Wild ungulates as sentinels of flaviviruses and tick-borne zoonotic pathogen circulation: an Italian perspective
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články
PubMed
37710273
PubMed Central
PMC10500747
DOI
10.1186/s12917-023-03717-x
PII: 10.1186/s12917-023-03717-x
Knihovny.cz E-zdroje
- Klíčová slova
- Flavivirus, Ixodes ricinus, Molecular biology, Vector-borne zoonotic pathogens, Virus neutralization test, Wild ungulates,
- MeSH
- Coxiella MeSH
- klíště * MeSH
- komáří přenašeči MeSH
- Rickettsia * MeSH
- savci MeSH
- séroepidemiologické studie MeSH
- viry klíšťové encefalitidy * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Evropa MeSH
BACKGROUND: Vector-borne zoonotic diseases are a concerning issue in Europe. Lyme disease and tick-borne encephalitis virus (TBEV) have been reported in several countries with a large impact on public health; other emerging pathogens, such as Rickettsiales, and mosquito-borne flaviviruses have been increasingly reported. All these pathogens are linked to wild ungulates playing roles as tick feeders, spreaders, and sentinels for pathogen circulation. This study evaluated the prevalence of TBEV, Borrelia burgdorferi sensu lato, Rickettsia spp., Ehrlichia spp., and Coxiella spp. by biomolecular screening of blood samples and ticks collected from wild ungulates. Ungulates were also screened by ELISA and virus neutralization tests for flaviviral antibody detection. RESULTS: A total of 274 blood samples were collected from several wild ungulate species, as well as 406 Ixodes ricinus, which were feeding on them. Blood samples tested positive for B. burgdorferi s.l. (1.1%; 0-2.3%) and Rickettsia spp. (1.1%; 0-2.3%) and showed an overall flaviviral seroprevalence of 30.6% (22.1-39.2%): 26.1% (17.9-34.3%) for TBEV, 3.6% (0.1-7.1%) for Usutu virus and 0.9% (0-2.7%) for West Nile virus. Ticks were pooled when possible and yielded 331 tick samples that tested positive for B. burgdorferi s.l. (8.8%; 5.8-11.8%), Rickettsia spp. (26.6%; 21.8-31.2%) and Neoehrlichia mikurensis (1.2%; 0-2.4%). TBEV and Coxiella spp. were not detected in either blood or tick samples. CONCLUSIONS: This research highlighted a high prevalence of several tick-borne zoonotic pathogens and high seroprevalence for flaviviruses in both hilly and alpine areas. For the first time, an alpine chamois tested positive for anti-TBEV antibodies. Ungulate species are of particular interest due to their sentinel role in flavivirus circulation and their indirect role in tick-borne diseases and maintenance as Ixodes feeders and spreaders.
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Boulanger N, Boyer P, Talagrand-Reboul E, Hansmann Y. Ticks and tick-borne diseases. Med Mal Infect. 2019;49:87–97. PubMed
Daszak P, Cunningham AA, Hyatt AD. Emerging infectious Diseases of Wildlife - Threats to biodiversity and human health. Sci Compass. 2000;287:443–9. PubMed
Dantas-Torres F. Climate change, biodiversity, ticks and tick-borne diseases: the butterfly effect. Int J Parasitol Parasites Wildl. 2015;4:452–61. PubMed PMC
Ostfeld RS, Brunner JL. Climate change and Ixodes tick-borne diseases of humans. Philos Trans R Soc B. 2015;370. PubMed PMC
Cunningham AA, Daszak P, Wood JLN. One health, emerging infectious diseases and wildlife: two decades of progress? Philos Trans R Soc B. 2017;372:20160167. PubMed PMC
Tasser E, Walde J, Tappeiner U, Teutsch A, Noggler W. Land-use changes and natural reforestation in the Eastern Central Alps. Agric Ecosyst Environ. 2007;118:115–29.
