Detection of Anaplasma phagocytophilum in European brown hares (Lepus europaeus) using three different methods.

Anaplasma phagocytophilum Lepus europaeus European brown hare digital droplet PCR qPCR zoonosis

Journal

Zoonoses and public health
ISSN: 1863-2378
Titre abrégé: Zoonoses Public Health
Pays: Germany
ID NLM: 101300786

Informations de publication

Date de publication:
12 2021
Historique:
revised: 12 07 2021
received: 01 04 2021
accepted: 19 07 2021
pubmed: 12 8 2021
medline: 29 3 2022
entrez: 11 8 2021
Statut: ppublish

Résumé

European brown hare (Lepus europaeus Pallas 1778) is a broadly distributed lagomorph species in Europe, recognized as a host for Ixodes ricinus and reservoir of a wide range of pathogens with zoonotic potential. Even though Lepus europaeus represents an important game animal in Central Europe, the data available on Anaplasma phagocytophilum in this lagomorph are scarce. In this study, three populations of brown hare from distinct localities in the Czech Republic were analysed for the presence of Anaplasma phagocytophilum DNA. We used standard qPCR, targeting the msp2 gene and adapted the same assay also for digital droplet PCR. Out of 91 samples, these two methods identified 9 and 12 as positive, respectively. For taxonomic analysis, we amplified the groEL gene from five of six samples that were found positive by both methods. In phylogenetic analyses, this haplotype belongs to ecotype 1, and to the subclade with isolates from cervids and I. ricinus. Our findings underline the importance of correct result interpretation and positivity cut-off set-up for different detection methods of A. phagocytophilum. This bacterium is characterized by a high intraspecific variability and highly sensitive detection itself, is not enough. Detailed molecular typing is necessary to define the zoonotic potential of different strains and their natural reservoirs.

Identifiants

pubmed: 34379883
doi: 10.1111/zph.12883
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

917-925

Informations de copyright

© 2021 Wiley-VCH GmbH.

