Abstract
Parasitic nematodes of Oesophagostomum spp., commonly known as ‘nodular worms’ are one of the most widely distributed and prevalent emerging zoonotic nematodes. However, little is known about the prevalence and gene characteristics of those parasites in Tibetan pigs. Therefore, a study was carried out to investigate the prevalence, isolation and identification of Oesophagostomum spp from Tibetan pigs by genetic markers of nad1,cox3 and ITS1 for the first time. The results revealed that the infection rate of O. dentatum and O. quadrispinulatum by genetic markers of nad1 was 81.13%; 35 (66.04%); the O. dentatum and O. quadrispinulatum by genetic markers cox3 was 66.04%, and O. dentatum and O. stephanostomum by genetic markers ITS1 was found to be 77.36%. Interestingly, the O. stephanostomum specie was identified and isolated from 90.48% stomach and 69.23% colon samples by genetic markers of ITS1. The present study, for the first time has described the presence and genetic characterization of Oesophagostomun spp of O. dentatum, O. quadrispinulatum and especially O. stephanostomum in Tibetan pigs from the high and remote Tibetan plateau. A public concern should be raised in terms of economical losses and severe public health problem.
Conflicts of interest: The authors declare that they have no competing interests.
Acknowledgements
This study was supported by Key Science Fund of Science and Technology Agency of Tibet Autonomous Region and projects in the National Science & Technology Pillar Program during the 12thFive-year Plan Period (2012BAD3B03) and the Chinese Agricultural Research Systems (CARS-38).
References
Boes J., Willingham III A.L., Shi F.H., Hu X.G., Eriksen L., Nansen P., Stewart T.B. 2000. Prevalence and distribution of pig helminthes in the Dongting Lake Region (Hunan Province) of the People’s Republic of China. Journal of Helmintholoy, 74, 45–52. 10.1017/S0022149X00000068Search in Google Scholar
Farhadi M., Fazaeli A., Haniloo A. 2015. Genetic characterization of livestock and human hydatid cyst isolates from northwest Iran, using the mitochondrial cox1 gene sequence. Parasitology Research, 114, 4363–4370. 10.1007/s00436-015-4673-ySearch in Google Scholar
Isozumi R., Fukui M., Kaneko A., Chan C.W., Kawamoto F., Kimura M. 2015. Improved detection of malaria cases in island settings of Vanuatu and Kenya by PCR that targets the Plasmodium mitochondrial cytochrome c oxidase III (cox3) gene. Parasitology International, 64, 304–308. 10.1016/ j.parint.2014.09.006Search in Google Scholar
Joachim A., Dülmer N., Daugschies A., Roepstorff A. 2001. Occurrence of helminthes in pig fattening units with different management systems in Northern Germany. Veterinary Parasitology, 96, 135–146. 10.1016/S0304-4017(00) 00431-3Search in Google Scholar
Krief S., Vermeulen B., Lafosse S., Kasenene J.M., Nieguitsila A., Berthelemy M., L’hostis M., Bain O., Guillot J. 2010. Nodular worm infection in wild chimpanzees in Western Uganda: a risk for human health? PLoS Neglected Tropical Disease, 4, e630. 10.1371/journal.pntd.0000630Search in Google Scholar PubMed PubMed Central
Lai M., Zhou R.Q., Huan H.C., Hu S.J. 2011. Prevalence and risk factors associated with intestinal parasites in pigs in Chongqing, China. Research in Veterinary Science, 91, e121–e124. 10.1016/j.rvsc.2011.01.025Search in Google Scholar PubMed
Legesse M., Erko B. 2004. Zoonotic intestinal parasites in Papio anubis (baboon) and Cercopithecus aethiops (vervet) from four localities in Ethiopia. Acta Tropica, 90, 231–236. 10.1016/j.actatropica.2003.12.003Search in Google Scholar PubMed
Li K., Luo H.Q., Zhang H., Lan Y.F., Han Z.Q., Shahzad M., Wang X.Q., Qiu G., Huang S.C., Jiang W.T., Li J.K. 2016. First report of Metastrongylus pudendotectus by the genetic characterization of mitochondria genome of cox1 in pigs from Tibet, China. Veterinary Parasitology, 223, 91–95. 10.1016/ j.vetpar.2016.04.036Search in Google Scholar
Li X.R. (Ed.) 2011. Color Atlas of Animal Parasitosis, second ed. China Agriculture Press, Beijing.Search in Google Scholar
