• 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: 1016.

    • Search Google Scholar
    • Export Citation
  • 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: 158168.

    • Search Google Scholar
    • Export Citation
  • 3.

    International Agency for Research on Cancer (IARC) , 2012. Biological agents. A review of human carcinogens. IARC monographs on the evaluation of carcinogenic risks to humans/World Health Organization. International Agency Research on Cancer 100B: 1441.

    • Search Google Scholar
    • Export Citation
  • 4.

    Andrews RH, Sithithaworn P, Petney TN , 2008. Opisthorchis viverrini: an underestimated parasite in world health. Trends Parasitol 24: 497501.

    • Search Google Scholar
    • Export Citation
  • 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: 3845.

    • Search Google Scholar
    • Export Citation
  • 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: 355358.

    • Search Google Scholar
    • Export Citation
  • 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: 545552.

    • Search Google Scholar
    • Export Citation
  • 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: 8793.

    • Search Google Scholar
    • Export Citation
  • 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: 19.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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: 33133321.

    • Search Google Scholar
    • Export Citation
  • 12.

    Mostafa OM , 2007. Effects of Schistosoma mansoni and Schistosoma haematobium infections on calcium content in their intermediate hosts. Parasitol Res 101: 963966.

    • Search Google Scholar
    • Export Citation
  • 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: 464469.

    • Search Google Scholar
    • Export Citation
  • 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: 109119.

    • Search Google Scholar
    • Export Citation
  • 15.

    Krist AC , 2000. Effect of the digenean parasite Proterometra macrostoma on host morphology in the freshwater snail Elimia livescens. J Parasitol 86: 262267.

    • Search Google Scholar
    • Export Citation
  • 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: 391396.

    • Search Google Scholar
    • Export Citation
  • 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: 235239.

    • Search Google Scholar
    • Export Citation
  • 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: 112117.

    • Search Google Scholar
    • Export Citation
  • 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: 151154.

    • Search Google Scholar
    • Export Citation
  • 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: 244252.

    • Search Google Scholar
    • Export Citation
  • 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: 252255.

    • Search Google Scholar
    • Export Citation
  • 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: 321331.

    • Search Google Scholar
    • Export Citation
  • 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: 13231328.

    • Search Google Scholar
    • Export Citation
  • 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: 2575725771.

    • Search Google Scholar
    • Export Citation
  • 25.

    Wang YC, Feng CC, Sithithaworn P , 2013. Environmental determinants of Opisthorchis viverrini prevalence in northeast Thailand. Geospat Health 8: 111123.

    • Search Google Scholar
    • Export Citation
  • 26.

    Wang YC , 2012. Examining landscape determinants of Opisthorchis viverrini transmission. EcoHealth 9: 328341.

  • 27.

    Brandt R , 1974. The non-marine aquatic Mollusca of Thailand. Arch Molluskenkd 105: 1423.

  • 28.

    Schell S , 1970. How to Know the Trematode. Dubuque, IA: WMC Brown Company Publishers, 355.

  • 29.

    Sohn WM , 2009. Fish-borne zoonotic trematode metacercariae in the Republic of Korea. Korean J Parasitol 47: 103113.

  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 32.

    Brady NC, Weil RR , 2002. The Nature and Properties of Soils. Upper Saddle River, NJ: Prentice Hall.

  • 33.

    Blume LJ, Schumacher BA, Schaffer PW, Cappo KA, Papp ML, Van Remortel RD, Coffey DS, Johnson MG, Chaloud DJ , 1990. Handbook of Methods for Acid Deposition Studies Laboratory Analyses for Soil Chemistry. Las Vegas, NV: Environmental Protection Agency, Environmental Monitoring Systems Laboratory.

    • Search Google Scholar
    • Export Citation
  • 34.

    ASTM , 2000. Standard Test Methods for Moisture, Ash, and Organic Matter of Peat and Other Organic Soils. West Conshohocken, PA: American Society for Testing and Materials.

    • Search Google Scholar
    • Export Citation
  • 35.

    Sarkar D, Haldar A , 2005. Physical and Chemical Methods in Soil Analysis. New Delhi, India: New Age International.

  • 36.

    Storti F, Balsamo F , 2010. Particle size distributions by laser diffraction: sensitivity of granular matter strength to analytical operating procedures. Solid Earth 1: 2548.

    • Search Google Scholar
    • Export Citation
  • 37.

    USEPA , 1996. Test Methods for Evaluating Solid Wastes, Physical and Chemical Methods (SW-846). Washington, DC: United States Environmental Protection Agency.

    • Search Google Scholar
    • Export Citation
  • 38.

    Lavkulich LM , 1981. Methods Manual, Pedology Laboratory. British Columbia, Canada: Department of Soil Science, University of British Columbia.

    • Search Google Scholar
    • Export Citation
  • 39.

