Abstract
Fish-borne zoonotic trematodes (FZT) including heterophyids and opisthorchiids are prevalent in native and aquaculture fish in Southeast Asia. FZT are reported highly prevalent in juvenile aquaculture fish that belonged to the family Heterophyidae, particularly Haplorchis taichui. Aquaculture fish are reported to have varying levels of natural infection with H. taichui, but data for their susceptibility as well as resistance to infection are not available. The aim of this study was to determine the susceptibility of five aquaculture fish to H. taichui. Experimental infections were performed by exposing fish individually to 0 (control), 50, 100, or 200 H. taichui cercariae for 12 h. Metacercarial burden was measured at 45 days postinfection. Three out of five fish species, silver barb (Barbonymus gonionotus), common carp (Cyprinus carpio), and mrigal (Cirrhinus mrigala), were highly susceptible to H. taichui infection with percentage ranging from 93.33 to 100 %. The Nile and red tilapia were not susceptible to infection. Among the susceptible fish species, silver barb had higher intensity of H. taichui metacercariae than common carp and mrigal (P < 0.001). Metacercarial burden significantly correlated with the dose of cercarial infection (P < 0.001). Our findings that common aquaculture fish species have varying degrees of susceptibility to H. taichui infection provide important information to reduce parasite transmission in aquaculture fish.
Similar content being viewed by others
References
Betancur RR, Broughton RE, Wiley EO, Carpenter K, Lopez JA, Li C, Holcroft NI, Arcila D, Sanciangco M, Cureton Ii JC, Zhang F, Buser T, Campbell MA, Ballesteros JA, Roa-Varon A, Willis S, Borden WC, Rowley T, Reneau PC, Hough DJ, Lu G, Grande T, Arratia G, Orti G (2013) The tree of life and a new classification of bony fishes. PLoS Curr 5 doi:10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288
Boerlage AS, Graat EAM, Verreth JAJ, De Jong MCM (2011) Effect of fish size on transmission of fish-borne trematodes (Heterophyidae) to common carps (Cyprinus carpio) and implications for intervention. Aquaculture 321:179–184
Boerlage AS, Graat EAM, Verreth JAJ, De Jong MCM (2012) Higher attack rate of fish-borne trematodes (Heterophyidae) in common carp fingerlings (Cyprinus carpio) at lower fish weight. Parasitol Res 111(2):875–879
Boerlage AS, Graat EAM, Verreth JAJ, De Jong MCM (2013) Survival of heterophyid metacercaria in common carp (Cyprinus carpio). Parasitol Res 112(7):2759–2762
Boerlage AS, Graat EAM, Verreth JAJ, De Jong MCM (2014) Transmission of fish-borne zoonotic trematodes (Heterophyidae) to common carp (Cyprinus carpio) is independent of density of fish and trematodes. J Helminthol 88:183–188
Chai JY, Murrell KD, Lymbery AJ (2005) Fish-borne parasitic zoonoses: status and issues. Int J Parasitol 35(11–12):1233–1254
Chai JY, Shin EH, Lee SH, Rim HJ (2009) Foodborne intestinal flukes in Southeast Asia. Korean J Parasitol 47(Suppl):S69–S102
Chai JY, Yong TS, Eom KS, Min DY, Jeon HK, Kim TY, Jung BK, Sisabath L, Insisiengmay B, Phommasack B, Rim HJ (2013) Hyperendemicity of Haplorchis taichui infection among Riparian people in Saravane and Champasak Province, Lao PDR. Korean J Parasitol 51(3):305–311
Chai JY, Sohn WM, Na BK, Yong TS, Eom KS, Yoon CH, Hoang EH, Jeoung HG, Socheat D (2014) Zoonotic trematode metacercariae in fish from phnom penh and pursat, cambodia. Korean J Parasitol 52(1):35–40
Chi TT, Dalsgaard A, Turnbull JF, Tuan PA, Murrell KD (2008) Prevalence of zoonotic trematodes in fish from a Vietnamese fish-farming community. J Parasitol 94(2):423–428
Chun SK (1964) Studies on the experimental mode of infections of Clonorchis sinensis: II. Experimental infection of Clonorchis sinensis cercaria to fry of fresh water fishes. Korean J Parasitol 2(3):137–147
Clausen JH, Madsen H, Murrell KD, Van PT, Nguyen Manh H, Nguyen Viet K, Dalsgaard A (2012) Relationship between snail population density and infection status of snails and fish with zoonotic trematodes in Vietnamese carp nurseries. PLoS Negl Trop Dis 6(12):e1945. doi:10.1371/journal.pntd.0001945
Combes C, Fournier A, Mone H, Theron A (1994) Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109(Suppl):S3–S13
Dung DT, Van DN, Waikagul J, Dalsgaard A, Chai JY, Sohn WM, Murrell KD (2007) Fishborne zoonotic intestinal trematodes, Vietnam. Emerg Infect Dis 13(12):1828–1833
Dung BT, Madsen H, The DT (2010) Distribution of freshwater snails in family-based VAC ponds and associated waterbodies with special reference to intermediate hosts of fish-borne zoonotic trematodes in Nam Dinh Province, Vietnam. Acta Trop 116(1):15–23
FAO (2010) The State of World Fisheries and Aquaculture, FAO Fisheries and Aquaculture Department. Food and Agriculture Organization of the United Nations, Rome
Faust EC, Nishigori M (1926) The life cycles of two new species of heterophyidae, parasitic in mammals and birds. J Parasitol 13:91–132
Grundy-Warr C, Andrews RH, Sithithaworn P, Petney TN, Sripa B, Laithavewat L, Ziegler AD (2012) Raw attitudes, wetland cultures, life-cycles: socio-cultural dynamics relating to Opisthorchis viverrini in the Mekong Basin. Parasitol Int 61(1):65–70
Haas W (1992) Physiological analysis of cercarial behavior. J Parasitol 78:243–255
Haas W (1994) Physiological analyses of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109(Suppl):S15–S29
Haas W (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106(4):349–364
Kaewkes S (2003) Taxonomy and biology of liver flukes. Acta Trop 88(3):177–186
Keiser J, Utzinger J (2005) Emerging foodborne trematodiasis. Emerg Infect Dis 11(10):1507–1514
Keiser J, Utzinger J (2009) Food-borne trematodiases. Clin Microbiol Rev 22(3):466–483
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(3):464–469
Komiya Y (1966) Clonorchis and clonorchiasis. Adv Parasitol 4:53–106
Kumchoo K, Wongsawad C, Chai JY, Vanittanakom P, Rojanapaibul A (2005) High prevalence of Haplorchis taichui metacercariae in cyprinoid fish from Chiang Mai Province, Thailand. Southeast Asian J Trop Med Public Health 36(2):451–455
Liang C, Hu XC, Lv ZY, Wu ZD, Yu XB, Xu J, Zheng HQ (2009) Experimental establishment of life cycle of Clonorchis sinensis. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 27(2):148–150
Lima dos Santos CAM, Howgate P (2011) Fishborne zoonotic parasites and aquaculture: a review. Aquaculture 318(3–4):253–261
Lovis L, Mak TK, Phongluxa K, Soukhathammavong P, Sayasone S, Akkhavong K, Odermatt P, Keiser J, Felger I (2009) PCR diagnosis of Opisthorchis viverrini and Haplorchis taichui infections in a Lao Community in an area of endemicity and comparison of diagnostic methods for parasitological field surveys. J Clin Microbiol 47(5):1517–1523
Lun ZR, Gasser RB, Lai DH, Li AX, Zhu XQ, Yu XB, Fang YY (2005) Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis 5(1):31–41
McDonald DL, Bonner TH, Brandt TM, Trevino GH (2006) Size susceptibility to trematode-induced mortality in the Endangered Fountain Darter (Etheostoma fonticola). J Freshw Ecol 21:293–299