Lin R.Q., Liu G.H., Hu M., Song H.Q., Wu X.Y., Li M.Y., Zhan Y., Zou F.C., Zhu X.Q. 2012. Oesophagostomum dentatum and Oesophagostomum quadrispinulatum: Characterization of the complete mitochondrial genome sequences of the two pig nodule worms. Experimental Parasitology, 131: 1–7. 10.1016/j.exppara.2012.02.015Search in Google Scholar PubMed
Lin R.Q., Shu L., Zhao G.H., Cheng T., Zou S.S., Zhang Y., et al. 2014. Characterization of the Intergenic Spacer rDNAs of Two Pig Nodule Worms, Oesophagostomum dentatum and O. quadrispinulatum. Scientific World Journal, 2014, 147963. 10.1155/2014/147963Search in Google Scholar PubMed PubMed Central
Lin R.Q., Zhang X.G., Hu Y.L., Li G.Q., Weng Y.B., Song H.Q., et al. 2006. Analysis of the ITS-1 and ITS-2 rDNA of Oesophagostomum from pig by PCR-SSCP. Chinese Journal of Preventive Veterinary Medicine, 28, 323–326. 1008-0589(2006)03-0323-04 (In Chinese)Search in Google Scholar
Lin R.Q., Zhu X.Q., Wei D.X., Deng Y., Liu W., Song H.Q., et al. 2007. Characterization of Oesophagostomum spp. from pigs in China by PCR-based approaches using genetic markers in the internal transcribed spacers of ribosomal DNA. Parasitology Research, 101, 351–356. 10.1007/s00436-007-0498-7Search in Google Scholar
Liu G.H., Wang Y., Song H.Q., Li M.W., Ai L., Yu X.L., Zhu X.Q. 2013. Characterization of the complete mitochondrial genome of Spirocerca lupi: sequence, gene organization and phylogenetic implications. Parasites & Vectors, 6,45. 10.1186/1756–3305-6-45Search in Google Scholar
McCarthy J., Moore T.A. 2000. Emerging helminth zoonoses. International Journal for Parasitology, 30, 1351–1360. S0020-7519(00)00122-3Search in Google Scholar
Permin A., Yelifari L., Bloch P., Steenhard N., Hansen N.P., Nansen P. 1999. Parasites in cross-bred pigs in the Upper East Region of Ghana. Veterinary Parasitology, 87, 63–71. S0304-4017(99)00159-4Search in Google Scholar
Polderman A.M., Blotkamp J. 1995. Oesophagostomum infections in humans. Parasitology Today, 11, 451–456. 10.1016/0169-4758(95)80058-1Search in Google Scholar
Polderman A.M., Anemana S.D., Asigri V. 1999. Human oesophagostomiasis: a regional public health problem in Africa. Parasitology Today, 15, 129–130. 10.1016/S0169-4758 (99)01428-3Search in Google Scholar
Roepstorff A., Nilsson O., Oksanen A., Gjerde B., Richter S.H., Örtenberg E., et al. 1998. Intestinal parasites in swine in the Nordic countries: prevalence and geographical distribution. Veterinary Parasitology, 76, 305–319. S0304-4017(97)00223-9Search in Google Scholar
Storey P.A., Faile G., Hewitt E., Yelifari L., Polderman A.M., Magnussen P. 2000. Clinical epidemiology and classification of human oesophagostomiasis. Transactions of the Royal Society Tropical Medicine and Hygiene, 94, 177–182.10.1016/S0035-9203(00)90267-0Search in Google Scholar
Verweij J.J., Pit D.S., van Lieshout L., Baeta S.M., Dery G.D., Gasser R.B., Polderman A.M. 2001. Determining the prevalence of Oesophagostomum bifurcum and Necator americanus infections using specific PCR amplification of DNA from faecal samples. Tropical Medicine and International Health, 6, 726–731. 10.1046/j.1365-3156.2001.00770.xSearch in Google Scholar PubMed
Weng Y.B., Hu Y.J., Li Y., Li B.S., Lin R.Q., Xie D.H., et al. 2005. Survey of intestinal parasites in pigs from intensive farms in Guangdong Province, People’s Republic of China. Veterinary Parasitology, 127, 333–336. 10.1016/j.vetpar.2004.09.030Search in Google Scholar PubMed
Zhang N.Z., Zhou D.H., Huang S.Y., Wang M., Shi X.C., Ciren D.B., Zhu X.Q. 2014. Seroprevalence and risk factors associated with Haemophilus parasuis infection in Tibetan pigs in Tibet. Acta Tropica, 132, 94–97. 10.1016/j.actatropica.2013. 12.021Search in Google Scholar
Zhao G.H., Hua B., Cheng W.Y., Jia Y.Q., Li H.M., Yu S.K., Liu G.H. 2013. The complete mitochondrial genomes of Oesophagostomum asperum and Oesophagostomum columbianum in small ruminants. Infection, Genetics and Evolution, 19, 205–211. 10.1016/j.meegid.2013.07.018Search in Google Scholar PubMed
© 2017 W. Stefański Institute of Parasitology, PAS
