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Commentary

An Update of Evidence for Pathogen Transmission by Ticks of the Genus Hyalomma

by
Sarah I. Bonnet
1,*,
Stéphane Bertagnoli
2,
Alessandra Falchi
3,
Julie Figoni
4,
Johanna Fite
5,
Thierry Hoch
6,
Elsa Quillery
5,
Sara Moutailler
7,
Alice Raffetin
8,
Magalie René-Martellet
9,10,
Gwenaël Vourc’h
9,10 and
Laurence Vial
11
1
Ecology and Emergence of Arthropod-borne Pathogens unit, Institut Pasteur, Université Paris-cité, Centre National de Recherche Scientifique (CNRS) UMR 2000, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) USC 1510, 75015 Paris, France
2
Interactions Hôtes-Agents Pathogènes unit, Université de Toulouse, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Ecole Nationale Vétérinaire de Toulouse (ENVT), F-31076 Toulouse, France
3
Bioscope Corse Méditerranée unit UR7310, Faculté de Sciences, Campus Grimaldi, Université de Corse, 20250 Corte, France
4
Santé publique France, 94410 Saint-Maurice, France
5
Risk Assessment Department, French Agency for Food, Environmental and Occupational Health & Safety (ANSES), 94700 Maisons-Alfort, France
6
Biologie Épidémiologie et Analyse de Risque en santé animale unit, Oniris, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), 44300 Nantes, France
7
Biologie Moléculaire et immunologie Parasitaire unit, Laboratoire de Santé Animale, Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail (ANSES), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Ecole Nationale Vétérinaire d’Alfort (ENVA), 94700 Maisons-Alfort, France
8
Reference Centre for Tick-Borne Diseases, Paris and Northern Region, Department of Infectious Diseases, General Hospital of Villeneuve-Saint-Georges, 94190 Villeneuve-Saint-Georges, France
9
Epidémiologie des maladies animales et zoonotiques unit, Université de Lyon, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), VetAgro Sup, 69280 Marcy l’Etoile, France
10
Epidémiologie des maladies animales et zoonotiques unit, Université Clermont Auvergne, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), VetAgro Sup, 63122 Saint-Genès-Champanelle, France
11
Animal Santé Territoires Risques Ecosystèmes unit, Centre de coopération international en recherche agronomique pour le développement (CIRAD), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université Montpellier II, F-34398 Montpellier, France
 
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*
Author to whom correspondence should be addressed.
Pathogens 2023, 12(4), 513; https://doi.org/10.3390/pathogens12040513
Submission received: 24 February 2023 / Revised: 15 March 2023 / Accepted: 22 March 2023 / Published: 25 March 2023
(This article belongs to the Special Issue Current Status and Challenges Associated with Tick-Borne Pathogens and Diseases)
Review Reports Versions Notes

Abstract

:
Current and likely future changes in the geographic distribution of ticks belonging to the genus Hyalomma are of concern, as these ticks are believed to be vectors of many pathogens responsible for human and animal diseases. However, we have observed that for many pathogens there are no vector competence experiments, and that the level of evidence provided by the scientific literature is often not sufficient to validate the transmission of a specific pathogen by a specific Hyalomma species. We therefore carried out a bibliographical study to collate the validation evidence for the transmission of parasitic, viral, or bacterial pathogens by Hyalomma spp. ticks. Our results show that there are very few validated cases of pathogen transmission by Hyalomma tick species.

