Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-19T16:34:57.879Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular detection of Trypanosoma spp. in Lipoptena cervi and Lipoptena fortisetosa (Diptera: Hippoboscidae) and their potential role in the transmission of pathogens

Published online by Cambridge University Press:  01 September 2020

Joanna Werszko Open the ORCID record for Joanna Werszko [Opens in a new window] ,
Żaneta Steiner-Bogdaszewska ,
Witold Jeżewski ,
Tomasz Szewczyk ,
Grzegorz Kuryło ,
Marek Wołkowycki ,
Piotr Wróblewski  and
Grzegorz Karbowiak
Joanna Werszko*
Affiliation:
Witold Stefański Institute of Parasitology, Polish Academy of Sciences, Twarda 51/55, 00-818, Warsaw, Poland
Żaneta Steiner-Bogdaszewska
Affiliation:
Witold Stefański Institute of Parasitology, Polish Academy of Sciences, Twarda 51/55, 00-818, Warsaw, Poland
Witold Jeżewski
Affiliation:
Witold Stefański Institute of Parasitology, Polish Academy of Sciences, Twarda 51/55, 00-818, Warsaw, Poland
Tomasz Szewczyk
Affiliation:
Witold Stefański Institute of Parasitology, Polish Academy of Sciences, Twarda 51/55, 00-818, Warsaw, Poland
Grzegorz Kuryło
Affiliation:
Institute of Forest Sciences, Faculty of Civil Engineering and Environmental Sciences, Białystok University of Technology, Wiejska 45e, 15-351, Białystok, Poland
Marek Wołkowycki
Affiliation:
Institute of Forest Sciences, Faculty of Civil Engineering and Environmental Sciences, Białystok University of Technology, Wiejska 45e, 15-351, Białystok, Poland
Piotr Wróblewski
Affiliation:
Witold Stefański Institute of Parasitology, Polish Academy of Sciences, Twarda 51/55, 00-818, Warsaw, Poland
Grzegorz Karbowiak
Affiliation:
Witold Stefański Institute of Parasitology, Polish Academy of Sciences, Twarda 51/55, 00-818, Warsaw, Poland
*
Author for correspondence: Joanna Werszko, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The family Hippoboscidae is a less known group of blood-sucking flies. Deer ked are particularly important for animal health; they may act as potential vectors of disease to ungulates, and may transmit pathogens to animals and humans. The aim of this study was to investigate the presence of Trypanosoma (Megatrypanum) DNA in deer keds using molecular methods. Results prove the presence of Megatrypanum trypanosome DNA in the studied winged adult deer keds and this is the first detection of this pathogen in Lipoptena fortisetosa. In addition, this paper evidences the occurrence of L. fortisetosa in two new locations: one in the Białowieża Primeval Forest, and another in the Strzałowo Forest Inspectorate (Piska Forest), both in north-eastern Poland.

Keywords

HippoboscidaeLipoptena cerviLipoptena fortisetosaMegatrypanumTrypanosoma
Type
Review Article
Information
Parasitology , Volume 147 , Issue 14 , December 2020 , pp. 1629 - 1635
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andreani, A, Sacchetti, P and Belcari, A (2019) Comparative morphology of the deer keds Lipoptena fortisetosa first recorded from Italy. Medical and Veterinary Entomology 33, 140–153.CrossRefGoogle ScholarPubMed
Bartoš, L (2009) Chapter 39. Sika deer in continental Europe. In McCullough, DR, Takatsuki, S and Kaji, K (eds), Sika Deer: Biology and Management of Native and Introduced Populations. Springer, pp. 573–594. doi: 10.1007/978-4-431-09429-6_39.CrossRefGoogle Scholar
Billeter, SA, Levy, MG, Chomel, BB and Breitschwerdt, EB (2008) Vector transmission of Bartonella species with emphasis on the potential for tick transmission. Medical and Veterinary Entomology 22, 1–15.CrossRefGoogle ScholarPubMed
