Hostname: page-component-76fb5796d-25wd4 Total loading time: 0 Render date: 2024-04-27T21:49:44.171Z Has data issue: false hasContentIssue false
  • English
  • Français

Cercarial trematodes in freshwater snails from Bangkok, Thailand: prevalence, morphological and molecular studies and human parasite perspective

Published online by Cambridge University Press:  26 October 2020

Pichit Wiroonpan ,
Thapana Chontananarth  and
Watchariya Purivirojkul Open the ORCID record for Watchariya Purivirojkul [Opens in a new window]
Pichit Wiroonpan
Affiliation:
Animal Systematics and Ecology Speciality Research Unit, Department of Zoology, Faculty of Science, Kasetsart University, Bang Khen Campus, Bangkok, 10900, Thailand
Thapana Chontananarth
Affiliation:
Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Srinakharinwirot University, Bangkok, Thailand Center of Excellence in Animal, Plant and Parasitic Biotechnology, Srinakharinwirot University, Bangkok, Thailand
Watchariya Purivirojkul*
Affiliation:
Animal Systematics and Ecology Speciality Research Unit, Department of Zoology, Faculty of Science, Kasetsart University, Bang Khen Campus, Bangkok, 10900, Thailand
*
Author for correspondence: Watchariya Purivirojkul, E-mail: fsciwyp@ku.ac.th
Get access Rights & Permissions [Opens in a new window]

Abstract

We investigated the prevalence, morphological characters and molecular classifications of trematode cercariae in freshwater snails randomly collected from 59 sampling localities in Bangkok from May 2018 to March 2019. We used a crushing technique to observe the cercarial stage inside each snail body and amplified the internal transcribed spacer 2 regions of cercarial DNA using polymerase chain reaction methodology. The associated phylogenetic tree was reconstructed using Bayesian inference analyses. A total of 517 of 15 621 examined snails were infected with trematode cercariae, and the infected snails were classified into 11 species of seven families with a 3.31% overall prevalence of the infection. The Bithynia siamensis siamensis snail displayed the highest prevalence of infection (16.16%), whereas the Physella acuta snail exhibited the lowest prevalence (0.08%) of infection. Eight morphological types of cercariae were observed. The highest prevalence of infection was observed in mutabile cercaria (1.86%). Based on molecular investigations, the phylogram revealed eight cercaria types assigned to at least nine digenean trematode families, of which five belong to groups of human intestinal flukes. Although, with the exception of schistosome cercaria, trematode cercariae are not known to directly damage humans, understanding the general biology of trematode cercariae (including diversity, distribution, infection rates and host range) is important and necessary for the prevention and control of parasitic transmission that impacts aquatic cultivations, livestock farming and human health.

Keywords

CercariaeITS2larval trematodesphylogenetic treesnail-transmitted parasites
Type
Research Article
Information
Parasitology , Volume 148 , Issue 3 , March 2021 , pp. 366 - 383
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abramoff, MD, Magalhaes, PJ and Ram, SJ (2004) Image processing with ImageJ. Biophotonics International 11, 36–42.Google Scholar
Anucherngchai, S, Tejangkura, T and Chontananarth, T (2016) Epidemiological situation and molecular identification of cercarial stage in freshwater snails in Chao-Phraya Basin, Central Thailand. Asian Pacific Journal of Tropical Biomedicine 6, 539–545.CrossRefGoogle Scholar
