Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T11:52:04.739Z Has data issue: false hasContentIssue false

Trypanosoma (Megatrypanum) pestanai in Eurasian badgers (Meles meles) and Ixodidae ticks, Italy

Published online by Cambridge University Press:  05 July 2021

Giovanni Sgroi
Affiliation:
Department of Veterinary Medicine, University of Bari, 70010 Valenzano, Italy
Roberta Iatta
Affiliation:
Department of Veterinary Medicine, University of Bari, 70010 Valenzano, Italy
Riccardo Paolo Lia
Affiliation:
Department of Veterinary Medicine, University of Bari, 70010 Valenzano, Italy
Maria Stefania Latrofa
Affiliation:
Department of Veterinary Medicine, University of Bari, 70010 Valenzano, Italy
Rossella Samarelli
Affiliation:
Department of Veterinary Medicine, University of Bari, 70010 Valenzano, Italy
Antonio Camarda
Affiliation:
Department of Veterinary Medicine, University of Bari, 70010 Valenzano, Italy Osservatorio Faunistico Regionale della Puglia, 70020 Bitetto, Italy
Domenico Otranto*
Affiliation:
Department of Veterinary Medicine, University of Bari, 70010 Valenzano, Italy Faculty of Veterinary Sciences, Bu-Ali Sina University, Hamedan, Iran
*
Author for correspondence: Domenico Otranto, E-mail: [email protected]

Abstract

Trypanosomes are haemoflagellate protozoa transmitted by blood-feeding arthropods causing infections in a wide range of mammals, including humans. Adult badgers (Meles meles, n = 2), displaying severe paralysis, ataxia and severe ectoparasite infestation, were rescued from a peri-urban area of Bari (southern Italy). Blood samples and ectoparasites were screened for Trypanosoma spp. by the combined PCR/sequencing approach, targeting a fragment of 18S rRNA gene. Smears of haemolymph, guts and salivary glands of the alive ticks were microscopically observed. No haematological alterations, except thrombocytopenia, were found. Trypomastigotes and epimastigotes were observed in the blood smears of both badgers and Trypanosoma pestanai was molecularly identified. Out of 33 ticks (i.e. n = 31 Ixodes canisuga, n = 2 Ixodes ricinus) and two fleas (Ctenocephalides felis), 11 specimens (n = 5 I. canisuga engorged nymphs, n = 4 engorged females and n = 2 I. ricinus engorged females) tested positive only for T. pestanai DNA. All smears from ticks were negative. The present study firstly revealed T. pestanai in Ixodidae and badgers from Italy, demonstrating the occurrence of the protozoan on the peninsula. Further studies are needed to clarify the occurrence of the only known vector of this parasite, Paraceras melis flea, as well as other putative arthropods involved in the transmission of T. pestanai.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. 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