Battaglini L, Bovolenta S, Gusmeroli F, Salvador S, Sturaro E. Environmental sustainability of Alpine livestock farms. Ital J Anim Sci. 2014;13(3155):431–43.
Apollonio M, Andersen R, Putman R. European ungulates and their management in the 21st Century. Cambridge, UK: Cambridge University Press; 2010.
Carnevali L. In: Pedrotti L, Riga F, Toso S, editors. Ungulates in Italy - Status, distribution, abundance, management and hunting of ungulate populations in Italy. Volume Rapporto 2. ISPRA (Istituto Superiore per la Protezione e Ricerca Ambientale); 2009. pp. 1–168.
Gray J, Kahl O, Zintl A. What do we still need to know about Ixodes ricinus? Ticks and Tick-borne Diseases. 2021;12(101682). PubMed
Otranto D, Dantas-Torres F, Giannelli A, Latrofa MS, Cascio A, Cazzin S et al. Ticks infesting humans in Italy and associated pathogens. Parasites and Vectors. 2014;7(328). PubMed PMC
Kazimírová M, Hamšíková Z, Špitalská E, Minichová L, Mahríková L, Caban R, et al. Diverse tick-borne microorganisms identified in free-living ungulates in Slovakia. Parasit Vectors. 2018;11:495. PubMed PMC
Medlock JM, Hansford KM, Bormane A, Derdakova M, Estrada-Peña A, George J-C et al. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit Vectors. 2013;6(1). PubMed PMC
Wolcott KA, Margos G, Fingerle V, Becker NS. Host association of Borrelia burgdorferi sensu lato: a review. Ticks Tick Borne Dis. 2021;12(101766). PubMed
Guccione C, Colomba C, Tolomeo M, Trizzino M, Iaria C, Cascio A. Rickettsiales in Italy. Pathogens. 2021;10(181). PubMed PMC
Höper L, Skoog E, Stenson M, Grankvist A, Wass L, Olsen B, et al. Vasculitis due to Candidatus Neoehrlichia mikurensis: a cohort study of 40 swedish patients. Clin Infect Dis. 2021;73(7):e2372–8. PubMed
Stuen S, Granquist EG, Silaghi C. Anaplasma phagocytophilum - A widespread multi-host pathogen with highly adaptive strategies. Front Cell Infect Microbiol. 2013;3:31. PubMed PMC
Michelitsch A, Wernike K, Klaus C, Dobler G, Beer M. Exploring the Reservoir Hosts of Tick-Borne Encephalitis Virus. Viruses. 2019;11(669). PubMed PMC
Trevisan G, Cinco M, Trevisini S, Di Meo N, Chersi K, Ruscio M et al. Borreliae Part 1: Borrelia Lyme Group and Echidna-Reptile Group. Biology. 2021;10(1036). PubMed PMC
Riccò M. Epidemiology of tick-borne encephalitis in north-eastern italy (2017–2020): International insights from national notification reports. Acta Biomed. 2021;92(5):e2021229. PubMed PMC
Grassi L, Franzo G, Martini M, Mondin A, Cassini R, Drigo M, et al. Ecotyping of Anaplasma phagocytophilum from wild ungulates and ticks shows circulation of zoonotic strains in northeastern Italy. Animals. 2021;11:310. PubMed PMC
Tomassone L, Portillo A, Nováková M, De Sousa R, Oteo JA. Neglected aspects of tick-borne rickettsioses. Parasit Vectors. 2018;11(263). PubMed PMC
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). PubMed PMC