Anucherngchai, S, Tejangkura, T and Chontananarth, T (2017) Molecular confirmation of trematodes in the snail intermediate hosts from Ratchaburi Province, Thailand. Asian Pacific Journal of Tropical Disease 7, 286–292.CrossRefGoogle Scholar
Appleton, CC (1983) Studies on Austrobilharzia terrigalensis (Trematoda: Schistosomatidae) in the Swan estuary, Western Australia: frequency of infection in the intermediate host population. International Journal for Parasitology 13, 51–60.CrossRefGoogle ScholarPubMed
Barber, KE, Mkoji, GM and Loker, ES (2000) PCR-RFLP analysis of the ITS2 region to identify Schistosoma haematobium and S. bovis from Kenya. The American Journal of Tropical Medicine and Hygiene 62, 434–440.CrossRefGoogle ScholarPubMed
Belizario, VYJ, de Leon, WU, Bersabe, MJJ, Baird, JK and Bangs, MJ (2004) A focus of human infection by Haplorchis taichui (Trematoda: Heterophyidae) in the southern Philippines. The Journal of Parasitology 90, 1165–1169.CrossRefGoogle ScholarPubMed
Belizario, VY, Geronilla, GG, Anastacio, MBM, de Leon, WU, Suba-an, AU, Sebastian, AC and Bangs, MJ (2007) Echinostoma malayanum infection, the Philippines. Emerging Infectious Diseases 13, 1130–1131.CrossRefGoogle Scholar
Bhaibulaya, M, Charoenlarb, P and Harinasuta, C (1964) Report of cases of Echinostoma malayanum and Hypoderaeum conoideum in Thailand. The Journal of Medical Association of Thailand 47, 720–731.Google Scholar
Bousset, L, Pointier, JP, David, P and Jarne, P (2014) Neither variation loss, nor change in selfing rate is associated with the worldwide invasion of Physa acuta from its native North America. Biological Invasions 16, 1769–1783.CrossRefGoogle Scholar
Brandt, RAM (1974) The non-marine aquatic mollusca of Thailand. Archiv für Molluskenkunde 105, 1–423.Google Scholar
Caffara, M, Davidovich, N, Falk, R, Smirnov, M, Ofek, T, Cummings, D, Gustinelli, A and Fioravanti, ML (2014) Redescription of Clinostomum phalacrocoracis metacercariae (Digenea: Clinostomidae) in cichlids from Lake Kinneret, Israel. Parasite 21, 32.CrossRefGoogle ScholarPubMed
Caffara, M, Locke, SA, Cristanini, C, Davidovich, N, Markovich, MP and Fioravanti, ML (2016) A combined morphometric and molecular approach to identifying metacercariae of Euclinostomum heterostomum (Digenea: Clinostomidae). The Journal of Parasitology 102, 239–248.CrossRefGoogle Scholar
Caffara, M, Locke, SA, Halajian, A, Luus-Powell, WJ, Benini, D, Tedesco, P, Kasembele, GK and Fioravanti, ML (2019) Molecular data show Clinostomoides Dollfus, 1950 is a junior synonym of Clinostomum Leidy, 1856, with redescription of metacercariae of Clinostomum brieni N. Comb. Parasitology 146, 805–813.CrossRefGoogle ScholarPubMed
Caron, Y, Rondelaud, D and Losson, B (2008) The detection and quantification of a digenean infection in the snail host with special emphasis on Fasciola sp. Parasitology Research 103, 735.CrossRefGoogle ScholarPubMed
Cech, G, Molnár, K and Székely, C (2017) Molecular biological studies of adult and metacercarial stages of Petasiger exaeretus Dietz, 1909 (Digenea: Echinostomatidae). Acta Veterinaria Hungarica 65, 198–207.CrossRefGoogle Scholar
Chai, J-Y (2019) Human Intestinal Flukes from Discovery to Treatment and Control. Dordrecht, Netherlands: Springer Nature B.V.CrossRefGoogle Scholar
Chai, J-Y, Shin, E-H, Lee, S-H and Rim, H-J (2009) Foodborne intestinal flukes in Southeast Asia. The Korean Journal of Parasitology 47, S69–S102.CrossRefGoogle ScholarPubMed
