wild species, set up in 2011 in France, i.e., Sylvatub, for detecting and monitoring M. bovis infection in European badger (Meles meles) populations. Sylvatub is a participatory program involving both national and local stakeholder systems in order to determine changes in bTb infection levels in domestic and wild animal species. This original work had two aims: to describe spatial disease dynamics in the three clusters under scrutiny using a complex Bayesian model; and to develop indicators for the monitoring of the M. bovis infection by stakeholders and decision-makers of the program. This paper is timely and very comprehensive.

In this cogent study, the authors illustrate this point by using epidemiological surveillance to obtain large amounts of data (which is generally lacking in human epidemiology, but more dramatically lacking in animal epidemiology) and a highly sophisticated biostatistical analysis (Callenge et al. 2024). It is in itself a demonstration of the current capabilities of population dynamics applied to infectious disease situations, in this case animal, in the rapidly developing discipline of disease ecology and evolution. One of the aims of the study is to propose statistical models that can be used by the different stakeholders in charge, for instance, of wildlife conservation or the regional or State veterinary services to assess disease risk in the most affected regions.

References

Assel AKHMETOVA​, Jimena GUERRERO​, Paul McADAM, Liliana CM SALVADOR​, Joseph CRISPELL​, John LAVERY​, Eleanor PRESHO​, Rowland R KAO​, Roman BIEK​, Fraser MENZIES​, Nigel TRIMBLE​, Roland HARWOOD​, P Theo PEPLER, Katarina ORAVCOVA​, Jordon GRAHAM​, Robin SKUCE​, Louis DU PLESSIS​, Suzan THOMPSON​, Lorraine WRIGHT​, Andrew W BYRNE​, Adrian R ALLEN. 2023. Genomic epidemiology of Mycobacterium bovis infection in sympatric badger and cattle populations in Northern Ireland. Microbial Genomics 9: mgen001023. https://doi.org/10.1099/mgen.0.001023

Roman BIEK, Anthony O’HARE, David WRIGHT, Tom MALLON, Carl McCORMICK, Richard J ORTON, Stanley McDOWELL, Hannah TREWBY, Robin A SKUCE, Rowland R KAO. 2012. Whole genome sequencing reveals local transmission patterns of Mycobacterium bovis in sympatric cattle and badger populations. PLoS Pathogens 8: e1003008. https://doi.org/10.1371/journal.ppat.1003008

Clément CALENGE, Ariane PAYNE, Edouard REVEILLAUD, Céline RICHOMME, Sébastien GIRARD, Stephanie DESVAUX. 2024. Assessing the dynamics of Mycobacterium bovis infection in three French badger populations. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community In Infections. https://doi.org/10.1101/2023.05.31.543041

Marc CHOISY, Pejman ROHANI. 2006. Harvesting can increase severity of wildlife disease epidemics. Proceedings of the Royal Society, London, Ser. B 273: 2025-2034. https://doi.org/10.1098/rspb.2006.3554

Shannon C DUFFY, Sreenidhi SRINIVASAN, Megan A SCHILLING, Tod STUBER, Sarah N DANCHUK, Joy S MICHAEL, Manigandan VENKATESAN, Nitish BANSAL, Sushila MAAN, Naresh JINDAL, Deepika CHAUDHARY, Premanshu DANDAPAT, Robab KATANI, Shubhada CHOTHE, Maroudam VEERASAMI, Suelee ROBBE-AUSTERMAN, Nicholas JULEFF, Vivek KAPUR, Marcel A BEHR. 2020. Reconsidering Mycobacterium bovis as a proxy for zoonotic tuberculosis: a molecular epidemiological surveillance study. Lancet Microbe 1: e66-e73. https://doi.org/10.1016/S2666-5247(20)30038-0

Jean-François GUEGAN. 2019. The nature of ecology of infectious disease. The Lancet Infectious Diseases 19. https://doi.org/10.1016/s1473-3099(19)30529-8

Brandon H HAYES, Timothée VERGNE, Mathieu ANDRAUD, Nicolas ROSE. 2023. Mathematical modeling at the livestock-wildlife interface: scoping review of drivers of disease transmission between species. Frontiers in Veterinary Science 10: 1225446. https://doi.org/10.3389/fvets.2023.1225446

David KING, Tim ROPER, Douglas YOUNG, Mark EJ WOOLHOUSE, Dan COLLINS, Paul WOOD. 2007. Bovine tuberculosis in cattle and badgers. Report to Secretary of State about tuberculosis in cattle and badgers. London, UK. https://www.bovinetb.info/docs/RBCT_david_%20king_report.pdf  

Robert MM SMITH , Francis DROBNIEWSKI, Andrea GIBSON, John DE MONTAGUE, Margaret N LOGAN, David HUNT, Glyn HEWINSON, Roland L SALMON, Brian O’NEILL. 2004. Mycobacterium bovis Infection, United Kingdom. Emerging Infectious Diseases 10: 539-541. https://doi.org/10.3201/eid1003.020819 

Assessing the dynamics of *Mycobacterium bovis* infection in three French badger populationsClement CALENGE, Ariane PAYNE, Edouard REVEILLAUD, Celine RICHOMME, Sebastien GIRARD, Stephanie DESVAUX<p>The Sylvatub system is a national surveillance program established in 2011 in France to monitor infections caused by <em>Mycobacterium bovis</em>, the main etiologic agent of bovine tuberculosis, in wild species. This participatory program, inv...Animal diseases, Ecohealth, Ecology of hosts, infectious agents, or vectors, Epidemiology, Geography of infectious diseases, Pathogenic/Symbiotic Bacteria, ZoonosesJean-Francois Guegan2023-06-05 10:50:49 View