Volume 93, Issue 1
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Seasonal changes play roles in the transmission success of fish-borne zoonotic trematodes (FZT). This study examined the seasonal transmission patterns of sensu lato (s.l.) and a virgulate cercaria (family Lecithodendriidae) in the snail intermediate host, in northeast Thailand. Snail samples were collected monthly during the rainy, cool, and hot seasons during 2012–2013 to determine the prevalence and intensity of larval trematode infections. The prevalence of s.l. varied significantly with season, being 0.31%, 1.05%, and 0.37% in the rainy, cool, and hot seasons, respectively ( < 0.05). Similarly, the prevalence of virgulate cercariae was 3.11%, 6.80%, and 1.64% in the rainy, cool, and hot seasons, respectively ( < 0.05). The intensity of larval trematode infections also varied between seasons and peaked in the hot season ( < 0.05) in both species. The snails infected with s.l. were significantly smaller ( < 0.05) and those infected with virgulate cercariae were significantly larger ( < 0.05) than uninfected snails. Seasonal variation and the different sizes of parasitized by s.l. and virgulate trematodes indicate complex host–parasite interactions with important implications for the epidemiology of s.l.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Sithithaworn P, Andrews R, Nguyen V, Wongsaroj T, Sinuon M, Odermatt P, Nawa Y, Liang S, Brindley P, Sripa B, , 2012. The current status of opisthorchiasis and clonorchiasis in the Mekong Basin. Parasitol Int 61: 1016.[Crossref] [Google Scholar]
  2. Saijuntha W, Sithithaworn P, Wongkham S, Laha T, Pipitgool V, Tesana S, Chilton NB, Petney TN, Andrews RH, , 2007. Evidence of a species complex within the food-borne trematode Opisthorchis viverrini and possible co-evolution with their first intermediate hosts. Int J Parasitol 37: 695703.[Crossref] [Google Scholar]
  3. Laoprom N, Saijuntha W, Sithithaworn P, Wongkham S, Laha T, Ando K, Andrews RH, Petney TN, , 2009. Biological variation within Opisthorchis viverrini sensu lato in Thailand and Lao PDR. J Parasitol 95: 13071313.[Crossref] [Google Scholar]
  4. Sripa B, Bethony J, Sithithaworn P, Kaewkes S, Mairiang E, Loukas A, Mulvenna J, Laha T, Hotez P, Brindley P, , 2011. Opisthorchiasis and Opisthorchis-associated cholangiocarcinoma in Thailand and Laos. Acta Trop 120: 158168.[Crossref] [Google Scholar]
  5. Sithithaworn P, Yongvanit P, Duenngai K, Kiatsopit N, Pairojkul C, , 2014. Roles of liver fluke infection as risk factor for cholangiocarcinoma. J Hepatobiliary Pancreat Sci 21: 301308.[Crossref] [Google Scholar]
  6. IARC, 2011. A review of human carcinogens: biological agents, Opisthorchis viverrini and Clonorchis sinensis . IARC Monogr Eval Carcinog Risks Hum 100: 351376. [Google Scholar]
  7. Brockelman W, Upatham E, Viyanant V, Ardsungnoen S, Chantanawat R, , 1986. Field studies on the transmission of the human liver fluke, Opisthorchis viverrini, in northeast Thailand: population changes of the snail intermediate host. Int J Parasitol 16: 545552.[Crossref] [Google Scholar]
  8. 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 J Trop Med Public Health 24: 697700. [Google Scholar]
  9. Sithithaworn P, Haswell-Elkins M, , 2003. Epidemiology of Opisthorchis viverrini . Acta Trop 88: 187194.[Crossref] [Google Scholar]
