Hostname: page-component-745bb68f8f-b6zl4 Total loading time: 0 Render date: 2025-01-23T12:06:50.421Z Has data issue: false hasContentIssue false

Molecular evidence of Macracanthorhynchus hirudinaceus (Pallas, 1781) in cockchafers in rural areas of Elazig, Türkiye

Published online by Cambridge University Press:  20 January 2025

F. Celik
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, University of Firat, 23119, Elazig, Türkiye
A.S. Tekin
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, University of Firat, 23119, Elazig, Türkiye Department of Parasitology, Faculty of Veterinary Medicine, Cukurova University, Adana, Türkiye
M. Uslug
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, University of Firat, 23119, Elazig, Türkiye
S. Simsek*
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, University of Firat, 23119, Elazig, Türkiye
*
Corresponding author: S. Simsek; Email: [email protected]

Abstract

The primary definitive host of the giant acanthocephalan, also known as the giant thorny-headed worm Macracanthorhynchus hirudinaceus (Pallas, 1781), is Sus scrofa. The definitive host ingests the parasite by consuming infected scarabaeoid or hydrophilid beetles. This study aimed to ascertain the presence of M. hirudinaceus in the intermediate hosts through molecular analysis. The cockchafers were collected from Elazig province of Türkiye. A total of 30 pools, comprising 10 pools for each of three districts were obtained from cockchafers collected from 10 areas. The gDNA was isolated and PCR was conducted using specific primers which amplify the mitochondrial cytochrome c oxidase subunit 1 (mt-CO1) gene of M. hirudinaceus. Then, the PCR-positive samples were sequenced, and phylogenetic and haplotype analyses were performed. A total of 300 cockchafer adults and/or larvae were collected for this study from different regions of three districts (Sivrice, Baskil, and Keban) in Elazig province of Türkiye. No PCR band was observed in any of the samples in Sivrice (0%). However, a total of 16 samples (5.3%), 10 from the Baskil (10%) and 6 from Keban (6%), showed a PCR band of 491 bp. All sequences were confirmed as M. hirudinaceus. Two distinct haplotypes were detected at two points. Of the total number of sequences, twelve were found to consist of a single haplotype. One of the two haplotypes was comprised of 10 isolates, while the other included six isolates. This study is one of the limited studies on the molecular identification and haplotyping of M. hirudinaceus in cockchafers.

Type
Research Paper
Copyright
© The Author(s), 2025. 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

