Serological and molecular screening for zoonotic pathogens among wild hedgehogs (Erinaceus europaeus) from urban areas of Poland

Turlewicz-Podbielska, Hanna; Ruszkowski, Jakub Jędrzej; Pisarek, Maria; Adaszek, Łukasz; Pomorska-Mól, Małgorzata

doi:10.2478/jvetres-2025-0022

References

Atif F.A., Mehnaz S., Qamar M.F., Roheen T., Sajid M.S., Ehtisham-Ul-Haque S., Kashif M., Ben Said M.: Epidemiology, Diagnosis, and Control of Canine Infectious Cyclic Thrombocytopenia and Granulocytic Anaplasmosis: Emerging Diseases of Veterinary and Public Health Significance. Vet Sci 2021, 8, 312, doi: 10.3390/vetsci8120312.
Open DOI Search in Google Scholar Back to article
Balti G., Galon C., Derghal M., Souguir H., Guerbouj S., Rhim A., Chemkhi J., Guizani I., Bouattour A., Moutailler S., M'ghirbi Y.: Atelerix algirus, the North African Hedgehog: Suitable Wild Host for Infected Ticks and Fleas and Reservoir of Vector-Borne Pathogens in Tunisia. Pathogens 2021, 10, 953, doi: 10.3390/pathogens10080953.
Open DOI Search in Google Scholar Back to article
Baptista C.J., Seixas F., Gonzalo-Orden J.M., Oliveira P.A.: Can the European Hedgehog (Erinaceus europaeus) Be a Sentinel for One Health Concerns? Biologics 2021, 1, 61–69, doi: 10.3390/biologics1010004.
Open DOI Search in Google Scholar Back to article
Barradas P.F., Mesquita J.R., Mateus T.L., Ferreira P., Amorim I., Gärtner F., de Sousa R.: Molecular detection of Rickettsia spp. in ticks and fleas collected from rescued hedgehogs (Erinaceus europaeus) in Portugal. Exp Appl Acarol 2021 83, 449–460, doi: 10.1007/s10493-021-00600-y.
Open DOI Search in Google Scholar Back to article
Battilani M., De Arcangeli S., Balboni A., Dondi F.: Genetic diversity and molecular epidemiology of Anaplasma. Infect Genet Evol 2017, 49, 195–211, doi: 10.1016/j.meegid.2017.01.021.
Open DOI Search in Google Scholar Back to article
Bergmann M., Englert T., Stuetzer B., Hawley J.R., Lappin M.R., Hartmann K.: Prevalence of selected rickettsial infections in cats in Southern Germany. Comp Immunol Microbiol Infect Dis 2015, 42, 33–36, doi: 10.1016/j.cimid.2015.08.003.
Open DOI Search in Google Scholar Back to article
Biernat B., Stańczak J., Michalik J., Sikora B., Wierzbicka A.: Prevalence of infection with Rickettsia helvetica in Ixodes ricinus ticks feeding on non-rickettsiemic rodent hosts in sylvatic habitats of west-central Poland. Ticks Tick Borne Dis 2016, 7, 135–141, doi: 10.1016/j.ttbdis.2015.10.001.
Open DOI Search in Google Scholar Back to article
Dumler J.S., Bakken J.S.: Ehrlichial diseases of humans: emerging tick-borne infections. Clin Infect Dis 1995, 20, 1102–1110, doi: 10.1093/clinids/20.5.1102.
Open DOI Search in Google Scholar Back to article
Dyczko D., Krysmann A., Kolanek A., Borczyk B., Kiewra D.: Bacterial pathogens in Ixodes ricinus collected from lizards Lacerta agilis and Zootoca vivipara in urban areas of Wrocław, SW Poland – preliminary study. Exp Appl Acarol 2024, 93, 409–420, doi: 10.1007/s10493-024-00927-2.
Open DOI Search in Google Scholar Back to article
Escudero A., Ribas M.P., Obón E., Almería S., Aguilar X.F., Gholipour H., Cabezón O., Molina-López R.: Exposure of Urban European Hedgehogs (Erinaceus europaeus) to Toxoplasma gondii in Highly Populated Areas of Northeast Spain. Animals 2024, 14, 1596, doi: 10.3390/ani14111596.
Open DOI Search in Google Scholar Back to article
Földvári G., Jahfari S., Rigó K., Jablonszky M., Szekeres S., Majoros G., Tóth M., Molnár V., Coipan E.C., Sprong H.: Candidatus Neoehrlichia mikurensis and Anaplasma phagocytophilum in urban hedgehogs. Emerg Infect Dis 2014, 20, 496–498, doi: 10.3201/eid2003.130935.
Open DOI Search in Google Scholar Back to article
Fournier P.E., Raoult D.: Bacteriology, taxonomy, and phylogeny of Rickettsia. In: Rickettsial Diseases, edited by D. Raoult, P. Parola, Informa Healthcare, New York, NY, USA, 2007, pp. 1–14.
Search in Google Scholar Back to article
Gajda E., Hildebrand J., Sprong H., Buńkowska-Gawlik K., Perec-Matysiak A., Coipan E.C.: Spotted fever rickettsiae in wild-living rodents from south-western Poland. Parasit Vectors 2017, 10, 413, doi: 10.1186/s13071-017-2356-5.