  10. Ngern-klun R, Sukontason K, Tesana S, Sripakdee D, Irvine K, Sukontason K, , 2006. Field investigation of Bithynia funiculata, intermediate host of Opisthorchis viverrini in northern Thailand. Southeast Asian J Trop Med Public Health 37: 662672. [Google Scholar]
  11. Kiatsopit N, Sithithaworn P, Saijuntha W, Boonmars T, Tesana S, Sithithaworn J, Petney T, Andrews R, , 2012. Exceptionally high prevalence of infection of Bithynia siamensis goniomphalos with Opisthorchis viverrini cercariae in different wetlands in Thailand and Lao PDR. Am J Trop Med Hyg 86: 464469.[Crossref] [Google Scholar]
  12. Tesana S, Thabsripair P, Suwannatrai A, Haruay S, Piratae S, Khampoosa P, Thammasiri C, Prasopdee S, Kulsantiwong J, Chalorkpunrut P, Jones M, , 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.[Crossref] [Google Scholar]
  13. Brooks D, O'Grady R, Glen D, , 1985. Phylogenetic analysis of the Digenea (Platyhelminthes: Cercomeria) with comments on their adaptive radiation. Can J Zool 63: 411443.[Crossref] [Google Scholar]
  14. Chanawong A, Waikagul J, , 1991. Laboratory studies on host-parasite relationship of Bithynia snails and the liver fluke, Opisthorchis viverrini . Southeast Asian J Trop Med Public Health 22: 235239. [Google Scholar]
  15. Prasopdee S, Kulsantiwong J, Piratae S, Khampoosa P, Thammasiri C, Suwannatrai A, Laha T, Grams R, Loukas A, Tesana S, , 2015. Temperature dependence of Opisthorchis viverrini infection in first intermediate host snail, Bithynia siamensis goniomphalos . Acta Trop 141: 112117.[Crossref] [Google Scholar]
  16. Kanokkanjana K, Garivait S, , 2013. Alternative rice straw management practices to reduce field open burning in Thailand. Int J Environ Sci Dev 4: 119123.[Crossref] [Google Scholar]
  17. 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 . Parasitol Int 61: 3845.[Crossref] [Google Scholar]
  18. Wang YC, Ho RC, Feng CC, Namsanor J, Sithithaworn P, , 2015. An ecological study of Bithynia snails, the first intermediate host of Opisthorchis viverrini in northeast Thailand. Acta Trop 141: 244252.[Crossref] [Google Scholar]
  19. Brandt R, , 1974. The non-marine aquatic Mollusca of Thailand. Arch für Molluskenkd 105: 1423. [Google Scholar]
  20. Upatham E, Sornmani S, Kitikoon V, Lohachit C, Bruch J, , 1983. Identification key for fresh-brackish water snails of Thailand. Malacol Rev 16: 107132. [Google Scholar]
  21. Schell S, , 1970. How to Know the Trematode. Dubuque, IA: WMC Brown Company Publishers, 355. [Google Scholar]
  22. Caron Y, Rondelaud D, Losson B, , 2008. The detection and quantification of a digenean infection in the snail host with special emphasis on Fasciola sp. Parasitol Res 103: 735744.[Crossref] [Google Scholar]
  23. Sunita K, Singh D, , 2011. Fascioliasis control: in vivo and in vitro phytotherapy of vector snail to kill Fasciola larva. J Parasitol Res 240807. doi:10.1155/2011/240807. [Google Scholar]
  24. Kaewkes S, , 2003. Taxonomy and biology of liver flukes. Acta Trop 88: 177186.[Crossref] [Google Scholar]
  25. Cheng T, , 1973. General Parasitology. New York, NY: Academic Press, 965. [Google Scholar]
  26. Upatham E, Sukhapanth N, , 1980. Field studies on the bionomics of Bithynia siamensis siamensis and the transmission of Opisthorchis viverrini in Bangna, Bangkok, Thailand. Southeast Asian J Trop Med Public Health 11: 355358. [Google Scholar]
  27. Lohachit C, , 2001. Ecological Studies of Bithynia siamensis goniomphalos A Snail Intermediate Host of Opisthorchis viverrini in Khon Kaen Province, Northeast Thailand. PhD thesis. Bangkok, Thailand: Mahidol University.