Acevedo, P, Vicente, J, Höfle, U, Cassinelo, J and Ruiz-Fons, F (2006) Estimation of European wild boar relative abundance and aggregation: A novel method in epidemiological risk assessment. Epidemiology and Infection 135, 519527. http://doi.org/10.1017/S0950268806007059CrossRefGoogle ScholarPubMed
Akkoc, N, Kuruuzum, Z, Akar, S, Yuce, A, Onen, F, Yapar, N, … and Izmir Trichinellosis Outbreak Study Group (2009) A large‐scale outbreak of trichinellosis caused by Trichinella britovi in Turkey. Zoonoses and Public Health 56(2), 6570.CrossRefGoogle ScholarPubMed
Amayour, A, El Alaqui, Z, Alkhali, A, Hassouni, T, Elkharrim, K and Belghyti, D (2017) Presence of very high prevalence of Macracanthorhynchus hirudinaceus infection in Wild Boars (Sus scrofa Barbarus) in El Hajeb province, Middle Atlas, Morocco. Journal of Entomology and Zoology Studies 5(2), 17841787.Google Scholar
Barbosa, JD, Silva, JB, Reis, ASB, Bomjardim, HA and Driemeier, D (2017) Identification of Macracanthorhynchus hirudinaceus, Stephanurus dentatus and Trichuris suis in native pigs of Marajó Island. Journal of Veterinary Science & Medical Diagnosis 6, 4. https://doi.org/10.4172/2325-9590.1000237CrossRefGoogle Scholar
Brianti, E, Gaglio, G, Ferlazzo, M, Abbene, S, Poglayen, G and Gianetto, S (2007) A review of parasites found in the Sicilian Black Pig. Proceedings of the 6th International Symposium on the Mediterranean Pig. Messina – Capo d’Orlando (ME), Italy, 11–13 October 2007.Google Scholar
Celik, F, Gunyakti Kilinc, S, Ceribasi, S, Kesik, HK and Simsek, S (2024) First histopathological and molecular characterization of giant thorny-headed worm, Macracanthorhynchus hirudinaceus (Pallas, 1781) (Acanthocephala: Oligacanthorhynchidae) in wild boars, Sus scrofa Linnaeus, 1758 from eastern Türkiye. Acta Parasitologica 69(3), 16401647. https://doi.org/10.1007/s11686-024-00873-4CrossRefGoogle ScholarPubMed
Coghlan, A, Tyagi, R, Cotton, JA, Holroyd, N, Rosa, BA, Tsai, IJ, Laetsch, DR, Beech, RN, Day, TA, Hallsworth-Pepin, K, Ke, HM, Kuo, TH, Lee, TJ, Martin, J, Maizels, RM, Mutowo, P, Ozersky, P,Parkinson, J,Reid, AJ, Rawlings, ND, Ribeiro, DM, Swapna, LS, Stanley, E, Taylor, DW, Wheeler, NJ, Zamanian, M, Zhang, X, Allan, F, Allen, JE, Asano, K, Babayan, SA, Bah, G, Beasley, H, Bennett, HM, Bisset, SA, Castillo, E, Cook, J, Cooper, PJ, Cruz-Bustos, T, Cuellar, C, Devaney, E, Doyle, SR, Eberhard, ML, Emery, A, Eom, KS, Gilleard, JS, Gordon, D, Harcus, Y, Harsha, B, Hawdon, JM, Hill, DE, Hodgkinson, J, Horak, P, Howe, KL, Huckvale, T, Kalbe, M, Kaur, G, Kikuchi, T, Koutsovoulos, G, Kumar, S, Leach, AR, Lomax, J, Makepeace, B, Matthews, JB, Muro, A, O’Boyle, NM, Olson, PD, Osuna, A, Partono, F, Pfarr, K, Rinaldi, G, Foronda, P, Rollinson, D, Samblas, MG, Sato, H, Schnyder, M, Scholz, T, Shafie, M, Tanya, VN, Toledo, R, Tracey, A, Urban, JF, Wang, LC, Zarlenga, D, Blaxter, ML, Mitreva, M and Berriman, M (2019) Comparative genomics of the major parasitic worms. International Helminth Genomes Consortium. Nature Genetics 51, 163174. https://doi.org/10.1038/s41588-018-0262-1Google Scholar
de Estrada, MBF (1997) Presentación del primer caso humano de parasitismo por Macracanthorhynchus hirudinaceus en el Perú y breve revisión. Revista Peruana de Medicina Experimental y Salud Pública. Revista Peruana de Medicina Experimental y Salud Pública 14, 4750.Google Scholar
Fu, YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915925.CrossRefGoogle ScholarPubMed
Gassó, D, Serrano, E, Castillo-Contreras, R, Fernández Aguilar, X, Colom Cadena, A, Velarde, R, Mentaberre, G, López-Olvera, JR, Risco, D, Gonçalves, P, Lavín, S, Fernandez-Llário, P, Segalés, J and Ferrer, D (2016) Coprological tests underestimate Macracanthorhynchus hirudinaceus burden in wild boar. Parasitology Research 115, 21032105. https://doi.org/10.1007/s00436-016-4976-7CrossRefGoogle ScholarPubMed
Kennedy, CR (2006) Ecology of Acanthocephala. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
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. https://doi.org/10.1093/molbev/msy096CrossRefGoogle ScholarPubMed
Leigh, J, Bryant, D and Steel, M (2015) PopART (Population Analysis with Reticulate Trees). Technical report, University of Otago, New Zealand, http://popart.otago.ac.nz.Google Scholar
Mansouri, M, Sarkari, B and Mowlavi, GR (2016) Helminth parasites of wild boars, Sus scrofa, in Bushehr province, Southwestern Iran. Iranian Journal of Parasitology 11(3), 377382.Google ScholarPubMed
Masuda, JI, Yano, K, Tamada, Y, Takii, Y, Ito, M, Omagari, K and Kohno, S (2005). Acute hepatitis E of a man who consumed wild boar meat prior to the onset of illness in Nagasaki, Japan. Hepatology Research 31(3), 178183.CrossRefGoogle Scholar