Alfano N, Tagliapietra V, Rosso F, Ziegler U, Arnoldi D, Rizzoli A. Tick-borne encephalitis foci in northeast Italy revealed by combined virus detection in ticks, serosurvey on goats and human cases. Emerg Microbes Infect. 2020;9:474–84. PubMed PMC
Špitalská E, Sparagano O, Stanko M, Schwarzová K, Zdenko Å, Škultéty Ľ, et al. Diversity of Coxiella-like and Francisella-like endosymbionts, and Rickettsia spp., Coxiella burnetii as pathogens in the tick populations of Slovakia, Central Europe. Ticks Tick Borne Dis. 2018;9:1207–11. PubMed
Knap N, Žele2 D, Glinšek Biškup U, Avšič-Županc T, Vengušt G. The prevalence of Coxiella burnetii in ticks and animals in Slovenia. BMC Vet Res. 2019;15(368). PubMed PMC
Yessinou ER, Mertens-scholz K, Neubauer H, Farougou S. Prevalence of Coxiella-infections in ticks - review and meta-analysis. Ticks Tick Borne Dis. 2022;13:101926. PubMed
González-Barrio D, Ruiz-Fons F. Coxiella burnetii in wild mammals: a systematic review. Transbound Emerg Dis. 2019;66(2):662–71. PubMed
Autorino GL, Battisti A, Deubel V, Ferrari G, Forletta R, Giovannini A, et al. West Nile virus Epidemic in Horses, Tuscany Region, Italy. Emerg Infect Dis. 2002;8(12):1372–8. PubMed PMC
Weissenböck H, Bakonyi T, Rossi G, Mani P, Nowotny N. Usutu virus, Italy, 1996. Emerg Infect Dis. 2013;19(2):274–7. PubMed PMC
Zecchin B, Fusaro A, Milani A, Schivo A, Ravagnan S, Ormelli S, et al. The central role of Italy in the spatial spread of USUTU virus in Europe. Virus Evol. 2021;7(1):veab048. PubMed PMC
Vilibic-Cavlek T, Petrovic T, Savic V, Barbic L, Tabain I, Stevanovic V et al. Epidemiology of Usutu Virus: the european scenario. Pathogens. 2020;9(699). PubMed PMC
Riccò M, Peruzzi S, Balzarini F. Epidemiology of West Nile Virus Infections in humans, Italy, 2012–2020: a summary of available evidences. Trop Med Infect Dis. 2021;6:61. PubMed PMC
Krzysiak MK, Anusz K, Konieczny A, Rola J, Salat J, Strakova P, et al. The european bison (Bison bonasus) as an indicatory species for the circulation of tick-borne encephalitis virus (TBEV) in natural foci in Poland. Ticks Tick Borne Dis. 2021;12:101799. PubMed
Holding M, Dowall SD, Medlock JM, Carter DP, Pullan ST, Lewis J, et al. Tick-borne encephalitis virus, United Kingdom. Emerg Infect Dis. 2020;26(1):90–6. PubMed PMC
Imhoff M, Hagedorn P, Schulze Y, Hellenbrand W, Pfeffer M, Niedrig M. Review: sentinels of tick-borne encephalitis risk. Ticks Tick Borne Dis. 2015;6:592–600. PubMed
Rizzoli A, Hauffe HC, Tagliapietra V, Neteler M, Rosà R. Forest structure and roe deer abundance predict tick-borne encephalitis risk in Italy. PLoS ONE. 2009;4(2):e4336. PubMed PMC
Rosà R, Tagliapietra V, Manica M, Arnoldi D, Hauffe HC, Rossi C, et al. Changes in host densities and co-feeding pattern efficiently predict tick-borne encephalitis hazard in an endemic focus in northern Italy. Int J Parasitol. 2019;49:779–87. PubMed
