BACKGROUND: Ixodes inopinatus was described from Spain on the basis of morphology and partial sequencing of 16S ribosomal DNA. However, several studies suggested that morphological differences between I. inopinatus and Ixodes ricinus are minimal and that 16S rDNA lacks the power to distinguish the two species. Furthermore, nuclear and mitochondrial markers indicated evidence of hybridization between I. inopinatus and I. ricinus. In this study, we tested our hypothesis on tick dispersal from North Africa to Southern Europe and determined the prevalence of selected tick-borne pathogens (TBPs) in I. inopinatus, I. ricinus, and their hybrids. METHODS: Ticks were collected in Italy and Algeria by flagging, identified by sequencing of partial TROSPA and COI genes, and screened for Borrelia burgdorferi s.l., B. miyamotoi, Rickettsia spp., and Anaplasma phagocytophilum by polymerase chain reaction and sequencing of specific markers. RESULTS: Out of the 380 ticks, in Italy, 92 were I. ricinus, 3 were I. inopinatus, and 136 were hybrids of the two species. All 149 ticks from Algeria were I. inopinatus. Overall, 60% of ticks were positive for at least one TBP. Borrelia burgdorferi s.l. was detected in 19.5% of ticks, and it was significantly more prevalent in Ixodes ticks from Algeria than in ticks from Italy. Prevalence of Rickettsia spotted fever group (SFG) was 51.1%, with significantly greater prevalence in ticks from Algeria than in ticks from Italy. Borrelia miyamotoi and A. phagocytophilum were detected in low prevalence (0.9% and 5.2%, respectively) and only in ticks from Italy. CONCLUSIONS: This study indicates that I. inopinatus is a dominant species in Algeria, while I. ricinus and hybrids were common in Italy. The higher prevalence of B. burgdorferi s.l. and Rickettsia SFG in I. inopinatus compared with that in I. ricinus might be due to geographical and ecological differences between these two tick species. The role of I. inopinatus in the epidemiology of TBPs needs further investigation in the Mediterranean Basin.

Biology Centre Institute of Parasitology Czech Academy of Sciences České Budějovice Czech Republic

CEITEC University of Veterinary Sciences Brno Czech Republic

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Department of Microbiology Nutrition and Dietetics Czech University of Life Sciences Prague Czech Republic

Department of Parasitology and Parasitic Diseases University of Agricultural Sciences and Veterinary Medicine of Cluj Napoca Cluj Napoca Romania

Department of Parasitology Faculty of Science Charles University Prague Czech Republic

Department of Veterinary Clinical Sciences City University of Hong Kong Hong Kong Hong Kong

Department of Veterinary Medicine and Animal Productions University of Naples Federico 2 Naples Italy

Department of Veterinary Medicine University of Bari Valenzano Italy

Department of Veterinary Sciences Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Czech Republic

Department of Veterinary Sciences University of Messina Messina Italy

Department of Zoology Palacky University Olomouc Olomouc Czech Republic

Faculty of Medicine in Pilsen Biomedical Center Charles University Pilsen Czech Republic

Instituto Zooprofilattico Sperimentale delle Venezie Legnaro Italy

Zobrazit více v PubMed

de Meeüs T, Béati L, Delaye C, Aeschlimann A, Renaud F. Sex-biased genetic structure in the vector of Lyme disease, Ixodes ricinus. Evolution. 2002;56:1802–7. PubMed

Noureddine R, Chauvin A, Plantard O. Lack of genetic structure among Eurasian populations of the tick Ixodes ricinus contrasts with marked divergence from north-African populations. Int J Parasitol. 2011;41:183–92. doi: 10.1016/j.ijpara.2010.08.010. PubMed DOI

Estrada-Peña A, Nava S, Petney T. Description of all the stages of Ixodes inopinatus n. sp. (Acari: Ixodidae) Ticks Tick Borne Dis. 2014;5:734–43. doi: 10.1016/j.ttbdis.2014.05.003. PubMed DOI

Chitimia-Dobler L, Rieß R, Kahl O, Wölfel S, Dobler G, Nava S, et al. Ixodes inopinatus—occurring also outside the Mediterranean region. Ticks Tick Borne Dis. 2018;9:196–200. doi: 10.1016/j.ttbdis.2017.09.004. PubMed DOI

