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Sequential development of the immune response in rainbow trout [Oncorhynchus mykiss (Walbaum, 1792)] to experimental plerocercoid infections of Diphyllobothrium dendriticum (Nitzsch, 1824)

Published online by Cambridge University Press:  06 April 2009

G. J. E. Sharp ,
A. W. Pike  and
C. J. Secombes
G. J. E. Sharp
Affiliation:
Department of Zoology, University of Aberdeen, Tillydrone Avenue, Aberdeen AB9 2TN, Scotland
A. W. Pike
Affiliation:
Department of Zoology, University of Aberdeen, Tillydrone Avenue, Aberdeen AB9 2TN, Scotland
C. J. Secombes
Affiliation:
Department of Zoology, University of Aberdeen, Tillydrone Avenue, Aberdeen AB9 2TN, Scotland
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Summary

Development of the inflammatory response of rainbow trout to experimental infections with Diphyllobothrium dendriticum plerocercoids is described using light and electron microscopy. The cellular response to plerocercoids occurred within 2 weeks post-infection (p.i.). This was followed by an increase in leucocyte numbers during weeks 3–6 p.i., with full encapsulation of plerocercoids by week 6 p.i. Neutrophils were the first leucocytes to engage the developing plerocercoid, followed by large influxes of macrophages which transformed into epithelioid cells. With longer times p.i. the accumulation of different leucocyte types increased, and a blood vascular network developed. Full development of the composite cyst was characterized by fibroplasia, particularly at the periphery of the cyst, and the subsequent deposition of a collagenous tissue matrix. Enzyme-linked immunosorbent assay (ELISA) examination of serum samples taken over the 20 week period showed that specific anti-D. dendriticum antibody titres were first detected at 5 weeks p.i. and increased to a maximum by 11 weeks p.i.