Aeschlimann, A, Burgdorfer, W, Malile, H, Peter, O and Wyler, R (1979) Aspects nouveaux du role de vecteur joué par lxodes ricinus L. en Suisse. Note préliminaire. Acta Tropica 36, 181191.Google Scholar
Ancillotto, L, Mazza, G, Menchetti, M and Mori, E (2014) Host specificity of the badger's flea (Paraceras melis) and first detection on a bat host. Parasitology Research 113, 39093912.CrossRefGoogle ScholarPubMed
Aregawi, WG, Agga, GE, Abdi, RD and Büscher, P (2019) Systematic review and meta-analysis on the global distribution, host range, and prevalence of Trypanosoma evansi. Parasites & Vectors 12, 67.CrossRefGoogle ScholarPubMed
Baker, PJ and Harris, S (2007) Urban mammals: what does the future hold? An analysis of the factors affecting patterns of use of residential gardens in Great Britain. Mammal Review 37, 297315.Google Scholar
Battisti, B, Zanet, S, Khalili, S, Trisciuoglio, A, Hertel, B and Ferroglio, E (2020) Molecular survey on vector-borne pathogens in alpine wild carnivorans. Frontiers in Veterinary Science 7, 1.CrossRefGoogle ScholarPubMed
Beaucournu, JC and Launay, H (1990) Les Puces de France et du Bassin Méditérranéen Occidental. Faune de France n° 76. Paris, FR: Fédération Française des Sociétés de Sciences naturelles.Google Scholar
Bezerra-Santos, MA, Nascimento Ramos, RA, Campos, AK, Dantas-Torres, F and Otranto, D (2021a) Didelphis spp. opossums and their parasites in the Americas: a One Health perspective. Parasitology Research. doi: 10.1007/s00436-021-07072-4CrossRefGoogle ScholarPubMed
Bezerra-Santos, MA, Mendoza-Roldan, JA, Thompson, RCA, Dantas-Torres, F and Otranto, D (2021b) Illegal wildlife trade: a gateway to zoonotic infectious diseases. Trends in Parasitology 37, 181184.CrossRefGoogle ScholarPubMed
Bezerra-Santos, MA, Mendoza-Roldan, JA, Thompson, RCA, Dantas-Torres, F and Otranto, D (2021c) Legal versus illegal wildlife trade: zoonotic disease risks. Trends in Parasitology 37, 360361.CrossRefGoogle ScholarPubMed
Bishop, CF (1911) Notes on a trypanosome, found in sheep tick, and its probable connection with the disease known as louping-ill. The Veterinary Journal 67, 709715.Google Scholar
Buscher, G and Friedhoff, KT (1984) The morphology of ovine Trypanosoma melophagium (Zoomastigophorea: Kinetoplastida). The Journal of Protozoology 31, 98101.CrossRefGoogle ScholarPubMed
da S. Ferreira, JIG, da Costa, AP, Ramirez, D, Roldan, JAM, Saraiva, D, da S. Founier, GFR, Sue, A, Zambelli, ER, Minervino, AHH, Verdade, VK, Gennari, SM and Marcili, A (2015) Anuran trypanosomes: phylogenetic evidence for new clades in Brazil. Systematic Parasitology 91, 6370.CrossRefGoogle ScholarPubMed
Desquesnes, M (2004) Livestock Trypanosomoses and Their Vectors in Latin America. Paris, FR: World Organisation for Animal Health.Google Scholar
Desquesnes, M, Dargantes, A, Lai, DH, Lun, ZR, Holzmuller, P and Jittapalapong, S (2013) Trypanosoma evansi and Surra: a review and perspectives on transmission, epidemiology and control, impact, and zoonotic aspects. BioMed Research International 2013, 321237.CrossRefGoogle Scholar
Dirie, MF, Wallbanks, KR, Aden, AA, Bornstein, S and Ibrahim, MD (1989) Camel trypanosomiasis and its vectors in Somalia. Veterinary Parasitology 32, 285291.CrossRefGoogle ScholarPubMed
Dunn, N, Wang, S and Adigun, R (2020) African Trypanosomiasis. Retrieved from StatPearls Publishing. Available at https://www.ncbi.nlm.nih.gov/books/NBK519580/ (Accessed 10 August 2020).Google Scholar
Dyachenko, V, Steinmann, M, Bangoura, B, Selzer, M, Munderloh, U, Daugschies, A and Barutzki, D (2017) Co-infection of Trypanosoma pestanai and Anaplasma phagocytophilum in a dog from Germany. Veterinary Parasitology: Regional Studies and Reports 9, 110114.Google Scholar
