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Trematode diversity in the freshwater snail Bithyniasiamensisgoniomphalos sensu lato from Thailand and Lao PDR

Published online by Cambridge University Press:  06 May 2015

N. Kiatsopit ,
P. Sithithaworn ,
K. Kopolrat ,
J. Namsanor ,
R.H. Andrews  and
T.N. Petney
N. Kiatsopit
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen40002, Thailand Liver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand
P. Sithithaworn*
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen40002, Thailand Liver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand
K. Kopolrat
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen40002, Thailand Liver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand
J. Namsanor
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen40002, Thailand Liver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand
R.H. Andrews
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen40002, Thailand Liver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand Cholangiocarcinoma Screening and Care Program (CASCAP), Khon Kaen University, 40002Thailand Imperial College London, Faculty of Medicine, St Mary's Campus, South Wharf Street, LondonW2 1NY, UK
T.N. Petney
Affiliation:
Cholangiocarcinoma Screening and Care Program (CASCAP), Khon Kaen University, 40002Thailand Institute of Zoology 1: Ecology and Parasitology, University of Karlsruhe, Kornblumen Strasse 13, Karlsruhe, Germany
*
*Fax: +66 43202475 E-mail: [email protected]
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Abstract

In order to obtain a comprehensive understanding of trematode diversity in Bithyniasiamensis goniomphalos sensu lato, the first intermediate host of the liver fluke Opisthorchis viverrini s.l., the prevalence of larval trematode species was investigated in different localities in Thailand and Lao People's Democratic Republic (Lao PDR). In Thailand, snail samples were collected from 29 localities in the nine provinces: Buri Ram, Surin, Chaiya Phum, Maha Sarakham, Khon Kaen, Kalasin, Mukdahan, Sakon Nakhon and Nakhon Phanom. In Lao PDR, snail samples were collected from 21 localities in Vientiane Province and six localities in Savannakhet Province. Snails were identified by standard morphological criteria and then examined for trematode infection using the cercarial shedding method. Twenty different types of cercariae were detected and identified, based on morphological criteria. Virgulate type 1 emerged as the most common cercaria, with an average prevalence of 10.90% (range 0.26–54.22%) in Thailand and 6.58% (range 1.15–89.77%) in Lao PDR. Opisthorchis viverrini s.l. cercariae were the fourth most common in Thailand, with an average prevalence of 1.59% (0.15–6.93), while in Lao PDR their prevalence was 0.96% (0.08–8.37). The high diversity of trematode cercariae observed in this study indicates that B. s. goniomphalos s.l. is highly susceptible to infection with a variety of trematode species. However, the role of non-opisthorchiid trematodes as fish-borne parasites in human health is not fully known and further molecular identification is required.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 3 , May 2016 , pp. 312 - 320
Copyright
Copyright © Cambridge University Press 2015 

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References

Adam, R., Arnold, H., Pipitgool, V., Sithithaworn, P., Hinz, E. & Storch, V. (1993) Studies on lophocercous cercariae from Bithynia siamensis goniomphalos (Prosobranchia: Bithyniidae). Southeast Asian Journal of Tropical Medicine and Public Health 24, 697–700.Google Scholar
Andrews, R.H., Sithithaworn, P. & Petney, T.N. (2008) Opisthorchis viverrini: an underestimated parasite in world health. Trends in Parasitology 24, 497–501.CrossRefGoogle ScholarPubMed
Beasley, V.R., Faeh, S.A., Wikoff, B., Staehle, C., Eisold, J., Nichols, D., Cole, R., Schotthoefer, A.M., Greenwll, M. & Brown, L.E. (2005) Risk factors and declines in northern cricket frogs (Acris crepitans). pp. 75–86 in Lannoo, M.J. (Ed.) Amphibian declines: the conservation status of United States species. Berkeley, University of California Press.Google Scholar
Brandt, R.A.M. (1974) The non-marine aquatic Mollusca of Thailand. Archiv für Molluskenkunde 105, 1–423.Google Scholar
Chitramvong, Y.P. (1992) The Bithyniidae (Gastropoda: Prosobranchia) of Thailand: comparative external morphology. Malacological Review 25, 21–38.Google Scholar
Chontananarth, T., Wongsawad, C. & Chai, J.Y. (2013) Epidemiology of cercarial stage of trematodes in freshwater snails from Chiang Mai province, Thailand. Asian Pacific Journal of Tropical Biomedicine 3, 237–243.Google Scholar
Chuboon, S. & Wongsawad, C. (2009) Molecular identification of larval trematode in intermediate hosts from Chiang Mai, Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 40, 1216–1220.Google ScholarPubMed
Ditrich, O., Scholz, T. & Giboda, M. (1990) Occurrence of some medically important flukes (Trematoda: Opisthorchiidae and Heterophyidae) in Nam Ngum water reservoir, Laos. Southeast Asian Journal of Tropical Medicine and Public Health 21, 482–488.Google Scholar
Ditrich, O., Nasincova, V., Scholz, T. & Giboda, M. (1992) Larval stages of medically important flukes (Trematoda) from Vientiane province, Laos. Part II. Cercariae. Annales de Parasitologie Humaine et Comparee 67, 75–81.CrossRefGoogle ScholarPubMed
Ditrich, O., Schoiz, T., Aguiree-Macedo, L. & Vargas-Vazquez, J. (1997) Larval stages of trematodes from freshwater molluscs of the Yucatan Peninsula, Mexico. Folia Parasitlogica 44, 109–127.Google Scholar
Esch, G.W., Curtis, L.A. & Barger, M.A. (2001) A perspective on the ecology of trematode communities in snails. Parasitology 123, S57–S75.Google Scholar
Faltynkova, A. & Haas, W. (2006) Larval trematodes in freshwater molluscs from the Elbe to Danube rivers (Southeast Germany): before and today. Parasitology Research 99, 572–582.CrossRefGoogle ScholarPubMed
Forrer, A., Sayasone, S., Vounatsou, P., Vonghachack, Y., Bouakhasith, D., Vogt, S., Glaser, R., Utzinger, J., Akkhavong, K. & Odermatt, P. (2012) Spatial distribution of, and risk factors for, Opisthorchis viverrini infection in southern Lao PDR. PLoS Neglected Tropical Diseases 6, e1481.Google Scholar
Gérard, C. (2001) Consequences of a drought on freshwater gastropod and trematode communities. Hydrobiologia 459, 9–18.CrossRefGoogle Scholar
Giboda, M., Ditrich, O., Scholz, T., Viengsay, T. & Bouaphanh, S. (1991) Human Opisthorchis and Haplorchis infections in Laos. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 538–540.CrossRefGoogle ScholarPubMed
Ito, J., Papasarathorn, T. & Tongkoom, B. (1962) Studies on cercariae from fresh water snails in Thailand. Japanese Journal of Medical Science and Biology 15, 249–270.Google Scholar
Kalbe, M., Haberl, B. & Haas, W. (1997) Miracidial host-finding in Fasciola hepatica and Trichobilharzia ocellata is stimulated by species-specific glycoconjugates released from the host snails. Parasitology Research 83, 806–812.Google Scholar
Kiatsopit, N., Sithithaworn, P., Saijuntha, W., Boonmars, T., Tesana, S., Sithithaworn, J., Petney, T.N. & Andrews, R.H. (2012) Exceptionally high prevalence of infection of Bithynia siamensis goniomphalos with Opisthorchis viverrini cercariae in different wetlands in Thailand and Lao PDR. American Journal of Tropical Medicine and Hygiene 86, 464–469.Google Scholar
Kiatsopit, N., Sithithaworn, P., Saijuntha, W., Petney, T.N. & Andrews, R.H. (2013) Opisthorchis viverrini: implications of the systematics of first intermediate hosts, Bithynia snail species in Thailand and Lao PDR. Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases 14, 313–319.CrossRefGoogle ScholarPubMed
Kodcharin, P. (2005) Genetic variation in Bithynia siamensis goniomphalos, first intermediate host of Opisthorchis viverrini in the basin of Mun and Chi rivers, Thailand by RAPD. MSc thesis, Khon Kaen University, Khon Kaen, Thailand.Google Scholar
Koprivnikar, J., Baker, R.L. & Forbes, M.R. (2006) Environmental factors influencing trematode prevalence in grey tree frog (Hyla versicolor) tadpoles in southern Ontario. Journal of Parasitology 92, 997–1001.Google Scholar
Koprivnikar, J., Lim, D., Fu, C. & Brack, S.H. (2010) Effects of temperature, salinity, and pH on the survival and activity of marine cercariae. Parasitology Research 106, 1167–1177.CrossRefGoogle ScholarPubMed
Kraus, T.J., Brant, S.V. & Adema, C.M. (2014) Characterization of trematode cercariae from Physella acuta in the Middle Rio Grande. Comparative Parasitology 81, 105–109.CrossRefGoogle Scholar
Kuris, A.M. & Lafferty, K.D. (1994) Community structure: larval trematodes in snail hosts. Annual Reviews of Ecology and Systematics 25, 189–217.Google Scholar
Laoprom, N., Saijuntha, W., Sithithaworn, P., Wongkham, S., Laha, T., Ando, K., Andrews, R.H. & Petney, T.N. (2009) Biological variation within Opisthorchis viverrini sensu lato in Thailand and Lao PDR. Journal of Parasitology 95, 1307–1313.Google Scholar
Laoprom, N., Sithithaworn, P., Ando, K., Sithithaworn, J., Wongkham, S., Laha, T., Klinbunga, S., Webster, J.P. & Andrews, R.H. (2010) Microsatellite loci in the carcinogenic liver fluke, Opisthorchis viverrini and their application as population genetic markers. Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases 10, 146–153.CrossRefGoogle ScholarPubMed
Laoprom, N., Sithithaworn, P., Andrews, R.H., Ando, K., Laha, T., Klinbunga, S., Webster, J.P. & Petney, T.N. (2012) Population genetic structuring in Opisthorchis viverrini over various spatial scales in Thailand and Lao PDR. PLoS Neglected Tropical Diseases 6, e1906.CrossRefGoogle ScholarPubMed
Lei, F. & Poulin, R. (2011) Effects of salinity on multiplication and transmission of an intertidal trematode parasite. Marine Biology 158, 995–1003.Google Scholar
Lohachit, C. (2004–2005) Ecological studies of Bithynia siamensis goniomphalos, a snail intermediate host of Opisthorchis viverrini, in Khon Kaen Province, Northeast Thailand. Malacological Review 37/38, 1–26.Google Scholar
Loy, C. & Haas, W. (2001) Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitology Research 87, 878–882.Google Scholar
Ngern-klun, R., Sukontason, K.L., Tesana, S., Sripakdee, D., Irvine, K.N. & Sukontason, K. (2006) Field investigation of Bithynia funiculata, intermediate host of Opisthorchis viverrini in northern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 37, 662–672.Google Scholar
Nithiuthai, S., Wiwanitkit, V., Suwansaksri, J. & Chaengphukeaw, P. (2002) A survey of trematode cercariae in Bithynia goniomphalos in northeast Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 33, 106–109.Google ScholarPubMed
Nolan, M.J. & Cribb, T.H. (2005) The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology 60, 101–163.Google Scholar
Olson, P.D. & Tkach, V.V. (2005) Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology 60, 165–243.Google Scholar
Petney, T., Sithithaworn, P., Andrews, R., Kiatsopit, N., Tesana, S., Grundy-Warr, C. & Ziegler, A. (2012) The ecology of the Bithynia first intermediate hosts of Opisthorchis viverrini . Parasitology International 61, 38–45.Google Scholar
Petney, T.N., Andrews, R.H., Saijuntha, W., Wenz-Mucke, A. & Sithithaworn, P. (2013) The zoonotic, fish-borne liver flukes Clonorchis sinensis, Opisthorchis felineus and Opisthorchis viverrini . International Journal for Parasitology 43, 1031–1046.Google Scholar
Routtu, J., Grunberg, D., Izhar, R., Dagan, Y., Guttel, Y., Ucko, M. & Ben-Ami, F. (2014) Selective and universal primers for trematode barcoding in freshwater snails. Parasitology Research 113, 2535–2540.Google Scholar
Saijuntha, W., Sithithaworn, P., Wongkham, S., Laha, T., Pipitgool, V., Tesana, S., Chilton, N.B., Petney, T.N. & Andrews, R.H. (2007) Evidence of a species complex within the food-borne trematode Opisthorchis viverrini and possible co-evolution with their first intermediate hosts. International Journal for Parasitology 37, 695–703.Google Scholar
Sayasone, S., Vonghajack, Y., Vanmany, M., Rasphone, O., Tesana, S., Utzinger, J., Akkhavong, K. & Odermatt, P. (2009) Diversity of human intestinal helminthiasis in Lao PDR. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 247–254.Google Scholar
Schell, S.C. (1970) How to know the trematodes. 355 pp. Dubuque, Iowa, W.C. Brown.Google Scholar
Sithithaworn, P., Pipitgool, V., Srisawangwong, T., Elkins, D.B. & Haswell-Elkins, M.R. (1997) Seasonal variation of Opisthorchis viverrini infection in cyprinoid fish in north-east Thailand: implications for parasite control and food safety. Bulletin of the World Health Organization 75, 125–131.Google Scholar
Sithithaworn, P., Andrews, R.H., Nguyen, V.D., Wongsaroj, T., Sinuon, M., Odermatt, P., Nawa, Y., Liang, S., Brindley, P.J. & Sripa, B. (2012a) The current status of opisthorchiasis and clonorchiasis in the Mekong Basin. Parasitology International 61, 10–16.Google Scholar
