Skip to main content Accessibility help

Trematode diversity in the freshwater snail Bithynia siamensis goniomphalos sensu lato from Thailand and Lao PDR

  • N. Kiatsopit (a1) (a2), P. Sithithaworn (a1) (a2), K. Kopolrat (a1) (a2), J. Namsanor (a1) (a2), R.H. Andrews (a1) (a2) (a3) (a4) and T.N. Petney (a3) (a5)...


In order to obtain a comprehensive understanding of trematode diversity in Bithynia siamensis 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.


Corresponding author

*Fax: +66 43202475 E-mail:


Hide All
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, 697700.
Andrews, R.H., Sithithaworn, P. & Petney, T.N. (2008) Opisthorchis viverrini: an underestimated parasite in world health. Trends in Parasitology 24, 497501.
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. 7586 in Lannoo, M.J. (Ed.) Amphibian declines: the conservation status of United States species. Berkeley, University of California Press.
Brandt, R.A.M. (1974) The non-marine aquatic Mollusca of Thailand. Archiv für Molluskenkunde 105, 1423.
Chitramvong, Y.P. (1992) The Bithyniidae (Gastropoda: Prosobranchia) of Thailand: comparative external morphology. Malacological Review 25, 2138.
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, 237243.
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, 12161220.
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, 482488.
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, 7581.
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, 109127.
Esch, G.W., Curtis, L.A. & Barger, M.A. (2001) A perspective on the ecology of trematode communities in snails. Parasitology 123, S57S75.
Faltynkova, A. & Haas, W. (2006) Larval trematodes in freshwater molluscs from the Elbe to Danube rivers (Southeast Germany): before and today. Parasitology Research 99, 572582.
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.
Gérard, C. (2001) Consequences of a drought on freshwater gastropod and trematode communities. Hydrobiologia 459, 918.
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, 538540.
Ito, J., Papasarathorn, T. & Tongkoom, B. (1962) Studies on cercariae from fresh water snails in Thailand. Japanese Journal of Medical Science and Biology 15, 249270.
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, 806812.
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, 464469.
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, 313319.
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.
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, 9971001.
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, 11671177.
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, 105109.
Kuris, A.M. & Lafferty, K.D. (1994) Community structure: larval trematodes in snail hosts. Annual Reviews of Ecology and Systematics 25, 189217.
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, 13071313.
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, 146153.
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.
Lei, F. & Poulin, R. (2011) Effects of salinity on multiplication and transmission of an intertidal trematode parasite. Marine Biology 158, 9951003.
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, 126.
Loy, C. & Haas, W. (2001) Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitology Research 87, 878882.
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, 662672.
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, 106109.
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, 101163.
Olson, P.D. & Tkach, V.V. (2005) Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology 60, 165243.
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, 3845.
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, 10311046.
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, 25352540.
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, 695703.
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, 247254.
Schell, S.C. (1970) How to know the trematodes. 355 pp. Dubuque, Iowa, W.C. Brown.
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, 125131.
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, 1016.
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, 3237.
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, 6675.
Sorensen, R. & Minchella, D.J. (1998) Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails. Oecologia 115, 188195.
Sousa, W.P. (1993) Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecological Monographs 63, 103128.
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, 653657.
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, 294301.
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, S158S168.
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, 12131222.
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, 183190.
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, 5460.
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, 355358.
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, 107132.
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, 138141.
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, 351357.
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, 244252.
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, 207214.
Yamaguti, S. (1975) A synoptical review of life histories of digenetic trematodes of vertebrates. Japan, Keiguku Publication.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of Helminthology
  • ISSN: 0022-149X
  • EISSN: 1475-2697
  • URL: /core/journals/journal-of-helminthology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed