Abstract
Lymnaeids are aquatic snails playing an important role in the transmission of many parasitic trematode species of veterinary and medical importance. In this study, we assessed the presence of cercarial flukes in naturally infected lymnaeid snails from Phayao province, Thailand, and determined the species diversity of both the intermediate snail hosts and parasite larvae. A total of 3,185 lymnaeid snails were collected from paddy fields at 31 sites in eight districts of Phayao province between October 2021 and December 2022. Larval fluke infection was assessed using the cercarial shedding method. The collected snails as well as emerging cercariae were identified at the species level via morphological and molecular methods. The sequences of snail internal transcribed spacer region 2 (ITS2) and cercarial 28S ribosomal RNA gene (28S rDNA) and cytochrome C oxidase1 (Cox1) were determined by PCR amplification and sequencing. Three species of lymnaeid snails were detected in this study, including Radix (Lymnaea) rubiginosa (Michelin, 1831), Radix (Lymnaea) swinhoei (Adams, 1866) and Austropeplea viridis (Quoy & Gaimard, 1832), of which R. rubiginosa was the most abundant, followed by A. viridis and R. swinhoei. The overall rate of trematode cercarial infection in the lymnaeid snails was 2.8% (90/3,185); the cercarial infection rate in R. rubiginosa and A. viridis was 3.5% (60/1,735) and 3.1% (30/981), respectively. No larval fluke infection was observed in the studied R. swinhoei (0/469). Nine morphotypes of cercariae were detected at 15 sites from four districts. The emerging cercariae were molecularly identified as Clinostomum sp., Aporocotylidae sp., Apharyngostrigea sp., Trichobilharzia sp., Apatemon sp., Pegosomum sp., Petasiger sp., Echinostoma revolutum and Plagiorchis sp. These findings emphasize the occurrence and diversity of trematode cercariae among naturally infected lymnaeid snails in Phayao province and could contribute to broadening our understanding of the host-parasite relationships between trematodes and their first intermediate hosts as well as developing effective interventions to control trematode parasitic diseases.
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Data availability
The sequences generated for the snail ITS2 and trematode 28S rDNA and Cox1 mtDNA in this study have been deposited in GenBank database under the following accession numbers: OR030136-159, OR030291-310 and OR030096-109.
References
Acosta AA, Caffara M, Fioravanti ML, Utsunomia R, Zago AC, Franceschini L, da Silva RJ (2016) Morphological and Molecular Characterization of Clinostomum detruncatum (Trematoda: Clinostomidae) Metacercariae Infecting Synbranchus marmoratus. J Parasitol 102(1):151–156. https://doi.org/10.1645/15-773
Adeyemo P, Léger E, Hollenberg E, Diouf N, Sène M, Webster JP, Häsler B (2022) Estimating the financial impact of livestock schistosomiasis on traditional subsistence and transhumance farmers keeping cattle, sheep and goats in northern Senegal. Parasit Vectors 15(1):101. https://doi.org/10.1186/s13071-021-05147-w
Al-Jubury A, Bygum A, SusannaTracz E, Koch CN, Buchmann K (2021) Cercarial Dermatitis at Public Bathing Sites (Region Zealand, Denmark): A Case Series and Literature Review. Case Rep Dermatol 13(2):360–365. https://doi.org/10.1159/000516981
Anucherngchai S, Tejangkura T, Chontananarth T (2016) Epidemiological situation and molecular identification of cercarial stage in freshwater snails in Chao-Phraya Basin, Central Thailand. Asian Pac J Trop Biomed 6(6):539–545. https://doi.org/10.1016/j.apjtb.2016.01.015
Bargues MD, Vigo M, Horak P, Dvorak J, Patzner RA, Pointier JP, Jackiewicz M, Meier-Brook C, Mas-Coma S (2001) European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences. Infect Genet Evol 1(2):85–107. https://doi.org/10.1016/S1567-1348(01)00019-3
Brandt RAM (1974) The Non-marine Aquatic Mollusca of Thailand. Waldeman Kramer, Germany
Catalano S, Nadler SA, Fall CB, Marsh KJ, Léger E, Sène M, Priestnall SL, Wood CL, Diouf ND, Bâ K, Webster JP (2019) Plagiorchis sp. in small mammals of Senegal and the potential emergence of a zoonotic trematodiasis. Int J Parasitol Parasites Wildl 8:164–170. https://doi.org/10.1016/j.ijppaw.2019.02.003