In addition to their direct impact as ectoparasites, ticks are of greater importance as vectors of pathogens to animals and are the second most important group of pathogen vectors affecting humans after mosquitoes, mainly due to their transmission of Borrelia burgdorferi sensu lato [1]. In addition, these arthropods are capable of transmitting the largest variety of pathogens including bacteria, parasites (protozoa, helminths), and viruses. However, like all biological vectors, ticks are not simple “syringes”, as is often believed. Each species, or even each tick population, has a vector competence corresponding to its intrinsic ability to acquire the pathogen by feeding on an infected host, allowing the multiplication/development of this agent and its retransmission to a new host during a new blood meal [2]. To this vector competence is added the set of factors that may influence transmission, thus defining the vector capacity—that is, the ability of a vector to transmit a pathogen at a given time and in a defined region, according to extrinsic conditions such as humidity, temperature, but also vector abundance, trophic preferences, etc. [3].
Ticks acquire pathogens during a blood meal taken on infected vertebrate hosts. Several routes of pathogen transmission to vertebrate hosts are then possible on the occasion of a new blood meal via a deposit on the skin of the host and penetration via the bite wound (via feces, by crushing or via coxal fluid excretion), or via the injection of saliva that accompanies the blood meal and represents the predominant route of pathogen transmission for ticks [4]. In addition, within the tick population, a pathogen may persist from one life stage to the next via transstadial transmission (essential for tick-borne transmission by hard ticks that take only one blood meal per life stage), from the female to its offspring via transovarial transmission, from male to female ticks during copulation via sexual transmission, or from an infected tick to a non-infected one via co-feeding when ticks feed adjacent to each other on the same host [2,5].
The unique detection of pathogenic DNA in a tick collected in the environment or on a vertebrate host does not prove vector competence, but only indicates the fact that the tick took a blood meal on an infected animal. Although such DNA detection in unfed hard ticks is more indicative than detection in engorged ones—as, considering that ixodid ticks feed only once per life stage, it suggests transstadial persistence—it should be noted that this does not imply the viability of the concerned pathogen. In fact, the persistence of DNA during the molting process is possible, as detection has been reported of some vertebrate DNA dating back to a blood meal taken by the previous life stage [6]. Furthermore, the DNA of pathogens that are not transmitted by the tick species concerned is often detected simply as a result of feeding on hosts that harbor such pathogens [7]. The detection of mRNA, a priori reflecting the presence of a living organism, presents an additional but still insufficient level of evidence of vectorial transmission. Additionally, the detection of a given pathogen in both ticks and samples from tick-infested vertebrate hosts collected in the same area, the co-occurrence with already known tick-borne pathogens, or a documented infection following a tick bite, can all represent indirect significant evidence of a given pathogen transmission. The demonstration of transstadial and/or transovarial persistence, which validates the existence of a development of the pathogen in ticks, is a strong indication in favor of biological vector transmission. However, conclusive evidence of vector competence for a given pathogen can only be provided by the demonstration of the ability of a tick species to acquire a pathogen on an infected host, to allow its development, and to transmit it to a new host. Unfortunately, very few vector competence experiments have been conducted due to the difficulties encountered in carrying out complete transmission cycles under experimental conditions. Indeed, it requires having pathogen-free tick colonies, vertebrate hosts suitable for both tick engorgement and pathogen replication (or to have effective artificial tick feeding methods combined with optimal cultivation methods of the pathogen), and can require high biosecurity levels depending on the pathogen concerned [8,9].
Ticks from the Hyalomma genus are considered to be expanding from some parts of their range, as reported for the invasion of H. marginatum into Europe since the late 20th century [10,11]. This is of concern, as these ticks are vectors of many pathogens responsible for human and animal diseases [12] and because there are few measures to control them, in particular during their off-host development [13]. Like other hard ticks, Hyalomma species take one blood meal per life stage before molting (larva and nymph) or, after fertilization, laying eggs (female). The majority of Hyalomma spp. ticks have a three-host cycle (each of the three life stages must find a new host on which to take a blood meal). However, some are diphasic, such as those of the marginatum group (larvae and nymphs taking their blood meals on the same host), and one species, Hyalomma scupense, is monophasic (all three life stages remain on the same host). Hyalomma ticks feed on domestic or wild vertebrate hosts, with some species such as H. marginatum or H. rufipes utilizing a large variety of hosts, which favors pathogen spillover. Humans, by entering the ecosystem of these hosts, can become accidental hosts of ticks, and thus, become exposed to pathogens [14]. The genus Hyalomma includes the most xerophilous species among all ticks and may be favored under future climate change [15].
Numerous pathogens—parasitic, viral, or bacterial—have been reported in the scientific literature as transmitted or potentially transmitted by ticks of the genus Hyalomma. The synthesis of these studies, with an attributed level of evidence of vectorial transmission, is reported in Table 1. The level of evidence ranges from a simple detection of pathogen DNA or RNA in ticks collected from vertebrate hosts to a formal demonstration of experimental transmission from an infected vertebrate host to a new naïve one, coupled with appropriate epidemiological data. To build this table, we considered the 27 Hyalomma species described by Guglielmone et al. in 2010 [16]. Species for which no evidence of a potential vector role has been reported to date have not been included, namely Hyalomma albiparmatum, Hyalomma arabica, Hyalomma brevipunctatum, Hyalomma glabrum, Hyalomma hystricis, Hyalomma nitidum, Hyalomma punt, Hyalomma rhipicephaloides, Hyalomma franchinii, and Hyalomma kumari. Our literature review includes the names of Hyalomma species that have been used for several past decades but have since been abandoned in favor of the currently used names, namely Hyalomma plumbeum (now H. marginatum) and Hyalomma detritum (now H. scupense). Note that the data identified for Hyalomma savignyi, now reclassified as H. lusitanicum, are not considered here, since H. savignyi is now considered to include several subspecies. Hyalomma savignyi data could therefore also apply to H. lusitanicum, as well as to H. anatolicum, H. impeltatum, H. impressum, H. marginatum, or H. truncatum. For bibliographic research, a narrative review was performed using the terms “Hyalomma” and “[pathogen sought]” (all microorganisms whose transmission by ticks has been reported in the scientific literature with de facto exclusion of symbionts) with the Boolean operator “AND” in the PubMed and Scopus databases without date restriction. The literature search was conducted in English. We retained peer-reviewed research articles and reviews (not including conference proceedings) and book sections. Screening was conducted first on titles, then on abstracts, and finally on the full text when available. After reading the entire articles, the ones that were eliminated corresponded to those that did not have available data or no original data. The number of references found in each of the two databases is shown in Table 1. All references concerning experimental validation and the epidemiological arguments for transmission are mentioned in the table, but the list concerning DNA/RNA detection is not exhaustive.
In conclusion, we observed that there are many missing pathogen vector competence experiments, and that the level of evidence provided by the scientific literature is often not sufficient to validate the existence of vectorial transmission. We conclude that the pathogen/tick associations for which transmission from an infected host to an initially healthy host via tick bite has been experimentally validated are the following:
  • Crimean–Congo Hemorrhagic Fever Virus (CCHFv) by H. dromedarii, H. impeltatum, H. marginatum, H. rufipes, and H. truncatum.
  • African Horse Sickness virus by H. dromedarii.
  • Venezuelan equine encephalitis virus by H. truncatum.
  • Theileria annulata by H. anatolicum, H. dromedarii, H. excavatum, H. lusitanicum, and H. scupense.
  • Theileria equi by H. anatolicum and H. excavatum.
  • Theileria lestoquardi by H. anatolicum.
  • Theileria ovis by H. anatolicum.
  • Babesia occultans by H. rufipes.
  • Coxiella burnetii by H. aegyptium.
  • Anaplasma marginale by H. excavatum.
  • Rickettsia aeschlimannii by H. marginatum and H. rufipes.