Hauck D, Springer A, Pachnicke S, Schunack B, Fingerle V, Strube C. Ixodes inopinatus in northern Germany: occurrence and potential vector role for Borrelia spp., Rickettsia spp., and Anaplasma phagocytophilum in comparison with Ixodes ricinus. Parasitol Res. 2019;118:3205–16. doi: 10.1007/s00436-019-06506-4. PubMed DOI

Chitimia-Dobler L, Lemhöfer G, Król N, Bestehorn M, Dobler G, Pfeffer M. Repeated isolation of tick-borne encephalitis virus from adult Dermacentor reticulatus ticks in an endemic area in Germany. Parasit Vectors. 2019;12:90. doi: 10.1186/s13071-019-3346-6. PubMed DOI PMC

Toma L, Mancuso E, d’Alessio SG, Menegon M, Spina F, Pascucci I, et al. Tick species from Africa by migratory birds: a 3-year study in Italy. Exp Appl Acarol. 2021 doi: 10.1007/s10493-020-00573-4. PubMed DOI

Younsi H, Fares W, Cherni S, Dachraoui K, Barhoumi W, Najjar C, et al. Ixodes inopinatus and Ixodes ricinus (Acari: Ixodidae) are sympatric ticks in North Africa. J Med Entomol. 2020;57:952–6. doi: 10.1093/jme/tjz216. PubMed DOI

Hornok S, Daccord J, Takács N, Kontschán J, Tuska-Szalay B, Sándor AD, et al. Investigation on haplotypes of ixodid ticks and retrospective finding of Borrelia miyamotoi in bank vole (Myodes glareolus) in Switzerland. Ticks Tick Borne Dis. 2022;13:101865. doi: 10.1016/j.ttbdis.2021.101865. PubMed DOI

Knoll S, Springer A, Hauck D, Schunack B, Pachnicke S, Fingerle V, et al. Distribution of Borrelia burgdorferi s.l. and Borrelia miyamotoi in Ixodes tick populations in Northern Germany, co-infections with Rickettsiales and assessment of potential influencing factors. Med Vet Entomol. 2021;35:595–606. doi: 10.1111/mve.12537. PubMed DOI

Glass A, Springer A, Strube C. A 15-year monitoring of Rickettsiales (Anaplasma phagocytophilum and Rickettsia spp.) in questing ticks in the city of Hanover, Germany. Ticks Tick Borne Dis. 2022;13:101975. doi: 10.1016/j.ttbdis.2022.101975. PubMed DOI

Plantard O, Poli P, Bouattour A, Sahir M, Dib L, Rispe C. Ixodes inopinatus cannot be distinguished from I. ricinus by the sole use of the 16S ribosomal gene. 2022. p. 73.

Rollins RE, Margos G, Brachmann A, Krebs S, Mouchet A, Dingemanse NJ, et al. German Ixodes inopinatus samples may not actually represent this tick species. Int J Parasitol. 2023;53:751–761. doi: 10.1016/j.ijpara.2023.06.007. PubMed DOI

Hrazdilova K, Danek O, Hrbatova A, Cervena B, Noskova E, Adamik P, et al. Genetic analysis challenges the presence of Ixodes inopinatus in Central Europe: development of a multiplex PCR to distinguish I. inopinatus from I. ricinus. Parasit Vectors. 2023 doi: 10.1186/s13071-023-05971-2. PubMed DOI PMC

Velez R, De Meeûs T, Beati L, Younsi H, Zhioua E, Antunes S, et al. Development and testing of microsatellite loci for the study of population genetics of Ixodes ricinus Linnaeus, 1758 and Ixodes inopinatus Estrada-Peña, Nava and Petney, 2014 (Acari: Ixodidae) in the western Mediterranean region. Acarologia. 2023;63:356–372. doi: 10.24349/bvem-4h49. DOI

del Cerro A, Oleaga A, Somoano A, Barandika JF, García-Pérez AL, Espí A. Molecular identification of tick-borne pathogens ( Rickettsia spp., Anaplasma phagocytophilum , Borrelia burgdorferi sensu lato, Coxiella burnetii and piroplasms) in questing and feeding hard ticks from North-Western Spain. Ticks Tick Borne Dis. 2022 doi: 10.1016/j.ttbdis.2022.101961. PubMed DOI

