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Trematode diversity in the freshwater snail Bithyniasiamensisgoniomphalos sensu lato from Thailand and Lao PDR

Published online by Cambridge University Press:  06 May 2015

N. Kiatsopit,
P. Sithithaworn,
K. Kopolrat,
J. Namsanor,
R.H. Andrews and
T.N. Petney
N. Kiatsopit
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, ThailandLiver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand
P. Sithithaworn*
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, ThailandLiver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand
K. Kopolrat
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, ThailandLiver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand
J. Namsanor
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, ThailandLiver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand
R.H. Andrews
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, ThailandLiver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, ThailandCholangiocarcinoma Screening and Care Program (CASCAP), Khon Kaen University, 40002 ThailandImperial College London, Faculty of Medicine, St Mary's Campus, South Wharf Street, London W2 1NY, UK
T.N. Petney
Affiliation:
Cholangiocarcinoma Screening and Care Program (CASCAP), Khon Kaen University, 40002 ThailandInstitute of Zoology 1: Ecology and Parasitology, University of Karlsruhe, Kornblumen Strasse 13, Karlsruhe, Germany
*
*Fax: +66 43202475 E-mail: paibsit@gmail.com
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Abstract

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

Information

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 3 , May 2016, pp. 312 - 320
Copyright
Copyright © Cambridge University Press 2015 

Introduction

Opisthorchis viverrini sensu lato is a carcinogenic, food-borne trematode endemic in continental South-East Asian countries, especially in Thailand and Lao PDR (Sithithaworn et al., Reference Sithithaworn, Andrews, Nguyen, Wongsaroj, Sinuon, Odermatt, Nawa, Liang, Brindley and Sripa2012a). Recent evidence shows that O. viverrini s.l. is a species complex, with distinct genetic groups in different wetlands (Saijuntha et al., Reference Saijuntha, Sithithaworn, Wongkham, Laha, Pipitgool, Tesana, Chilton, Petney and Andrews2007, Andrews et al., Reference Andrews, Sithithaworn and Petney2008; Laoprom et al., Reference Laoprom, Saijuntha, Sithithaworn, Wongkham, Laha, Ando, Andrews and Petney2009, Reference Laoprom, Sithithaworn, Ando, Sithithaworn, Wongkham, Laha, Klinbunga, Webster and Andrews2010, Reference Laoprom, Sithithaworn, Andrews, Ando, Laha, Klinbunga, Webster and Petney2012). Members of this complex cause major medical problems, including bile duct cancer (cholangiocarcinoma), which lead to significant levels of human morbidity and mortality (Saijuntha et al., Reference Saijuntha, Sithithaworn, Wongkham, Laha, Pipitgool, Tesana, Chilton, Petney and Andrews2007; Andrews et al., Reference Andrews, Sithithaworn and Petney2008; Sithithaworn et al., Reference Sithithaworn, Andrews, Petney, Saijuntha and Laoprom2012b). High prevalences of infection with O. viverrini s.l. of up to 50% in human and fish intermediate hosts have been reported (Vichasri et al., Reference Vichasri, Viyanant and Upatham1982; Sithithaworn et al., Reference Sithithaworn, Pipitgool, Srisawangwong, Elkins and Haswell-Elkins1997, Reference Sithithaworn, Andrews, Nguyen, Wongsaroj, Sinuon, Odermatt, Nawa, Liang, Brindley and Sripa2012a), but the prevalences in snails are much lower, ranging from < 1% to about 9% (Lohachit, 2004–Reference Lohachit2005; Sri-Aroon et al., Reference Sri-Aroon, Butraporn, Limsomboon, Kerdpuech, Kaewpoolsri and Kiatsiri2005, Reference Sri-Aroon, Butraporn, Limsoomboon, Kaewpoolsri, Chusongsang, Charoenjai, Chusongsang, Numnuan and Kiatsiri2007; Kiatsopit et al., Reference Kiatsopit, Sithithaworn, Saijuntha, Boonmars, Tesana, Sithithaworn, Petney and Andrews2012; Petney et al., Reference Petney, Sithithaworn, Andrews, Kiatsopit, Tesana, Grundy-Warr and Ziegler2012). The flukes have a complex life cycle, including freshwater snails as first intermediate hosts. A wide variety of freshwater cyprinid fishes act as second intermediate hosts, while humans are the most important final hosts, although cats and dogs can harbour adult worms (Sithithaworn et al., Reference Sithithaworn, Andrews, Nguyen, Wongsaroj, Sinuon, Odermatt, Nawa, Liang, Brindley and Sripa2012a; Petney et al., Reference Petney, Andrews, Saijuntha, Wenz-Mucke and Sithithaworn2013).