Chai, J-Y, Sohn, W-M, Yong, T-S, Eom, KS, Min, D-Y, Lee, MY, Lim, H, Insisiengmay, B, Phommasack, B and Rim, H-J (2013) Centrocestus formosanus (Heterophyidae): human infections and the infection source in Lao PDR. The Journal of Parasitology 99, 531–536.CrossRefGoogle ScholarPubMed
Chai, J-Y, Kim, J-L and Seo, M (2014) Four human cases of Acanthotrema felis (Digenea: Heterophyidae) infection in Korea. The Korean Journal of Parasitology 52, 291–294.CrossRefGoogle ScholarPubMed
Chanawong, A and Waikagul, J (1991) Laboratory studies on host-parasite relationship of Bithynia snails and the liver fluke, Opisthorchis viverrini. The Southeast Asian Journal of Tropical Medicine and Public Health 22, 235–239.Google ScholarPubMed
Chantima, K, Suk-Ueng, K and Kampan, M (2018) Freshwater snail diversity in Mae Lao agricultural basin (Chiang Rai, Thailand) with a focus on larval trematode infections. The Korean Journal of Parasitology 56, 247–257.CrossRefGoogle Scholar
Chaudhary, A, Tripathi, R, Gupta, S and Shanker Singh, H (2017) First report on molecular evidence of Tylodelphys cerebralis (Diplostomulum cerebralis) Chakrabarti, 1968 (Digenea: Diplostomidae) from snakehead fish Channa punctata. Acta Parasitologica 62, 386–392.CrossRefGoogle ScholarPubMed
Chipev, NH (1993) Decoy effect and host infection by miracidia within snail communities. Parasitology 106, 265–276.CrossRefGoogle ScholarPubMed
Chontananarth, T and Wongsawad, C (2013) Epidemiology of cercarial stage of trematodes in freshwater snails from Chiang Mai province, Thailand. Asian Pacific Journal of Tropical Biomedicine, 3, 237–243.CrossRefGoogle Scholar
Chontananarth, T and Wongsawad, C (2017) The pleurophocercous cercariae infection in snail Family Thiaridae Grey, 1847 Northern, Thailand. Asian Pacific Journal of Tropical Disease 7, 205–210.CrossRefGoogle Scholar
Chontananarth, T, Wongsawad, C, Chomdej, S, Krailas, D and Chai, JY (2014) Molecular phylogeny of trematodes in Family Heterophyidae based on mitochondrial cytochrome c oxidase subunit I (mCOI). Asian Pacific Journal of Tropical Medicine 7, 446–450.CrossRefGoogle Scholar
Chontananarth, T, Tejangkura, T, Wetchasart, N and Chimburut, C (2017) Morphological characteristics and phylogenetic trends of trematode cercariae in freshwater snails from Nakhon Nayok Province, Thailand. The Korean Journal of Parasitology 55, 47–54.CrossRefGoogle ScholarPubMed
Chuboon, S and Wongsawad, C (2009) Molecular identification of larval trematode in intermediate hosts from Chiang Mai, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 40, 1216–1220.Google ScholarPubMed
Clausen, JH, Madsen, H, Murrell, KD, Phan Thi, V, Nguyen Manh, H, Viet, KN and Dalsgaard, A (2012) Relationship between snail population density and infection status of snails and fish with zoonotic trematodes in Vietnamese carp nurseries. PLoS Neglected Tropical Diseases 6, e1945.CrossRefGoogle ScholarPubMed
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Dechruksa, W, Krailas, D, Ukong, S, Inkapatanakul, W and Koonchornboon, T (2007) Trematode infections of the freshwater snail family Thiaridae in the Khek River, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 38, 1016–1028.Google ScholarPubMed
Detwiler, JT, Bos, DH and Minchella, DJ (2010) Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Molecular Phylogenetics and Evolution 55, 611–620.CrossRefGoogle ScholarPubMed
Devkota, R, Budha, P and Gupta, R (2011) Trematode cercariae infections in freshwater snails of Chitwan District, central Nepal. Himalayan Journal of Sciences 7, 9–14.CrossRefGoogle Scholar