Norte AC, Boyer PH, Castillo-Ramirez S, Chvostáč M, Brahami MO, Rollins RE, et al. The population structure of Borrelia lusitaniae is reflected by a population division of its Ixodes vector. Microorganisms. 2021 doi: 10.3390/microorganisms9050933. PubMed DOI PMC

Younsi H, Postic D, Baranton G, Bouattour A. High prevalence of Borrelia lusitaniae in Ixodes ricinus ticks in Tunisia. Eur J Epidemiol. 2001;17:53–6.http://www.ncbi.nlm.nih.gov/pubmed/11523576. PubMed

Falchi A, Dantas-Torres F, Lorusso V, Malia E, Lia RP, Otranto D. Autochthonous and migratory birds as a dispersion source for Ixodes ricinus in southern Italy. Exp Appl Acarol. 2012;58:167–174. doi: 10.1007/s10493-012-9571-8. PubMed DOI

Dantas-Torres F, Otranto D. Species diversity and abundance of ticks in three habitats in southern Italy. Ticks Tick Borne Dis. 2013;4:251–255. doi: 10.1016/j.ttbdis.2012.11.004. PubMed DOI

Dantas-Torres F, Otranto D. Seasonal dynamics of Ixodes ricinus on ground level and higher vegetation in a preserved wooded area in southern Europe. Vet Parasitol. 2013;192:253–258. doi: 10.1016/j.vetpar.2012.09.034. PubMed DOI

Dantas-Torres F, Lia RP, Capelli G, Otranto D. Efficiency of flagging and dragging for tick collection. Exp Appl Acarol. 2013;61:119–127. doi: 10.1007/s10493-013-9671-0. PubMed DOI

Estrada-Peña A, Mihalca AD, Petney TN, editors. Ticks of Europe and North Africa. Cham: Springer International Publishing; 2017.

Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, et al. Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol. 2004;42:90–98. doi: 10.1128/JCM.42.1.90-98.2004. PubMed DOI PMC

Regnery RL, Spruill CL, Plikaytis BD, Branch RZ. Genotypic identification of Rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol. 1991 doi: 10.1128/jb.173.5.1576-1589.1991. PubMed DOI PMC

Roux V, Fournier P-E, Raoult D. Differentiation of spotted fever group rickettsiae by sequencing and analysis of restriction fragment length polymorphism of PCR-amplified DNA of the gene encoding the protein ompA. J Clin Microbiol. 1996 doi: 10.1128/jcm.34.9.2058-2065.1996. PubMed DOI PMC

Lesiczka PM, Hrazdilova K, Hönig V, Modrý D, Zurek L. Distant genetic variants of Anaplasma phagocytophilum from Ixodes ricinus attached to people. Parasit Vectors. 2023 doi: 10.1186/s13071-023-05654-y. PubMed DOI PMC

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC

Jahfari S, Coipan EC, Fonville M, Van Leeuwen AD, Hengeveld P, Heylen D, et al. Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasit Vectors. 2014;7:1–11. doi: 10.1186/1756-3305-7-365. PubMed DOI PMC

Jaarsma RI, Sprong H, Takumi K, Kazimirova M, Silaghi C, Mysterud A, et al. Anaplasma phagocytophilum evolves in geographical and biotic niches of vertebrates and ticks. Parasit Vectors. 2019;12:1–17. doi: 10.1186/s13071-019-3583-8. PubMed DOI PMC

Rar V, Tkachev S, Tikunova N. Genetic diversity of Anaplasma bacteria: twenty years later. Infect Genet Evol. 2021 doi: 10.1016/j.meegid.2021.104833. PubMed DOI

Kovalev SY, Golovljova IV, Mukhacheva TA. Natural hybridization between Ixodes ricinus and Ixodes persulcatus ticks evidenced by molecular genetics methods. Ticks Tick Borne Dis. 2016;7:113–118. doi: 10.1016/j.ttbdis.2015.09.005. PubMed DOI

