Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Morphological Characteristics and Phylogenetic Trends of Trematode Cercariae in Freshwater Snails from Nakhon Nayok Province, Thailand

  • Chontananarth, Thapana (Parasitology Research Laboratory, Department of Biology, Faculty of Science, Srinakharinwirot University) ;
  • Tejangkura, Thanawan (Parasitology Research Laboratory, Department of Biology, Faculty of Science, Srinakharinwirot University) ;
  • Wetchasart, Napat (Parasitology Research Laboratory, Department of Biology, Faculty of Science, Srinakharinwirot University) ;
  • Chimburut, Cherdchay (Parasitology Research Laboratory, Department of Biology, Faculty of Science, Srinakharinwirot University)
  • Received : 2016.09.04
  • Accepted : 2016.12.24
  • Published : 2017.02.28
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Abstract

The prevalence of cercarial infection in freshwater snails and their evolutionary trends were studied in Nakhon Nayok province, Thailand. A total of 2,869 individual snails were examined for parasitic infections. The results showed that 12 snail species were found to host larval stages of trematodes with an overall prevalence of 4.7%. The infected specimens included 7 types at the cercarial stage; cercariae, megalurous cercariae, echinostome cercariae, furcocercous cercariae, parapleurolophocercous cercariae, virgulate cercariae, and xiphidiocercariae. Regarding molecular identification, ITS2 sequence data of each larval trematode were analyzed, and a dendrogram was constructed using the neighbor-joining method with 10,000 replicates. The dendrogram was separated into 6 clades (order/family), including Echinostomatida/Echinostomatidae, Echinostomatida/Philophthalmidae, Opisthorchiida/Heterophyidae, Plagiorchiida/Prosthogonimidae, Plagiorchiida/Lecithodendriidae, and Strigeatida/Cyathocotylidae. These findings were used to confirm morphological characteristics and evolutionary trends of each type of cercariae discovered in Nakhon Nayok province. Furthermore, this investigation confirmed that the ITS2 data of cercariae could be used to study on phylogenetic relationships or to determine classification of this species at order and/or family level when possible.

