Abstract
Among the snail species acting as hosts for medically significant trematodes, only three taxa of Bithynia are responsible for transmitting the carcinogenic liver fluke Opisthorchis viverrini to humans in different geographical areas. Although B. siamensis goniomphalos is the primary species responsible for O. viverrini transmission in endemic areas, B. siamensis siamensis and B. funiculata remain potential hosts for transmission. This study objects to determine the susceptibility of B. siamensis siamensis and B. funiculata to O. viverrini to assess the risk of O. viverrini transmission in non-endemic areas. The snails of both species were first introduced to O. viverrini eggs, after which O. viverrini infection was investigated using specific PCR primers after a period of 1, 7, 14, 28, and 56 days post-infection (dpi). Opisthorchis viverrini infection in both B. siamensis siamensis and B. funiculata was high in the early period (1 and 7 dpi) while decreasing over time. It was also shown that the odds of susceptibility to O. viverrini infection in B. siamensis siamensis were 64.5% higher relative to the odds of susceptibility in B. funiculata (P < 0.05). Results of this study provide an early insight into the Bithynia-Opisthorchis relationship and thus have great potential to assess risk and raise awareness of opisthorchiasis in non-endemic regions, especially in regions endemic for B. siamensis siamensis.
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References
Adema CM, Deutekom-Mulder ECV, Knaap WPWVD, Sminia T (1994) Schistosomicidal activities of Lymnaea stagnalis haemocytes: the role of oxygen radicals. Parasitol 109:479–485. https://doi.org/10.1017/S0031182000080732
Aung WPP, Htoon TT, Tin HH, Thinn KK, Sanpool O, Jongthawin J, Sadaow L, Phosuk I, Rodpai R, Intapan PM, Maleewong W (2017) First report and molecular identification of Opisthorchis viverrini infection in human communities from Lower Myanmar. PLoS One 12:e0177130. https://doi.org/10.1371/journal.pone.0177130
Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V (2009) WHO International Agency for Research on Cancer Monograph Working Group. A review of human carcinogens–Part B: biological agents. Lancet Oncol 10:321–322. https://doi.org/10.1016/S1470-2045(09)70096-8
Brandt RAM (1974) The non-marine aquatic Mollusca of Thailand. Archiv Für Molluskenkunde 105:1–423
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 22:235–239
Chitramvong YP (1992) The Bithyniidae (Gastropoda: Prosobanchia) of Thailand: comparative external morphology. Malacol Rev 25:21–38
Dao HTT, Dermauw V, Gabriel S, Suwannatrai A, Tesana S, Nguyen GTT, Dorny P (2017) Opisthorchis viverrini infection in the snail and fish intermediate hosts in Central Vietnam. Acta Trop 170:120–125. https://doi.org/10.1016/j.actatropica.2017.02.028
Harinasuta C, Harinasuta T (1984) Opisthorchis viverrini: life cycle, intermediate hosts, transmission to man and geographical distribution in Thailand. Arzneimittelforschung 34:1164–1167
Humbert E, Coustau C (2001) Refractoriness of host haemocytes to parasite immunosuppressive factors as a putative resistance mechanism in the Biomphalaria glabrata-Echinostoma caproni system. Parasitology 122:651–660. https://doi.org/10.1017/S003118200100782X
IARC (2002) Cancer incidence in five continents. Volume VIII. IARC Scientific Publications No. 155, Lyon
Jongsuksuntigul P, Imsomboon T (2003) Opisthorchiasis control in Thailand. Acta Trop 88:229–232. https://doi.org/10.1016/j.actatropica.2003.01.002