Author Contributions

Conceptualization, Methodology, Formal Analysis, Investigation, Review and Editing, S.I.B., S.B., A.F., J.F. (Julie Figoni), J.F. (Johanna Fite), T.H., E.Q., S.M., A.R., M.R.-M., G.V. and L.V.; Original Draft writing and preparation, S.I.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets generated during and/or analyzed during the current study can be find in the main text.

Acknowledgments

This narrative review was conducted by the ad hoc subgroup from the working expert group on the risks related to Hyalomma ticks at the French Agency for Food, Environmental and Occupational Health & Safety (ANSES) commissioned by the French authorities. The authors thank the other experts who were part of this group for stimulating discussions and for their feedback on the expert report: S. Baize and F. Stachurski. We also thank Richard Paul and Jeremy Gray for proofreading the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. Bibliographic review of evidence in favor of the transmission of pathogens by ticks of the Hyalomma genus.
Table 1. Bibliographic review of evidence in favor of the transmission of pathogens by ticks of the Hyalomma genus.
Tick SpeciesNumber of References in PubMed/ScopusPathogen Transmitted/Suspected to Be TransmittedDetection of DNA/RNA/Antigen/Pathogen in TicksEpidemiological Arguments of Possible Transmission *Experimental Validation of Transmission **References
H. aegyptium96/110CCHFvRNAyes0[17]
Coxiella burnetiiDNAno2, 4[18,19]
Borrelia turcica
Borrelia spp.		DNA and RNAno2[20,21,22,23,24,25]
Bartonella bovisDNAno0[26]
Ehrlichia canis
Ehrlichia spp.		DNAyes0[18,25,26,27]
Anaplasma phagocytophilumDNAyes0[18]
Rickettsia africaeDNAno0[28]
Rickettsia aeschlimanniiDNAyes0[26,29,30]
Rickettsia sibirica mongolitimonaeDNAno0[30,31]
Rickettsia slovacaDNAno0[30]
Meram virusRNAno0[32]
Tamdy virusRNAno0[32]
H. anatolicum381/546Babesia caballiDNAno0[33]
Theileria equiDNA, pathogen yes2, 4[33,34,35,36,37]
Babesia occultansDNAno0[38,39,40]
Babesia bovisDNAno0[38,39,40,41]
Theileria annulataDNA, pathogen yes2, 4[35,39,41,42,43,44,45,46,47,48,49,50,51]
Theileria lestoquardiDNAyes2, 4[35,44,49,52,53,54,55,56]
Theileria ovisDNAyes2, 4[33,35,38,40,57,58]
Babesia ovisDNAno0[55]
CCHFvRNA, antigen, viral particleuncertain 1[59,60,61,62,63,64,65]
AlphavirusRNAno0[66]
Zahedan RhabdovirusRNAno0[67]
Tick Borne Encephalitis virusnono5[68]
Kadam virusRNAno0[66]
Karshi virusno no0, 1[69]
Karyana virusRNA, virus isolationyes0[70]
Kundal virusRNA, virus isolationyes0[70]
Sindbis virusRNAno0[71]
Coxiella burnetiiDNAno0[72,73,74]
Bartonella spp.DNAno0[38]
Borrelia spp.DNAno0[38]
Anaplasma marginale, Anaplasma phagocytophilum, Anaplasma ovis, Anaplasma centrale, Ehrlichia spp., Rickettsia massiliae, Rickettsia spp.,DNAno0[38,41,75]
H. asiaticum145/192Theileria annulataDNAno0[76,77,78]
Babesia occultansDNAno0[79]
Babesia caballiDNAno0[80,81]
Theileria equiDNAno0[80]
CCHFvRNA, viral particles yes1[65,82,83,84,85]
Chim virusRNAno0[86]
Syr-Darya valley fever virusRNAno0[86]
Karshi virusRNAno0, 1[69,87,88]
Tamdy virusVirus isolationyes 0[89,90,91,92]
Coxiella burnetiiDNAno2[74,93,94,95]
Rickettsia sibericaDNAno0[96]
Borrelia burgdorferi s.l.RNAno0[97]
Rickettsia sibirica mongolitimonaeisolationyes 0[98]
H. dromedarii232/344Theileria equiDNA, pathogen in ticksno1, 2, 4[99,100,101,102]
Theileria camelensisPathogen in ticksyes1, 2, 4[103,104,105]
Theileria annulataDNAyes2, 4 [48,106,107,108,109,110,111,112]
Theileria ovisDNAno0[40]
Babesia caballiDNAno0[101]
Babesia occultansDNAno0[101]
CCHFvRNA, antigen, viral particlesyes1, 2, 4[64,113,114]
AlphavirusRNAno0[66]
Chick Ross virusRNAno0[66]
Dera Ghazi Khan virusRNAno0[115]
Dhori virusRNAno0[116]
Kadam virusRNAno0[66,117]
African horse sickness virusno no2, 4 [118]
Quaranfil virusRNA no0[119]
Sindbis virusRNA no0[66]
Coxiella burnetiiDNA no0[101,120,121,122,123,124]
Francisella persicaDNA no0 [125]