Charoenchai A, Tesana S, Pholpark M (1997) Natural infection of trematodes in Lymnaea (Radix) auricularia rubiginosa in water reservoirs in Amphoe Muang, Khon Kaen Province. Southeast Asian J Trop Med Public Health 28(Suppl 1):209–212
Chontananarth T, Wongsawad C (2013) Epidemiology of cercarial stage of trematodes in freshwater snails from Chiang Mai province, Thailand. Asian Pac J Trop Biomed 3(3):237–243. https://doi.org/10.1016/s2221-1691(13)60058-1
Chung DI, Moon CH, Kong HH, Choi DW, Lim DK (1995) The first human case of Clinostomum complanatum (Trematoda: Clinostomidae) infection in Korea. Korean J Parasitol 33(3):219–223. https://doi.org/10.3347/kjp.1995.33.3.219
Cichy A, Faltýnková A, Żbikowska E (2011) Cercariae (Trematoda, Digenea) in European freshwater snails – a checklist of records from over one hundred years. Folia Malacol 19(3):165–189. https://doi.org/10.2478/v10125-011-0023-6
Devkota R, Budha P, Gupta R (2011) Trematode cercariae infections in freshwater snails of Chitwan District, central Nepal. Himalayan J H Sci 7:9–14. https://doi.org/10.3126/hjs.v7i9.2183
Doanh PN, Hien HV, Dung BT, Loan HT (2019) Infection status and molecular identification of digenean cercariae in snails in Kim Son district, Ninh Binh Province and Ba Vi district, Ha Noi. AJB 41(3) https://doi.org/10.15625/0866-7160/v41n3.13893
Dung BT, Doanh PN, The DT, Loan HT, Losson B, Caron Y (2013) Morphological and molecular characterization of lymnaeid snails and their potential role in transmission of Fasciola spp. in Vietnam. Korean J Parasitol 51(6):657–662. https://doi.org/10.3347/kjp.2013.51.6.657
Estuningsih SE, Copeman DB (1996) Trematode Larvae in Lymnaea Rubiginosa and their Definitive Host in Irrigated Rice Fields in West Java. Jurnal Ilmu Ternak Dan Veteriner 1(3):200–205
Gordon CA, Acosta LP, Gobert GN, Jiz M, Olveda RM, Ross AG, Gray DJ, Williams GM, Harn D, Li Y, McManus DP (2015) High Prevalence of Schistosoma japonicum and Fasciola gigantica in Bovines from Northern Samar, the Philippines. PLoS Negl Trop Dis 9(2):e0003108. https://doi.org/10.1371/journal.pntd.0003108
Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27(2):221–224. https://doi.org/10.1093/molbev/msp259
Graczyk TK, Fried B (1998) Echinostomiasis: a common but forgotten food-borne disease. Am J Trop Med Hyg 58(4):501–504. https://doi.org/10.4269/ajtmh.1998.58.501
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–21. https://doi.org/10.1093/sysbio/syq010
Hara H, Miyauchi Y, Tahara S, Yamashita H (2014) Human laryngitis caused by Clinostomum complanatum. Nagoya J Med Sci 76(1–2):181–185
Japa O, Siriwechviriya P, Prakhammin K (2020) Occurrence of fluke infection in beef cattle around Phayao Lake, Phayao. Thailand Vet World 13(2):334–337. https://doi.org/10.14202/vetworld.2020.334-337
Japa O, Suwancharoen C, Bunsong T, Phuangsri C (2021) Parasitological and molecular characterization of the avian schistosomatid cercariae infecting lymnaeidae snails in Phayao. Northern Thailand Vet World 14(10):2655–2661. https://doi.org/10.14202/vetworld.2021.2655-2661
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587–589. https://doi.org/10.1038/nmeth.4285
Kamo H, Ogino K, Hatsushika R (1962) A unique infection of man with Clinostomum sp., a small trematode causing acute laryngitis. Yonago Acta Med 6(2):37–40
Kaset C, Eursitthichai V, Vichasri-Grams S, Viyanant V, Grams R (2010) Rapid identification of lymnaeid snails and their infection with Fasciola gigantica in Thailand. Exp Parasitol 126(4):482–488. https://doi.org/10.1016/j.exppara.2010.05.021
Kitagawa N, Oda M, Totoki T, Washizaki S, Oda M, Kifune T (2003) Lidocaine spray used to capture a live clinostomum parasite causing human laryngitis. Am J Otolaryngol 24(5):341–343. https://doi.org/10.1016/S0196-0709(03)00060-7
Krailas D, Namchote S, Komsuwan J, Wongpim T, Apiraksena K, Glaubrecht M, Sonthiporn P, Sansawang C, Suwanrit S (2022) Cercarial dermatitis outbreak caused by ruminant parasite with intermediate snail host: schistosome in Chana, South Thailand. Evol Syst 6:151–173. https://doi.org/10.3897/evolsyst.6.87670