Références

Alberti, A., Zobba, R., Chessa, B., Addis, M. F., Sparagano, O., Pinna Parpaglia, M. L., Cubeddu, T., Pintori, G., & Pittau, M. (2005). Equine and canine Anaplasma phagocytophilum strains isolated on the island of Sardinia (Italy) are phylogenetically related to pathogenic strains from the United States. Applied and Environmental Microbiology, 71, 6418-6422. https://doi.org/10.1128/AEM.71.10.6418-6422.2005
Bown, K. J., Lambin, X., Ogden, N. H., Begon, M., Telford, G., Woldehiwet, Z., & Birtles, R. J. (2009). Delineating Anaplasma Phagocytophilum Ecotypes in Coexisting, Discrete Enzootic Cycles. Emerging Infectious Diseases, 15(12), 1948-1954.
Chastagner, A., Dugat, T., Vourc’h, G., Verheyden, H., Legrand, L., Bachy, V., Chabanne, L., Joncour, G., Maillard, R., Boulouis, H.-J., Haddad, N., Bailly, X., & Leblond, A. (2014). Multilocus Sequence Analysis of Anaplasma Phagocytophilum Reveals Three Distinct Lineages with Different Host Ranges in Clinically Ill French Cattle. Veterinary Research, 45(1), 1-12. https://doi.org/10.1186/s13567-014-0114-7
Courtney, J. W., Kostelnik, L. M., Zeidner, N. S., & Massung, R. F. (2004). Multiplex Real-Time PCR for Detection of Anaplasma Phagocytophilum and Borrelia Burgdorferi. Journal of Clinical Microbiology, 42(7), 3164-3168.
Cukor, J., Havranek, F., Linda, R., Bukovjan, K., Painter, M. S., & Hart, V. (2018). First Findings of Brown Hare (Lepus Europaeus) Reintroduction in Relation to Seasonal Impact. PLoS One, 13(10), 1-16. https://doi.org/10.1371/journal.pone.0205078
Dugat, T., Chastagner, A., Lagrée, A.-C., Petit, E., Durand, B., Thierry, S., Corbière, F., Verheyden, H., Chabanne, L., Bailly, X., Leblond, A., Vourc’h, G., Boulouis, H.-J., Maillard, R., & Haddad, N. (2014). A New Multiple-Locus Variable-Number Tandem Repeat Analysis Reveals Different Clusters for Anaplasma Phagocytophilum Circulating in Domestic and Wild Ruminants. Parasites and Vectors, 7(1), 1-11. https://doi.org/10.1186/1756-3305-7-439
Ebani, V. V., Poli, A., Rocchigiani, G., Bertelloni, F., Nardoni, S., Papini, R. A., & Mancianti, F. (2016). Serological Survey on Some Pathogens in Wild Brown Hares (Lepus Europaeus) in Central Italy. Asian Pacific Journal of Tropical Medicine, 9(5), 465-469. https://doi.org/10.1016/j.apjtm.2016.03.032
Fourie, J. J., Evans, A., Labuschagne, M., Crafford, D., Madder, M., Pollmeier, M., & Schunack, B. (2019). Transmission of Anaplasma Phagocytophilum (Foggie, 1949) by Ixodes Ricinus (Linnaeus, 1758) Ticks Feeding on Dogs and Artificial Membranes. Parasites and Vectors, 12(1), 1-10. https://doi.org/10.1186/s13071-019-3396-9
Galindo, R. C., Ayllán, N., Smrdel, K. S., Boadella, M., Beltrán-Beck, B., Mazariegos, M., García, N., Pére, J. M., La Lastra, D. E., Avsic-Zupanc, T., Kocan, K. M., Gortazar, C., & De La Fuente, J. (2012). Gene Expression Profile Suggests That Pigs (Sus Scrofa) Are Susceptible to Anaplasma Phagocytophilum but Control Infection. Parasites and Vectors, 5(1), 1-14. https://doi.org/10.1186/1756-3305-5-181
Hamšíková, Z., Silaghi, C., Takumi, K., Rudolf, I., Gunár, K., Sprong, H., & Kazimírová, M. (2019). Presence of Roe Deer Affects the Occurrence of Anaplasma Phagocytophilum Ecotypes in Questing Ixodes Ricinus in Different Habitat Types of Central Europe. International Journal of Environmental Research and Public Health, 16(23), 4725. https://doi.org/10.3390/ijerph16234725
Heylen, D., Lasters, R., Adriaensen, F., Fonville, M., Sprong, H., & Matthysen, E. (2019). Ticks and tick-borne diseases in the city: Role of landscape connectivity and green space characteristics in a metropolitan area. Science of the Total Environment, 670, 941-949. https://doi.org/10.1016/j.scitotenv.2019.03.235
Hrazdilová, K., Lesiczka, P. M., Bardoň, J., Vyroubalová, Š., Šimek, B., Zurek, L., & Modrý, D. (2021). Wild Boar as a Potential Reservoir of Zoonotic Tick-Borne Pathogens. Ticks and Tick-Borne Diseases, 12(1), 101558. https://doi.org/10.1016/j.ttbdis.2020.101558
Huhn, C., Winter, C., Wolfsperger, T., Wüppenhorst, N., Smrdel, K. S., Skuballa, J., Pfäffle, M., Petney, T., Silaghi, C., Dyachenko, V., Pantchev, N., Straubinger, R. K., Schaarschmidt-Kiener, D., Ganter, M., Aardema, M. L., & Von Loewenich, F. D. (2014). Analysis of the Population Structure of Anaplasma Phagocytophilum Using Multilocus Sequence Typing. PLoS One, 9(4), e93725. https://doi.org/10.1371/journal.pone.0093725
Hulínská, D., Langrová, K., Pejčoch, M., & Pavlásek, I. (2004). Detection of Anaplasma Phagocytophilum in Animals by Real-Time Polymerase Chain Reaction. Apmis, 112(4-5), 239-247. https://doi.org/10.1111/j.1600-0463.2004.apm11204-0503.x
Jaarsma, R. I., Sprong, H., Takumi, K., Kazimirova, M., Silaghi, C., Mysterud, A., Rudolf, I., Beck, R., Földvári, G., Tomassone, L., Groenevelt, M., Everts, R. R., Rijks, J. M., Ecke, F., Hörnfeldt, B., Modrý, D., Majerová, K., Votýpka, J., & Estrada-Peña, A. (2019). Anaplasma Phagocytophilum Evolves in Geographical and Biotic Niches of Vertebrates and Ticks. Parasites and Vectors, 12(1), 1-17. https://doi.org/10.1186/s13071-019-3583-8
Jahfari, S., Claudia Coipan, E., Fonville, M., Leeuwen, A. D. V., Hengeveld, P., Heylen, D., Heyman, P., Van Maanen, C., Butler, C. M., Földvári, G., Szekeres, S., Van Duijvendijk, G., Tack, W., Rijks, J. M., Van Der Giessen, J., Takken, W., Van Wieren, S. E., Takumi, K., & Sprong, H. (2014). Circulation of Four Anaplasma Phagocytophilum Ecotypes in Europe. Parasites and Vectors, 7(1), 1-11. https://doi.org/10.1186/1756-3305-7-365
Jahfari, S., Ruyts, S. C., Frazer-Mendelewska, E., Jaarsma, R., Verheyen, K., & Sprong, H. (2017). Melting Pot of Tick-Borne Zoonoses: The European Hedgehog Contributes to the Maintenance of Various Tick-Borne Diseases in Natural Cycles Urban and Suburban Areas. Parasites and Vectors, 10(1), 1-9. https://doi.org/10.1186/s13071-017-2065-0
Katoh, K., Rozewicki, J., & Yamada, K. D. (2018). MAFFT Online Service: Multiple Sequence Alignment, Interactive Sequence Choice and Visualization. Briefings in Bioinformatics, 20(4), 1160-1166. https://doi.org/10.1093/bib/bbx108