Elmayan, A, Tu, W, Duhon, B, Marx, P, Wolfson, W, Balsamo, G, Herrera, C and Dumonteil, E (2019) High prevalence of Trypanosoma cruzi infection in shelter dogs from southern Louisiana, USA. Parasites & Vectors 12, 322.CrossRefGoogle ScholarPubMed
Eloy, LJ and Lucheis, SB (2009) Canine trypanosomiasis: etiology of infection and implications for public health. Journal of Venomous Animals and Toxins including Tropical Diseases 15, 589611.CrossRefGoogle Scholar
Estrada-Peña, A, Mihalca, AD and Petney, TN (2017) Ticks of Europe and North Africa: A Guide to species Identification. Cham, CH: Springer NatureCrossRefGoogle Scholar
Gern, L, Toutoungi, LN, Hu, CM and Aeschlimann, A (1991) Ixodes (Pholeoixodes) hexagonus, an efficient vector of Borrelia burgdorferi in the laboratory. Medical and Veterinary Entomology 5, 431435.CrossRefGoogle ScholarPubMed
Golding, N (2013) Review of ‘Trypanosomes and Trypanosomiasis’ by Stefan Magez and Magdalena Radwanska (Editors). Parasites & Vectors 6, 365.CrossRefGoogle Scholar
Gürtler, RE and Cardinal, MV (2015) Reservoir host competence and the role of domestic and commensal hosts in the transmission of Trypanosoma cruzi. Acta Tropica 151, 3250.CrossRefGoogle ScholarPubMed
Hamill, LC, Kaare, MT, Welburn, SC and Picozzi, K (2013) Domestic pigs as potential reservoirs of human and animal trypanosomiasis in Northern Tanzania. Parasites & Vectors 6, 322.CrossRefGoogle ScholarPubMed
Hofmeester, TR, Krawczyk, AI, van Leeuwen, AD, Fonville, M, Montizaan, MGE, van den Berge, K, Gouwy, J, Ruyts, SC, Verheyen, K and Sprong, H (2018) Role of mustelids in the life-cycle of ixodid ticks and transmission cycles of four tickborne pathogens. Parasites & Vectors 11, 600.CrossRefGoogle Scholar
Ideozu, EJ, Whiteoak, AM, Tomlinson, AJ, Robertson, A, Delahay, RJ and Hide, G (2015) High prevalence of trypanosomes in European badgers detected using ITs-PRC. Parasites & Vectors 8, 480.CrossRefGoogle Scholar
Kalyaanamoorthy, S, Minh, BQ, Wong, TKF, von Haeseler, A and Jermiin, LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587589.CrossRefGoogle ScholarPubMed
Karbowiak, G, Wita, I and Czaplińska, U (2009) The occurrence and ultrastructure of Trypanosoma (Herpetosoma) lewisi (Kent, 1880) Laveran and Mesnil, 1901, the parasite of rats (Rattus norvegicus) in Poland. Wiadomości parazytologiczne 55, 249258.Google ScholarPubMed
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 and Drummond, A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 16471649.Google ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 15471549.CrossRefGoogle ScholarPubMed
Linhart, P, Bandouchova, H, Zukal, J, Votypka, J, Kokurewicz, T, Dundarova, H, Apoznanski, G, Heger, T, Kubickova, A, Nemcova, M, Piacek, V, Sedlackova, J, Seidlova, V, Berkova, H, Hanzal, V and Pikula, J (2020) Trypanosomes in Eastern and Central European bats. Acta Veterinaria Brno 89, 6978.CrossRefGoogle Scholar
Lizundia, R, Newman, C, Buesching, CD, Ngugi, D, Blake, D, Sin, YW, Macdonald, DW, Wilson, A and McKeever, D (2011) Evidence for a role of the host-specific flea (Paraceras melis) in the transmission of Trypanosoma (Megatrypanum) pestanai to the European badger. PLoS ONE 6, e16977.CrossRefGoogle Scholar
Luu, L, Bown, KJ, Palomar, AM, Kazimírová, M and Bell-Sakyi, L (2020) Isolation and partial characterisation of a novel Trypanosoma from the tick Ixodes ricinus. Ticks and Tick-borne Diseases 11, 101501.CrossRefGoogle ScholarPubMed
McCarthy, G, Shiel, R, O'Rourke, L, Murphy, D, Corner, L, Costello, E and Gormley, E (2009) Bronchoalveolar lavage cytology from captive badgers. Veterinary Clinical Pathology 38, 381387.CrossRefGoogle ScholarPubMed
Mei, M (1996) Nuovi dati corologici su alcuni sifonatteri della fauna Italiana. Fragmenta Entomologica 27, 253553.Google Scholar