Borowiec, L (1984) Wpleszczowate – Hippoboscidae. Klucze do oznaczania owadów Polski Cz. 28, z. 21. Wydawnictwo PWN, Warszawa.Google Scholar
Borowiec, L and Zatwarnicki, T (1989) Lipoptena fortisetosa Maa, 1965 (Diptera, Hippoboscidae), nowy gatunek dla fauny Polski. Przegląd Zoologiczny 33, 579–582.Google Scholar
Böse, R and Petersen, K (1991) Lipoptena cervi (Diptera), a potential vector of Megatrypanum trypanosomes of deer (Cervidae). Parasitology Research 77, 723–725.CrossRefGoogle Scholar
Böse, R, Friedhoff, KT and Olbrich, S (1987) Transmission of Trypanosoma theileri to cattle by Tabanidae. Parasitology Research 73, 421–424.CrossRefGoogle ScholarPubMed
Dehio, C, Lanz, C, Pohl, R, Behrens, P, Bermond, D, Piemont, Y, Pelz, K and Sander, A (2001) Bartonella Schoenbuchii sp. nov., isolated from the blood of wild roe deer. International Journal Systematic Evolutionary Microbiology 51, 1557–1565.CrossRefGoogle ScholarPubMed
Dehio, C, Sauder, U and Hiestand, R (2004) Isolation of Bartonella schoenbuchensis from Lipoptena cervi, a blood-sucking arthropod causing deer ked dermatitis. Journal of Clinical Microbiology 42, 5320–5323.CrossRefGoogle ScholarPubMed
De La Fuente, J, Naranjo, V, Ruiz-Fons, F, Höfle, U, Fernández De Mera, IG, Villanúa, D, Almazán, C, Torina, A, Caracappa, S, Kocan, KM and Gortázar, C (2005) Potential vertebrate reservoir hosts and invertebrate vectors of Anaplasma marginale and A. phagocytophilum In Central Spain. Vector Borne and Zoonotic Diseases 5, 390–401.CrossRefGoogle Scholar
Demiaszkiewicz, AW and Lachowicz, J (1991) Trypanosoma theileri Laveran, 1902 – pasożytem bydła w Polsce. Medycyna Weterynaryjna 47, 112–113.Google Scholar
Dick, CW (2006). Checklist of World Hippoboscidae (Diptera: Hippoboscoidea), Chicago: Department of Zoology, Field Museum of Natural History, pp. 1–7.Google Scholar
Duodu, S, Madslien, K, Hjelm, E, Molin, Y, Paziewska-Harris, A, Harris, PD, Colquhoun, DJ and Ytrehus, B (2013) Bartonella infections in deer keds (Lipoptena cervi) and moose (Alces alces) in Norway. Applied and Environmental Microbiology 79, 322–327.CrossRefGoogle ScholarPubMed
Garcia, H, Kamyingkird, K, Rodrigues, AC, Jittapalapong, S, Teixeira, MMG and Desquesnes, M (2011 a) High genetic diversity in field isolates of Trypanosoma theileri assessed by analysis of cathepsin L-like sequences disclosed multiple and new genotypes infecting cattle in Thailand. Veterinary Parasitology 17, 363–367.CrossRefGoogle Scholar
Garcia, HA, Rodrigues, AC, Martinković, F, Minervino, AH, Campaner, M, Nunes, VL, Paiva, F, Hamilton, PB and Teixeira, MM (2011 b) Multilocus phylogeographical analysis of Trypanosoma (Megatrypanum) genotypes from sympatric cattle and water buffalo populations supports evolutionary host constraint and close phylogenetic relationships with genotypes found in other ruminants. International Journal for Parasitology 41, 1385–1396.CrossRefGoogle ScholarPubMed
Haarløv, N (1964) Life cycle and distribution pattern of Lipoptena cervi (L.) (Dipt, Hippobosc.) on Danish deer. Oikos 15, 93–129.CrossRefGoogle Scholar
Halos, L, Jamal, T, Maillard, R, Girard, B, Guillot, J, Chomel, B, Vayssier-Taussat, M and Boulouis, HJ (2004) Role of Hippoboscidae flies as potential vectors of Bartonella spp. infecting wild and domestic ruminants. Applied and Environmental Microbiology 70, 6302–6305.CrossRefGoogle Scholar