Da Rold G, Obber F, Monne I, Milani A, Ravagnan S, Toniolo F et al. Clinical Tick-Borne Encephalitis in a Roe deer (Capreolus capreolus L.). Viruses. 2022;14(300). PubMed PMC
Potkonjak A, Petrović T, Ristanović E, Lalić I, Vračar V, Savić S, et al. Molecular Detection and Serological evidence of Tick-Borne Encephalitis Virus in Serbia. Vector-Borne Zoonotic Dis. 2017;17(12):813–20. PubMed
Paulsen KM, das Neves CG, Granquist EG, Madslien K, Stuen S, Pedersen BN, et al. Cervids as sentinel-species for tick-borne encephalitis virus in Norway - A serological study. Zoonoses Public Health. 2020;67:342–51. PubMed
Tonteri E, Jokelainen P, Matala J, Pusenius J, Vapalahti O. Serological evidence of tick-borne encephalitis virus infection in moose and deer in Finland: sentinels for virus circulation. Parasites and Vectors. 2016;9(54). PubMed PMC
Bournez L, Umhang G, Faure E, Boucher J-M, Boué F, Jourdain E et al. Exposure of wild ungulates to the Usutu and Tick-borne encephalitis viruses in France in 2009–2014: evidence of undetected Flavivirus circulation a decade ago. Viruses. 2020;12(10). PubMed PMC
García-Bocanegra I, Paniagua J, Gutiérrez-Guzmán AV, Lecollinet S, Boadella M, Arenas-Montes A et al. Spatio-temporal trends and risk factors affecting West Nile virus and related flavivirus exposure in spanish wild ruminants. BMC Vet Res. 2016;12(249). PubMed PMC
Fabri ND, Sprong H, Hofmeester TR, Heesterbeek H, Donnars BF, Widemo F et al. Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens. Parasites and Vectors. 2021;14(360). PubMed PMC
Hofmeester T, Coipan E, Evan Wieren S, Prins H, Takken W, Sprong H. Few vertebrate species dominate the Borrelia burgdorferi s.l. life cycle. Environ Res Lett. 2016;11:043001.
Garcia-Vozmediano A, Krawczyk AI, Sprong H, Rossi L, Ramassa E, Tomassone L. Ticks climb the mountains: ixodid tick infestation and infection by tick-borne pathogens in the Western Alps. Ticks Tick Borne Dis. 2020;11(5). PubMed
Pistone D, Pajoro M, Novakova E, Vicari N, Gaiardelli C, Viganò R, et al. Ticks and bacterial tick-borne pathogens in Piemonte region, Northwest Italy. Exp Appl Acarol. 2017;73:477–91. PubMed
Díaz-Cao JM, Adaszek Ł, Dzięgiel B, Paniagua J, Caballero-Gómez J, Winiarczyk S, et al. Prevalence of selected tick-borne pathogens in wild ungulates and ticks in southern Spain. Transbound Emerg Dis. 2022;69(3):1084–94. PubMed
Michalski MM, Kubiak K, Szczotko M, Dmitryjuk M. Tick-borne pathogens in ticks collected from wild ungulates in North-Eastern Poland. Pathogens. 2021;10:587. PubMed PMC
Portillo A, Santibáñez P, Palomar AM, Santibáñez S, Oteo JA. Candidatus Neoehrlichia mikurensis ’ in Europe. New Microbes New Infect. 2018;22:30–6. PubMed PMC
Stefanidesova K, Kocianova E, Boldis V, Kostanova Z, Kanka P, Nemethova D, et al. Evidence of Anaplasma phagocytophilum and Rickettsia helvetica infection in free-ranging ungulates in central Slovakia. Eur J Wildl Res. 2008;54(3):519–24.