Kovalev SY, Mikhaylishcheva MS, Mukhacheva TA. Natural hybridization of the ticks Ixodes persulcatus and Ixodes pavlovskyi in their sympatric populations in Western Siberia. Infect Genet Evol. 2015;32:388–395. doi: 10.1016/j.meegid.2015.04.003. PubMed DOI

Hekimoğlu O. Phylogenetic placement of Turkish populations of Ixodes ricinus and Ixodes inopinatus. Exp Appl Acarol. 2022;88:179–189. doi: 10.1007/s10493-022-00750-7. PubMed DOI

Krčmar S, Klobučar A, Vucelja M, Boljfetić M, Kučinić M, Madić J, et al. DNA barcoding of hard ticks (Ixodidae), notes on distribution of vector species and new faunal record for Croatia. Ticks Tick Borne Dis. 2022 doi: 10.1016/j.ttbdis.2022.101920. PubMed DOI

Wodecka B, Kolomiiets V. Genetic diversity of Borreliaceae species detected in natural populations of Ixodes ricinus ticks in northern Poland. Life. 2023 doi: 10.3390/life13040972. PubMed DOI PMC

Sorokina YV, Korenberg EI, Belyi YF. The first data on the TROSPA Gene structure in Ixodes persulcatus and Ixodes ricinus ticks from Russia. Russ J Genet. 2018;54:457–463. doi: 10.1134/S1022795418040142. DOI

Araya-Anchetta A, Scoles GA, Giles J, Busch JD, Wagner DM. Hybridization in natural sympatric populations of Dermacentor ticks in northwestern North America. Ecol Evol. 2013;3:714–724. doi: 10.1002/ece3.496. PubMed DOI PMC

Steinbrink A, Brugger K, Margos G, Kraiczy P, Klimpel S. The evolving story of Borrelia burgdorferi sensu lato transmission in Europe. Parasitol Res. 2022 doi: 10.1007/s00436-022-07445-3. PubMed DOI PMC

Majerová K, Hönig V, Houda M, Papežík P, Fonville M, Sprong H, et al. Hedgehogs, squirrels, and blackbirds as sentinel hosts for active surveillance of Borrelia miyamotoi and Borrelia burgdorferi complex in urban and rural environments. Microorganisms. 2020;8:1–16. doi: 10.3390/microorganisms8121908. PubMed DOI PMC

Sarih M, Jouda F, Gern L, Postic D. First isolation of Borrelia burgdorferi sensu lato from Ixodes ricinus ticks in Morocco. Vector-Borne Zoo Dis. 2003;3:133–139. doi: 10.1089/153036603768395834. PubMed DOI

Trevisan G, Ruscio M, Cinco M, Nan K, Forgione P, Di Meo N, et al. The history of Lyme disease in Italy and its spread in the Italian territory. Front Pharmacol. 2023 doi: 10.3389/fphar.2023.1128142. PubMed DOI PMC

Da Rold G, Ravagnan S, Soppelsa F, Porcellato E, Soppelsa M, Obber F, et al. Ticks are more suitable than red foxes for monitoring zoonotic tick-borne pathogens in northeastern Italy. Parasit Vectors. 2018;11:137. doi: 10.1186/s13071-018-2726-7. PubMed DOI PMC

Wodecka B, Skotarczak B. First isolation of Borrelia lusitaniae DNA from Ixodes ricinus ticks in Poland. Scand J Infect Dis. 2005;37:27–34. doi: 10.1080/00365540410026059. PubMed DOI

Tarageľová VR, Mahríková L, Selyemová D, Václav R, Derdáková M. Natural foci of Borrelia lusitaniae in a mountain region of Central Europe. Ticks Tick Borne Dis. 2016;7:350–356. doi: 10.1016/j.ttbdis.2015.12.006. PubMed DOI

Okeyo M, Hepner S, Rollins RE, Hartberger C, Straubinger RK, Marosevic D, et al. Longitudinal study of prevalence and spatio-temporal distribution of Borrelia burgdorferi sensu lato in ticks from three defined habitats in Latvia, 1999–2010. Environ Microbiol. 2020;22:5033–5047. doi: 10.1111/1462-2920.15100. PubMed DOI