Dillon, RT Jr, Wethington, AR, Rhett, JM and Smith, TP (2002) Populations of the European freshwater pulmonate Physa acuta are not reproductively isolated from American Physa heterostropha or Physa integra. Invertebrate Biology, 121, 226–234.CrossRefGoogle Scholar
Dobson, M (2004) Replacement of native freshwater snails by the exotic Physa acuta (Gastropoda: Physidae) in southern Mozambique; a possible control mechanism for schistosomiasis. Annals of Tropical Medicine & Parasitology 98, 543–548.CrossRefGoogle ScholarPubMed
Dzikowski, R, Levy, MG, Poore, MF, Flowers, JR and Paperna, I (2004) Use of rDNA polymorphism for identification of Heterophyidae infecting freshwater fishes. Diseases of Aquatic Organisms 59, 35–41.CrossRefGoogle ScholarPubMed
Ebbs, ET, Loker, ES and Brant, SV (2018) Phylogeography and genetics of the globally invasive snail Physa acuta Draparnaud 1805, and its potential to serve as an intermediate host to larval digenetic trematodes. BMC Evolutionary Biology 18, 103.CrossRefGoogle ScholarPubMed
Esch, GW and Fernandez, JC (1994) Snail-trematode interactions and parasite community dynamics in aquatic systems: a review. The American Midland Naturalist 131, 209–237.CrossRefGoogle Scholar
Frandsen, F and Christensen, NO (1984) An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Tropica 41, 181–202.Google ScholarPubMed
Fretter, V and Graham, A (1962) British Prosobranch Molluscs: Their Functional Anatomy and Ecology. London, United Kingdom: Ray Society.Google Scholar
Gordy, MA and Hanington, PC (2019) A fine-scale phylogenetic assessment of digenean trematodes in central Alberta reveals we have yet to uncover their total diversity. Ecology and Evolution 9, 3153–3238.CrossRefGoogle ScholarPubMed
Graczyk, T and Fried, B (1998) Echinostomiasis: a common but forgotten food-borne disease. The American Journal of Tropical Medicine and Hygiene 58, 501–504.CrossRefGoogle ScholarPubMed
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Hall, JE and Groves, AE (1963) Virgulate Xiphidiocercariae from Nitocris dilatatus Conrad. The Journal of Parasitology 49, 249–263.CrossRefGoogle ScholarPubMed
Haruay, S and Piratae, S (2019) Situation and cercarial infection of freshwater mollusk from Sirindhorn Reservoir, Ubon Ratchathani Province, Thailand. Iranian Journal of Parasitology 14, 421–429.Google ScholarPubMed
Heneberg, P, Sitko, J and Těšínský, M (2020) Paraphyly of Conodiplostomum Dubois, 1937. Parasitology International 76, 102033.CrossRefGoogle ScholarPubMed
Hostettler, R, Cutmore, SC and Cribb, TH (2018) Two new species of Haplorchoides Chen, 1949 (Digenea: Heterophyidae) infecting an Australian siluriform fish, Neoarius graeffei Kner & Steindachner. Systematic Parasitology 95, 201–211.CrossRefGoogle ScholarPubMed
Huang, X and Madan, A (1999) CAP3: a DNA sequence assembly program. Genome Research 9, 868–877.CrossRefGoogle ScholarPubMed
Hung, N, Madsen, H and Fried, B (2013) Global status of fish-borne zoonotic trematodiasis in humans. Acta Parasitologica 58, 231–258.CrossRefGoogle ScholarPubMed
Izrailskaia, AV, Besprozvannykh, VV, Tatonova, YV, Nguyen, HM and Ngo, HD (2019) Developmental stages of Notocotylus magniovatus Yamaguti, 1934, Catatropis vietnamensis N. sp., Pseudocatatropis dvoryadkini N. sp., and phylogenetic relationships of Notocotylidae Lühe, 1909. Parasitology Research 118, 469–481.CrossRefGoogle ScholarPubMed