  28. 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 J Trop Med Public Health 36: 653657. [Google Scholar]
  29. 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, Kearney M, Tesana S, , 2011. Effect of soil surface salt on the density and distribution of the snail Bithynia siamensis goniomphalos in northeast Thailand. Geospat Health 5: 183190.[Crossref] [Google Scholar]
  30. Kaewkes W, Kaewkes S, Tesana S, Laha T, Sripa B, , 2012. Fecal bacterial contamination in natural water reservoirs as an indicator of seasonal infection by Opisthorchis viverrini in snail intermediate hosts. Parasitol Int 61: 4951.[Crossref] [Google Scholar]
  31. Harinasuta C, Harinasuta T, , 1984. Opisthorchis viverrini: life cycle, intermediate hosts, transmission to man and geographical distribution in Thailand. Arzneimittelforschung 34: 11641167. [Google Scholar]
  32. Poulin R, , 2006. Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132: 143151.[Crossref] [Google Scholar]
  33. Rondelaud D, Barthe D, , 1987. Fasciola hepatica L.: the productivity of a sporocyst as a function of the size of Lymnaea truncatula Muller. Parasitol Res 74: 155160.[Crossref] [Google Scholar]
  34. Richards C, , 1977. Schistosoma mansoni: susceptibility reversal with age in the snail host Biomphalaria glabrata . Exp Parasitol 42: 165168.[Crossref] [Google Scholar]
  35. Dikkeboom R, Van der Knapp W, Meuleman E, Sminia T, , 1984. Differences between blood cells of juvenile and adult specimens of the pond snail Lymnaea stagnalis . Cell Tissue Res 238: 4347.[Crossref] [Google Scholar]
  36. Dreyfuss G, Vignoles P, Rondelaud D, , 2000. Variability of Fasciola hepatica infection in Lymnaea ovata in relation to snail population and snail age. Parasitol Res 86: 6973.[Crossref] [Google Scholar]
  37. Seppälä O, Karvonen A, Kuosa M, Haataja M, Jokela J, , 2013. Are sick individuals weak competitors? Competitive ability of snails parasitized by a gigantism-inducing trematode. PLoS ONE 8: e79366.[Crossref] [Google Scholar]
  38. Sandland G, Minchella D, , 2003. Effects of diet and Echinostoma revolutum infection on energy allocation patterns in juvenile Lymnaea elodes snails. Oecologia 134: 479486.[Crossref] [Google Scholar]
  39. McCarthy H, Fitzpatrick S, Irwin S, , 2004. Parasite alteration of host shape: a quantitative approach to gigantism helps elucidate evolutionary advantages. Parasitology 128: 714.[Crossref] [Google Scholar]
  40. Lim H, Heyneman D, , 1972. Intramolluscan inter-trematode antagonism: a review of factors influencing the host-parasite system and its possible role in biological control. Adv Parasitol 10: 191268.[Crossref] [Google Scholar]
  41. Sousa W, , 1993. Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecol Monogr 63: 103128.[Crossref] [Google Scholar]
  42. Kuris A, Lafferty K, , 1994. Community structure: larval trematodes in snail hosts. Annu Rev Ecol Syst 25: 189217.[Crossref] [Google Scholar]
  43. Lafferty K, Sammond D, Kuris A, , 1994. Analysis of larval trematode communities. Ecology 75: 22752285.[Crossref] [Google Scholar]
  44. ErhardovaÌ-KotrlaÌ B, , 1971. The Occurrence of Fascioloides magna (Bassi, 1875) in Czechoslovakia. Prague, Czech Republic: Academia, 155. [Google Scholar]

Data & Media loading...

  • Received : 14 Oct 2014
  • Accepted : 18 Mar 2015
  • Published online : 08 Jul 2015

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error