Khampoosa P, Jones MK, Lovas EM, Srisawangwong T, Laha T, Piratae S, Thammasiri C, Suwannatrai A, Sripanidkulchai B, Eursitthichai V, Tesana S (2012) Light and electron microscopy observations of embryogenesis and egg development in the human liver fluke, Opisthorchis viverrini (Platyhelminthes, Digenea). Parasitol Res 110:799–808. https://doi.org/10.1007/s00436-011-2557-3
Kiatsopit N, Sithithaworn P, Saijuntha W, Boonmars T, Tesana S, Sithithaworn J, Petney TN, Andrews RH (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 86:464–469. https://doi.org/10.4269/ajtmh.2012.11-0217
Kulsantiwong J, Prasopdee S, Ruangsittichai J, Ruangjirachuporn W, Boonmars T, Viyanant V, Pierossi P, Hebert PD, Tesana S (2013) DNA barcode identification of freshwater snails in the family Bithyniidae from Thailand. PLoS One 8:e79144. https://doi.org/10.1371/journal.pone.0079144
Kulsantiwong J, Prasopdee S, Piratae S, Khampoosa P, Thammasiri C, Suwannatrai A, Boonmars T, Viyanant V, Ruangsitichai J, Tarbsripair P, Tesana S (2015) Trematode infection of freshwater snail, Family Bithyniidae in Thailand. Southeast Asian J Trop Med Public Health 46:396–405
Lea I (1856) Description of thirteen new species of exotic Peristomata. Proc Acad Natl Sci Phila 8(3):109–111
Leiper RT (1915) Notes of the occurence of parasites presumably rare in man in man. J R Army Med Corps 24:569–575
Miyamoto K, Kirinoki M, Matsuda H, Hayashi N, Chigusa Y, Sinuon M, Chuor CM, Kitikoon V (2014) Field survey focused on Opisthorchis viverrini infection in five provinces of Cambodia. Parasitol Int 63:366–373. https://doi.org/10.1016/j.parint.2013.12.003
MolluscaBase (2021) MolluscaBase Eds. Genus Bithynia (Leach, 1818). [Online]. http://www.molluscabase.org/aphia.php?p=taxdetails&id=182698. Accessed 3 Mar 2021
Morelet A (1866) Diagnoses de coquilles nouvelles de l'Indo-Chine. Revue et magasin de zoologie pure et appliquée (sér. 2) 18:165–168
Ngern-Klun R, Sukontason KL, Tesana S, Sripakdee D, Irvine KN, Sukontason K (2006) Field investigation of Bithynia funiculata, intermediate host of Opisthorchis viverrini in northern Thailand. Southeast Asian J Trop Med Public Health 37:662–672
Prasopdee S, Sotillo J, Tesana S, Laha T, Kulsantiwong J, Nolan MJ, Loukas A, Cantacessi C (2014) RNA-Seq reveals infection-induced gene expression changes in the snail intermediate host of the carcinogenic liver fluke, Opisthorchis viverrini. Plos Negl Trop Dis 8:e2765. https://doi.org/10.1371/journal.pntd.0002765
Prasopdee S, Kulsantiwong J, Piratae S, Khampoosa P, Thammasiri C, Suwannatrai A, Laha T, Grams R, Loukas A, Tesana S (2015a) Temperature dependence of Opisthorchis viverrini infection in first intermediate host snail, Bithynia siamensis goniomphalos. Acta Trop 141:112–117. https://doi.org/10.1016/j.actatropica.2013.10.011
Prasopdee S, Tesana S, Cantacessi C, Laha T, Mulvenna J, Grams R, Loukas A, Sotillo J (2015b) Proteomic profile of Bithynia siamensis goniomphalos snails upon infection with the carcinogenic liver fluke Opisthorchis viverrini. J Proteomics 113:281–291. https://doi.org/10.1016/j.jprot.2014.09.018
Prasopdee S, Thitapakorn V, Sathavornmanee T, Tesana S (2019) A comprehensive review of omics and host-parasite interplays studies, towards control of Opisthorchis viverrini infection for prevention of cholangiocarcinoma. Acta Trop 196:76–82. https://doi.org/10.1016/j.actatropica.2019.05.011
Prasopdee S, Kulsantiwong J, Sathavornmanee T, Thitapakorn V (2020) The effects of temperature and salinity on the longevity of Opisthorchis viverrini cercariae: a climate change concern. J Helminthol 94:e165. https://doi.org/10.1017/S0022149X20000498
Sithithaworn P, Haswell-Elkins M (2003) Epidemiology of Opisthorchis viverrini. Acta Trop 88:187–194. https://doi.org/10.1016/j.actatropica.2003.02.001