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(5):1068–71. PubMed PMC
Hajduskova E, Literak I, Papousek I, Costa FB, Novakova M, Labruna MB, et al. Candidatus Rickettsia mendelii, a novel basal group rickettsia detected in Ixodes ricinus ticks in the Czech Republic. Ticks Tick Borne Dis. 2016;7(3):482–6. PubMed
Stańczak J, Biernat B, Racewicz M, Zalewska M, Matyjasek A. Prevalence of different Rickettsia spp. in Ixodes ricinus and Dermacentor reticulatus ticks (Acari: Ixodidae) in north-eastern Poland. Ticks Tick Borne Dis. 2018;9(2):427–34. PubMed
Pajoro M, Pistone D, Boccazzi IV, Mereghetti V, Bandi C, Fabbi M et al. Molecular screening for bacterial pathogens in ticks (Ixodes ricinus) collected on migratory birds captured in northern Italy. Folia Parasitol (Praha). 2018;65(008). PubMed
Ceglie L, Guerrini E, Rampazzo E, Barberio A, Tilburg JJHC, Hagen F, et al. Molecular characterization by MLVA of Coxiella burnetii strains infecting dairy cows and goats of north-eastern Italy. Microbes Infect. 2015;17:776–81. PubMed
Barberio A. Coxiella burnetii infection in dairy cows and goats: assessment of diagnostic methods, and evaluation of immune response in shedders. PhD Dissertation Thesis. 2015; Università degli studi di Milano, Facoltà di Medicina Veterinaria, Dipartimento di Scienze veterinarie e Sanità pubblica (Accessed on 29/03/2023:https://air.unimi.it/retrieve/handle/2434/352272/515810/phd_unimi_R10106.pdf).
D’Agaro P, Martinelli E, Burgnich P, Nazzi F, Del Fabbro S, Iob A, et al. Prevalence of Tick-Borne Encephalitis Virus in Ixodes Ricinus from a Novel Endemic Area of North Eastern Italy. J Med Virol. 2009;81:309–16. PubMed
Duscher GG, Wetscher M, Baumgartner R, Walder G. Roe deer sera used for TBE surveillance in Austria. Ticks Tick Borne Dis. 2015;6(4):489–93. PubMed
Kiffner C, Vor T, Hagedorn P, Niedrig M, Rühe F. Determinants of tick-borne encephalitis virus antibody presence in roe deer (Capreolus capreolus) sera. Med Vet Entomol. 2012;26:18–25. PubMed
Balling A, Plessow U, Beer M, Pfeffer M. Prevalence of antibodies against tick-borne encephalitis virus in wild game from Saxony, Germany. Ticks Tick Borne Dis. 2014;5:805–9. PubMed
Caracciolo I, Mora-Cardenas E, Aloise C, Carletti T, Segat L, Burali MS, et al. Comprehensive response to usutu virus following first isolation in blood donors in the Friuli Venezia Giulia region of Italy: development of recombinant NS1-based serology and sensitivity to antiviral drugs. PLoS Negl Trop Dis. 2020;14(3):e0008156. PubMed PMC
Escribano-Romero E, Lupulović D, Merino-Ramos T, Blázquez AB, Lazić G, Lazić S, et al. West Nile virus serosurveillance in pigs, wild boars, and roe deer in Serbia. Vet Microbiol. 2015;176:365–9. PubMed
Hubálek Z, Juricová Z, Straková P, Blazejová H, Betásová L, Rudolf I. Serological survey for West Nile Virus in Wild Artiodactyls, Southern Moravia (Czech Republic) Vector-Borne Zoonotic Dis. 2017;17(9):654–7. PubMed
Estrada-Peña A, Palomar AM, Santibáñez P, Sánchez N, Habela MA, Portillo A et al. Crimean-Congo Hemorrhagic Fever Virus in Ticks, Southwestern Europe, 2010. Emerg Infect Dis. 2012;18(1). PubMed PMC
Negredo A, de la Calle-Prieto F, Palencia-Herrejón E, Mora-Rillo M, Astray-Mochales J, Sánchez-Seco MP, et al. Autochthonous Crimean–Congo Hemorrhagic Fever in Spain. N Engl J Med. 2017;377(2):154–61. PubMed
ARPA FVG - Osservatorio metereologico regionale del Friuli Venezia Giulia. Accessed on 29/03/23:https://www.clima.fvg.it/archivio.php?ln=&p=dati
ARPA Veneto - Agenzia Regionale per la Prevenzione e Protezione Ambientale del Veneto. Accessed on 29/03/23: https://www.arpa.veneto.it/dati-ambientali/dati-storici.