Johnson, PTJ, Lund, PJ, Hartson, RB and Yoshino, TP (2009) Community diversity reduces Schistosoma mansoni transmission, host pathology and human infection risk. Proceedings of the Royal Society B: Biological Sciences 276, 1657–1663.CrossRefGoogle ScholarPubMed
Kaewkes, S, Elkins, DB, Haswell-Elkins, MR and Sithithaworn, P (1991) Phaneropsolus spinicirrus N. sp. (Digenea: Lecithodendriidae), a human parasite in Thailand. The Journal of Parasitology 77, 514–516.CrossRefGoogle Scholar
Keane, RM and Crawley, MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution 17, 164–170.CrossRefGoogle Scholar
Kiatsopit, N, Sithithaworn, P, Kopolrat, K, Namsanor, J, Andrews, RH and Petney, TN (2015) Trematode diversity in the freshwater snail Bithynia siamensis goniomphalos Sensu lato from Thailand and Lao PDR. Journal of Helminthology 90, 312–320.CrossRefGoogle ScholarPubMed
Krailas, D, Namchote, S, Koonchornboon, T, Dechruksa, W and Boonmekam, D (2014) Trematodes obtained from the thiarid freshwater snail Melanoides tuberculata (Müller, 1774) as vector of human infections in Thailand. Zoosystematics and Evolution 90, 57–86.CrossRefGoogle Scholar
Krailas, D, Veeravechsukij, N, Chuanprasit, C, Boonmekam, D and Namchote, S (2016) Prevalence of fish-borne trematodes of the family Heterophyidae at Pasak Cholasid Reservoir, Thailand. Acta Tropica 156, 79–86.CrossRefGoogle ScholarPubMed
Kraus, TJ, Brant, SV and Adema, CM (2014) Characterization of trematode cercariae from Physella acuta in the Middle Rio Grande. Comparative Parasitology 81, 105–109.CrossRefGoogle Scholar
Kudlai, O, Tkach, VV, Pulis, EE and Kostadinova, A (2015) Redescription and phylogenetic relationships of Euparyphium capitaneum Dietz, 1909, the type-species of Euparyphium Dietz, 1909 (Digenea: Echinostomatidae). Systematic Parasitology 90, 53–65.CrossRefGoogle Scholar
Kulsantiwong, J, Prasopdee, S, Piratae, S, Khampoosa, P, Thammasiri, C, Suwannatrai, A, Boonmars, T, Viyanant, V, Ruangsitichai, J, Tarbsripair, P and Tesana, S (2015) Trematode infection of freshwater snail, family Bithyniidae in Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 396, 396–405.Google Scholar
Kulsantiwong, J, Prasopdee, S, Labbunruang, N, Chaiyasaeng, M and Tesana, S (2017) Habitats and trematode infection of Bithynia siamensis goniomphalos in Udon Thani Province, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 48, 975–982.Google Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Lie, KJ and Virik, HK (1963) Human infection with Echinostoma malayanum Leiper, 1911 (Trematoda: Echinostomatidae). The American Journal of Tropical Medicine and Hygiene 66, 77–82.Google Scholar
Locke, SA, Van Dam, A, Caffara, M, Pinto, HA, López-Hernández, D and Blanar, CA (2018) Validity of the Diplostomoidea and Diplostomida (Digenea, Platyhelminthes) upheld in phylogenomic analysis. International Journal for Parasitology 48, 1043–1059.CrossRefGoogle ScholarPubMed
Lydeard, C, Campbell, D and Golz, M (2016) Physa acuta Draparnaud, 1805 should be treated as a native of North America, not Europe. Malacologia 59, 347–350.CrossRefGoogle Scholar
Maldonado, A, Loker, E, Morgan, J, Rey, L and Lanfredi, R (2001) Description of the adult worms of a new Brazilian isolate of Echinostoma paraensei (Platyhelminthes: Digenea) from its natural vertebrate host Nectomys squamipes by light and scanning electron microscopy and molecular analysis. Parasitology Research 87, 840–848.Google ScholarPubMed