Kudlai O, Pantoja C, O’Dwyer K, Jouet D, Skírnisson K, Faltýnková A (2021) Diversity of Plagiorchis (Trematoda: Digenea) in high latitudes: Species composition and snail host spectrum revealed by integrative taxonomy. J Zoolog Syst Evol Res 59(5):937–962. https://doi.org/10.1111/jzs.12469
Kullavanijaya P, Wongwaisayawan H (1993) Outbreak of cercarial dermatitis in Thailand. Int J Dermatol 32(2):113–115. https://doi.org/10.1111/j.1365-4362.1993.tb01448.x
Lagrue C, Poulin R (2007) Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions? J Evol Biol 20(3):1189–1195. https://doi.org/10.1111/j.1420-9101.2006.01277.x
Lockyer AE, Olson PD, Ostergaard P, Rollinson D, Johnston DA, Attwood SW, Southgate VR, Horak P, Snyder SD, Le TH, Agatsuma T, McManus DP, Carmichael AC, Naem S, Littlewood DT (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitol 126(Pt 3):203–224. https://doi.org/10.1017/s0031182002002792
Loy C, Haas W (2001) Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitol Res 87(10):878–882. https://doi.org/10.1007/s004360100462
Mardin S, Sardjono TW, Fitri LE, Aulanni’am, Ramadhan A (2018) Effect of Ecological Factors on Snails Infection by Schistosoma japonicum in Central Sulawesi, Indonesia. Am J Environ Sci 14(2) https://doi.org/10.3844/ajessp.2018.55.62
Mas-Coma S, Valero MA, Bargues MD (2009) Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis. Vet Parasitol 163(4):264–280. https://doi.org/10.1016/j.vetpar.2009.03.024
McAllister CT, Bursey CR, Crawford JA, Kuhns AR, Shaffer C, Trauth SE (2010) Metacercariae of Clinostomum (Trematoda: Digenea) from three species of Ambystoma (Caudata: Ambystomatidae) from Arkansas and Illinois, USA. Comp Parasitol 77(1):25–30
Mereta S, Abaya S, Tulu F, Takele K, Ahmednur M, Melka G, Nanyingi M, Vineer H, Graham-Brown J, Caminade C, Mor S (2023) Effects of Land-Use and Environmental Factors on Snail Distribution and Trematode Infection in Ethiopia. Trop Med Infect Dis 8:154. https://doi.org/10.3390/tropicalmed8030154
Niewiadomska K, Pojmańska T (2011) Multiple strategies of di-genean trematodes to complete their life cycles. Wiad Parazytol 57:233–241
Olivier L, Schneiderman M (1956) A method for estimating the density of aquatic snail populations. Exp Parasitol 5(2):109–117. https://doi.org/10.1016/0014-4894(56)90008-X
Park C-W, Kim J-S, Joo H-S, Kim J (2009) A human case of Clinostomum complanatum infection in Korea. Korean J Parasitol 47(4):401
Pietrock M, Marcogliese DJ (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol 19(7):293–299. https://doi.org/10.1016/s1471-4922(03)00117-x
Poulin R, Cribb TH (2002) Trematode life cycles: short is sweet? Trends Parasitol 18(4):176–183. https://doi.org/10.1016/s1471-4922(02)02262-6
Poulin R, Mouritsen KN (2006) Climate change, parasitism and the structure of intertidal ecosystems. J Helminthol 80(2):183–191. https://doi.org/10.1079/joh2006341
Radomyos P, Bunnag D, Harinasuta T (1989) A new intestinal fluke, Plagiorchis harinasutai n.sp. Southeast Asian J Trop Med Public Health 20(1):101–7
Radomyos P, Radomyos B, Tungtrongchitr A (1994) Multi-infection with helminths in adults from northeast Thailand as determined by post-treatment fecal examination of adult worms. Trop Med Parasitol 45(2):133–135
Rivaz S, Nasiri V, Karimi G, Abdigoudarzi M, Paykari H, Motamedi G, Azizi H, Pirali K, Pac A, Trop J (2014) Lymnaea stagnalis (Linnaeus, 1758) snails’ infection to trematoda larval stages in Shahrekord city’s springs. Asian Pac J Trop Dis 4 https://doi.org/10.1016/S2222-1808(14)60448-5
Ross AG, Bartley PB, Sleigh AC, Olds GR, Li Y, Williams GM, McManus DP (2002) Schistosomiasis. N Engl J Med 346(16):1212–1220. https://doi.org/10.1056/NEJMra012396
Russell-Pinto F, Gonçalves JF, Bowers E (2006) Digenean larvae parasitizing Cerastoderma edule (Bivalvia) and Nassarius reticulatus (Gastropoda) from Ria de Aveiro. Portugal J Parasitol 92(2):319–332. https://doi.org/10.1645/ge-3510.1
Sah R, Khadka S, Hamal R, Poudyal S (2018) Human echinostomiasis: a case report. BMC Res Notes 11(1):17. https://doi.org/10.1186/s13104-018-3133-z
Saleha AA (1991) Liver fluke disease (fascioliasis): epidemiology, economic impact and public health significance. Southeast Asian J Trop Med Public Health 22(Suppl):361–364