ARPA Lombardia - Agenzia Regionale per la Protezione dell’Ambiente. Accessed on 29/03/23: https://www.arpalombardia.it/Pages/Meteorologia/Richiesta-dati-misurati.aspx#.
Mourey J, Marcuzzi M, Ravanel L, Pallandre F. Effects of climate change on high Alpine mountain environments: evolution of mountaineering routes in the Mont Blanc massif (Western Alps) over half a century. Arct Antarct Alp Res. 2019;51(1):176–89.
Gobiet A, Kotlarski S, Beniston M, Heinrich G, Rajczak J, Stoffel M. 21st century climate change in the european Alps - a review. Sci Total Environ. 2014;493:1138–51. PubMed
Map chart. https://www.mapchart.net/italy.html (Accessed 12 June 2023).
Manilla G. Ixodida, Acari (Fauna d’Italia) Bologna - Italy: Edizioni Calderini; 1998. pp. 1–280.
Cringoli G, Iori A, Rinaldi L, Veneziano V, Genchi C. Zecche - Mappe parassitologiche. Rolando editore, Naples, Italy. 2005. 1–263 p.
Schwaiger M, Cassinotti P. Development of a quantitative real-time RT-PCR assay with internal control for the laboratory detection of tick borne encephalitis virus (TBEV) RNA. J Clin Virol. 2003;27(2):136–45. PubMed
Courtney JW, Kostelnik LM, Zeidner NS, Massung RF. Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol. 2004;42(7):3164–8. PubMed PMC
Lee SH, Lee JH, Park HS, Jang WJ, Koh SE, Yang YM, et al. Differentiation of Borrelia burgdorferi sensu lato through groEL gene analysis. FEMS Microbiol Lett. 2003;222(1):51–7. PubMed
Rolain JM, Bitam I, Buffet S, Marié JL, Bourry O, Portelli-Clerc C, et al. Presence or absence of plasmid in Rickettsia felis depending on the source of fleas. Eur Soc Clin Microbiol Infect Dis. 2009;15(Suppl 2):296–7. PubMed
Choi YJ, Jang WJ, Kim JH, Ryu JS, Lee SH, Park KH, et al. Spotted fever group and typhus group rickettsioses in humans, South Korea. Emerg Infect Dis. 2005;11(2):237–44. PubMed PMC
Klee SR, Tyczka J, Ellerbrok H, Franz T, Linke S, Baljer G, et al. Highly sensitive real-time PCR for specific detection and quantification of Coxiella burnetii. BMC Microbiol. 2006;6:1–8. PubMed PMC
Guillemi EC, Tomassone L, Farber MD. Tick-borne Rickettsiales: molecular tools for the study of an emergent group of pathogens. J Microbiol Methods. 2015;119:87–97. PubMed
Krücken J, Schreiber C, Maaz D, Kohn M, Demeler J, Beck S, et al. A novel high-resolution melt PCR assay discriminates Anaplasma phagocytophilum and Candidatus Neoehrlichia mikurensis. J Clin Microbiol. 2013;51(6):1958–61. PubMed PMC
Goodman JL, Nelson C, Vitale B, Madigan JE, Dumler JS, Kurtti TJ, et al. Direct cultivation of the Causative Agent of Human granulocytic ehrlichiosis. N Engl J Med. 1996;334(4):209–15. PubMed
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic Local Alignment Search Tool. Vol. 215, J Mol Biol. 1990. PubMed
Šimánek V, Pecen L, Krátká Z, Fürst T, Řezáčková H, Topolčan O, Fajfrlík K, Sedláček D, Šín R, Pazdiora P, et al. Five commercial Immunoassays for SARS-CoV-2 antibody determination and their comparison and correlation with the Virus neutralization test. Diagnostics. 2021;11:593. PubMed PMC