Musilová L, Kybicová K, Fialová A, Richtrová E, Kulma M. First isolation of Borrelia lusitaniae DNA from green lizards (Lacerta viridis) and Ixodes ricinus ticks in the Czech Republic. Ticks Tick Borne Dis. 2022;13:101887. doi: 10.1016/j.ttbdis.2021.101887. PubMed DOI

Mendoza-Roldan JA, Colella V, Lia RP, Nguyen VL, Barros-Battesti DM, Iatta R, et al. Borrelia burgdorferi (sensu lato) in ectoparasites and reptiles in southern Italy. Parasit Vectors. 2019;12:35. doi: 10.1186/s13071-019-3286-1. PubMed DOI PMC

Cinco M, Padovan D, Murgia R, Poldini L, Frusteri L, Pol I, et al. Rate of infection of Ixodes ricinus ticks with Borrelia burgdorferi sensu stricto, Borrelia garinii, Borrelia afzelii and group VS116 in an endemic focus of Lyme disease in Italy. Eur J Clin Microbiol Infect Dis. 1998;17:90–94. PubMed

Otranto D, Dantas-Torres F, Giannelli A, Latrofa M, Cascio A, Cazzin S, et al. Ticks infesting humans in Italy and associated pathogens. Parasit Vectors. 2014;7:328. doi: 10.1186/1756-3305-7-328. PubMed DOI PMC

Pintore MD, Ceballos L, Iulini B, Tomassone L, Pautasso A, Corbellini D, et al. Detection of invasive Borrelia burgdorferi strains in north-eastern Piedmont, Italy. Zoonoses Public Health. 2015;62:365–374. doi: 10.1111/zph.12156. PubMed DOI

Bertola M, Montarsi F, Obber F, Da Rold G, Carlin S, Toniolo F, et al. Occurrence and identification of Ixodes ricinus borne pathogens in Northeastern Italy. Pathogens. 2021;10:1181. doi: 10.3390/pathogens10091181. PubMed DOI PMC

Cleveland DW, Anderson CC, Brissette CA. Borrelia miyamotoi: a comprehensive review. Pathogens. 2023;12:267. doi: 10.3390/pathogens12020267. PubMed DOI PMC

Burri C, Schumann O, Schumann C, Gern L. Are Apodemus spp. mice and Myodes glareolus reservoirs for Borrelia miyamotoi, Candidatus Neoehrlichia mikurensis, Rickettsia helvetica, R. monacensis and Anaplasma phagocytophilum? Ticks Tick Borne Dis. 2014;5:245–51. doi: 10.1016/j.ttbdis.2013.11.007. PubMed DOI

Gryczyńska A, Sokół M, Gortat T, Kowalec M. Borrelia miyamotoi infection in Apodemus spp mice populating an urban habitat (Warsaw, Poland) Int J Parasitol Parasites Wildl. 2021;14:138–40. doi: 10.1016/j.ijppaw.2021.01.009. PubMed DOI PMC

Ravagnan S, Tomassone L, Montarsi F, Krawczyk AI, Mastrorilli E, Sprong H, et al. First detection of Borrelia miyamotoi in Ixodes ricinus ticks from northern Italy. Parasit Vectors. 2018;11:130. doi: 10.1186/s13071-018-2713-z. PubMed DOI PMC

Garcia-Vozmediano A, Tomassone L, Fonville M, Bertolotti L, Heylen D, Fabri ND, et al. The genetic diversity of rickettsiella symbionts in Ixodes ricinus throughout Europe. Microb Ecol. 2022;84:613–626. doi: 10.1007/s00248-021-01869-7. PubMed DOI PMC

Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, et al. Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev. 2013;26:657–702. doi: 10.1128/CMR.00032-13. PubMed DOI PMC

de Sousa R, dos Santos ML, Cruz C, Almeida V, Garrote AR, Ramirez F, et al. Rare case of rickettsiosis caused by Rickettsia monacensis, Portugal, 2021. Emerg Infect Dis. 2022;28:1068–1071. doi: 10.3201/eid2805.211836. PubMed DOI PMC

