Parasitology Research

, Volume 114, Issue 4, pp 1433–1442

Susceptibility, metacercarial burden, and mortality of juvenile silver barb, common carp, mrigal, and tilapia following exposure to Haplorchis taichui

  • Kulthida Kopolrat
  • Paiboon Sithithaworn
  • Smarn Tesana
  • Ross H. Andrews
  • Trevor N. Petney
Original Paper

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.

Keywords

Aquaculture fish Silver barb Common carp Mrigal Fish-borne zoonotic trematodes Haplorchis taichui 

References

  1. 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
  2. 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 321:179–184CrossRefGoogle Scholar
  3. 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):875–879CrossRefPubMedGoogle Scholar
  4. Boerlage AS, Graat EAM, Verreth JAJ, De Jong MCM (2013) Survival of heterophyid metacercaria in common carp (Cyprinus carpio). Parasitol Res 112(7):2759–2762Google Scholar
  5. 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 88:183–188Google Scholar
  6. Chai JY, Murrell KD, Lymbery AJ (2005) Fish-borne parasitic zoonoses: status and issues. Int J Parasitol 35(11–12):1233–1254CrossRefPubMedGoogle Scholar
  7. Chai JY, Shin EH, Lee SH, Rim HJ (2009) Foodborne intestinal flukes in Southeast Asia. Korean J Parasitol 47(Suppl):S69–S102CrossRefPubMedCentralPubMedGoogle Scholar
  8. 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):305–311CrossRefPubMedCentralPubMedGoogle Scholar
  9. 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):35–40CrossRefPubMedCentralPubMedGoogle Scholar
  10. 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):423–428CrossRefPubMedGoogle Scholar
  11. 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):137–147CrossRefGoogle Scholar
  12. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  13. Combes C, Fournier A, Mone H, Theron A (1994) Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109(Suppl):S3–S13CrossRefPubMedGoogle Scholar
  14. 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):1828–1833CrossRefPubMedCentralGoogle Scholar
  15. 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):15–23CrossRefPubMedGoogle Scholar
  16. FAO (2010) The State of World Fisheries and Aquaculture, FAO Fisheries and Aquaculture Department. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  17. Faust EC, Nishigori M (1926) The life cycles of two new species of heterophyidae, parasitic in mammals and birds. J Parasitol 13:91–132CrossRefGoogle Scholar
  18. 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):65–70CrossRefPubMedGoogle Scholar
  19. Haas W (1992) Physiological analysis of cercarial behavior. J Parasitol 78:243–255CrossRefPubMedGoogle Scholar
  20. Haas W (1994) Physiological analyses of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109(Suppl):S15–S29CrossRefPubMedGoogle Scholar
  21. Haas W (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106(4):349–364CrossRefPubMedGoogle Scholar
  22. Kaewkes S (2003) Taxonomy and biology of liver flukes. Acta Trop 88(3):177–186CrossRefPubMedGoogle Scholar
  23. Keiser J, Utzinger J (2005) Emerging foodborne trematodiasis. Emerg Infect Dis 11(10):1507–1514CrossRefPubMedCentralPubMedGoogle Scholar
  24. Keiser J, Utzinger J (2009) Food-borne trematodiases. Clin Microbiol Rev 22(3):466–483CrossRefPubMedCentralPubMedGoogle Scholar
  25. 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):464–469CrossRefPubMedCentralPubMedGoogle Scholar
  26. Komiya Y (1966) Clonorchis and clonorchiasis. Adv Parasitol 4:53–106CrossRefPubMedGoogle Scholar
  27. 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):451–455PubMedGoogle Scholar
  28. 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):148–150PubMedGoogle Scholar
  29. Lima dos Santos CAM, Howgate P (2011) Fishborne zoonotic parasites and aquaculture: a review. Aquaculture 318(3–4):253–261CrossRefGoogle Scholar
  30. 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):1517–1523CrossRefPubMedCentralPubMedGoogle Scholar
  31. 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):31–41CrossRefPubMedGoogle Scholar
  32. 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 21:293–299CrossRefGoogle Scholar
  33. 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 64:55–59CrossRefGoogle Scholar
  34. Murray AM (2001) The fossil record and biogeography of the Cichlidae (Actinopterygii: Labroidei). Biol J Linn Soc 74(4):517–532CrossRefGoogle Scholar
  35. 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):66–72PubMedGoogle Scholar