Rickettsia aeschlimanniiDNA no0[121,126,127]
Rickettsia africaeDNA no0[128]
Anaplasma spp./Ehrlichia spp.DNA no0[101]
Bartonella bovis et Bartonella rochalimaeDNA no0[129]
H. excavatum149/211Theileria equiDNA, pathogen no2, 4[34,130,131]
Babesia bigeminaDNAno0[41]
Babesia bovisDNAno0[132]
Babesia occultansDNAno3 [30,132]
Theileria annulataDNAuncertain2, 4[31,41,51,76,78,132,133,134]
Theileria capreoliDNAno0[31]
Theileria ovisDNAno0[40,135]
Borrelia spp.DNAno0[136]
Coxiella burnetiiDNAno0[121,124,137,138,139]
Rickettsia africaeDNAno0[140]
Rickettsia aeschlimanniiDNAno0[140]
Anaplasma marginaleDNAyes4[141]
Anaplasma centraleDNAyes0[141]
Ehrlichia ruminantiumDNAno0[41]
Rickettsia sibirica mongolotimonaeDNAno0[142]
CCHFvRNA, antigenuncertain0[59,61,143]
H. hussaini4/7Coxiella burnetiiDNA no0[144]
Rickettsia massiliae, Rickettsia spp.DNA no0[38]
H. impeltatum62/88Theileria annulataDNAno2, 4 [41,108,112,145]
Theileria lestoquardi (Theileria hirci)no uncertain0[146]
Theileria ovisDNAno0[35]
Babesia occultansDNAno0[101]
Babesia bigeminaDNAno0[41]
Babesia bovisDNAno0[41]
Babesia pecorumDNAno0[35]
CCHFvRNA, antigen virus isolationyes1, 2, 4
cofeeding		[61,113,147,148,149]
Coxiella burnetiiDNAno0[123,124]
AlphavirusRNAno0[66]
Dhori virusRNAno0[66]
Sindbis virusRNAno0[66]
Rickettsia africaeDNAno0[140]
Rickettsia aeschlimanniiDNAno0[121,150,151]
H. impressum10/17CCHFvantigenuncertain 0[64]
Theileria annulataDNAno0[108]
Anaplasma/Ehrlichia spp.DNAno 0[101]
Rickettsia africaeDNAno0[152]
H. isaaci5/5Kyasanur forest virusRNA - 2, 4[153]
H. lusitanicum68/83Theileria equipathogen no1, 2, 4[99,100]
Babesia pecorum Noyes0[154]
Theileria annulata Noyes4 [107,155,156]
CCHFvRNA, antigen yes0[157,158]
Anaplasma phagocytophilumDNA no0[159]
Borrelia burgdorferiDNAno0[160]
Borrelia lusitaniaeDNAno0[161]
Coxiella burnetiiDNA no0[162,163,164,165]
H. marginatum451/620Theileria equiDNAyes0[130,131,166,167]
Theileria annulataDNAyes2 [41,51,111]
Theileria sergenti/orientalis/buffeliDNAno0[159,166,168]
Theileria ovisDNAno0[40,49,169]
Theileria lestoquardiDNAno0[170]
Babesia ovisDNA, pathogen in ticksno1[55,171]
Babesia caballiDNAyes 0[130,131,169,172]
Babesia bigeminaDNA no0[41,167]
Babesia bovisDNA no0[41,167]
Babesia occultansDNAyes2, 3 [30,31,130,134,136,166,173,174,175,176]
Babesia microtiDNAno0[174]
Babesia sp. Tavsan1DNAno0[31]
CCHFvRNA, antigenyes1, 2, 3, 4[64,65,143,158,177,178,179,180,181,182,183,184,185,186,187,188]
FlavivirusRNA no0[189]
PhlebovirusRNA no0[190]
Bahig virusRNA no0[191]
Batken virus (close to Dhori virus)RNA no0[192]
Bhanja virusRNA no0[193]
Dhori virusRNA no0[194,195]
Tick Borne Encephalitis virusRNA no0[196]
Jingmen virusRNA, virus isolationyes0
[197]
Matruh virusRNAno 0[198]
Tamdy virusRNA no0[89]
Wanowrie virusRNAyes0[153,199]
West Nile virusRNAno2, 3[189,200,201,202]
Rickettsia aeschlimanniiDNAyes3[31,136,151,203,204,205,206,207,208]
Rickettsia sibirica mongolitimonaeDNAno0[31]
Anaplasma marginaleDNAno0[31,209]
Rickettsia africaeDNAno 0[210]
Anaplasma phagocytophilumDNAno0[204,211]
Anaplasma platysDNAno 0[211]
Coxiella burnetiiDNAno0[139,142,211,212,213]
Francisella tularensisDNAno0[214]
Ehrlichia monacensis (minasensis)DNAno0[204]
Ehrlichia ruminantiumDNAno 0[41]
Bartonella spp.DNAno0[205,213]
Borrelia burgdoferi s.l.DNAno0[212,213]
Borrelia spp.DNAno0[136,152]
H. rufipes189/238Babesia occultansDNA, pathogen no2, 3, 4 [175,176]
Theileria ovisDNAno0[40]
Theileria annulataDNAno2, 4 [108,109,215]
CCHFvRNA, antigen, viral particlesyes1, 2, 3, 4[64,216,217,218,219,220,221,222,223,224,225]
FlavivirusRNA no0[189]
Dugbe virusRNA no2 [226]
Alkhurma hemorrhagic fever virusRNA no0[227]
St Croix River like virusRNA no0[228]
Rickettsia aeschlimanniiDNAno 0[35]
Rickettsia conoriiDNA no0[229]
Anaplasma marginale, centrale, platysDNAno 0[230]
Coxiella burnetiiDNA no0[74,212,231,232]
Borrelia burgdorferiRNA and DNAno0[212,233]
H. schulzei17/27Dhori virusRNAno 0[66]
H. scupense34/47