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647-1649. https://doi.org/10.1093/bioinformatics/bts199
Kocan, K. M., de la Fuente, J., Blouin, E. F., Coetzee, J. F., & Ewing, S. A. (2010). The Natural History of Anaplasma Marginale. Veterinary Parasitology, 167(2-4), 95-107. https://doi.org/10.1016/j.vetpar.2009.09.012
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. (2021). The role of peridomestic animals in the eco-epidemiology of Anaplasma phagocytophilum. Microbial Ecology, https://doi.org/10.1007/s00248-021-01704-z
Li, H., Bai, R., Zhao, Z., Tao, L., Ma, M., Ji, Z., Jian, M., Ding, Z., Dai, X., Bao, F., & Liu, A. (2018). Application of Droplet Digital PCR to Detect the Pathogens of Infectious Diseases. Bioscience Reports, 38(6), 1-8. https://doi.org/10.1042/BSR20181170
Liz, J. S., Sumner, J. W., Pfister, K., & Brossard, M. (2002). PCR detection and serological evidence of granulocytic ehrlichial infection in roe deer (Capreolus capreolus) and chamois (Rupicapra rupicapra). Journal of Clinical Microbiology, 40(3), 892-897. https://doi.org/10.1128/JCM.40.3.892-897.2002
Matei, I. A., Estrada-Peña, A., Cutler, S. J., Vayssier-Taussat, M., Varela-Castro, L., Potkonjak, A., Zeller, H., & Mihalca, A. D. (2019). A review on the eco-epidemiology and clinical management of human granulocytic Anaplasmosis and its agent in Europe. Parasites and Vectors, 12(1), 1-19. https://doi.org/10.1186/s13071-019-3852-6
Mukhacheva, T. A., Shaikhova, D. R., & Kovalev, S. Y. (2019). Asian Isolates of Anaplasma Phagocytophilum: Multilocus Sequence Typing. Ticks and Tick-Borne Diseases, 10(4), 775-780. https://doi.org/10.1016/j.ttbdis.2019.03.011
Mukhacheva, T. A., Shaikhova, D. R., Kovalev, S. Y., & von Loewenich, F. D. (2020). Phylogeographical diversity of Anaplasma phagocytophilum in the Asian part of Russia based on multilocus sequence typing and analysis of the ankA gene. Infection, Genetics and Evolution, 80, 104234. https://doi.org/10.1016/j.meegid.2020.104234
Polin, H., Hufnagl, P., Haunschmid, R., Gruber, F., & Ladurner, G. (2004). Molecular Evidence of Anaplasma Phagocytophilum in Ixodes Ricinus Ticks and Wild Animals in Austria. Journal of Clinical Microbiology, 42(5), 2285-2286.
Prevalence and co-infection with tick-borne Anaplasma phagocytophilum and Babesia spp. in red deer (Cervus elaphus) and roe deer (Capreolus capreolus) in Southern Norway. International Journal for Parasitology: Parasites and Wildlife, 8, 127-134. https://doi.org/10.1016/j.ijppaw.2019.01.003
Razanske, I., Rosef, O., Radzijevskaja, J., Bratchikov, M., Griciuviene, L., & Paulauskas, A. (2019). Prevalence and co-infection with tick-borne Anaplasma phagocytophilum and Babesia Spp. in red deer (Cervus elaphus) and roe deer (Capreolus capreolus) in Southern Norway. International Journal for Parasitology: Parasites and Wildlife, 8, 127-134.
Remesar, S., Díaz, P., Prieto, A., García-Dios, D., Fernández, G., López, C. M., Panadero, R., Díez-Baños, P., & Morrondo, P. (2020). Prevalence and Molecular Characterization of Anaplasma Phagocytophilum in Roe Deer (Capreolus Capreolus) from Spain. Ticks and Tick-Borne Diseases, 11(2), 101351. https://doi.org/10.1016/j.ttbdis.2019.101351
Reppert, E., Galindo, R. C., Breshears, M. A., Kocan, K. M., Blouin, E. F., & de la Fuente, J. (2013). Demonstration of Transplacental Transmission of a Human Isolate of Anaplasma Phagocytophilum in an Experimentally Infected Sheep. Transboundary and Emerging Diseases, 60(Suppl. 2), 93-96.
Rizzoli, A., Silaghi C., Obiegala A., Rudolf I., Hubálek Z., Földvári G., Plantard O., Vayssier-Taussat M., Bonnet S., Špitalská E., Kazimírová M. (2014) Ixodes Ricinus and Its Transmitted Pathogens in Urban and Peri-Urban Areas in Europe: New Hazards and Relevance for Public Health. Frontiers in Public Health 2(DEC).
Rocchigiani, G., Ebani, V. V., Nardoni, S., Bertelloni, F., Bascherini, A., Leoni, A., Mancianti, F., & Poli, A. (2018). Molecular Survey on the Occurrence of Arthropod-Borne Pathogens in Wild Brown Hares (Lepus Europaeus) from Central Italy. Infection, Genetics and Evolution, 59, 142-147.
Scharf, W., Schauer, S., Freyburger, F., Petrovec, M., Schaarschmidt-Kiener, D., Liebisch, G., Runge, M., Ganter, M., Alexandra Kehl, J., Dumler, S., Garcia-Perez, A. L., Jensen, J., Fingerle, V., Meli, M. L., Ensser, A., Stuen, S., & Von Loewenich, F. D. (2011). Distinct Host Species Correlate with Anaplasma Phagocytophilum AnkA Gene Clusters. Journal of Clinical Microbiology, 49(3), 790-796. https://doi.org/10.1128/JCM.02051-10
Stuen, S., Granquist, E. G., & Silaghi, C. (2013). Anaplasma phagocytophilum-a widespread multi-host pathogen with highly adaptive strategies. Frontiers in Cellular and Infection Microbiology, 3, 1-33. https://doi.org/10.3389/fcimb.2013.00031
Treml, F., Pikula, J., Bandouchova, H., & Horakova, J. (2007). European brown hare as a potential source of zoonotic agents. Veterinarni Medicina, 52(10), 451-456.
Tsokana, C. N., Sokos, C., Giannakopoulos, A., Birtsas, P., Valiakos, G., Spyrou, V., Athanasiou, L. V., Burriel, A. R., & Billinis, C. (2020). European Brown Hare (Lepus europaeus) as a Source of Emerging and Re-emerging Pathogens of Public Health Importance: A Review. Veterinary Medicine and Science, 550-564.
Wilson, M., Glaser, K. C., Adams-Fish, D., Boley, M., Mayda, M., & Molestina, R. E. (2015). Development of Droplet Digital PCR for the Detection of Babesia Microti and Babesia Duncani. Experimental Parasitology, 149, 24-31. https://doi.org/10.1016/j.exppara.2014.12.003
Wouters, Y., Dalloyaux, D., Christenhusz, A., Roelofs, H. M. J., Wertheim, H. F., Bleeker-Rovers, C. P., te Morsche, R. H., & Wanten, G. J. A. (2020). Droplet Digital Polymerase Chain Reaction for Rapid Broad-Spectrum Detection of Bloodstream Infections. Microbial Biotechnology, 13(3), 657-668. https://doi.org/10.1111/1751-7915.13491
Wu, X., Xiao, L. U., Lin, H., Chen, S., Yang, M., An, W., Wang, Y., Yang, Z., Yao, X., & Tang, Z. (2018). Development and Application of a Droplet Digital Polymerase Chain Reaction (DDPCR) for Detection and Investigation of African Swine Fever Virus. Canadian Journal of Veterinary Research, 82(1), 70-74.