  36. 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):109–112CrossRefPubMedCentralPubMedGoogle Scholar
  37. 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):35–60PubMedGoogle Scholar
  38. 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):e742CrossRefPubMedCentralPubMedGoogle Scholar
  39. 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):861–866CrossRefPubMedCentralPubMedGoogle Scholar
  40. 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):1905–1909CrossRefPubMedCentralPubMedGoogle Scholar
  41. 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):255–260CrossRefPubMedGoogle Scholar
  42. 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):35–41CrossRefPubMedGoogle Scholar
  43. Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132(Pt 1):143–151PubMedGoogle Scholar
  44. 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):11–19CrossRefGoogle Scholar
  45. Rim HJ (2005) Clonorchiasis: an update. J Helminthol 79(3):269–281CrossRefPubMedGoogle Scholar
  46. 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):253–260CrossRefPubMedCentralPubMedGoogle Scholar
  47. 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):175–179CrossRefPubMedGoogle Scholar
  48. Salmon MJ (2000) Impact of an undescribed heterophyid trematode on the fountain darter, Etheostoma fonticola. Dissertation, Southwest Texas State UniversityGoogle Scholar
  49. Schell SC (1970) How to know the trematodes. Brown, Dubuque, pp 1–335Google Scholar
  50. 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):443–448PubMedGoogle Scholar
  51. 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):125–131PubMedCentralPubMedGoogle Scholar
  52. 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):10–16CrossRefPubMedCentralPubMedGoogle Scholar
  53. 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):66–75CrossRefPubMedGoogle Scholar
  54. 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:74–80CrossRefGoogle Scholar
  55. Speed P, Pauley G (1984) The susceptibility of four salmonid species to the eyefluke, Diplostomum spathaceum. Northwest Sci 58:312–316Google Scholar
  56. Sukudeo MVK, Sukudeo SC (2004) Trematode behaviours and the perceptual worlds of parasites. Can J Zool 82:292–315CrossRefGoogle Scholar
  57. 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):1277–1284CrossRefPubMedGoogle Scholar
  58. 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):1–5CrossRefGoogle Scholar
  59. Toledo R, Esteban JG, Fried B (2006) Immunology and pathology of intestinal trematodes in their definitive hosts. Adv Parasitol 63:285–365Google Scholar
  60. Touch S, Komalamisra C, Radomyos P, Waikagul J (2009) Discovery of Opisthorchis viverrini metacercariae in freshwater fish in southern Cambodia. Acta Trop 111(2):108–113CrossRefPubMedGoogle Scholar
  61. Velasquez CC (1973a) Observations on some Heterophyidae (Trematoda: Digenea) encysted in Philippine fishes. J Parasitol 59:77–84CrossRefPubMedGoogle Scholar
  62. Velasquez CC (1973b) Life cycle of Procerovum calderoni (Africa and Garcia, 1935), Price, 1940 (Trematoda: Digenea: Heterophyidae). J Parasitol 59:813–816CrossRefGoogle Scholar
  63. 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):108–112CrossRefGoogle Scholar
  64. Waikagul J (1991) Intestinal fluke infections in Southeast Asia. Southeast Asian J Trop Med Public Health 22(Suppl):158–162PubMedGoogle Scholar
  65. WHO (1995) Control of foodborne trematode infections. WHO Tech Rep Ser 849, pp 1–157. World Health Organization, Geneva, SwitzerlandGoogle Scholar
  66. 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 1–58Google Scholar
  67. 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):53–57PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Kulthida Kopolrat
    • 1
    • 2
  • Paiboon Sithithaworn
    • 1
    • 2
  • Smarn Tesana
    • 1
  • Ross H. Andrews
    • 1
    • 2
    • 3
    • 4
  • Trevor N. Petney
    • 3
    • 5
  1. 1.Department of Parasitology, Faculty of MedicineKhon Kaen UniversityKhon KaenThailand
  2. 2.Liver Fluke and Cholangiocarcinoma Research Center, Faculty of MedicineKhon Kaen UniversityKhon KaenThailand
  3. 3.Cholangiocarcinoma Screening and Care Program (CASCAP)Khon Kaen UniversityKhon KaenThailand
  4. 4.Imperial College London, Faculty of MedicineSt Mary’s CampusLondonUK
  5. 5.Institute of Zoology 1: Ecology and ParasitologyUniversity of KarlsruheKarlsruheGermany

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