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Kiatsopit N, Sithithaworn P, Kopolrat K, Andrews RH, Petney TN , 2014. Seasonal cercarial emergence patterns of Opisthorchis viverrini infecting Bithynia siamensis goniomphalos from Vientiane Province Lao PDR. Parasit Vectors 7: 551.
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Laoprom N, Kiatsopit N, Sithithaworn P, Kopolrat K, Namsanor J, Andrews RH, Petney TN , 2016. Cercarial emergence patterns for Opisthorchis viverrini sensu lato infecting Bithynia siamensis goniomphalos from Sakon Nakhon Province, Thailand. Parasitol Res 115: 3313–3321.
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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.
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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: 112–117.
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Afomezie PI, Ebenebe CI, Njoku OO, Ufele AN, Okonko JC , 2011. Effects of different soil treatments on weight gain, shell length and shell aperture of snails (Archachatina marginata). Pak J Nutr 10: 151–154.
-
20.
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: 244–252.
-
21.
White MM, Chejlava M, Fried B, Sherma J , 2005. Effects of various larval digeneans on the calcium carbonate content of the shells of Helisoma trivolvis, Biomphalaria glabrata, and Physa sp. Parasitol Res 95: 252–255.
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Chiu YW, Chen HC, Lee SC, Chen CA, 2002. Morphometric analysis of shell and operculum variations in the Viviparid snail, Cipangopaludina chinensis (Mollusca: Gastropoda), in Taiwan. Zool Stud 41: 321–331.
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Miura O, Kuris AM, Torchin ME, Hechinger RF, Chiba S , 2006. Parasites alter host phenotype and may create a new ecological niche for snail hosts. Proc Biol Sci 273: 1323–1328.
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Parveen S, Chakraborty A, Kr. Chanda D, Pramanik S, Barik A, Aditya G , 2020. Microstructure analysis and chemical and mechanical characterization of the shells of three freshwater snails. ACS Omega 40: 25757–25771.
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Effects of Environmental Factors and Infecting Trematodes on the Size and Inorganic Elements of Bithynia siamensis goniomphalos Snails in Northeast Thailand
Yi-Chen Wang
Yi-Chen Wang
Department of Geography, National University of Singapore, Singapore;
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Siew Ping Yeo
Siew Ping Yeo
Department of Geography, National University of Singapore, Singapore;
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Jutamas Namsanor
Jutamas Namsanor
Department of Geography, National University of Singapore, Singapore;
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Paiboon Sithithaworn
Paiboon Sithithaworn
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand
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Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand
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Shuhan Yang
Shuhan Yang
Department of Geography, National University of Singapore, Singapore;
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ABSTRACT.
Infection with the foodborne trematode, Opisthorchis viverrini, is a major public health issue in southeast Asia. The freshwater snail, Bithynia siamensis goniomphalos, is an intermediate host of O. viverrini and other trematode species. Understanding the effects of environmental conditions and infecting trematodes on B.s. goniomphalos snails is thus crucial for the potential influences on trematode transmission. This study measured environmental variables of water and soil properties, and analyzed B.s. goniomphalos snails for their trematode infection, snail shell length, and inorganic elemental concentration, from 30 localities in northeast Thailand. The results showed that prevalence of trematode infection in B.s. goniomphalos was 3.82%. Nine types of trematode cercariae were identified, with virgulate type 1 as the most common (1.23%). Opisthorchis viverrini-infected snails were mostly found in low-humic gley soils in Sakon Nakhon Province, and were associated with water dissolved oxygen and soil pH. Compared with uninfected snails, larger sizes were observed in virgulate type 1 and pleurolophocerca-infected snails, whereas hypercalcification was noticed in virgulate type 1, virgulate type 3, and pleurolophocerca-infected snails. Infected snails were more sensitive toward environmental conditions, possibly because of the dynamic parasitic processes between trematodes and hosts. Among the environmental factors, soil texture (i.e., sand, silt, and clay compositions) exhibited more significant correlations with B.s. goniomphalos shell characteristics regardless of the trematode infection types. The findings of this study underscore the need to consider the effects of environmental conditions and trematode species-specific pathogenic processes for a more effective and sustainable parasitic control and prevention effort.
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Author Notes
Financial support: The project is supported by the National University of Singapore through the Academic Research Fund (Grant Number: FY2017-FRC3-008, WBS: R-109-000-235-115).
Authors’ addresses: Yi-Chen Wang, Siew Ping Yeo, and Shuhan Yang, Department of Geography, National University of Singapore, Singapore, E-mails: geowyc@nus.edu.sg, yeosiewping@gmail.com, and yangshuhanaz@163.com. Jutamas Namsanor, Department of Geography, National University of Singapore, Singapore, and Department of Parasitology, Faculty of Medicine, Khon Kaen University, Thailand, E-mail: jutamas.namsanor@gmail.com. Paiboon Sithithaworn, Department of Parasitology, Faculty of Medicine, Khon Kaen University, Thailand, and Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Thailand, E-mail: paibsit@gmail.com.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
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.
-
2.
Sripa B, Bethony JM, Sithithaworn P, Kaewkes S, Mairiang E, Loukas A, Mulvenna J, Laha T, Hotez PJ, Brindley PJ , 2012. Opisthorchiasis and Opisthorchis-associated cholangiocarcinoma in Thailand and Laos. Acta Trop 120: 158–168.
-
3.
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4.
Andrews RH, Sithithaworn P, Petney TN , 2008. Opisthorchis viverrini: an underestimated parasite in world health. Trends Parasitol 24: 497–501.
-
5.
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: 38–45.
-
6.
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.
-
7.