H. detritum: 61/90		Theileria equiNono4 [234,235]
Theileria annulata Noyes2, 4[107,236,237,238]
Babesia ovisDNAno0[40]
Theileria ovisDNAno0[40]
Rickettsia aeschlimanniiDNAno 0[14,205]
Rickettsia slovacaDNA no0[205]
Anaplasma phagocytophilumDNA no0[205]
Coxiella burnetiiDNA no2, 3[139,239]
CCHFvRNAuncertain0[83]
H. somalicum2/2R. conoriiDNAno 0[14]
H. truncatum142/193Theileria equiDNAno0[101]
Babesia caballiNono3, 4[240,241]
Theileria annulataDNAno0[108]
CCHFvRNA, viral particlesyes1, 2, 3, 4, 5
Cofeeding		[113,148,149,217,218,220,222,242,243,244,245,246]
Bunyamwera virusRNAno0[247]
Dugbe virusRNAno0[248]
Venezuelan Equine Encephalitis Virus no2, 4[249]
Kupe virusRNAno0[248]
Semliki forest virusRNAno0[247]
Coxiella burnetiiDNAno0[152,232,250]
Borrelia spp.DNAno0[152,232]
H. turanicum24/36CCHFvRNAno0[187]
Rickettsia sibirica mongolitimonaeDNAno0[140]
CCHFv: Crimean–Congo Hemorrhagic Fever Virus; * epidemiological arguments of possible transmission: for example co-occurrence of a given pathogen in a tick species and in infested vertebrate hosts of the same area, host co-infection with pathogens known to be transmitted by ticks, or the onset of a disease as a result of tick bites: YES, NO, uncertain. ** Experimental validation. 0: none; 1: pathogen reproduction/replication success in ticks; 2: transstadial transmission; 3: transovarial transmission; 4: transmission to a vertebrate host via a tick bite; 5: sexual transmission between male and female ticks.
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MDPI and ACS Style