Mendoza-Roldan, J, Ribeiro, SR, Castilho-Onofrio, V, Grazziotin, FG, Rocha, B, Ferreto-Fiorillo, B, Pereira, JS, Benelli, G, Otranto, D and Barros-Battesti, DM (2020) Mites and ticks of reptiles and amphibians in Brazil. Acta Tropica 208, 105515.CrossRefGoogle ScholarPubMed
Minh, BQ, Nguyen, AT and von Haeseler, A (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30, 11881195.CrossRefGoogle ScholarPubMed
Mori, E, Sforzi, A, Menchetti, M, Mazza, G, Lovari, S and Pisanu, B (2015) Ectoparasite load in the crested porcupine Hystrix cristata Linnaeus, 1758 in Central Italy. Parasitology Research 114, 22232229.CrossRefGoogle ScholarPubMed
Murphy, M, Macchiaverna, NP, Cardinal, MV, Bhattacharyya, T, Mertens, P, Zeippen, N, Gustin, Y, Gilleman, Q, Gürtler, RE and Miles, MA (2019) Lineage-specific rapid diagnostic tests can resolve Trypanosoma cruzi TcII/V/VI ecological and epidemiological associations in the Argentine Chaco. Parasites & Vectors 12, 424.CrossRefGoogle ScholarPubMed
Neumüller, M, Nilsson, K and Påhlson, K (2012) Trypanosoma spp. in Swedish game animals. Parasitology Research 110, 135139.CrossRefGoogle ScholarPubMed
Nguyen, LT, Schmidt, HA, von Haeseler, A and Minh, BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution 32, 268274.CrossRefGoogle ScholarPubMed
Otranto, D, Cantacessi, C, Dantas-Torres, F, Brianti, E, Pfeffer, M, Genchi, C, Guberti, V, Capelli, G and Deplazes, P (2015) The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part II: Helminths and arthropods. Veterinary Parasitology 213, 2437.CrossRefGoogle ScholarPubMed
Peirce, MA and Neal, C (1974) Trypanosoma (Megatrypanum) pestanai in British badgers (Meles meles). International Journal for Parasitology 4, 439440.CrossRefGoogle ScholarPubMed
Piaton, E, Fabre, M, Goubin-Versini, I, Bretz-Grenier, MF, Courtade-Saïdi, M, Vincent, S, Belleannée, G, Thivolet, F, Boutonnat, J, Debaque, H, Fleury-Feith, J, Vielh, P, Cochand-Priollet, B, Egelé, C, Bellocq, JP and Michiels, JF (2015) [Technical recommendations and best practice guidelines for May-Grünwald-Giemsa staining: literature review and insights from the quality assurance]. Annales de Pathologie 35, 294330.CrossRefGoogle ScholarPubMed
Radwanska, M, Vereecke, N, Deleeuw, V, Pinto, J and Magez, S (2018) Salivarian trypanosomosis: a review of parasites involved, their global distribution and their interaction with the innate and adaptive mammalian host immune system. Frontiers in Immunology 9, 2253.CrossRefGoogle ScholarPubMed
Rioux, JA, Albaret, JL, Bres, A and Dumas, A (1966) Presence of Trypanosoma pestanai Bettencourt and Franca, 1905, in badgers from the south of France. Annales de Parasitologie Humaine et Comparée 41, 281288.CrossRefGoogle ScholarPubMed
Smit, FGAM (1957) Handbooks for The Identification of British Insects. Siphonaptera. London, UK: Royal Entomological Society of London.Google Scholar
Villa, A, Gutierrez, C, Gracia, E, Moreno, B, Chacon, G, Sanz, PV, Buscher, P and Touratier, L (2008) Presence of Trypanosoma theileri in Spanish cattle. Annals of the New York Academy of Sciences 1149, 352354.CrossRefGoogle ScholarPubMed
Waiswa, C, Olaho-Mukani, W and Katunguka-Rwakishaya, E (2003) Domestic animals as reservoirs for sleeping sickness in three endemic foci in south-eastern Uganda. Annals of Tropical Medicine & Parasitology 97, 149155.CrossRefGoogle ScholarPubMed
Zeb, J, Szekeres, S, Takács, N, Kontschán, J, Shams, S, Ayaz, S and Hornok, S (2019) Genetic diversity, piroplasms and trypanosomes in Rhipicephalus microplus and Hyalomma anatolicum collected from cattle in northern Pakistan. Experimental and Applied Acarology 79, 233243.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Sgroi et al. supplementary material

Figure S1

Download Sgroi et al. supplementary material(PDF)
PDF 629.8 KB