Sithithaworn P, Yongvanit P, Tesana S, Pairojkul C (2008) Liver flukes. In: Murrell KD, Fried B (eds) Food-borne parasitic zoonoses. Springer Verlag, New York, pp 1–51
Sithithaworn P, Andrews RH, Nguyen VD, Wongsaroj T, Sinuon M, Odermatt P, Nawa Y, Liang S, Brindley PJ, Sripa B (2012) The current status of opisthorchiasis and clonorchiasis in the Mekong Basin. Parasitol Int 61:10–16. https://doi.org/10.1016/j.parint.2011.08.014
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 36:653–657
Sumethanurungkul P (1970) Studies on physical effects on snail intermediate hosts of a liver fluke (Opisthorchis viverrini). Mahidol University, Thesis for The Degree of Master of Science
Suwannatrai K, Suwannatrai A, Tabsripair P, Welbat JU, Tangkawattana S, Cantacessi C, Mulvenna J, Tesana S, Loukas A, Sotillo J (2016) Differential protein expression in the hemolymph of Bithynia siamensis goniomphalos infected with Opisthorchis viverrini. PLoS Negl Trop Dis 10:e0005104. https://doi.org/10.1371/journal.pntd.0005104
Suwannatrai A, Saichua P, Haswell M (2018) Epidemiology of Opisthorchis viverrini infection. Adv Parasitol 101:41–67. https://doi.org/10.1016/bs.apar.2018.05.002
Upatham ES, 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 11:355–358
Upatham ES, Santasiri S, Kitikoon V, Lohachit C, Burch JB (1983) Identification key for the fresh-and brackish-water snails of Thailand. Malacol Rev 16:107–132
Walker B (1927) The molluscan hosts of Clonorchis sinensis (Cobbold) in Japan, China and South-Eastern Asia, and other species of molluscs closely related to them. American Journal of Hygiene. Monographic Series 8:208–250
WHO (1995) Control of foodborne trematode infections. Report of a WHO Study Group. World Health Organ Tech Rep Ser 849:1–157
Winnepenninckx B, Backeljau T, De Wachter R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9:407. https://doi.org/10.1016/0168-9525(93)90102-N
Wongratanacheewin S, Pumidonming W, Sermswan RW, Maleewong W (2001) Development of a PCR-based method for the detection of Opisthorchis viverrini in experimentally infected hamsters. Parasitology 122:175–180. https://doi.org/10.1017/S0031182001007235
Wykoff DE, Harinasuta C, Juttijudata P, Winn MM (1965) Opisthorchis viverrini in Thailand–the life cycle and comparison with O. felineus. J Parasitol 51:207–214. https://doi.org/10.2307/3276083
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The authors wish to thank Ms. Montinee Pholhelm for her technical assistance.
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This work was supported by Thailand Research Fund (TRF) grant for New Researchers (grant number TRG5880212).
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Jutharat Kulsantiwong: methodology, investigation, data analysis, writing-original draft. Veerachai Thitapakorn: methodology, validation, writing-review and editing. Thanakrit Sathavornmanee: data analysis, writing-review and editing. Siraphatsorn Yusuk: investigation, visualization. Opal Pitaksakulrat: validation, writing-review and editing. Smarn Tesana: conceptualization, methodology, writing-review and editing. Sattrachai Prasopdee: conceptualization, methodology, investigation, data analysis, writing-original draft, funding acquisition.
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Kulsantiwong, J., Thitapakorn, V., Sathavornmanee, T. et al. Susceptibility patterns of Bithynia siamensis siamensis and Bithynia funiculata to Opisthorchis viverrini infection: an indication of the risk of opisthorchiasis transmission in non-endemic areas. Parasitol Res 121, 3495–3501 (2022). https://doi.org/10.1007/s00436-022-07672-8
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DOI: https://doi.org/10.1007/s00436-022-07672-8