Nilsson K. Septicaemia with Rickettsia helvetica in a patient with acute febrile illness, rash and myasthenia. J Infect. 2009;58:79–82. doi: 10.1016/j.jinf.2008.06.005. PubMed DOI

Dib L, Bitam I, Bensouilah M, Parola P, Raoult D. First description of Rickettsia monacensis in Ixodes ricinus in Algeria. Clin Microbiol Infect. 2009;15:261–262. doi: 10.1111/j.1469-0691.2008.02277.x. PubMed DOI

Kernif T, Messaoudene D, Ouahioune S, Parola P, Raoult D, Bitam I. Spotted fever group rickettsiae identified in Dermacentor marginatus and Ixodes ricinus ticks in Algeria. Ticks Tick Borne Dis. 2012;3:380–381. doi: 10.1016/j.ttbdis.2012.10.012. PubMed DOI

Sfar N, M’Ghirbi Y, Letaïef A, Parola P, Bouattour A, Raoult D. First report of Rickettsia monacensis and Rickettsia helvetica from Tunisia. Ann Trop Med Parasitol. 2008;102:561–564. doi: 10.1179/136485908X311795. PubMed DOI

Mendoza-Roldan JA, Ravindran Santhakumari Manoj R, Latrofa MS, Iatta R, Annoscia G, Lovreglio P, et al. Role of reptiles and associated arthropods in the epidemiology of rickettsioses: a one health paradigm. PLoS Negl Trop Dis. 2021;15:e0009090. doi: 10.1371/journal.pntd.0009090. PubMed DOI PMC

Jensen BB, Andersen NS, Wölfel S, Chen M, Paarup HM, Olesen CR, et al. Rickettsiosis in Denmark: a nation-wide survey. Ticks Tick Borne Dis. 2023;14:102236. doi: 10.1016/j.ttbdis.2023.102236. PubMed DOI

Arz C, Król N, Imholt C, Jeske K, Rentería-Solís Z, Ulrich RG, et al. Spotted fever group Rickettsiae in ticks and small mammals from grassland and forest habitats in Central Germany. Pathogens. 2023;12:933. doi: 10.3390/pathogens12070933. PubMed DOI PMC

Václavík T, Balážová A, Baláž V, Tkadlec E, Schichor M, Zechmeisterová K, et al. Landscape epidemiology of neglected tick-borne pathogens in central Europe. Transbound Emerg Dis. 2021;68:1685–1696. doi: 10.1111/tbed.13845. PubMed DOI

Ivan T, Matei IA, Ștefania NC, Kalmár Z, Borșan S-D, Panait L-C, et al. Spotted fever group Rickettsia spp. diversity in ticks and the first report of Rickettsia hoogstraalii in Romania. Vet Sci. 2022;9:343. doi: 10.3390/vetsci9070343. PubMed DOI PMC

May K, Strube C. Prevalence of Rickettsiales (Anaplasma phagocytophilum and Rickettsia spp.) in hard ticks (Ixodes ricinus) in the city of Hamburg, Germany. Parasitol Res. 2014;113:2169–75. doi: 10.1007/s00436-014-3869-x. PubMed DOI

Blazejak K, Janecek E, Strube C. A 10-year surveillance of Rickettsiales (Rickettsia spp. and Anaplasma phagocytophilum) in the city of Hanover, Germany, reveals Rickettsia spp. as emerging pathogens in ticks. Parasit Vectors. 2017;10:588. doi: 10.1186/s13071-017-2537-2. PubMed DOI PMC

De Sousa R, de Carvalho IL, Santos AS, Bernardes C, Milhano N, Jesus J, et al. Role of the lizard Teira dugesii as a potential host for Ixodes ricinus tick-borne pathogens. Appl Environ Microbiol. 2012;78:3767–3769. doi: 10.1128/AEM.07945-11. PubMed DOI PMC

Stuen S, Granquist EG, Silaghi C. Anaplasma phagocytophilum—a widespread multi-host pathogen with highly adaptive strategies. Front Cell Infect Microbiol. 2013 doi: 10.3389/fcimb.2013.00031. PubMed DOI PMC