    Robertson GP, Coleman DC, Bledsoe CS, Sollins P , 1999. Standard Soil Methods for Long-Term Ecological Research. New York, NY: Oxford University Press, 106114.

    • Search Google Scholar
    • Export Citation
  • 40.

    Ter Braak CJ , 1986. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67: 11671179.

    • Search Google Scholar
    • Export Citation
  • 41.

    Hammer Ø, Harper DA, Ryan PD , 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electronica 4: 19.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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: 975982.

    • Search Google Scholar
    • Export Citation
  • 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).

  • 45.

    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: 183190.

    • Search Google Scholar
    • Export Citation
  • 46.

    Satrawaha R, Prathepha P, Andrews R, Petney T , 2008. Fundamental hydrochemical parameters of the Songkhram River in northeast Thailand: foundation data for the study of an endangered tropical wetland ecosystem. Limnology 10: 715.

    • Search Google Scholar
    • Export Citation
  • 47.

    Pratumchart K, Suwannatrai K, Sereewong C, Thinkhamrop K, Chaiyos J, Boonmars T, Suwannatrai AT , 2019. Ecological niche model based on maximum entropy for mapping distribution of Bithynia siamensis goniomphalos, first intermediate host snail of Opisthorchis viverrini in Thailand. Acta Trop 193: 183191.

    • Search Google Scholar
    • Export Citation
  • 48.

    Souza WP, Grosholz ED, Bell SS, McCoy ED, Mushinsky HRHabitat Structure: The Physical Arrangement of Objects in Space. London, United Kingdom: Chapman and Hall, 300324.

    • Search Google Scholar
    • Export Citation
  • 49.

    Jigyasu HV, Singh VK , 2010. Effect of environmental factor on the fecundity, hatchability and survival of the snail Lymnaea acuminata (Lamark): vector of fascioliasis. J Water Health 8: 109115.

    • Search Google Scholar
    • Export Citation
  • 50.

    Rojanasoonthon S , 1971. Morphology and Genesis of Gray Podzolic Soils in Thailand. PhD thesis, Oregon State University Corvallis, OR.

  • 51.

    Cheng TC, Lee FO , 1971. Glucose levels in the mollusc Biomphalaria glabrata infected with Schistosoma mansoni. J Invertebr Pathol 18: 395399.

    • Search Google Scholar
    • Export Citation
  • 52.

    Layman LR, Dory AC, Koehnlein KM, Fried B, Sherma J , 1996. Effects of Echinostoma trivolvis (trematoda) infection on metallic ions in the host snail Helisoma trivolvis (gastropoda). Parasitol Res 82: 1921.

    • Search Google Scholar
    • Export Citation
  • 53.

    Ong JH, Chejlava M, Fried B, Koehnlein KM, Bosavage GL, Sherma J , 2004. Effects of Schistosoma mansoni infection on inorganic elements in the snail Biomphalaria glabrata. J Helminthol 78: 343346.

    • Search Google Scholar
    • Export Citation
  • 54.

    Clausen JH, Madson H, Phan TV, Dalsgaard A, Murrell KD , 2015. Integrated parasite management: path to sustainable control of fishborne trematodes in aquaculture. Trends Parasitol 31: 815.

    • Search Google Scholar
    • Export Citation
  • 55.

    Wang YC, Liew TZ, Namsanor J, Sithithaworn P , 2020. Assessing the role of Filopaludina martensi martensi as a biocontrol agent of Bithynia siamensis goniomphalos, the first intermediate host of Opisthorchis viverrini. Parasitol Res 119: 34153431.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 8495 8495 50
Full Text Views 45 45 3
PDF Downloads 47 47 2
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

Effects of Environmental Factors and Infecting Trematodes on the Size and Inorganic Elements of Bithynia siamensis goniomphalos Snails in Northeast Thailand

Yi-Chen WangDepartment of Geography, National University of Singapore, Singapore;

Search for other papers by Yi-Chen Wang in
Current site
Google Scholar
PubMed
Close
,
Siew Ping YeoDepartment of Geography, National University of Singapore, Singapore;

Search for other papers by Siew Ping Yeo in
Current site
Google Scholar
PubMed
Close
,
Jutamas NamsanorDepartment of Geography, National University of Singapore, Singapore;
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;

Search for other papers by Jutamas Namsanor in
Current site
Google Scholar
PubMed
Close
,
Paiboon SithithawornDepartment of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

Search for other papers by Paiboon Sithithaworn in
Current site
Google Scholar
PubMed
Close
, and
Shuhan YangDepartment of Geography, National University of Singapore, Singapore;

Search for other papers by Shuhan Yang in
Current site
Google Scholar
PubMed
Close
Restricted access

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.

    • Supplemental Materials (PDF 353 KB)

Author Notes

Address correspondence to Yi-Chen Wang, Department of Geography, National University of Singapore, 1 Arts Link, Singapore 117570, Singapore. E-mail: geowyc@nus.edu.sg

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.

Save