Sandoval N, Siles-Lucas M, Pérez-Arellano JL, Carranza C, Puente S, López-Abán J, Muro A (2006) A new PCR-based approach for the specific amplification of DNA from different Schistosoma species applicable to human urine samples. Parasitol 133(Pt 5):581–587. https://doi.org/10.1017/s0031182006000898
Sangwan A, Jackson B, De Glanville W, Pfeiffer D, Stevens K (2016) Spatial analysis and identification of environmental risk factors affecting the distribution of Indoplanorbis and Lymnaea species in semi-arid and irrigated areas of Haryana, India. Parasite Epidemiol Control 1 https://doi.org/10.1016/j.parepi.2016.05.005
Schell SC (1970) How to know the trematodes. W.C. Brown Company, Iowa
Sherman A (2018) Medical parasitology. ED-Tech Press, Waltham Abbey Essex
Soldánová M, Selbach C, Kalbe M, Kostadinova A, Sures B (2013) Swimmer’s itch: etiology, impact, and risk factors in Europe. Trends Parasitol 29(2):65–74. https://doi.org/10.1016/j.pt.2012.12.002
Thanasuwan S, Piratae S, Tankrathok A (2021) Prevalence of gastrointestinal parasites in cattle in Kalasin Province. Thailand Vet World 14(8):2091–2096. https://doi.org/10.14202/vetworld.2021.2091-2096
Tiewchaloern S, Udomkijdecha S, Suvouttho S, Chunchamsri K, Waikagul J (1999) Clinostomum trematode from human eye. Southeast Asian J Trop Med Public Health 30(2):382–384
Toledo R, Álvarez-Izquierdo M, Esteban JG, Muñoz-Antoli C (2022) Neglected food-borne trematodiases: echinostomiasis and gastrodiscoidiasis. Parasitol 149(10):1319–1326. https://doi.org/10.1017/s0031182022000385
Tookhy NA, Isa NMM, Mansor R, Rahaman YA, Ahmad NI, Bui DT, Idris LH, Hamzah NH, Zulkifli N (2023) Morphological and molecular identification of lymnaeid snail and trematodes cercariae in different water bodies in Perak. Parasitol Res, Malaysia. https://doi.org/10.1007/s00436-023-07845-z
Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44(W1):W232–W235. https://doi.org/10.1093/nar/gkw256%JNucleicAcidsResearch
Vázquez Perera A, Alda P, Lounnas M, Sabourin E, Alba A, Pointier J-P, Hurtrez-Boussès S (2018) Lymnaeid snails hosts of Fasciola hepatica and Fasciola gigantica (Trematoda: Digenea): A worldwide review. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 13:1–15. https://doi.org/10.1079/PAVSNNR201813062
Verbrugge LM, Rainey JJ, Reimink RL, Blankespoor HD (2004) Swimmer’s itch: incidence and risk factors. Am J Public Health 94(5):738–741. https://doi.org/10.2105/ajph.94.5.738
Vinarski M, Serbina E (2012) Distribution and quantitative characteristics of common species of pond snails of the subgenera Peregriana and Radix (Mollusca: Gastropoda: Lymnaeidae) in waterbodies of the south of Western Siberia. Inland Water Biol 5:192–198. https://doi.org/10.1134/S1995082912020150
You H, Cai P, Tebeje BM, Li Y, McManus DP (2018) Schistosome Vaccines for Domestic Animals. Trop Med Infect Dis 3(2):68
Acknowledgements
The authors are grateful for the technical assistance provided by Ms Thanawadee Chaiphutorn and Ms Wannapha Kanameung.
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This research project was supported by the Thailand Science Research and Innovation Fund and the University of Phayao (Grant No. FF65-RIM118), Phayao, Thailand.
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OJ conceived and designed the study. OJ, CS and CP surveyed and collected snail samples. OJ, CS, CP and PS performed parasite detection and identification. OJ, CP and TB carried out parasite drawing and imaging. OJ performed molecular work, sequencing and bioinformatics analyses. OJ, CS and CP collected, analysed and interpreted data. OJ wrote the first draft of the manuscript. OJ and CS revised and edited the manuscript. All authors read and approved the final manuscript.
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Suwancharoen, C., Phuangsri, C., Siriwechviriya, P. et al. Diversity of trematode cercariae among naturally infected lymnaeid snails from Phayao, Thailand. Parasitol Res 122, 2691–2708 (2023). https://doi.org/10.1007/s00436-023-07971-8
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DOI: https://doi.org/10.1007/s00436-023-07971-8