Martínez-Salazar, EA and León-Règagnon, V (2010) Molecular evidence that Langeronia macrocirra and Langeronia cf. parva (Trematoda: Pleurogenidae) parasites of anurans from Mexico are conspecific. Mitochondrial DNA 21, 3–11.CrossRefGoogle ScholarPubMed
McKinney, ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosystems 11, 161–176.CrossRefGoogle Scholar
Mereta, ST, Bedewi, J, Yewhalaw, D, Mandefro, B, Abdie, Y, Tegegne, D, Birke, W, Mulat, WL and Kloos, H (2019) Environmental determinants of distribution of freshwater snails and trematode infection in the Omo Gibe River Basin, southwest Ethiopia. Infectious Diseases of Poverty 8, 93.CrossRefGoogle ScholarPubMed
Morgan, JAT and Blair, D (1995) Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology 111, 609–615.CrossRefGoogle ScholarPubMed
Muñoz-Antoli, C, Trelis, M, Gozalbo, M, Toledo, R, Haberl, B and Esteban, J-G (2003) Interactions related to non-host snails in the host-finding process of Euparyphium albuferensis and Echinostoma friedi (Trematoda: Echinostomatidae) miracidia. Parasitology Research 91, 353–356.Google ScholarPubMed
Namsanor, J, Sithithaworn, P, Kopolrat, K, Kiatsopit, N, Pitaksakulrat, O, Tesana, S, Andrews, RH and Petney, TN (2015) Seasonal transmission of Opisthorchis viverrini Sensu lato and a lecithodendriid trematode species in Bithynia siamensis goniomphalos Snails in northeast Thailand. The American Journal of Tropical Medicine and Hygiene 93, 87–93.CrossRefGoogle Scholar
Nasr, M (1941) The occurrence of Prohemistomum vivax (Sonsino, 1892) Azim, 1933. Infection in man, with a redescription of the parasite. Laboratory and Medical Progress 2, 135–149.Google Scholar
Ng, TH, Limpanont, Y, Chusongsang, Y, Chusongsang, P and Panha, S (2018) Correcting misidentifications and first confirmation of the globally-invasive Physa acuta Draparnaud, 1805 (Gastropoda: Physidae) in Thailand and Laos. BioInvasions Records 7, 15–19.CrossRefGoogle Scholar
Ngern-klun, R, Sukontason, KL, Tesana, S, Sripakdee, D, Irvine, KN and Sukontason, K (2006) Field investigation of Bithynia funiculata, intermediate host of Opisthorchis viverrini in northern Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 37, 662–672.Google ScholarPubMed
Olivier, L and Schneiderman, M (1956) A method for estimating the density of aquatic snail populations. Experimental Parasitology 5, 109–117.CrossRefGoogle ScholarPubMed
Outa, JO, Sattmann, H, Köhsler, M, Walochnik, J and Jirsa, F (2020) Diversity of digenean trematode larvae in snails from Lake Victoria, Kenya: First reports and bioindicative aspects. Acta Tropica 206, 105437.CrossRefGoogle Scholar
Patarwut, L, Chontananarth, T, Chai, J-Y and Purivirojkul, W (2020) Infections of digenetic trematode metacercariae in Wrestling Halfbeak, Dermogenys pusilla from Bangkok Metropolitan Region in Thailand. The Korean Journal of Parasitology 58, 27–35.CrossRefGoogle ScholarPubMed
Poulin, R and Cribb, TH (2002) Trematode life cycles: short is sweet? Trends in Parasitology 18, 176–183.CrossRefGoogle ScholarPubMed
Pulis, EE, Tkach, VV and Newman, RA (2011) Helminth parasites of the wood frog, Lithobates sylvaticus, in Prairie Pothole Wetlands of the Northern Great Plains. Wetlands 31, 675–685.CrossRefGoogle Scholar
Purivirojkul, W and Sumontha, M (2013) Euclinostomum heterostomum (Rudolphi, 1809) metacercarial infection in three osphronemid fish species. Walailak Journal of Science and Technology 10, 97–102.Google Scholar
QGIS Development Team (2020) QGIS Geographic Information System. Open Source Geospatial Foundation Project.Google Scholar