All trematodes use molluscs, in which asexual reproduction occurs, as intermediate hosts. Thus, molluscs play a critical role in the life cycle of the trematodes as multiplying hosts. The freshwater snail Bithynia siamensis goniomphalos sensu lato is widely distributed in north-east Thailand and Lao PDR (Petney et al., Reference Petney, Sithithaworn, Andrews, Kiatsopit, Tesana, Grundy-Warr and Ziegler2012; Kiatsopit et al., Reference Kiatsopit, Sithithaworn, Saijuntha, Petney and Andrews2013). Bithynia s. goniomphalos is a species complex containing two groups with potentially at least nine morphologically similar but genetically distinct cryptic species (taxa) (Kiatsopit et al., Reference Kiatsopit, Sithithaworn, Saijuntha, Petney and Andrews2013). Snails from this complex play a crucial role in the life cycle of O. viverrini, being its first intermediate host (Sithithaworn et al., Reference Sithithaworn, Andrews, Nguyen, Wongsaroj, Sinuon, Odermatt, Nawa, Liang, Brindley and Sripa2012a). A survey of previously published data on trematode cercariae from Thailand and Lao PDR shows that several taxonomic groups infect these snails. In B. s. goniomphalos s.l. from Thailand, 15 groups of cercariae have been found: amphistome, echinostome, monostome, strigea, furcocercaria, pleurolophocercous, parapleurolophocercous, lophocercous, virgulate, ubiquita, xiphidiocercaria, ophthalmoxiphidiocercaria, tailless cercariae, cystophorous and gymnocephalous cercariae (Ito et al., Reference Ito, Papasarathorn and Tongkoom1962; Wykoff et al., Reference Wykoff, Harinasuta, Juttijudata and Winn1965; Adam et al., Reference Adam, Arnold, Pipitgool, Sithithaworn, Hinz and Storch1993; Nithiuthai et al., Reference Nithiuthai, Wiwanitkit, Suwansaksri and Chaengphukeaw2002; Lohachit, 2004–Reference Lohachit2005; Kodcharin, Reference Kodcharin2005; Sri-Aroon et al., Reference Sri-Aroon, Butraporn, Limsomboon, Kerdpuech, Kaewpoolsri and Kiatsiri2005, Reference Sri-Aroon, Butraporn, Limsoomboon, Kaewpoolsri, Chusongsang, Charoenjai, Chusongsang, Numnuan and Kiatsiri2007; Tesana et al., Reference Tesana, Thapsripair, Suwannatrai, Harauy, Piratae, Khampoosa, Thammasiri, Prasopdee, Kulsantiwong, Chalorkpunrut and Jones2014). Only O. viverrini and one pleurolophocercous species have been reported so far from B. s. goniomphalos s.l. from Lao PDR (Ditrich et al., Reference Ditrich, Scholz and Giboda1990, Reference Ditrich, Nasincova, Scholz and Giboda1992; Giboda et al., Reference Giboda, Ditrich, Scholz, Viengsay and Bouaphanh1991). Cercariae from eight groups were shed from Bithynia siamensis siamensis (Upatham & Sukhapanth, Reference Upatham and Sukhapanth1980; Chontananarth et al., Reference Chontananarth, Wongsawad and Chai2013) and four from Bithynia funiculata (Ngern-klun et al., Reference Ngern-klun, Sukontason, Tesana, Sripakdee, Irvine and Sukontason2006), both of which can also act as hosts for O. viverrini.

The aim of the present study was to establish a comprehensive understanding of the diversity of larval-stage trematodes occurring in B. s. goniomphalos s.l. in Thailand and Lao PDR.

Materials and methods

Study localities

Bithynia s. goniomphalos s.l. (n= 11,756) were collected from 29 Thai localities in nine provinces: Buri Ram, Surin, Chaiya Phum, Maha Sarakham, Khon Kaen, Kalasin, Mukdahan, Sakon Nakhon and Nakhon Phanom. In Lao PDR, snail samples (n= 10,507) were collected from 21 localities in Vientiane Province and six localities in Savannakhet Province (table 1). Snails were collected from 2009 to 2014 by handpicking and dredging the sediment with a scoop. They were then cleaned, dried and placed into plastic bags in the field before being transported to the laboratory, where they were identified using standard morphological criteria (Brandt, Reference Brandt1974; Upatham et al., Reference Upatham, Sornmani, Kitikoon, Lohachit and Bruch1983; Chitramvong, Reference Chitramvong1992).