Mitchell AJ, Goodwin AE, Salmon MJ, Brandt TM, Dupree HK (2002) Experimental infection of an exotic heterophyid trematode, Centrocestus formosanus, in four aquaculture fishes. N Am J Aquac 64:55–59
Murray AM (2001) The fossil record and biogeography of the Cichlidae (Actinopterygii: Labroidei). Biol J Linn Soc 74(4):517–532
Nguyen TH, Nguyen VD, Murrell D, Dalsgaard A (2007) Occurrence and species distribution of fishborne zoonotic trematodes in wastewater-fed aquaculture in northern Vietnam. Trop Med Int Health 12(Suppl 2):66–72
Nithikathkul C, Wongsawad C (2008) Prevalence of Haplorchis taichui and Haplorchoides sp. metacercariae in freshwater fish from water reservoirs, Chiang Mai, Thailand. Korean J Parasitol 46(2):109–112
Pearson JC, Ow-Yang CK (1982) New species of Haplorchis from Southeast Asia. together with keys to the Haplorchis-group of heterophyid trematodes of the region. Southeast Asian J Trop Med Public Health 13(1):35–60
Phan VT, Ersboll AK, Nguyen KV, Madsen H, Dalsgaard A (2010a) Farm-level risk factors for fish-borne zoonotic trematode infection in integrated small-scale fish farms in northern Vietnam. PLoS Negl Trop Dis 4(7):e742
Phan VT, Ersboll AK, Bui TQ, Nguyen HT, Murrell D, Dalsgaard A (2010b) Fish-borne zoonotic trematodes in cultured and wild-caught freshwater fish from the Red River Delta, Vietnam. Vector Borne Zoonotic Dis 10(9):861–866
Phan VT, Ersboll AK, Nguyen TT, Nguyen KV, Nguyen HT, Murrell D, Dalsgaard A (2010c) Freshwater aquaculture nurseries and infection of fish with zoonotic trematodes, Vietnam. Emerg Infect Dis 16(12):1905–1909
Phan VT, Ersboll AK, Do DT, Dalsgaard A (2011) Raw-fish-eating behavior and fishborne zoonotic trematode infection in people of northern Vietnam. Foodborne Pathog Dis 8(2):255–260
Pitaksakulrat O, Sithithaworn P, Laoprom N, Laha T, Petney TN, Andrews RH (2013) A cross-sectional study on the potential transmission of the carcinogenic liver fluke Opisthorchis viverrini and other fishborne zoonotic trematodes by aquaculture fish. Foodborne Pathog Dis 10(1):35–41
Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132(Pt 1):143–151
Rhee JK, Kim PG, Baek BK, Lee SB, Ahn BZ (1983) Experimental infection of Clonorchis sinensis To Cyprinus carpio nudus. Korean J Parasitol 21(1):11–19
Rim HJ (2005) Clonorchiasis: an update. J Helminthol 79(3):269–281
Rim HJ, Sohn WM, Yong TS, Eom KS, Chai JY, Min DY, Lee SH, Hoang EH, Phommasack B, Insisengmay S (2008) Fishborne trematode metacercariae detected in freshwater fish from Vientiane Municipality and Savannakhet Province, Lao PDR. Korean J Parasitol 46(4):253–260
Saenphet S, Wongsawad C, Saenphet K, Rojanapaibul A, Vanittanakom P, Chai JY (2008) Haplorchis taichui: worm recovery rate and immune responses in infected rats (Rattus norvegicus). Exp Parasitol 120(2):175–179
Salmon MJ (2000) Impact of an undescribed heterophyid trematode on the fountain darter, Etheostoma fonticola. Dissertation, Southwest Texas State University
Schell SC (1970) How to know the trematodes. Brown, Dubuque, pp 1–335
Scholz T, Ditrich O, Tuma M, Giboda M (1991) Study of the body surface of Haplorchis yokogawai (Katsuta, 1932) and H. taichui (Nishigori, 1924) (Trematoda:Heterophyidae). Southeast Asian J Trop Med Public Health 22(3):443–448
Sithithaworn P, Pipitgool V, Srisawangwong T, Elkins DB, Haswell-Elkins MR (1997) Seasonal variation of Opisthorchis viverrini infection in cyprinoid fish in north-east Thailand: implications for parasite control and food safety. Bull World Health Organ 75(2):125–131