Open DOI Search in Google Scholar Back to article
Government of the Republic of Poland: Rozporządzenie Ministra Środowiska z dnia 16 grudnia 2016 r. w sprawie ochrony gatunkowej zwierząt (Regulation of the Minister of the Environment of 16 December 2016 on the protection of animal species – in Polish). Dz U 2016, poz. 2183 (Official Journal of Laws 2016, item 2183).
Search in Google Scholar Back to article
Government of the Republic of Poland: Rozporządzenie Ministra Klimatu z dnia 18 grudnia 2019 zmieniające rozporządzenie w sprawie ochrony gatunkowej zwierząt. (Regulation of the Minister of Climate of 18 December 2019 amending the regulation on the protection of animal species – in Polish). Dz U 2020, poz. 26 (Official Journal of Laws 2020, item 26).
Search in Google Scholar Back to article
Hosni M.M., El Maghrbi A.A., Ganghish K.S.: Occurrence of Trichinella spp. in wild animals in northwestern Libya. Open Vet J 2013, 3, 85–88, doi: 10.5455/OVJ.2013.v3.i2.p85.
Open DOI Search in Google Scholar Back to article
Khodadadi N., Nabavi R., Sarani A., Saadati D., Ganjali M., Mihalca A.D., Otranto D., Sazmand A.: Identification of Anaplasma marginale in long-eared hedgehogs (Hemiechinus auritus) and their Rhipicephalus turanicus ticks in Iran. Ticks Tick Borne Dis 2021, 12, 101641, doi: 10.1016/j.ttbdis.2020.101641.
Open DOI Search in Google Scholar Back to article
Kiewra D., Zaleśny G., Czułowska A.: The prevalence of Anaplasma phagocytophilum in questing Ixodes ricinus ticks in SW Poland. Pol J Microbiol 2014, 63, 89–93, doi: 10.33073/pjm-2014-013.
Open DOI Search in Google Scholar Back to article
Krawczyk A.I., van Leeuwen A.D., Jacobs-Reitsma W., Wijnands L.M., Bouw E., Jahfari S., van Hoek A.H., van der Giessen J.W., Roelfsema J.H., Kroes M., Kleve J., Dullemont Y., Sprong H., de Bruin A.: Presence of zoonotic agents in engorged ticks and hedgehog faeces from Erinaceus europaeus in (sub) urban areas. Parasit Vectors 2015, 8, 1–6, doi: 10.1186/s13071-015-0814-5.
Open DOI Search in Google Scholar Back to article
Lee S.H., Healy J., Lambert J.S.: Single Core Genome Sequencing for Detection of both Borrelia burgdorferi Sensu Lato and Relapsing Fever Borrelia Species. Int J Environ Res Public Health 2019, 16, 1779, doi: 10.3390/ijerph16101779.
Open DOI Search in Google Scholar Back to article
Lesiczka P.M., Hrazdilová K., Majerová K., Fonville M., Sprong H., Hönig V., Hofmannová L., Papežík P., Růžek D., Zurek L., Votýpka J., Modrý D.: The Role of Peridomestic Animals in the Eco-Epidemiology of Anaplasma phagocytophilum. Microb Ecol 2021, 82, 60–612, doi: 10.1007/s00248-021-01704-z.
Open DOI Search in Google Scholar Back to article
Lesiński G., Gryz J., Krauze-Gryz D., Stolarz P.: Population increase and synurbization of the yellow-necked mouse Apodemus flavicollis in some wooded areas of Warsaw agglomeration, Poland, in the years 1983–2018. Urban Ecosyst 2021, 24, 481–489, doi: 10.1007/s11252-020-01046-7.
Open DOI Search in Google Scholar Back to article
Maurin M., Raoult D.F.: Q fever. Clin Microbiol Rev 1999, 12, 518–553, doi: 10.1128/CMR.12.4.518.
Open DOI Search in Google Scholar Back to article
Myczka A.W., Steiner-Bogdaszewska Ż., Filip-Hutsch K., Oloś G., Czopowicz M., Laskowski Z.: Detection of Anaplasma phagocytophilum in Wild and Farmed Cervids in Poland. Pathogens 2021, 10, 1190, doi: 10.3390/pathogens10091190
Open DOI Search in Google Scholar Back to article
Ooteman M.C., Vago A.R., Koury M.C.: Evaluation of MAT, IgM ELISA and PCR methods for the diagnosis of human leptospirosis. J Microbiol Methods 2006, 65, 247–257, doi: 10.1016/j.mimet.2005.07.015.
Open DOI Search in Google Scholar Back to article
Orkun Ö., Çakmak A., Nalbantoğlu S., Karaer Z.: Molecular detection of a novel Babesia sp. and pathogenic spotted fever group rickettsiae in ticks collected from hedgehogs in Turkey: Haemaphysalis erinacei, a novel candidate vector for the genus Babesia. Infect Genet Evol 2019, 69, 190–198, doi: 10.1016/j.meegid.2019.01.028.
Open DOI Search in Google Scholar Back to article