Table 1

The composition of cercarial types and the number of infected snails in Bithynia siamensis goniomphalos samples collected from localities in Thailand and Lao PDR (see fig. 1 for cercarial types and table 2 for prevalence values).

Other cercarial types: D, 1 snail; E, no data; J, 5 snails; P, 2 snails; R, 1 snail (all types were found in Thailand, Sakon Nakhon province, Songkram River).

Screening of snails for cercariae

Snails collected from each site were examined by the cercarial shedding method (Kiatsopit et al., Reference Kiatsopit, Sithithaworn, Saijuntha, Boonmars, Tesana, Sithithaworn, Petney and Andrews2012). Each snail was placed separately into a small plastic container (3 cm in diameter by 2.5 cm high) filled with 5 ml dechlorinated water. The containers were covered with a lid studded with pins to prevent the snail from escaping. The snails were exposed to artificial light (1200 lx) for 5 h during the day at room temperature (25 ± 2°C) during which shedding took place. The containers were checked for the presence of cercariae under a stereomicroscope. Trematode cercariae were identified morphologically under a high-magnification compound microscope. One drop of water containing live, vigorous cercariae was observed carefully on a slide containing 10% formalin or stained with 1% iodine. Cercariae were photographed using a digital camera (Olympus DP 25; Olympus, Tokyo, Japan) fitted to a microscope (Olympus BX 51). They were identified using the taxonomic keys of Ito et al. (Reference Ito, Papasarathorn and Tongkoom1962), Schell (Reference Schell1970), Yamaguti (Reference Yamaguti1975) and Ditrich et al. (Reference Ditrich, Schoiz, Aguiree-Macedo and Vargas-Vazquez1997). Cercariae were drawn using a light microscope and camera lucida. The different types of cercariae found were coded alphabetically.

Results

The 11,756 B. s. goniomphalos collected from Thailand harboured 20 morphologically distinct types of cercariae belonging to 10 groups: virgulate (5 types), amphistome (1), pleurolophocercous (1), monostome (1), parapleurolophocercous (2), mutabile (1), cystophorous (2), ophthalmoxiphidiocercariae (1), furcocercous (4) and echinostome (2) (table 2, fig. 1). Of the 10,507 snails collected from Lao PDR, 10 groups with 13 types of cercariae were found, all of which also occurred in Thailand (table 2).

Table 2

Mean prevalences (ranges given in brackets) of type of cercariae (A–T) from field-infected Bithynia siamensis goniomphalos from Thailand and Lao PDR (see fig. 1 for cercarial codes).

ND, no data available.

Fig. 1

Type of cercariae infecting Bithynia siamensis goniomphalos from Thailand and Lao PDR. (A–E) Xiphidiocercariae, type virgulate 1 to 5; (F) amphistome cercariae; (G) pleurolophocercous cercariae (Opisthorchis viverrini); (H) monostome cercariae; (I–J) parapleurolophocercariae 1 and 2; (K) mutabile cercariae; (L) ophthalmoxiphidiocercariae; (M–N) cystophorous cercariae 1 and 2; (O–P) furcocercous cercariae 1 and 2; (Q–R) longifurcate-pharyngeate cercariae 1; (S–T) echinostome cercariae 1 and 2.

Virgulate type 1 were the most common (table 1) and had the highest prevalences in snails, with a mean of 10.90% in Thailand and 6.58% in Lao PDR (table 2). This type was found in all samples from Lao PDR and in 27 of 29 samples from Thailand. The second highest prevalence occurred in amphistome cercariae, with a mean of 6.08% in Thailand and 2.13% in Lao PDR. Monostome cercariae had the third highest prevalence, with 1.40% in Thailand and 2.22% in Lao PDR. The pleurolophocercous cercariae of O. viverrini s.l. had the fourth highest prevalence, with 1.59% in Thailand and 0.96% in Lao PDR. Lower mean prevalences were noted in the two countries for nine types of cercariae, with percentages ranging from 0.10% (echinostome cercariae type 2) to 1.15% (parapleurolophocercous cercariae type 1) in Thailand, and from 0.03% (echinostome cercariae type 2) to 1.53% (xiphidiocercariae, type virgulate 2) in Lao PDR. Six other types of cercariae – xiphidiocercariae, type virgulate 4 (prevalence, 0.83%); echinostome cercariae type 1 (0.39%); furcocercous cercariae type 2 (0.25%); parapleurolophocercous cercariae type 2 (0.24%); cystophorous cercariae type 2 (0.10%) and longifurcate-pharyngeate cercariae type 2 (0.05%) – were only recorded in snail samples collected from Thailand (table 2 and fig. 1). The virgulate type 5 was found only in Sakon Nakhon Province, Thailand, but prevalence data are not available.