Matei IA, Estrada-Peña A, Cutler SJ, Vayssier-Taussat M, Varela-Castro L, Potkonjak A, et al. A review on the eco-epidemiology and clinical management of human granulocytic anaplasmosis and its agent in Europe. Parasit Vectors. 2019;12:599. doi: 10.1186/s13071-019-3852-6. PubMed DOI PMC

Mantelli B, Pecchioli E, Hauffe HC, Rosà R, Rizzoli A. Prevalence of Borrelia burgdorferi s.l. and Anaplasma phagocytophilum in the wood tick Ixodes ricinus in the province of Trento, Italy. Eur J Clin Microbiol Infect Dis. 2006;25:737–9. doi: 10.1007/s10096-006-0208-x. PubMed DOI

Aureli S, Foley J, Galuppi R, Rejmanek D, Tampieri MP. Anaplasma phagocytophilum in ticks from parks in the Emilia-Romagna region of northern Italy. Vet Ital. 2012;48:413–23. http://www.ncbi.nlm.nih.gov/pubmed/23277122. PubMed

Baráková I, Derdáková M, Carpi G, Rosso F, Collini M, Tagliapietra V, et al. Genetic and ecologic variability among Anaplasma phagocytophilum strains, Northern Italy. Emerg Infect Dis. 2014;20:1082–1084. doi: 10.3201/eid2006.131023. PubMed DOI PMC

Zanet S, Battisti E, Pepe P, Ciuca L, Colombo L, Trisciuoglio A, et al. Tick-borne pathogens in Ixodidae ticks collected from privately-owned dogs in Italy: a country-wide molecular survey. BMC Vet Res. 2020;16:46. doi: 10.1186/s12917-020-2263-4. PubMed DOI PMC

Sgroi G, Iatta R, Veneziano V, Bezerra-Santos MA, Lesiczka P, Hrazdilová K, et al. Molecular survey on tick-borne pathogens and Leishmania infantum in red foxes (Vulpes vulpes) from southern Italy. Ticks Tick Borne Dis. 2021 doi: 10.1016/j.ttbdis.2021.101669. PubMed DOI

Dahmani M, Davoust B, Benterki MS, Fenollar F, Raoult D, Mediannikov O. Development of a new PCR-based assay to detect Anaplasmataceae and the first report of Anaplasma phagocytophilum and Anaplasma platys in cattle from Algeria. Comp Immunol Microbiol Infect Dis. 2015;39:39–45. doi: 10.1016/j.cimid.2015.02.002. PubMed DOI

Sarih M, M’Ghirbi Y, Bouattour A, Gern L, Baranton G, Postic D. Detection and identification of Ehrlichia spp. in ticks collected in Tunisia and Morocco. J Clin Microbiol. 2005;43:1127–32. doi: 10.1128/JCM.43.3.1127-1132.2005. PubMed DOI PMC

Ben Said M, Belkahia H, Messadi L. <i>Anaplasma<i> spp. in North Africa: a review on molecular epidemiology, associated risk factors and genetic characteristics. Ticks Tick Borne Dis. 2018;9:543–55. doi: 10.1016/j.ttbdis.2018.01.003. PubMed DOI

Nieto NC, Foley JE, Bettaso J, Lane RS. Reptile infection withAnaplasma phagocytophilum, the causative agent of granulocytic anaplasmosis. J Parasitol. 2009;95:1165–1170. doi: 10.1645/GE-1983.1. PubMed DOI

de la Fuente J, Torina A, Naranjo V, Caracappa S, Di Marco V, Alongi A, et al. Infection with Anaplasma phagocytophilum in a seronegative patient in Sicily, Italy: case report. Ann Clin Microbiol Antimicrob. 2005;4:15. doi: 10.1186/1476-0711-4-15. PubMed DOI PMC

Vieira JP, Brito MJ, de Carvalho IL. Borrelia lusitaniae infection mimicking headache, neurologic deficits, and cerebrospinal fluid lymphocytosis. J Child Neurol. 2019;34:748–750. doi: 10.1177/0883073819858263. PubMed DOI

Botelho-Nevers E, Socolovschi C, Raoult D, Parola P. Treatment of Rickettsia spp. infections: a review. Expert Rev Anti Infect Ther. 2012;10:1425–37. doi: 10.1586/eri.12.139. PubMed DOI