Keywords

CestodaDiphyllobothriumplerocercoidrainbow troutinflammationultrastructure
Type
Research Article
Information
Parasitology , Volume 104 , Issue 1 , February 1992 , pp. 169 - 178
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Andersen, K. & Gibson, D. I. (1989). A key to three species of larval Diphyllobothrium Cobbold, 1858 (Cestoda: Pseudophyllidea) occurring in European and North American freshwater fishes. Systematic Parasitology 13, 3–9.CrossRefGoogle Scholar
Arme, C. & Owen, R. W. (1967). Infections of the three spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Muller, 1776), with special reference to pathological effects. Parasitology 57, 301–14.CrossRefGoogle ScholarPubMed
Arme, C. & Owen, R. W. (1968). Occurrence and pathology of Ligula intestinalis infections in British fishes. Journal of Parasitology 54, 272–80.CrossRefGoogle ScholarPubMed
Arme, C. & Owen, R. W. (1970). Observations on a tissue response within the body cavity of fish infected with the plerocercoid larvae of Ligula intestinalis (L.) (Cestoda: Pseudophyllidea). Journal of Fish Biology 2, 35–7.CrossRefGoogle Scholar
Avtalion, R. R., Weiss, E., Moalem, T. & Milgrom, L. (1975). Evidence for cooperation of T and B cells in fish. Israel Journal of Medical Science 11, 1385.Google Scholar
Balkwill, F. R. & Burke, F. (1989). The cytokine network. Immunology Today 10, 299–304.CrossRefGoogle ScholarPubMed
Berezantsev, Yu. A. (1975). Inhibition of the inflammatory cell response by helminth larvae and the specificity of their encapsulation in the host tissues. Doklady Akademii Nauk, SSSR 220, 227–9.Google Scholar
Bullock, W. L. (1963). Intestinal histology of some salmonid fishes with particular reference to the histopathology of Acanthocephalan infections. Journal of Morphology 112, 23–43.CrossRefGoogle Scholar
Bylund, G. (1972). Pathogenic effects of a Diphyllobothrium plerocercoid on its host fishes. Commentationes Biologicae 58, 3–11.Google Scholar
Caspi, R. R. & Avtalion, R. R. (1984). Evidence for the existence of an IL-2 like lymphocyte growth promoting factor in a bony fish, Cyprinus carpio. Developmental and Comparative Immunology 8, 51–60.CrossRefGoogle Scholar
Clem, L. W., Sizemore, R. C., Ellsaesser, C. F. & Miller, N. W. (1985). Monocytes as accessory cells in fish immune responses. Developmental and Comparative Immunology 9, 803–9.CrossRefGoogle ScholarPubMed
Cosgrove, G. E. (1975). Parasites in tissue sections: recognition and reaction. In Pathology of Fishes (ed. Ribelin, W. E. & Migaki, G.), pp. 205–45. Madison, Wisconsin: University of Wisconsin Press.Google Scholar
Ellis, A. E. (1986). The function of teleost fish lymphocytes in relation to inflammation. International Journal on Tissue Reactions 8, 263–70.Google ScholarPubMed
Ellsaesser, C. & Clem, L. W. (1989). Structural and functional similarities between channel catfish and mammalian IL-1. Developmental and Comparative Immunology 13, 362–3.CrossRefGoogle Scholar
Finn, J. P. & Nielson, N. O. (1971). The inflammatory response of rainbow trout. Journal of Fish Biology 3, 463–78.CrossRefGoogle Scholar
Gonzalez, H., Torres, P., Figueroa, L., Contreras, B. & Franjola, R. (1978). Researches on pseudophyllidae (Carus, 1813) in the south of Chile. II Hepatic and splenic pathology by plerocercoid infections of Diphyllobothrium spp. in Salmo gairdnerii Richardson, 1836 of Calafquen lake. Indian Journal of Parasitology 2, 127–9.Google Scholar
Graham, S. & Secombes, C. J. (1988). The production of a macrophage-activating factor from rainbow trout Salmo gairdneri leucocytes. Immunology 65, 293–7.Google ScholarPubMed
Graham, S. & Secombes, C. J. (1990 a). Cellular requirements for lymphokine secretion by rainbow trout Salmo gairdneri leucocytes. Developmental and Comparative Immunology 14, 59–68.CrossRefGoogle ScholarPubMed
Graham, S. & Secombes, C. J. (1990 b). Do fish lymphocytes secrete interferon-γ? Journal of Fish Biology 36, 563–73.CrossRefGoogle Scholar
Halvorsen, O. (1970). Studies of the helminth fauna of Norway XV: On the taxonomy and biology of plerocercoids of Diphyllobothrium Cobbold, 1858 (Cestoda, Pseudophyllidea) from north-western Europe. Nytt Magasin for Zoologi 18, 113–74.Google Scholar
Hoole, D. & Arme, C. (1982). Ultrastructural studies on the cellular response of roach, Rutilus rutilus L., to the plerocercoid larvae of the pseudophyllidean cestode, Ligula intestinalis. Journal of Fish Diseases 5, 131–44.CrossRefGoogle Scholar
Hoole, D. & Arme, C. (1983). Ligula intestinalis (Cestoda: Pseudophyllidea): An ultrastructural study on the cellular response of roach fry, Rutilus rutilus. International Journal for Parasitology 13, 359–63.CrossRefGoogle Scholar
Howell, C. J. StG. (1987). A chemokinetic factor in the carp Cyprinus carpio. Developmental and Comparative Immunology 11, 139–46.CrossRefGoogle ScholarPubMed