Brockelman WY, Upatham ES, Viyanant V, Ardsungnoen S, Chantanawat R , 1986. Field studies on the transmission of the liver fluke, Opisthorchis viverrini, in northeast Thailand: population changes of the snail intermediate host. Int J Parasitol 16: 545–552.
-
8.
Namsanor J, Sithithaworn P, Kopolrat K, Kiatsopit N, Pitaksakulrat O, Tesana S, Andrews RH, Petney TN , 2015. Seasonal transmission of Opisthorchis viverrini sensu lato and a lecithodendriid trematode species in Bithynia siamensis goniomphalos snails in northeast Thailand. Am J Trop Med Hyg 93: 87–93.
-
9.
Kiatsopit N, Sithithaworn P, Kopolrat K, Namsanor J, Andrews RH, Petney TN , 2016. Trematode diversity in the freshwater snail Bithynia siamensis goniomphalos sensu lato from Thailand and Lao PDR. J Helminthol 6: 1–9.
-
10.
Kiatsopit N, Sithithaworn P, Kopolrat K, Andrews RH, Petney TN , 2014. Seasonal cercarial emergence patterns of Opisthorchis viverrini infecting Bithynia siamensis goniomphalos from Vientiane Province Lao PDR. Parasit Vectors 7: 551.
-
11.
Laoprom N, Kiatsopit N, Sithithaworn P, Kopolrat K, Namsanor J, Andrews RH, Petney TN , 2016. Cercarial emergence patterns for Opisthorchis viverrini sensu lato infecting Bithynia siamensis goniomphalos from Sakon Nakhon Province, Thailand. Parasitol Res 115: 3313–3321.
-
12.
Mostafa OM , 2007. Effects of Schistosoma mansoni and Schistosoma haematobium infections on calcium content in their intermediate hosts. Parasitol Res 101: 963–966.
-
13.
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.
-
14.
Wilson RA, Denison J , 1980. The parasitic castration and gigantism of Lymnaea truncatula infected with the larval stages of Fasciola hepatica. Z Parasitenkd 61: 109–119.
-
15.
Krist AC , 2000. Effect of the digenean parasite Proterometra macrostoma on host morphology in the freshwater snail Elimia livescens. J Parasitol 86: 262–267.
-
16.
Chapuis E , 2009. Correlation between parasite prevalence and adult size in a trematode-mollusc system: evidence for evolutionary gigantism in the freshwater snail Galba truncatula? J Molluscan Stud 75: 391–396.
-
17.
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.
-
18.
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: 112–117.
-
19.
Afomezie PI, Ebenebe CI, Njoku OO, Ufele AN, Okonko JC , 2011. Effects of different soil treatments on weight gain, shell length and shell aperture of snails (Archachatina marginata). Pak J Nutr 10: 151–154.
-
20.
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: 244–252.
-
21.
White MM, Chejlava M, Fried B, Sherma J , 2005. Effects of various larval digeneans on the calcium carbonate content of the shells of Helisoma trivolvis, Biomphalaria glabrata, and Physa sp. Parasitol Res 95: 252–255.
-
22.
Chiu YW, Chen HC, Lee SC, Chen CA, 2002. Morphometric analysis of shell and operculum variations in the Viviparid snail, Cipangopaludina chinensis (Mollusca: Gastropoda), in Taiwan. Zool Stud 41: 321–331.
-
23.
Miura O, Kuris AM, Torchin ME, Hechinger RF, Chiba S , 2006. Parasites alter host phenotype and may create a new ecological niche for snail hosts. Proc Biol Sci 273: 1323–1328.
-
24.
Parveen S, Chakraborty A, Kr. Chanda D, Pramanik S, Barik A, Aditya G , 2020. Microstructure analysis and chemical and mechanical characterization of the shells of three freshwater snails. ACS Omega 40: 25757–25771.
-
25.
Wang YC, Feng CC, Sithithaworn P , 2013. Environmental determinants of Opisthorchis viverrini prevalence in northeast Thailand. Geospat Health 8: 111–123.
-
26.
Wang YC , 2012. Examining landscape determinants of Opisthorchis viverrini transmission. EcoHealth 9: 328–341.
-
27.
Brandt R , 1974. The non-marine aquatic Mollusca of Thailand. Arch Molluskenkd 105: 1–423.
-
28.
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-
29.
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-
30.
Gottdenker NL, Calzada JE, Saldaña A, Carroll CR , 2011. Association of anthropogenic land use change and increased abundance of the Chagas disease vector Rhodnius pallescens in a rural landscape of Panama. Am J Trop Med Hyg 84: 70.
-
31.
Lemaitre M, Watier L, Briand V, Garcia A, Le Hesran JY, Cot M , 2014. Coinfection with Plasmodium falciparum and Schistosoma haematobium: additional evidence of the protective effect of Schistosomiasis on malaria in Senegalese children. Am J Trop Med Hyg 90: 329.
-
32.
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33.
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35.
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36.
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37.
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-
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-
41.
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-
42.
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.
-
43.
Kulsantiwong J, Prasopdee S, Labbunruang N, Chaiyasaeng M, Tesana S , 2017. Habitats and trematode infection of Bithynia siamensis goniomphalos in Udon Thani Province, Thailand. Southeast Asian J Trop Med Public Health 48: 975–982.
-
44.
Bureau of Epidemiology, Department of Disease Control, Ministry of Public Health, Thailand, 2001–2006. Reported the Surveillance of Liver Fluke. National Notifiable Disease Surveillance (Report 506).
-
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Suwannatrai A et al.2011. Effect of soil surface salt on the density and distribution of the snail Bithynia siamensis goniomphalos in northeast Thailand. Geospat Health 5: 183–190.
-
46.
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