Radomyos, P, Bunnag, D and Harinasuta, T (1983) Haplorchis pumilio (Looss) infection in man in northeastern Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 14, 223–227.Google ScholarPubMed
Ramakant, M, Rahul, G and Anand, MS (2018) A new species of Asymphylodora (Trematoda: Lissorchiidae) from Bata, Labeo bata (Cyprinidae), in the Sharda Canal of India, and amendment of the diagnosis for Asymphylodora. Comparative Parasitology 85, 153–158.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Saijuntha, W, Duenngai, K and Tantrawatpan, C (2013) Zoonotic echinostome infections in free-grazing ducks in Thailand. The Korean Journal of Parasitology 51, 663–667.CrossRefGoogle ScholarPubMed
Schell, SC (1970) How to Know the Trematodes. Dubuque, Iowa: Wm. C. Brown Company.Google Scholar
Selbach, C, Soldánová, M, Feld, CK, Kostadinova, A and Sures, B (2020) Hidden parasite diversity in a European freshwater system. Scientific Reports 10, 2694.CrossRefGoogle Scholar
Senapin, S, Phiwsaiya, K, Laosinchai, P, Kowasupat, C, Ruenwongsa, P and Panijpan, B (2014) Phylogenetic analysis of parasitic trematodes of the genus Euclinostomum found in Trichopsis and Betta fish. The Journal of Parasitology 100, 368–371.CrossRefGoogle ScholarPubMed
Sewell, RB (1922) Cercariae Indica. The Indian Journal of Medical Research 10, 1–370.Google Scholar
Shchenkov, SV, Denisova, SA, Kremnev, GA and Dobrovolskij, AA (2019) Five new morphological types of virgulate and microcotylous xiphidiocercariae based on morphological and molecular phylogenetic analyses. Journal of Helminthology 94, e94.CrossRefGoogle ScholarPubMed
Shimazu, T (2016) Digeneans parasitic in freshwater fishes (Osteichthyes) of Japan VI. Lissorchiidae. Bulletin of the National Museum of Nature and Science. Series A, Zoology 42, 1–22.Google Scholar
Sokolov, SG, Atopkin, DM and Urabe, M (2019) Redescription and supplementary molecular characteristics of Aspidogaster ijimai Kawamura, 1915 (Trematoda, Aspidogastrea, Aspidogastridae), a parasite of Cyprinus carpio Linnaeus, 1758 s. lato (Actinopterygii) and freshwater bivalves in East Asia. Parasitology International 71, 167–176.CrossRefGoogle ScholarPubMed
Sri-Aroon, P, Lohachit, C and Harada, M (2004) Survey of brackish-water snails in Eastern Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 35, 150–155.Google Scholar
Sripa, B, Bethony, JM, Sithithaworn, P, Kaewkes, S, Mairiang, E, Loukas, A, Mulvenna, J, Laha, T, Hotez, PJ and Brindley, PJ (2011) Opisthorchiasis and Opisthorchis-associated cholangiocarcinoma in Thailand and Laos. Acta Tropica 120, S158–S168.CrossRefGoogle ScholarPubMed
Sripa, J, Kiatsopit, N and Piratae, S (2016) Prevalence of trematode larvae in intermediate hosts: snails and fish in Ko Ae Sub-District of Khueang Nai, Ubon Ratchathani Province, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 47, 399–409.Google Scholar
Suwannatrai, A, Saichua, P and Haswell, M (2018) Chapter two – Epidemiology of Opisthorchis viverrini infection. In Sripa, B and Brindley, PJ (eds), Advances in Parasitology, vol. 101. United States: Academic Press, pp. 41–67.Google Scholar
Tantrawatpan, C, Saijuntha, W, Sithithaworn, P, Andrews, RH and Petney, TN (2013) Genetic differentiation of Artyfechinostomum malayanum and A. sufrartyfex (Trematoda: Echinostomatidae) based on internal transcribed spacer sequences. Parasitology Research 112, 437–441.CrossRefGoogle Scholar