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References

  1. Roberts LS, Janovy J Jr, Gerald D. Foundations of Parasitology, 8th ed. New York, USA. McGraw-Hill. 2009.
  2. Chontananarth T, Wongsawad C. Prevalence of Haplorchis taichui in field collected snails: a molecular approach. Korean J Parasitol 2010; 48: 343-346. https://doi.org/10.3347/kjp.2010.48.4.343
  3. Schell SC. How to Know the Trematodes. Dubuque, Iowa, USA. W.C. Brown. 1970, pp 1-335.
  4. Chontananarth T, Wongsawad C. Epidemiology of cercarial stage of trematodes in freshwater snails from Chiang Mai province, Thailand. Asian Pac J Trop Biomed 2013; 3; 237-243. https://doi.org/10.1016/S2221-1691(13)60058-1
  5. Frandsen F, Christensen NO. An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Trop 1984; 41: 181-202.
  6. Wongsawad C, Kumchoo K. Studies on prevalence and intensity of Transversotrema patialensis (Trematoda: Transversotrematidae) in the snail intermediate host, Thiara scabra. J Med Appl Malacol 2000; 10: 37-40.
  7. Ngern-klun R, Sukontason KL, Tesana S, Sripakdee D, Irvine KN, Sukontason K. Field investigation of Bithynia funiculata, intermediate host of Opisthorchis viverrini in northern Thailand. Southeast Asian J Trop Med Public Health 2006; 37: 662-672.
  8. Dechruksa W, Krailas D, Ukong S, Inkapatanakul W, Koonchornboon T. Trematode infections of the freshwater snail family Thiaridae in the Khek river, Thailand. Southeast Asian J Trop Med Public Health 2007; 38: 1016-1028.
  9. Mard-arhin N, Prawang T, Wongsawad C. Helminths of freshwater animals from five provinces in northern Thailand. Southeast Asian J Trop Med Public Health 2001; 32 (suppl): 206-209.
  10. Krailas D, Chotesaengsri S, Dechruksa W, Namchote S, Chuanprasit C,Veeraveebsakij N, Boonmekam D, Koonchornboon T. Species diversity of aquatic mollusks and their cercarial infections; Khao Yai National Park, Thailand. J Trop Med Parasitol 2012; 35: 37-47.
  11. Anucherngchai S, Tejangkura T, Chontananarth T. Epidemiological situation and molecular identification of cercarial stage in freshwater snails in Chao-Phraya basin, Central Thailand. Asian Pac J Trop Biomed 2016; 6; 539-545.
  12. Pearson JC, Ow-Yang CK. New species of Haplorchis from Southeast Asia, together with Key to the Haplorchis-group of heterophyid trematode of the Region. Southeast Asian J Trop Med Public Health 1982; 13: 35-60.
  13. Jousson O, Bartoli P, Pawlowski J. Molecular identification of developmental stages in Opecoelidae (Digenea). Int J Parasitol 1999; 29: 1853-1858. https://doi.org/10.1016/S0020-7519(99)00124-1
  14. Kaset C, Eursitthichai V, Vichasri-Grams S, Viyanant V, Grams R. Rapid identification of lymnaeid snails and their infection with Fasciola gigantica in Thailand. Exp Parasitol 2010; 126: 482-488. https://doi.org/10.1016/j.exppara.2010.05.021
  15. Erensoy A, Kuk S, Ozden M. Genetic identification of Fasciola hepatica by ITS-2 sequence of nuclear ribosomal DNA in Turkey. Parasitol Res 2009; 105: 407-412. https://doi.org/10.1007/s00436-009-1399-8
  16. Thaenkham U, Dekumyoy P, Komalamisra C, Sato M, Dung DT, Waikagul J. Systematics of the subfamily Haplorchiinae (Trematoda: Heterphyidae), based on nuclear ribosomal DNA genes and ITS2 region. Parasitol Int 2010; 59: 460-465. https://doi.org/10.1016/j.parint.2010.06.009
  17. Sripalwit P, Wongsawad C, Chontananarth T, Anuntalabhochai S, Wongsawad P, Chai JY. Worm developmental and phylogenetic characteristic of Stellantchasmus falcatus (Trematoda: Heterophyidae) from Thailand. Korean J Parasitol 2015; 53: 201-207. https://doi.org/10.3347/kjp.2015.53.2.201
  18. Kong Q, Fan L, Zhang J, Akao N, Dong K, Lou D, Ding J, Tong Q, Zheng B, Chen R, Ohta N, Lu S. Molecular identification of Anisakis and Hysterothylacium larvae in marine fishes from the East China Sea and the Pacific Coast of central Japan. Int J Food Microbiol 2015; 199: 1-7. https://doi.org/10.1016/j.ijfoodmicro.2015.01.007
  19. Sato M, Thaenkham U, Dekumyoy P, Waikagul J. Discrimination of O. viverrini, C. sinensis, H. pumilio and H. taichui using nuclear DNA-based PCR targeting ribosomal DNA ITS regions. Acta Trop 2008; 109: 81-83.