Sithithaworn, P., Andrews, R.H., Petney, T.N., Saijuntha, W. & Laoprom, N. (2012b) The systematics and population genetics of Opisthorchis viverrini sensu lato: implications in parasite epidemiology and bile duct cancer. Parasitology International 61, 32–37.Google Scholar
Skov, J., Kania, P.W., Dalsgaard, A., Jorgensen, T.R. & Buchmann, K. (2009) Life cycle stages of heterophyid trematodes in Vietnamese freshwater fishes traced by molecular and morphometric methods. Veterinary Parasitology 160, 66–75.CrossRefGoogle ScholarPubMed
Sorensen, R. & Minchella, D.J. (1998) Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails. Oecologia 115, 188–195.Google Scholar
Sousa, W.P. (1993) Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecological Monographs 63, 103–128.CrossRefGoogle Scholar
Sri-Aroon, P., Butraporn, P., Limsomboon, J., Kerdpuech, Y., Kaewpoolsri, M. & Kiatsiri, S. (2005) Freshwater mollusks of medical importance in Kalasin Province, northeast Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 36, 653–657.Google Scholar
Sri-Aroon, P., Butraporn, P., Limsoomboon, J., Kaewpoolsri, M., Chusongsang, Y., Charoenjai, P., Chusongsang, P., Numnuan, S. & Kiatsiri, S. (2007) Freshwater mollusks at designated areas in eleven provinces of Thailand according to the water resource development projects. Southeast Asian Journal of Tropical Medicine and Public Health 38, 294–301.Google Scholar
Sripa, B., Bethony, J.M., Sithithaworn, P., Kaewkes, S., Mairiang, E., Loukas, A., Mulvenna, J., Laha, T., Hotez, P.J. & Brindley, P.J. (2011) Opisthorchiasis and Opisthorchis-associated cholangiocarcinoma in Thailand and Laos. Acta Tropica 120, S158–S168.CrossRefGoogle ScholarPubMed
Studer, A., Poulin, R. & Tompkins, D.M. (2013) Local effects of a global problem: modelling the risk of parasite-induced mortality in an intertidal trematode-amphipod system. Oecologia 172, 1213–1222.Google Scholar
Suwannatrai, A., Suwannatrai, K., Haruay, S., Piratae, S., Thammasiri, C., Khampoosa, P., Kulsantiwong, J., Prasopdee, S., Tarbsripair, P., Suwanwerakamtorn, R., Sukchan, S., Boonmars, T., Malone, J.B., Kearney, M.T. & Tesana, S. (2011) Effect of soil surface salt on the density and distribution of the snail Bithynia siamensis goniomphalos in northeast Thailand. Geospatial Health 5, 183–190.Google Scholar
Tesana, S., Thapsripair, P., Suwannatrai, A., Harauy, S., Piratae, S., Khampoosa, P., Thammasiri, C., Prasopdee, S., Kulsantiwong, J., Chalorkpunrut, P. & Jones, M.K. (2014) Parasite surveys and environmental management for prevention of parasitic infection in cultivated Barbonymus gonionotus (Cyprinidae) in fishponds, in an opisthorchiasis endemic area of northeast Thailand. Aquaculture 428–429, 54–60.Google Scholar
Upatham, E.S. & Sukhapanth, N. (1980) Field studies on the bionomics of Bithynia siamensis siamensis and the transmission of Opisthorchis viverrini in Bangna, Bangkok, Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 11, 355–358.Google Scholar
Upatham, E.S., Sornmani, S., Kitikoon, V., Lohachit, C. & Bruch, J.B. (1983) Identification key for fresh-brackish water snails of Thailand. Malacological Review 16, 107–132.Google Scholar
Vichasri, S., Viyanant, V. & Upatham, E.S. (1982) Opisthorchis viverrini: intensity and rates of infection in cyprinoid fish from an endemic focus in Northeast Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 13, 138–141.Google Scholar
Voutilainen, A., van Ooik, T., Puurtinen, M., Kortet, R. & Taskinen, J. (2009) Relationship between prevalence of trematode parasite Diplostomum sp. and population density of its snail host Lymnaea stagnalis in lakes and ponds in Finland. Aquatic Ecology 43, 351–357.Google Scholar
Wang, Y.C., Ho, R.C., Feng, C.C., Namsanor, J. & Sithithaworn, P. (2015) An ecological study of Bithynia snails, the first intermediate host of Opisthorchis viverrini in northeast Thailand. Acta Tropica 141, 244–252.Google Scholar
Wykoff, D.E., Harinasuta, C., Juttijudata, P. & Winn, M.M. (1965) Opisthorchis viverrini in Thailand – the life cycle and comparison with O. felineus . Journal of Parasitology 51, 207–214.Google Scholar
Yamaguti, S. (1975) A synoptical review of life histories of digenetic trematodes of vertebrates. Japan, Keiguku Publication.Google Scholar