Discussion

Bithynia s. goniomphalos s.l. from Thailand and Lao PDR harbours a wide variety of trematode cercariae. Unfortunately, identification to species level is difficult for most of the taxa involved, as the complete life cycles are known for only a few species. This study confirms the need for molecular identification to species level (Nolan & Cribb, Reference Nolan and Cribb2005; Olson & Tkach, Reference Olson and Tkach2005; Skov et al., Reference Skov, Kania, Dalsgaard, Jorgensen and Buchmann2009) and, if possible, the use of experimental studies to determine the life cycles in the laboratory.

There are relatively few reports of cercariae in B. s. goniomphalos s.l. from Thailand or Lao PDR. The 20 morphologically identified larval trematodes that were recorded from the present study contained similar types to those found in other studies; however, we found more cercarial types than were previously known. This might be a result of the larger sampling size and more localities sampled than previous reports. The cystophorous type 2 (furcocystocercous) was discovered for the first time in B. s. goniomphalos s.l. This group was found previously in another snail (Pyrgophorus coronatus) in Mexico (Ditrich et al., Reference Ditrich, Schoiz, Aguiree-Macedo and Vargas-Vazquez1997). Bithynia s. goniomphalos s.l. shows a particularly high susceptibility to virgulate type 1 infection, the cercariae of which dominate the cercarial fauna.

The occurrence of O. viverrini cercariae in B. s. goniomphalos s.l. is highly significant, although not unexpected, as this species poses the greatest threat to human health throughout the Mekong area of South-East Asia. The data presented here correspond with those found in previous studies for both Thailand (Sripa et al., Reference Sripa, Bethony, Sithithaworn, Kaewkes, Mairiang, Loukas, Mulvenna, Laha, Hotez and Brindley2011; Sithithaworn et al., Reference Sithithaworn, Andrews, Nguyen, Wongsaroj, Sinuon, Odermatt, Nawa, Liang, Brindley and Sripa2012a) and Lao PDR (Sayasone et al., Reference Sayasone, Vonghajack, Vanmany, Rasphone, Tesana, Utzinger, Akkhavong and Odermatt2009; Forrer et al., Reference Forrer, Sayasone, Vounatsou, Vonghachack, Bouakhasith, Vogt, Glaser, Utzinger, Akkhavong and Odermatt2012). Natural infection of O. viverrini in B. s. goniomphalos ranged from 0.22 to 6.93% with an average of 3.04% in Thailand, while in Lao PDR prevalences ranged from 0.37 to 8.37% with an average of 2.01% (Kiatsopit et al., Reference Kiatsopit, Sithithaworn, Saijuntha, Boonmars, Tesana, Sithithaworn, Petney and Andrews2012).

Trematodes are a diverse group of parasites requiring molluscs and vertebrates as intermediate and definitive hosts. Trematode parasitism of intermediate hosts is frequently associated with the alteration of a host's growth, fecundity and/or survival, and snail susceptibility to trematodes is highly specific (Kalbe et al., Reference Kalbe, Haberl and Haas1997; Sorensen & Minchella, Reference Sorensen and Minchella1998). DNA studies have been carried out to detect the larval stages of trematodes and their taxonomic determination in snails (Chuboon & Wongsawad, Reference Chuboon and Wongsawad2009; Kraus et al., Reference Kraus, Brant and Adema2014; Routtu et al., Reference Routtu, Grunberg, Izhar, Dagan, Guttel, Ucko and Ben-Ami2014). Recent genetic analyses of B. s. goniomphalos s.l. indicate that this taxon represents a species complex containing at least nine cryptic species that have specific associations with defined wetlands in Thailand and Lao PDR (Kiatsopit et al., Reference Kiatsopit, Sithithaworn, Saijuntha, Petney and Andrews2013). Furthermore, the cryptic species of B. s. goniomphalos s.l. are associated with cryptic species and/or genetic groups of O. viverrini from the corresponding wetlands. How this diversity influences the parasitic trematode community remains to be determined.

