Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-29T02:15:23.965Z Has data issue: false hasContentIssue false

Molecular phylogenetic relationships of Metastrongylus nematodes with emphasis on specimens from domestic pigs in Vietnam

Published online by Cambridge University Press:  06 September 2021

N.V. Tuyen
Affiliation:
Dien Bien Technical Economic College, Dien Bien Phu city, 380000, Vietnam
N.T.K. Lan
Affiliation:
Thai Nguyen University of Agriculture and Forestry, Thai Nguyen city, 250000, Vietnam
P.N. Doanh*
Affiliation:
Institute of Ecology and Biological Resources, Vietnamese Academy of Science and Technology (VAST), Hanoi, 122100, Vietnam Graduate University of Sciences and Technology, VAST, Hanoi, 122100, Vietnam
*
Author for correspondence: P.N. Doanh, E-mail: pndoanh@yahoo.com

Abstract

Lungworms of the genus Metastrongylus are parasitic nematodes in the respiratory tract of swine. Although they infect both wild boars and domestic pigs, studies on Metastrongylus infections in wild boars in Europe, the Americas and Africa are numerous, while those in domestic pigs are few. There are several studies analysing the molecular phylogenetic relationships of few individual Metastrongylus species with other nematode taxa, but there are no studies on the phylogenetic relationships of species within the genus Metastrongylus. In Southeast Asia, reports on swine lungworms are extremely scarce and do not include any nucleotide sequence data. Therefore, the aim of the present study is to survey Metastrongylus infection in domestic pigs raised in Dien Bien Province, Northern Vietnam, and to analyse the molecular phylogenetic relationships of Metastrongylus species. Based on morphological and molecular data, we identified two species: Metastrongylus apri and Metastrongylus pudendotectus. The prevalence of the former species was found to be significantly higher than the latter one (24.1% vs. 2.3%). We observed pigs exhibiting a coinfection with the two lungworm species or a single infection with only M. apri. However, we did not observe any pigs being infected with just M. pudendotectus. Vietnamese Metastrongylus specimens showed slight morphological and molecular differences compared to those from other countries. The molecular analyses revealed a close genetic relationship between M. apri and Metastrongylus salmi, while both these species were far distant from M. pudendotectus. The present study highlights the needs for further studies to clarify the morphological features and ecological and phylogenetic relationships of Metastrongylus species at the global scale.

