An extensive review of Ixodes ricinus in European France
The distribution, phenology, host range and pathogen prevalence of Ixodes ricinus in France: a systematic map and narrative review
Recommendation: posted 10 April 2023, validated 25 April 2023
Santos, A. (2023) An extensive review of Ixodes ricinus in European France. Peer Community In Infections, 100076. 10.24072/pci.infections.100076
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.
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.
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 recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
This work is issued from a scientific report commanded by of the Direction Générale de la Santé (Ministry of Health) to ANSES (French Agency for Food, Environmental and Occupational Health & Safety) who delegated through a research and development agreement to the École nationale vétérinaire d’Alfort (national veterinary School of Alfort) and allocated funds to hire GP for a 13 months postdoc contract (the complete report in French is available at https://hal-anses.archives-ouvertes.fr/anses-03263410).
Evaluation round #1
DOI or URL of the preprint: https://drive.google.com/drive/folders/1Uy-kVzEle9xg1DGxRUmsXeqVT7EjGZCM?usp=share_link
Version of the preprint: 1
Author's Reply, 02 Apr 2023
Decision by Ana Sofia Santos, posted 27 Feb 2023, validated 28 Feb 2023
Thank you for submitting your article in PCI infections.
This paper merits publication as it is important to increase knowledge on the ecology and eco-epidemiology of I. ricinus, aspects focused by the authors. Experts have evaluated the paper and I should first advice changes to the text according to the reviewer’s comments. I am also adding some suggestions myself:
1. Pag 2, Introduction, line 1 – “Among the forty or so tick species present in European France (…)” Please replace by an accurate sentence/number, “forty or so” sounds strange in a scientist article.
2. Pag4, table 1, 2nd row –“context”- Please note that context description in tabl 1 is different from what is found in the text body, right below table 1 “The “context” corresponded to European France as the target area (…)”
3. Pag5, 2.1 Research approach, last line (regarding the Outcome) – “The assessment of tick-borne pathogens in ticks was also considered as an outcome variable”
and SI 03 “Exclusion criteria - No comparator was excluded”
If the objective was to provide a complete image of tick-borne occurrence it would be interesting to include studies that does not have temporal or spacial and ecological comparator.
Saying in other words, the present review may not provide a complete view of the tick-borne agents present in France, as some studies might have been skipped for not having a temporal/special/ecological comparator, and this should be clearly stated in the text.
4. Pag5, 2.2 Search strategy – No clear indication if the first search using the keyword combinations “Ixodes ricinus” AND (abundance OR activity OR [behaviour OR behavior] OR burden OR density OR dispersal OR distribution OR dynamics OR infestation OR presence OR prevalence OR questing).”, and that retrieved 19,654 references, was just performed on titles. Please clarify that. The authors mention in pag 6 (2.3 Eligibility screening , 2.3.1 Eligibility criteria) that “Screening was conducted by GP, first on titles, then on abstracts, and finally on the full text when available.” but is not clear if this was applied to all. Please clarify this in the text. What is GP?
It seems reasonable to think that the first round was not based just on title analysis, otherwise several paper having a more generalist title, such as “Ixodes” or “ticks”, may have been skipped from this revision.
5. Pag10, Figure 1 heading – “Refer to SI 5 for the name of the departments.” Should be SI 7
6. Pag10, fist 6 lines of the text – “In south-western France (…). Thus, I. ricinus ticks seem to be present in some Mediterranean departments, but only under specific environmental conditions and above a certain altitude (Stachurski & Vial 2018).
Please note that, Sevestre et al, 2021 has published a paper on tick-borne agents found on questing I. ricinus (but also, host-feeding ticks) above 400 m in the Alpes Maritimes region, questioning the general idea of considering Mediterranean rim unsuitable for this ticks species. Maybe this should be, as well commented, in the paper, as post-analysis reference.
Sevestre J, Diarra AZ, Oumarou AH, Durant J, Delaunay P, Parola P. Detection of emerging tick-borne disease agents in the Alpes-Maritimes region, southeastern France. Ticks Tick Borne Dis. (2021) 12:101800. doi: 10.1016/j.ttbdis.2021.101800
7. Pag17, 3.3.1. The genus Anaplasma, “These ecotypes also differ by their vectors. Ecotypes I and II are mainly transmitted by I. ricinus, but ecotype III seems mainly transmitted by I. trianguliceps; vectors of ecotype IV are still uncertain, but are suspected to be among the hard ticks that specifically exploit birds.”
Please note that in Europe I. ventalloi was found associated with an A. phagocytophilum ecotype IV-like. This A. phagocytophilum variant was found in I. ventalloi from Portugal (Santos et al, 2004, 2017) and is sharing only 95% homology to those sequences of the agent derived from birds, and included in ecotype IV (Jaarsma et al, 2019). Beside I. triangulicepts and I. ventalloi other species may as well be associated with A. phagocytophilum.
Jaarsma et al, 2019 doi.org/10.1186/s13071-019-3583-8
Santos AS, Santos-Silva MM, Almeida VC, Bacellar F, Dumler JS. Detection of Anaplasma phagocytophilum DNA in Ixodes ticks (Acari: Ixodidae) from Madeira Island and Setúbal District, mainland Portugal. Emerging Infectious Diseases. 2004;10(9):1643-1648
Santos AS, de Bruin A, Veloso AR, Marques C, Pereira da Fonseca I, de Sousa I, et al. Detection of Anaplasma phagocytophilum, Candidatus Neoehrlichia sp., Coxiella burnetii, and Rickettsia spp. in questing ticks from a recreational park, Portugal. Tick and Tick-Borne Diseases. 2018;9(6):1555-1564. DOI: 10.1016/j.ttbdis.2018.07.010
8. Pag 18-19, “Only five studies have attempted to detect the DNA of other Anaplasma species in questing I. ricinus ticks in France (Bonnet et al. 2013; Michelet et al. 2014; Lejal et al. 2019a; Lejal et al. 2019b; Grech-Angelini et al. 2020a).”
Which Anaplasma spp were detected in questing I. ricinus? Not stated in the text. Please be clearer if the studies in questing ticks ever found any other Anaplasma sp..
9. Pag 28, 3.3.7 The genus Rickettsia, Fig 8 – why not presenting a map of R. monacensis distribution too?
10. SI 4 –Description of the dataset encoding fields
Please correct the number of this Supplementary information – is 4 not 3
First row – Study type – “Data were obtained from field sampling or in laboratory or it was a review: field/lab/review (…)”
Laboratory reared colonies were not included, right? What does it means to have data obtained from laboratory?
Please address all these points and submit both a revised version of your manuscript and rebuttal letter.
I look forward to receiving your revised manuscript.
Com os melhores cumprimentos,
Ana Sofia Pereira dos Santos, PhD
LNR de Doenças Infeciosas Transmitidas por Vetores
Departamento de Doenças Infeciosas