Prpić J., Keros T., Vucelja M., Bjedov L., Daković Rode O., Margaletić J., Habrun B., Jemeršić L.: First evidence of hepatitis E virus infection in a small mammal (yellow-necked mouse) from Croatia. PLoS One 2019, 14, e0225583, doi: 10.1371/journal.pone.0225583.
Open DOI Search in Google Scholar Back to article
Qi Y., Ai L., Zhu C., Ye F., Lv R., Wang J., Mao Y., Lu N., Tan W.: Wild hedgehogs and their parasitic ticks coinfected with multiple tick-borne pathogens in Jiangsu Province, Eastern China. Microbiol Spectr 2022, 10, e02138-22, doi: 10.1128/spectrum.02138-22.
Open DOI Search in Google Scholar Back to article
R Core Team: R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2021, https://www.R-project.org.
Search in Google Scholar Back to article
Roux V., Raoult D.: Phylogenetic analysis of members of the genus Rickettsia using the gene encoding the outer-membrane protein rOmpB (ompB). Int J Syst Evol Microbiol 2000, 50, 1449–1455, doi: 10.1099/00207713-50-4-1449.
Open DOI Search in Google Scholar Back to article
Ruszkowski J.J., Hetman M., Turlewicz-Podbielska H., Pomorska-Mól M.: Hedgehogs as a potential source of zoonotic pathogens—A review and an update of knowledge. Animals 2021, 11, 1754, doi: 10.3390/ani11061754.
Open DOI Search in Google Scholar Back to article
Sarani S., Enferadi A., Hasani S.J., Sarani M.Y., Rahnama M., Sarani F.: Identification of zoonotic pathogenic bacteria from blood and ticks obtained from hares and long-eared hedgehogs (Hemiechinus megalofis) in eastern Iran. Comp Immunol Microbiol Infect Dis 2024, 104, 102097, doi: 10.1016/j.cimid.2023.102097.
Open DOI Search in Google Scholar Back to article
Sawczyn-Domańska A., Wójcik-Fatla A.: Detection and prevalence of Anaplasma phagocytophilum in Ixodes ricinus ticks in eastern Poland. Ann Agric Environ Med 2024, 31, 439–441, doi: 10.26444/aaem/192238.
Open DOI Search in Google Scholar Back to article
Silaghi C., Skuballa J., Thiel C., Pfister K., Petney T., Pfäffle M., Taraschewski H., Passos L.M.: The European hedgehog (Erinaceus europaeus) – a suitable reservoir for variants of Anaplasma phagocytophilum? Ticks Tick Borne Dis 2012, 3, 49–54, doi: 10.1016/j.ttbdis.2011.11.005.
Open DOI Search in Google Scholar Back to article
Skuballa J., Oehme R., Hartelt K., Petney T., Bücher T., Kimmig P., Taraschewski H.: European hedgehogs as hosts for Borrelia spp., Germany. Emerg Infect Dis 2007, 13, 952–953, doi: 10.3201/eid1306.070224.
Open DOI Search in Google Scholar Back to article
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, 427–434, doi: 10.1016/j.ttbdis.2017.12.010.
Open DOI Search in Google Scholar Back to article
nStańczak J., Racewicz M., Michalik J., Cieniuch S., Sikora B., Skoracki M.: Prevalence of infection with Rickettsia helvetica in feeding ticks and their hosts in western Poland. Clin Microbiol Infect 2009, 15 Suppl 2, 328–329, doi: 10.1111/j.1469-0691.2008.02261.x.
Open DOI Search in Google Scholar Back to article
Stewart A.G., Stewart A.G.A.: An Update on the Laboratory Diagnosis of Rickettsia spp. Infection. Pathogens 2021, 10, 1319, doi: 10.3390/pathogens10101319.
Open DOI Search in Google Scholar Back to article
Szewczyk T., Werszko J., Myczka A.W., Laskowski Z., Karbowiak G.: Molecular detection of Anaplasma phagocytophilum in wild carnivores in north-eastern Poland. Parasit Vectors 2019, 12, 465, doi: 10.1186/s13071-019-3734-y.
Open DOI Search in Google Scholar Back to article
Xiao X., Han H.J., Qi R., Gong X., Lei S.C., Liu J.W., Qin X.R., Zhou C.M., Ma X.J., Chu M., Yu X.J.: Co-infection of Anaplasma and Ehrlichia in Hedgehogs from China. Research Square 2019, doi: 10.21203/rs.2.14515/v2.
Open DOI Search in Google Scholar Back to article
Zhu C., Ai L., Qi Y., Liu Y., Li H., Ye F., Wang Q., Luo Y., Tan W., Shi C.: Molecular detection of spotted fever group rickettsiae in hedgehogs (Erinaceus amurensis) and hedgehog-attached ticks in Xuyi County, Southeast China. Exp Appl Acarol 2022, 88, 97–111, doi: 10.1007/s10493-022-00721-y.
Open DOI Search in Google Scholar Back to article

Serological and molecular screening for zoonotic pathogens among wild hedgehogs (Erinaceus europaeus) from urban areas of Poland

References

Paradigm

My account