Type
Short Communication
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

Adedokun, OA, Adejinmi, JO and Ukoikpoko, GB (2001) Effect of husbandry system on the incidence of lungworm (Metastrongylus spp.) in pigs in Ibadan, Nigeria. Tropical Veterinarian 19, 175177.Google Scholar
Alcaide, M, Frontera, E, Rodríguez, MJ, Sáez, IE, Domínguez–Alpízar, JL, Reina, D and Navarrete, I (2005) Parasitosis pulmonares del cerdo ibérico: situación actual de la metastrongilosis en España. Mundo Ganadero 176, 4044.Google Scholar
Amayour, A, Alaoui, Z, Alkhali, A, Hassouni, T, Kharrim, K and Belghyti, D (2016) Lung parasites of the genus Metastrongylus Molin, 1861 (Nematoda: Metastrongilidae) in wild boar (Suc scrofa barbarus) in middle atlas region of Morocco: an epidemiological study. Journal of Biological Research 6, 20202025.Google Scholar
Arambulo, PV, Hernandez, VC and Soria-Abaga, A (1967) On the prevalent species of swine lungworm (genus Metastrongylus Molin, 1861) in the Philippines. Journal of Parasitology 53, 988.Google Scholar
Bowles, J, Hope, M, Tiu, WU, Liu, SX and McManus, DP (1993) Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Tropica 55, 217229.CrossRefGoogle ScholarPubMed
Bowles, J, Blair, D and McManus, DP (1995) A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution 4, 103109.CrossRefGoogle ScholarPubMed
Calvopina, M, Caballero, H, Morita, T and Korenaga, M (2016) Human pulmonary infection by the zoonotic Metastrongylus salmi nematode. The first reported case in the Americas. American Journal of Tropical Medicine and Hygiene 95, 871873.CrossRefGoogle ScholarPubMed
Carreno, RA and Nadler, SA (2003) Phylogenetic analysis of the metastrongyloidea (Nematoda: Strongylida) inferred from ribosomal RNA gene sequences. Journal of Parasitology 89, 965973.CrossRefGoogle ScholarPubMed
Carstensen, L, Vaarst, M and Roepstorff, A (2002) Helminth infections in Danish organic swine herds. Veterinary Parasitology 106, 253264.CrossRefGoogle ScholarPubMed
Conole, JC, Chilton, NB, Järvis, T and Gasser, RB (1999) Intraspecific and interspecific variation in the second internal transcribed spacer (ITS-2) sequence for Metastrongylus (Nematoda: Metastrongyloidea) detected by high resolution PCR-RFLP. International Journal for Parasitology 29, 19351940.CrossRefGoogle ScholarPubMed
Conole, JC, Chilton, NB, Jarvis, T and Gasser, RB (2001) Mutation scanning analysis of microsatellite variability in the second internal transcribed spacer (precursor ribosomal RNA) for three species of Metastrongylus (Strongylida: Metastrongyloidea). Parasitology 122, 195206.CrossRefGoogle Scholar
Dougherty, EC (1944) The genus Metastrongylus Molin, 1861 (Nematoda: Metatorngylidae). Proceedings of the Helminthological Society of Washington 11, 6873.Google Scholar
Epe, C, Spellmeyer, O and Stoye, M (1997) Investigations on the occurrence of endoparasites in wild boars. Zeitschrift für Jagdwissenschaft 43, 99104.Google Scholar
Ewing, MS, Ewing, SA, Keener, MS and Mulholland, RJ (1982) Mutualism among parasitic nematodes: a population model. Ecological Modelling 15, 353366.CrossRefGoogle Scholar
Forrester, DJ, Porter, JH, Belden, RC and Frankenberger, WB (1982) Lungworms of feral swine in Florida. Journal of the American Veterinary Medical Association 181, 12781280.Google ScholarPubMed
García–González, ÁM, Pérez–Martín, JE, Gamito–Santos, JA, Calero–Bernal, R, Alcaide–Alonso, M and Frontera–Carrión, EM (2013) Epidemiologic study of lung parasites (Metastrongylus spp.) in wild boar (Sus scrofa) in southwestern Spain. Journal of Wildlife Diseases 49, 157162.CrossRefGoogle Scholar
Gassó, D, Rossi, L, Mentaberre, G, et al. (2014) An identification key for the five most common species of Metastrongylus. Parasitology Research 113, 34953500.CrossRefGoogle ScholarPubMed
Jex, AR, Hall, RS, Littlewood, DT and Gasser, RB (2010) An integrated pipeline for next-generation sequencing and annotation of mitochondrial genomes. Nucleic Acids Research 38, 522533.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.CrossRefGoogle ScholarPubMed
Leignel, V, Humbert, JF and Elard, L (1997) Study by ribosomal DNA ITS-2 sequencing and RAPD analysis on the systematics of four Metastrongylus species (Nematoda: Metastrongyloidea). Journal of Parasitology 83, 606611.CrossRefGoogle Scholar
Li, K, Shahzad, M, Zhang, H, Mehmood, K, Jiang, X, Luo, H, Zhang, L, Dong, X and Li, J (2018) Characterization of the complete mitochondrial genome of Metastrongylus salmi (M. Salmi) derived from Tibetan pigs in Tibet, China. Acta Parasitologica 63, 280286.CrossRefGoogle ScholarPubMed
Li, K, Luo, H, Zhang, H, et al. (2016) First report of Metastrongylus pudendotectus by the genetic characterization of mitochondria genome of cox1 in pigs from Tibet, China. Veterinary Parasitology 223, 9195.CrossRefGoogle ScholarPubMed
Miloshev, B (1956) Case of triple infection with Metastrongylus elongatus, Thaeniarhynchus saginatus and Enterobius vermicularis. Suvremenna Meditsina 7, 9497 (in Bulgarian).Google ScholarPubMed
Nosal, P, Kowal, J and Nowosad, B (2010) Structure of Metastrongylidae in wild boars from southern Poland. Helminthologia 47, 212218.CrossRefGoogle Scholar
Nssien, MAS and Adesehinwa, AOK (1999) Seasonal variation and prevalence of lungworm infection in the three different breeds of pigs slaughtered at Bodija municipal government abattoir, Ibadan, Nigeria. Tropical Animal Science Journal 2, 209214.Google Scholar
Poglayen, G, Marchesi, B, Dall'Oglio, G, Barlozzari, G, Galuppi, R and Morandi, B (2015) Lung parasites of the genus Metastrongylus Molin, 1861 (Nematoda: Metastrongilidae) in wild boar (Sus scrofa L., 1758) in central-Italy: an eco-epidemiological study. Veterinary Parasitology 217, 4552.CrossRefGoogle Scholar
Railliet, A and Henry, A (1911) Helminthes du pore recueillis par M. Bauche en Annam. Bulletin de la Societe de Pathologie Exotique 4, 693699.Google Scholar
Yong, HS, Song, SL, Eamsobhana, P and Lim, PE (2016) Complete mitochondrial genome of Angiostrongylus malaysiensis lungworm and molecular phylogeny of metastrongyloid nematodes. Acta Tropica 161, 3340.CrossRefGoogle ScholarPubMed