Mehlhorn, H (2016) Macracanthorhynchus hirudinaceus. In Mehlhorn, H (ed), Encyclopedia of Parasitology. Chapter 5. Berlin: Springer. doi: 10.1007/978-3-662-43978-4_1810.CrossRefGoogle Scholar
Merdivenci, A (1964) Türkiye’de evcil domuzlarda Macracanthorhynchus hirudinaceus. Veteriner Hekimler Derneği Dergisi 34(3–4), 131135.Google Scholar
Migliore, S, Puleio, R, Gaglio, G, Vicari, D, Seminara, S, Sicilia, ER, Galluzo, P, Cumbo, V and Loria, GR (2021) A neglected parasite: Macracanthorhynchus hirudinaceus, first report in feral pigs in a Natural Park of Sicily (Southern Italy). Frontiers in Veterinary Science 8, 659306. https://doi.org/10.3389/fvets.2021.659306CrossRefGoogle Scholar
Moore, DV (1942) Studies on the Life History and Development of Certain Acanthocephala of the Order Archiacanthocephala (Meyer, 1931). Thesis, University of Nebraska.Google Scholar
Mowlavi, G, Massoud, J, Mobedi, I, Solaymani-Mohammadi, S, Gharagozlou, M and Mas-Coma, S (2006) Very highly prevalent Macracanthorhynchus hirudinaceus infection of wild boar Sus scrofa in Khuzestan province, south-western Iran. Helminthologia 43, 8691. https://doi.org/10.2478/s11687-006-0017-xCrossRefGoogle Scholar
Nagy, G, Csivincsik, Á, Ács, K, Varga, G and Sugár, L (2015) Macracanthorhynchus hirudinaceus (Pallas, 1781) larvae in cockchafer (Melolontha spp.) grubs in different habitat conditions. European Journal of Wildlife Research 61, 487489. https://doi.org/10.1007/s10344-015-0910-zCrossRefGoogle Scholar
Papini, RA, Vannucci, S, Rocchigiani, G, Nardoni, S and Mancianti, F (2018) Prevalence of and potentially zoonotic helminths in wild boars hunted in Central Italy. Macedonian Veterinary Review 41(1), 8393. https://doi.org/10.2478/macvetrev-2018-0012CrossRefGoogle Scholar
Pavlović, IN, Kulišić, ZB, Tambur, and Protić, NM (2010) Scarabaeidae-intermediate host for Macracanthorhynchus hirudinaceus. Proceedings of the National Academy of Sciences 119, 8995. https://doi.org/10.2298/ZMSPN1019089PGoogle Scholar
Rana, A, Chandel, RS and Verma, KS (2022) Morphological description and identification of Melolontha cuprescens, Melolontha furcicauda and Melolontha indica (Coleoptera: Scarabaeidae): Serious root feeding and defoliating pests in India. Phytoparasitica 50 (2), 281305. https://doi.org/10.1007/s12600-021-00961-5CrossRefGoogle Scholar
Rozas, J, Ferrer-Mata, A, Sánchez-DelBarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Sánchez-Gracia, A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34(12), 32993302. https://doi.org/10.1093/molbev/msx248.CrossRefGoogle ScholarPubMed
Ruiz-Fons, F, Segalés, J and Gortázar, C (2008) A review of viral diseases of the European wild boar: Effects of population dynamics and reservoir role. The Veterinary Journal 176, 158169. https://doi.org/10.1016/j.tvjl.2007.02.017CrossRefGoogle ScholarPubMed
Sarkari, B, Mansouri, M, Najjari, M, Derakhshanfar, A and Mowlavi, GR (2016) Macracanthorhynchus hirudinaceus: The most common helminthic infection of wild boars in southwestern Iran. Journal of Parasitic Diseases 40, 15631566. https://doi.org/10.1007/s12639-015-0728-3CrossRefGoogle ScholarPubMed
Schmidt, GD (1985) Development and life cycle. In Crompton, DWT and Nicol, BB (eds), Biology of Acanthocephalan. Cambridge: Cambridge University Press, 273305.Google Scholar
Senlik, B, Cirak, VY, Girisgin, O and Akyol, CV (2011) Helminth infections of wild boars (Sus scrofa) in the Bursa province of Turkey. Journal of Helminthology 85(4), 404408. https://doi.org/10.1017/s0022149x1000074xCrossRefGoogle ScholarPubMed
Sorensen, A, van Beest, FM and Brook, RK (2013) Impacts of wildlife baiting and supplemental feeding on infectious disease transmission risk: A synthesis of knowledge. Preventive Veterinary Medicine 113(4), 356363. https://doi.org/10.1016/j.prevetmed.2013.11.010CrossRefGoogle Scholar
Stilesi, CW (1891) Echinorhynchus gigas and its intermediates hosts. The Journal of Comparative Medicine and Veterinary Archives 12, 657661.Google Scholar
Svetska, M (2006) Distribution of tribes of cockchafers of the genus Melolontha in forests of the Czech Republic and the dependence of their swarming on temperature. Journal of Forest Science 52, 520530. https://doi.org/10.17221/4532-JFSGoogle Scholar
Tajima, F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3), 585595.CrossRefGoogle ScholarPubMed
Taylor, MA, Coop, RL and Wall, RL (2015) Veterinary Parasitology, 4th edn. Chichester: Wiley Blackwell.CrossRefGoogle Scholar
Ucarli, Y (2011) Effects of wild boar (Sus scrofa) on farming activities: A case study of Turkey. African Journal of Biotechnology 10(44), 88238828. https://doi.org/10.5897/AJB10.2698Google Scholar
Wilson, CJ (2005) Feral wild boar in England. Status, impact and management. In A Report on Behalf of Defra European Wildlife Division. London: Department for Environment, Food and Rural Affairs, 47.Google Scholar