Härkönen, S, Laine, M, Vornanen, M and Renuala, T (2009) Deer ked (Lipoptena cervi) dermatitis in humans an increasing nuisance in Finland. Alces 45, 73–79.Google Scholar
Hermosilla, C, Pantchev, N, Bachmann, R and Bauer, C (2006) Lipoptena cervi (deer ked) in two naturally infested dogs. Veterinary Research 159, 286–288.Google ScholarPubMed
Hoare, CA (1972) The Trypanosomes of Mammals. Oxford and Edinburgh: Blackwell Scientific Publications.Google Scholar
Karbowiak, G, Wita, I and Rychlik, L (2005) Trypanosoma (Megatrypanum) ornata sp. n., a parasite of the Eurasian water shrew Neomys fodiens (Pennant, 1771). Acta Protozoologica 44, 363–367.Google Scholar
Karbowiak, G, Demiaszkiewicz, AW, Pyziel, AM, Wita, I, Moskwa, B, Werszko, J, Bień, J, Goździk, K, Lachowicz, J and Cabaj, W (2014) The parasitic fauna of the European bison (Bison bonasus) (Linnaeus, 1758) and their impact on the conservation. Part 1. The summarising list of parasites noted. Acta Parasitologica 59, 363–371.Google ScholarPubMed
Kingston, N, Bobek, B, Perzanowski, K, Wita, I and Maki, L (1992) Description of Trypanosoma (Megatrypanum) stefanskii sp. n. from roe deer (Capreolus capreolus) in Poland. Journal of the Helminthological Society of Washington 59, 89–95.Google Scholar
Korhonen, EM, Pérez Vera, C, Pulliainen, AT, Sironen, T, Aaltonen, K, Kortet, R, Härkönen, L, Härkönen, S, Paakkonen, T, Nieminen, P, Mustonen, AM, Ylönen, H and Vapalahti, O (2015) Molecular detection of Bartonella spp. in deer ked pupae, adult keds and moose blood in Finland. Epidemiology and infection 143, 578–585.CrossRefGoogle ScholarPubMed
Kortet, R, Harkonen, L, Hokkanen, P, Harkonen, S, Kaitala, A, Kaunisto, S, Laaksonen, S, Kekalainen, J and Ylonen, H (2010) Experiments on the ectoparasitic deer ked that often attacks humans; preferences for body parts, colour and temperature. Bulletin of Entomological Research 100, 279–285.CrossRefGoogle ScholarPubMed
Kowal, J, Nosal, P, Rościszewska, M and Matysek, M (2009) New records of Lipoptena fortisetosa Maa, 1965 (Diptera: Hippoboscidae) in Poland. Dipteron 25, 27–29.Google Scholar
Kowal, J, Nosal, P, Kornaś, S, Wajdzik, M, Matysek, M and Basiaga, M (2016) Różnorodność i znaczenie muchówek z rodziny narzępikowatych – pasożytów jeleniowatych. Medycyna Weterynaryjna 72, 745–749.CrossRefGoogle Scholar
Kurina, O, Kirik, H, Õunap, H and Õunap, E (2019) The northernmost record of a blood-sucking ectoparasite, Lipoptena fortisetosa Maa (Diptera: Hippoboscidae), in Estonia. Biodiversity Data Journal 7, e47857.CrossRefGoogle Scholar
Lee, S-H, Kim, K-T, Kwon, O-D, Ock, Y, Kim, T, Choi, D and Kwak, D (2016) Novel detection of Coxiella spp., Theileria luwenshuni, and T. ovis endosymbionts in deer keds (Lipoptena fortisetosa). PLoS ONE 11, e0156727.CrossRefGoogle Scholar
Lipa, JJ (1968) Układ pasożyt-żywiciel u pierwotniaków pasożytujących w stawonogach I kręgowcach. Kosmos 17, 41–55.Google Scholar
Martinković, F, Matanović, K, Rodrigues, AC, Garcia, HA and Teixeira, MMG (2012) Trypanosoma (Megatrypanum) melophagium in the sheep ked Melophagus ovinus from organic farms in Croatia: phylogenetic inferences support restriction to sheep and sheep keds and close relationship with trypanosomes from other ruminant species. The Journal of Eukaryotic Microbiology 59, 134–144.CrossRefGoogle ScholarPubMed
Matsumoto, Y, Sato, A, Hozumi, M, Onishi, H, Kabeya, M, Sugawara, M and Takaishi, H (2011) A case of a Japanese black cow developing trypanosomosis together with enzootic bovine leucosis. Journal of the Japan Veterinary Medical Association 64, 941–945.CrossRefGoogle Scholar