Auteurs

Paulina Maria Lesiczka (PM)

Department of Pathology and Parasitology, University of Veterinary Sciences Brno, Brno, Czech Republic.
CEITEC-Central European Institute of Technology, University of Veterinary Sciences Brno, Brno, Czech Republic.

David Modry (D)

Department of Pathology and Parasitology, University of Veterinary Sciences Brno, Brno, Czech Republic.
Biology Centre, Institute of Parasitology, Czech Academy of Sciences, České Budějovice, Czech Republic.
Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic.
Department of Veterinary Sciences/CINeZ, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Prague, Czech Republic.

Hein Sprong (H)

Laboratory for Zoonoses and Environmental Microbiology, National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands.

Manoj Fonville (M)

Laboratory for Zoonoses and Environmental Microbiology, National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands.

Jiri Pikula (J)

Department of Ecology & Diseases of Zoo Animals, Game, Fish and Bees, University of Veterinary Sciences Brno, Brno, Czech Republic.

Vladimir Piacek (V)

Department of Ecology & Diseases of Zoo Animals, Game, Fish and Bees, University of Veterinary Sciences Brno, Brno, Czech Republic.

Tomas Heger (T)

Department of Ecology & Diseases of Zoo Animals, Game, Fish and Bees, University of Veterinary Sciences Brno, Brno, Czech Republic.

Kristyna Hrazdilova (K)

CEITEC-Central European Institute of Technology, University of Veterinary Sciences Brno, Brno, Czech Republic.
Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Plzeň, Czech Republic.

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