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(1):10–16
Skov J, Kania PW, Dalsgaard A, Jorgensen TR, Buchmann K (2009) Life cycle stages of heterophyid trematodes in Vietnamese freshwater fishes traced by molecular and morphometric methods. Vet Parasitol 160(1–2):66–75
Sohn WM, Yong TS, Eom KS, Min DY, Lee D, Jung BK, Banouvong V, Insisiengmay B, Phommasack B, Rim HJ, Chai JY (2014) Prevalence of Haplorchis taichui among humans and fish in Luang Prabang Province, Lao PDR. Acta Trop 136C:74–80
Speed P, Pauley G (1984) The susceptibility of four salmonid species to the eyefluke, Diplostomum spathaceum. Northwest Sci 58:312–316
Sukudeo MVK, Sukudeo SC (2004) Trematode behaviours and the perceptual worlds of parasites. Can J Zool 82:292–315
Thien PC, Dalsgaard A, Thanh BN, Olsen A, Murrell KD (2007) Prevalence of fishborne zoonotic parasites in important cultured fish species in the Mekong Delta, Vietnam. Parasitol Res 101(5):1277–1284
Thien PC, Dalsgaard A, Thanh NN, Olsen A, Murrell KD (2009) Prevalence of zoonotic trematode parasites in fish fry and juveniles in fish farms of the Mekong Delta, Vietnam. Aquaculture 295(1–2):1–5
Toledo R, Esteban JG, Fried B (2006) Immunology and pathology of intestinal trematodes in their definitive hosts. Adv Parasitol 63:285–365
Touch S, Komalamisra C, Radomyos P, Waikagul J (2009) Discovery of Opisthorchis viverrini metacercariae in freshwater fish in southern Cambodia. Acta Trop 111(2):108–113
Velasquez CC (1973a) Observations on some Heterophyidae (Trematoda: Digenea) encysted in Philippine fishes. J Parasitol 59:77–84
Velasquez CC (1973b) Life cycle of Procerovum calderoni (Africa and Garcia, 1935), Price, 1940 (Trematoda: Digenea: Heterophyidae). J Parasitol 59:813–816
Voutilainen A, Valdez H, Karvonen A, Kortet R, Kuukka H, Peuhkuri N, Piironen J, Taskinen J (2009) Infectivity of trematode eye flukes in farmed salmonid fish—effects of parasite and host origins. Aquaculture 293(1–2):108–112
Waikagul J (1991) Intestinal fluke infections in Southeast Asia. Southeast Asian J Trop Med Public Health 22(Suppl):158–162
WHO (1995) Control of foodborne trematode infections. WHO Tech Rep Ser 849, pp 1–157. World Health Organization, Geneva, Switzerland
WHO (2004) Report of joint WHO/FAO Workshop on food-borne trematode infections in Asia, Ha Noi, Vietnam, 26–28 November, 2002. World Health Organization, WPRO, pp 1–58
Wongsawad P, Wongsawad C (2011) Infection dynamics and molecular identification of metacercariae in cyprinoids from Chiang Mai and Sakon Nakhon Provinces. Southeast Asian J Trop Med Public Health 42(1):53–57
Acknowledgments
We acknowledge the support of the Faculty of Medicine Khon Kaen University, Visiting International Professor Program and the Cholangiocarcinoma Screening and Care Program (CASCAP), Khon Kaen University, 40002 Thailand. This work was supported by the Liver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University and Higher Education Research Promotion and National Research University Project of Thailand, Office of the Higher Education Commission, through health cluster (SHeP-GMS).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kopolrat, K., Sithithaworn, P., Tesana, S. et al. Susceptibility, metacercarial burden, and mortality of juvenile silver barb, common carp, mrigal, and tilapia following exposure to Haplorchis taichui . Parasitol Res 114, 1433–1442 (2015). https://doi.org/10.1007/s00436-015-4326-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-015-4326-1