Previous studies have shown that individual species of snails can act as intermediate hosts for a number of trematode species (Sousa, Reference Sousa1993; Esch et al., Reference Esch, Curtis and Barger2001; Loy & Haas, Reference Loy and Haas2001; Faltynkova & Haas, Reference Faltynkova and Haas2006). This varies in space and time depending on environmental conditions, which can be strongly associated with host availability, such as climatic factors including temperature (Koprivnikar et al., Reference Koprivnikar, Lim, Fu and Brack2010; Studer et al., Reference Studer, Poulin and Tompkins2013) and drought (Gérard, Reference Gérard2001), the size of the water body (Voutilainen et al., Reference Voutilainen, van Ooik, Puurtinen, Kortet and Taskinen2009), salinity (Koprivnikar et al., Reference Koprivnikar, Lim, Fu and Brack2010; Lei & Poulin, Reference Lei and Poulin2011; Suwannatrai et al., Reference Suwannatrai, Suwannatrai, Haruay, Piratae, Thammasiri, Khampoosa, Kulsantiwong, Prasopdee, Tarbsripair, Suwanwerakamtorn, Sukchan, Boonmars, Malone, Kearney and Tesana2011), pH (Koprivnikar et al., Reference Koprivnikar, Lim, Fu and Brack2010; Wang et al., Reference Wang, Ho, Feng, Namsanor and Sithithaworn2015), land use (Koprivnikar et al., Reference Koprivnikar, Baker and Forbes2006; Wang et al., Reference Wang, Ho, Feng, Namsanor and Sithithaworn2015) and habitat complexity (Beasley et al., Reference Beasley, Faeh, Wikoff, Staehle, Eisold, Nichols, Cole, Schotthoefer, Greenwll, Brown and Lannoo2005). In addition to such abiotic/host-related factors, an early meta-analysis by Kuris & Lafferty (Reference Kuris and Lafferty1994) showed that the number of multispecies infections in individual snails is on average 10% less than expected, due to interspecific competition.

Recognition of the wide variety of trematode species detected in B. s. goniomphalos leads to a number of questions that also bear on the epidemiology of O. viverrini. How do the trematode species interact within the snail hosts? How often do mixed infections occur? Do different species inhibit infection with other species? These remain to be answered. Also of significance is the fact the most cercarial species cannot be identified to the species level. Thus molecular identification based on known adults could serve as an effective way to assess the risk posed by the unknown cercariae to human and/or animal health.

Acknowledgements

We acknowledge the support of the Faculty of Medicine, Khon Kaen University, Visiting International Professor Program.

Financial support

This work was supported by the Higher Education Research Promotion and office of the Higher Education Commission, through the health cluster (SHeP-GMS), the Thailand Research Fund through the Basic Research Grant Scheme and the Cholangiocarcinoma Screening and Care Program (CASCAP), Khon Kaen University. We would like to thank the Deutsche Forschungsgemeinschaft (PE1611/1-3), the National Research Council of Thailand, and the International Excellence Fund of Karlsruhe Institute of Technology, as well as ASEAN-EU Year of Science, Technology and Innovation, 2012 for providing funding for co-operative workshops.

Conflict of interest

None.