Nelson, WA (1956) Mortality in the sheep ked, Melophagus ovinus (L.) caused by Trypanosoma melophagium. Nature 178, 750.CrossRefGoogle ScholarPubMed
Oboňa, J, Sychra, O, Greš, S, Heřman, P, Manko, P, Roháček, J, Šestáková, A, Šlapák, J and Hromada, M (2019) A revised annotated checklist of louse flies (Diptera, Hippoboscidae) from Slovakia. Zoo Keys 862, 129–152.Google ScholarPubMed
Petersen, FT (2013) Fauna Europaea: hippoboscidae. In Beuk, P and Pape, T (eds), Fauna Europaea: Diptera, Brachycera. Fauna Europaea. 2.6. https://fauna-eu.org.Google Scholar
Petersen, FT, Meier, R, Kutty, SN and Wiegmann, BM (2007) The phylogeny and evolution of host choice in the Hippoboscoidea (Diptera) as reconstructed using four molecular markers. Molecular Phylogenetics and Evolution 45, 111–122.CrossRefGoogle ScholarPubMed
Rahola, N, Goodman, SM and Robert, V (2011) The Hippoboscidae (Insecta: Diptera) from Madagascar, with new records from the ‘Parc National de Midongy Befotaka’. Parasite 18, 127–140.CrossRefGoogle Scholar
Rodrigues, AC, Garcia, HA, Batista, JS, Minervino, AH, Góes-Cavalcante, G, Maia da Silva, F, Ferreira, RC, Campaner, M, Paiva, F and Teixeira, MMG (2010 a) Characterization of spliced leader genes of Trypanosoma (Megatrypanum) theileri: phylogeographical analysis of Brazilian isolates from cattle supports spatial clustering of genotypes and parity with ribosomal markers. Parasitology 137, 111–122.CrossRefGoogle ScholarPubMed
Rodrigues, AC, Garcia, HA, Ortiz, PA, Cortez, AP, Martinkovic, F, Paiva, F, Batista, JS, Minervino, AH, Campaner, M, Pral, EM, Alfieri, SC and Teixeira, MMG (2010 b) Cysteine proteases of Trypanosoma (Megatrypanum) theileri: cathepsin L-like gene sequences as targets for phylogenetic analysis, genotyping diagnosis. Parasitology International 59, 318–325.CrossRefGoogle Scholar
Salvetti, M, Bianchi, A, Marangi, M, Barlaam, A, Giacomelli, S, Bertoletti, I, Roy, L and Giangaspero, A (2020) Deer keds on wild ungulates in northern Italy, with a taxonomic key for the identification of Lipoptena spp. of Europe. Medical and Veterinary Entomology 34, 74–85.CrossRefGoogle ScholarPubMed
Sokół, R and Gałęcki, R (2017) Prevalence of keds on city dogs in central Poland. Medical and Veterinary Entomology 31, 114–116.CrossRefGoogle ScholarPubMed
Sol, D, Jovani, R and Torres, J (2000) Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23, 307–314.CrossRefGoogle Scholar
Szewczyk, T, Werszko, J, Steiner-Bogdaszewska, Ż, Laskowski, Z and Karbowiak, G (2017) Molecular detection of Bartonella spp. in deer ked (Lipoptena cervi) in Poland. Parasites and Vectors 10, 487.CrossRefGoogle ScholarPubMed
Víchová, B, Majláthová, V, Nováková, M, Majláth, I, Čurlík, J, Bona, M and Peťko, B (2011) PCR detection of re-emerging tick-borne pathogen, Anaplasma phagocytophilum, in deer ked (Lipoptena cervi) a blood-sucking ectoparasite of cervids. Biologia 66, 1082.CrossRefGoogle Scholar
Werszko, J, Szewczyk, T, Steiner-Bogdaszewska, Ż, Wróblewski, P, Karbowiak, G and Laskowski, Z (2020) Molecular detection of Megatrypanum trypanosomes in tabanid flies. Medical and Veterinary Entomology 34, 69–73.CrossRefGoogle ScholarPubMed
Wita, I and Kingston, N (1999) Trypanosoma cervi in red deer, Cervus elaphus, in Poland. Acta Parasitologica 44, 93–98.Google Scholar
Wrublewski, KJ (1912) Die Trypanosomose (Schlafkrankheit) der Wisente. Zeitschrift fűr Infektionskrankheiten, parasitäre Krankheiten und Hygiene der Haustiere 12, 376–384.Google Scholar