Tesana, S, Thabsripair, P, Suwannatrai, A, Haruay, S, Piratae, S, Khampoosa, P, Thammasiri, C, Prasopdee, S, Kulsantiwong, J, Chalorkpunrut, P and Jones, MK (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.CrossRefGoogle Scholar
Thaenkham, U, Dekumyoy, P, Komalamisra, C, Sato, M, Dung, DT and Waikagul, J (2010) Systematics of the subfamily Haplorchiinae (Trematoda: Heterphyidae), based on nuclear ribosomal DNA genes and ITS2 region. Parasitology International 59, 460–465.CrossRefGoogle Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids research 22, 4673–4680.CrossRefGoogle Scholar
Toledo, R and Esteban, JG (2016) An update on human echinostomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 110, 37–45.CrossRefGoogle ScholarPubMed
Toledo, R, Muñoz-Antolí, C, Pérez, M and Esteban, JG (1998) Larval trematode infections in freshwater gastropods from the Albufera Natural Park in Spain. Journal of Helminthology 72, 79–82.CrossRefGoogle ScholarPubMed
Toledo, R, Esteban, JG and Fried, B (2006) Immunology and pathology of intestinal trematodes in their definitive hosts. Advances in Parasitology 63, 285–365.CrossRefGoogle ScholarPubMed
Torchin, ME, Lafferty, KD, Dobson, AP, McKenzie, VJ and Kuris, AM (2003) Introduced species and their missing parasites. Nature 421, 628–630.CrossRefGoogle ScholarPubMed
Ukong, S, Krailas, D, Dangprasert, T and Channgarm, P (2007) Studies on the morphology of cercariae obtained from freshwater snails at Erawan Waterfall, Erawan National Park, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 38, 302–312.Google ScholarPubMed
Upatham, E, Sormani, S, Kitikoon, V, Lohachit, C and Burch, J (1983) Identification key for the fresh and brackish-water snails of Thailand. Malacological Review 16, 107–132.Google Scholar
Veeravechsukij, N, Namchote, S, Neiber, MT, Glaubrecht, M and Krailas, D (2018) Exploring the evolutionary potential of parasites: larval stages of pathogen digenic trematodes in their thiarid snail host Tarebia granifera in Thailand. Zoosystematics and Evolution 94, 425–460.CrossRefGoogle Scholar
Vidthayanon, C (2005) Aquatic alien species in Thailand (Part 1): biodiversity. In Bartley, DM, Bhujel, RC, Funge-Smith, S, Olin, PG and Phillips, MJ (eds), International Mechanisms for the Control and Responsible use of Alien species in Aquatic Ecosystems. Rome, Italy: Food and Agriculture Organization of the United Nations (FAO), pp. 113–117.Google Scholar
Walker, JC (1979) Austrobilharzia terrigalensis: a schistosome dominant in interspecific interactions in the molluscan host. International Journal for Parasitology 9, 137–140.CrossRefGoogle Scholar
Wethington, AR and Lydeard, C (2007) A molecular phylogeny of Physidae (Gastropoda: Basommatophora) based on mitochondrial DNA sequences. Journal of Molluscan Studies 73, 241–257.CrossRefGoogle Scholar
Wongsawad, C, Rojtinnakorn, J, Wongsawad, P, Rojanapaibul, A, Marayong, T, Suwattanacoupt, S, Sirikanchana, P, Sey, O and Jadhav, BV (2004) Helminths of vertebrates in Mae Sa Stream, Chiang Mai, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 35, 140–146.Google Scholar
Wongsawad, C, Wongsawad, P, Sukontason, K, Phalee, A, Noikong-Phalee, W and Chai, JY (2016) Discrimination 28S ribosomal gene of trematode cercariae in snails from Chiang Mai Province, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 47, 199–206.Google Scholar
Zhytova, EP, Romanchuk, LD, Guralska, SV, Andreieva, OY and Shvets, MV (2019) Circulation pathways of trematodes of freshwater gastropod mollusks in forest biocenoses of the Ukrainian Polissia. Vestnik Zoologii 53, 13–22.CrossRefGoogle Scholar