References

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, 697–700.Google Scholar
Andrews, R.H., Sithithaworn, P. & Petney, T.N. (2008) Opisthorchis viverrini: an underestimated parasite in world health. Trends in Parasitology 24, 497–501.CrossRefGoogle ScholarPubMed
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. 75–86 in Lannoo, M.J. (Ed.) Amphibian declines: the conservation status of United States species. Berkeley, University of California Press.Google Scholar
Brandt, R.A.M. (1974) The non-marine aquatic Mollusca of Thailand. Archiv für Molluskenkunde 105, 1–423.Google Scholar
Chitramvong, Y.P. (1992) The Bithyniidae (Gastropoda: Prosobranchia) of Thailand: comparative external morphology. Malacological Review 25, 21–38.Google Scholar
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, 237–243.Google Scholar
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, 1216–1220.Google ScholarPubMed
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, 482–488.Google Scholar
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, 75–81.CrossRefGoogle ScholarPubMed
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, 109–127.Google Scholar
Esch, G.W., Curtis, L.A. & Barger, M.A. (2001) A perspective on the ecology of trematode communities in snails. Parasitology 123, S57–S75.Google Scholar
Faltynkova, A. & Haas, W. (2006) Larval trematodes in freshwater molluscs from the Elbe to Danube rivers (Southeast Germany): before and today. Parasitology Research 99, 572–582.CrossRefGoogle ScholarPubMed
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.Google Scholar
Gérard, C. (2001) Consequences of a drought on freshwater gastropod and trematode communities. Hydrobiologia 459, 9–18.CrossRefGoogle Scholar
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, 538–540.CrossRefGoogle ScholarPubMed
Ito, J., Papasarathorn, T. & Tongkoom, B. (1962) Studies on cercariae from fresh water snails in Thailand. Japanese Journal of Medical Science and Biology 15, 249–270.Google Scholar
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, 806–812.Google Scholar
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, 464–469.Google Scholar
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, 313–319.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 997–1001.Google Scholar
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, 1167–1177.CrossRefGoogle ScholarPubMed
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, 105–109.CrossRefGoogle Scholar
Kuris, A.M. & Lafferty, K.D. (1994) Community structure: larval trematodes in snail hosts. Annual Reviews of Ecology and Systematics 25, 189–217.Google Scholar
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, 1307–1313.Google Scholar
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, 146–153.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Lei, F. & Poulin, R. (2011) Effects of salinity on multiplication and transmission of an intertidal trematode parasite. Marine Biology 158, 995–1003.Google Scholar
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, 1–26.Google Scholar
Loy, C. & Haas, W. (2001) Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitology Research 87, 878–882.Google Scholar
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, 662–672.Google Scholar
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, 106–109.Google ScholarPubMed
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, 101–163.Google Scholar
Olson, P.D. & Tkach, V.V. (2005) Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology 60, 165–243.Google Scholar
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, 38–45.Google Scholar
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, 1031–1046.Google Scholar
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, 2535–2540.Google Scholar
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, 695–703.Google Scholar
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, 247–254.Google Scholar
Schell, S.C. (1970) How to know the trematodes. 355 pp. Dubuque, Iowa, W.C. Brown.Google Scholar
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, 125–131.Google Scholar
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, 10–16.Google Scholar
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, 32–37.Google Scholar
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, 66–75.CrossRefGoogle ScholarPubMed
Sorensen, R. & Minchella, D.J. (1998) Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails. Oecologia 115, 188–195.Google Scholar
Sousa, W.P. (1993) Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecological Monographs 63, 103–128.CrossRefGoogle Scholar
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, 653–657.Google Scholar
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, 294–301.Google Scholar
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, S158–S168.CrossRefGoogle ScholarPubMed
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, 1213–1222.Google Scholar
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, 183–190.Google Scholar
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, 54–60.Google Scholar
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, 355–358.Google Scholar
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, 107–132.Google Scholar
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, 138–141.Google Scholar
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, 351–357.Google Scholar
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, 244–252.Google Scholar
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, 207–214.Google Scholar
Yamaguti, S. (1975) A synoptical review of life histories of digenetic trematodes of vertebrates. Japan, Keiguku Publication.Google Scholar
Figure 0

Table 1The composition of cercarial types and the number of infected snails in Bithynia siamensis goniomphalos samples collected from localities in Thailand and Lao PDR (see fig. 1 for cercarial types and table 2 for prevalence values).

Figure 1

Table 2Mean prevalences (ranges given in brackets) of type of cercariae (A–T) from field-infected Bithynia siamensis goniomphalos from Thailand and Lao PDR (see fig. 1 for cercarial codes).

Figure 2

Fig. 1Type of cercariae infecting Bithynia siamensis goniomphalos from Thailand and Lao PDR. (A–E) Xiphidiocercariae, type virgulate 1 to 5; (F) amphistome cercariae; (G) pleurolophocercous cercariae (Opisthorchis viverrini); (H) monostome cercariae; (I–J) parapleurolophocercariae 1 and 2; (K) mutabile cercariae; (L) ophthalmoxiphidiocercariae; (M–N) cystophorous cercariae 1 and 2; (O–P) furcocercous cercariae 1 and 2; (Q–R) longifurcate-pharyngeate cercariae 1; (S–T) echinostome cercariae 1 and 2.