  20. Van Van K, Dalsgaard A, Blair D, Le TH. Haplorchis pumilio and H. taichui in Vietnam discriminated using ITS-2 DNA sequence data from adults and larvae. Exp Parasitol 2009; 123: 146-151. https://doi.org/10.1016/j.exppara.2009.06.011
  21. Wongsawad C, Wongsawad P. Anuntalaphochai S, Chai JY, Sukontason K. Occurrence and molecular identification of liver and minute intestinal flukes metacercariae in freshwater fish from Fang-Mae Ai Agricultural Basin, Chiang Mai province, Thailand. Asian Biomed 2013; 7: 97-104.
  22. Ghobadi H, Farahnak A. A faunistic survey on the cercariae of Bellamya (Viviparus) bengalensis snails and their zoonotic importance. Iran J Public Health 2004; 33: 38-42.
  23. Loffy WM, Brant SV, Ashmawy KI, Devkota R, Mkoji GM, Loker ES. A molecular approach for identification of paramphistomes from Africa and Asia. Vet Parasitol 2010; 174: 234-240. https://doi.org/10.1016/j.vetpar.2010.08.027
  24. Brandt RAM. The non-marine aquatic mollusca of Thailand. Arch Moll Band 1974; 105: 1-423.
  25. La Rue GR. The classification of digenetic trematode: a review and a new system. Exp Parasitol 1957; 6: 306-349. https://doi.org/10.1016/0014-4894(57)90025-5
  26. Olsen OW. Animal Parasites: Their Life Cycles and Ecology. Baltimore, Maryland, USA. University Park. 1974, pp 1-565.
  27. Ito J. Studies on Cercariae in Japan. Shizuoka, Japan. Shizuoka University. 1980, pp 516-538.
  28. Barber KE, Mkoji GM, Loker ES. PCR-RFLP analysis of the ITS2 region to identify Schistosoma haematobium and S. bovis from Kenya. Am J Trop Med Hyg 2000; 2: 434-440.
  29. Supian Z, Ikhwanuddin AM. Population dynamics of freshwater molluscs (Gastropod: Melanoides tuberculata) in Crocker Range Park, Sabah. Review of Biodiversity and Environmental Conservation (ARBEC) 2002; 1: 1-9.
  30. Bogea T, Cordeiro FM, Gouveia JS. Melanoides tuberculata (Gastropoda: Thiaridae) as intermediate host of Heterophyidae (Trematoda: Digenea) in Rio de Janeiro Metropolitan Area, Brazil. Rev Inst Med Trop S Paulo 2005; 47: 87-90. https://doi.org/10.1590/S0036-46652005000200005
  31. Tum S, Puotinen ML, Copeman DB. A geographic information systems model for mapping risk of fasciolosis in cattle and buffaloes in Cambodia. Vet Parasitol 2004; 12: 141-149.
  32. Fernandez MV, Hamann MI, Ostrowski-de Nunez M. Echinostome cercariae from Biomphalaria straminea (Mollusca: Planorbidae) in a rice field from Northeastern Argentina. Rev Mex Biodivers 2014; 85: 1024-1031. https://doi.org/10.7550/rmb.43875
  33. Umadevi K, Madhavi R. The life cycle of Haplorchis pumilio (Trematoda: Heterophyidae) from the Indian region. J Helminthol 2006; 80: 327-332. https://doi.org/10.1017/JOH2006359
  34. Diaz MT, Hernandez LE, Bashirullah AK. Studies on the life cycle of Haplorchis pumilio (Looss, 1896) (Trematoda: Heterophyidae) in Venezuela. Rev Cientfica 2008; 18: 35-42.
  35. Skov J, Kania PW, Dalsgaard A, Jorgensen TR, Buchmann K. Life cycle stages of heterophyid trematodes in Vietnamese freshwater fishes traced by molecular and morphometric methods. Vet Parasitol 2009; 160: 66-75. https://doi.org/10.1016/j.vetpar.2008.10.088
  36. Pinto HA, de Melo AL. Melanoides tuberculata (Mollusca: Thiaridae) as an intermediate host of Centrocestus formosanus (Trematoda: Heterophyidae) in Brazil. Rev Inst Med Trop Sap Paulo 2010; 52: 207-210. https://doi.org/10.1590/S0036-46652010000400008
  37. Saijuntha W, Duenngai K, Tantrawatpan C. Zoonotic echinostome infections in free-grazing ducks in Thailand. Korean J Parasitol 2013; 51: 663-667. https://doi.org/10.3347/kjp.2013.51.6.663
  38. Krailas D, Veeravechsukij N, Chuanprasit C, Boonmekam D, Namchote S. Prevalence of fish-borne trematodes of the family Heterophyidae at Pasak Cholasid Reservoir, Thailand. Acta Trop 2016; 156: 79-86. https://doi.org/10.1016/j.actatropica.2016.01.007
  39. Nithikathkul C, Wongsawad C. Prevalence of Haplorchis taichui and Haplorchoides sp. metacercariae in freshwater fish from water reservoirs, Chiang Mai, Thailand. Korean J Parasitol 2008; 46: 109-112. https://doi.org/10.3347/kjp.2008.46.2.109

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