Van Kruiningen, H.J., Placke, M. E. & Wojan, L. D. (1987). Diphyllobothrium plerocercoid infestation in landlocked salmon. Veterinary Pathology 24, 285–6.CrossRefGoogle ScholarPubMed
Kuperman, B. I. & Davydov, V. G. (1981). The fine structure of glands in oncospheres, procercoids and plerocercoids of pseudophyllidea (Cestoidea). International Journal for Parasitology 12, 135–44.CrossRefGoogle Scholar
O'Neill, J. G., White, M. G., Sims, T. A. & Barber, D. L. (1988). An inflammatory response of the antarctic silverfish, Pleuragramma antarcticum, Boulenger 1902 (Teleostei: Notothenioidei), to infestation by the plerocercoid of a pseudopyllidean cestode (Diphyllobothrium sp.). British Antarctic Survey Bulletin 79, 51–63.Google Scholar
Otto, T. N. & Heckmann, R. A. (1984). Host tissue response for trout infected with Diphyllobothrium cordiceps larvae. Great Basin Naturalist 44, 125–32.Google Scholar
Powell, M. D., Wright, G. M. & Burka, J. F. (1990). Eosinophilic granule cells in the gills of rainbow trout, Oncorhynchus mykiss: evidence of migration ? Journal of Fish Biology 37, 495–7.CrossRefGoogle Scholar
Pulsford, A. & Matthews, R. A. (1984). An ultrastructural study of the cellular response of the plaice, Pleuronectes platessa L., to Rhipidocotyle johnstonei nom. nov. (pro-Gasterostomum sp. Johnstone, 1905) Matthews, 1968 (Digenea: Bucephalidae). Journal of Fish Diseases 7, 3–14.CrossRefGoogle Scholar
Roitt, I., Brostoff, J. & Male, D. (1989). Immunology. London: Gower Medical Publishing.Google Scholar
Rosen, R. & Dick, T. A. (1984 a). Growth and migration of plerocercoids of Triaenophorus crassus Forel and pathology in experimentally infected whitefish, Coregonus clupeaformis (Mitchill). Canadian Journal of Zoology 62, 203–11.CrossRefGoogle Scholar
Rosen, R. & Dick, T. A. (1984 b). Experimental infections of rainbow trout, Salmo gairdneri Richardson, with plerocercoids of Triaenophorus crassus Forel. Journal of Wildlife Diseases 20, 34–8.CrossRefGoogle ScholarPubMed
Secombes, C. J. (1987). Lymphokine-release from rainbow trout leucocytes stimulated with concanavalin a. Effects upon macrophage spreading and adherence. Developmental and Comparative Immunology 11, 513–20.CrossRefGoogle ScholarPubMed
Sharp, G. J. E. (1990). Studies on the host–parasite interaction between Diphyllobothrium spp. (Cestoda, Pseudophyllidea) and rainbow trout, Oncorhynchus mykiss (Walbaum, 1792). Ph.D. thesis, University of Aberdeen, Scotland, U.K.Google Scholar
Sharp, G. J. E., Pike, A. W. & Secombes, C. J. (1989). The immune response of wild rainbow trout, Salmo gairdneri Richardson, to naturally acquired plerocercoid infections of Diphyllobothrium dendriticum (Nitzsch, 1824) and D. ditremum (Creplin, 1825). Journal of Fish Biology 35, 781–93.CrossRefGoogle Scholar
Sharp, G. J. E., Secombes, C. J. & Pike, A. W. (1990). The laboratory maintenance of Diphyllobothrium dendriticum (Nitzsch, 1824). Parasitology 101, 153–61.CrossRefGoogle ScholarPubMed
Sharp, G. J. E., Pike, A. W. & Secombes, C. J. (1991 a). Leucocyte migration in rainbow trout [Oncorhynchus mykiss (Walbaum)]: Optimisation of migration conditions and responses to host and pathogen [Diphyllobothrium dendriticum (Nitzsch)] derived chemoattractants. Developmental and Comparative Immunology (in the Press).CrossRefGoogle Scholar
Sharp, G. J. E., Pike, A. W. & Secombes, C. J. (1991 b). Rainbow trout [Oncorhynchus mykiss (Walbaum, 1792)] leucocyte interactions with metacestode stages of Diphyllobothrium dendriticum (Nitzsch, 1824), (Cestoda, Pseudophyllidea). Fish and Shellfish Immunology 1, 195–211.CrossRefGoogle Scholar
Sommer, C. V. & Bartos, J. M. (1981). In vitro leukocyte migration assay in rainbow trout with a flexible silicone coverslip. Journal of Comparative Pathology 91, 443–5.CrossRefGoogle Scholar
Sommerville, C. (1981). A comparative study of the tissue response to invasion and encystment by Stephanochasmus baccatus (Nicoll, 1907) (Digenea: Acanthocolpidae) in four species of flatfish. Journal of Fish Diseases 4, 53–68.CrossRefGoogle Scholar
Stromberg, P. C. & Crites, J. L. (1974). Triaenophoriasis in lake Erie white bass, Morone chrysops. Journal of Wildlife Diseases 10, 352–8.CrossRefGoogle ScholarPubMed
Vallejo, A. N. & Ellis, A. E. (1989). Ultrastructural study of the response of eosinophil granule cells to Aeromonas salmonicida extracellular products and histamine liberators in rainbow trout Salmo gairdneri Richardson. Developmental and Comparative Immunology 13, 133–48.CrossRefGoogle ScholarPubMed
Weiland, K. A. & Meyers, T. R. (1989). Histopathology of Diphyllobothrium ditremum plerocercoids in coho salmon Oncorhynchus kisutch. Diseases of Aquatic Organisms 6, 175–8.CrossRefGoogle Scholar
Yasutake, W. T. & Wales, J. H. (1983). Microscopic Anatomy of Salmonids:An Atlas. United States Department of the Interior, Fish and Wildlife Service Resource Publication 150, Washington, DC.Google Scholar