Bonnet, S.I.; Bertagnoli, S.; Falchi, A.; Figoni, J.; Fite, J.; Hoch, T.; Quillery, E.; Moutailler, S.; Raffetin, A.; René-Martellet, M.; et al. An Update of Evidence for Pathogen Transmission by Ticks of the Genus Hyalomma. Pathogens 2023, 12, 513. https://doi.org/10.3390/pathogens12040513

AMA Style

Bonnet SI, Bertagnoli S, Falchi A, Figoni J, Fite J, Hoch T, Quillery E, Moutailler S, Raffetin A, René-Martellet M, et al. An Update of Evidence for Pathogen Transmission by Ticks of the Genus Hyalomma. Pathogens. 2023; 12(4):513. https://doi.org/10.3390/pathogens12040513

Chicago/Turabian Style

Bonnet, Sarah I., Stéphane Bertagnoli, Alessandra Falchi, Julie Figoni, Johanna Fite, Thierry Hoch, Elsa Quillery, Sara Moutailler, Alice Raffetin, Magalie René-Martellet, and et al. 2023. "An Update of Evidence for Pathogen Transmission by Ticks of the Genus Hyalomma" Pathogens 12, no. 4: 513. https://doi.org/10.3390/pathogens12040513

APA Style

Bonnet, S. I., Bertagnoli, S., Falchi, A., Figoni, J., Fite, J., Hoch, T., Quillery, E., Moutailler, S., Raffetin, A., René-Martellet, M., Vourc’h, G., & Vial, L. (2023). An Update of Evidence for Pathogen Transmission by Ticks of the Genus Hyalomma. Pathogens, 12(4), 513. https://doi.org/10.3390/pathogens12040513

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