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Pollutant-induced effects on immunological and physiological interactions in aquatic host–trematode systems: implications for parasite transmission

Published online by Cambridge University Press:  12 April 2024

N.J. Morley*
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK
J.W. Lewis
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK
D. Hoole
Affiliation:
School of Life Sciences, Keele University, Keele, Staffs, ST5 5BG, UK
*
* Fax: +44 (0)1784 434326, E-mail: [email protected]
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Abstract

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Under conditions of pollution both host and parasite are susceptible to the pathogenic effects of toxicants, which in turn may result in detrimental changes to their immunological and physiological processes. Digenetic trematodes, which encompass species of both medical and economic importance, possess complex life cycles and are common parasites of both vertebrates and molluscs. The combined stress induced by pollution and parasitism influences the physiology of the host which can have implications not only on host survival but also on the functional biology of resident parasite populations. The present paper reviews the effects of pollutants on the immunology and physiology in both vertebrate and molluscan host–trematode systems and the implications for parasite transmission.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2006

References

Al-Aaser, A.A., Merzabani, M.M., Higgy, N.A. & Abdel-Kader, M.M. (1978) A study on the etiological factors of bilharzial bladder cancer in Egypt 3. Urinary b-glucuronidase. European Journal of Cancer 15, 573583.CrossRefGoogle Scholar
Au, W.W. (2001) Life style factors and acquired susceptibility to environmental disease. International Journal of Hygiene and Environmental Health 204, 1722.CrossRefGoogle ScholarPubMed
Awney, H.A., Ghzlan, H.E., Sheweita, S.A. & Mostafa, M.H. (2001) Different levels of Schistosoma mansoni infection increased the mutagenicity of benzo(a)pyrene, the activity of aryl hydrocarbon hydroxylase and the formation of hepatic microsomal hydrogen peroxide. Toxicology 163, 213218.CrossRefGoogle ScholarPubMed
Barrett, J. (1997) Helminth detoxification mechanisms. Journal of Helminthology 71, 8589.CrossRefGoogle ScholarPubMed
Barrett, J. (1998) Cytochrome P450 in parasitic protozoa and helminths. Comparative Biochemistry and Physiology 121C, 181183.Google Scholar
Baudrimont, M., de Montaudouin, X. & Palvadeau, A. (2003) Bivalve vulnerability is enhanced by parasites through the deficit of metallothionein synthesis: a field monitoring on cockles (Cerastoderma edule). Journal de Physique IV France 107, 131134.Google Scholar
Baudrimont, M., de Montaudouin, X., & Palvadeau, A. (2006) Impact of digenean parasite infection on metallothionein synthesis by the cockle (Cerastoderma edule): a multivariate field monitoring. Marine Pollution Bulletin, in press.CrossRefGoogle ScholarPubMed
Benkova, M., Soltys, J. & Boroskova, Z. (1993) Modulation of the blood leucocyte and sheep complement activity by heavy metal emmission in experimental fasciolosis. Helminthologia 30, 2934.Google Scholar
Booth, G.H. Jr. & Schulbert, A.R. (1968) Zinc metabolism in schistosomes. Proceedings of the Society for Experimental Biology and Medicine 127, 700704.CrossRefGoogle ScholarPubMed
Boroskova, Z., Benkova, M., Soltys, J. & Krupicer, I. (1994) Effect of heavy metal emission on the immune response of sheep with experimental fascioliasis. Parasite Immunology 16, 389391.CrossRefGoogle Scholar
Cheng, T.C. & Sullivan, J.T. (1973) The effect of copper on the heart-rate of Biomphalaria glabrata (Mollusca: Pulmonata). Comparative and General Pharmacology 4, 3741.CrossRefGoogle Scholar
Cross, M.A., Irwin, S.W.B. & Fitzpatrick, S.M. (2001) Effects of heavy metal pollution on swimming and longevity in cercariae of Cryptocotyle lingua (Digenea: Heterophyidae). Parasitology 123, 499507.CrossRefGoogle ScholarPubMed
Cross, M.A., Irwin, S.W.B., Fitzpatrick, S. & Manga, N. (2003) Trematode parasite influence on copper, iron and zinc content of polluted Littorina littorea: infection, host sex and time effects. Journal of the Marine Biological Association of the United Kingdom 83, 12691272.CrossRefGoogle Scholar
Cross, M.A., Irwin, S.W.B. & Fitzpatrick, S.M. (2005) Effects of host habitat quality on the viability of Cryptocotyle lingua (Trematoda: Digenea) cercariae. Parasitology 130, 195201.CrossRefGoogle ScholarPubMed
Dailey, M.D. & Morris, R. (1995) Relationship of parasites (Trematoda: Spirorchidae) and their eggs to the occurrence of fibropapillomas in the green turtle (Chelonia mydas). Canadian Journal of Fisheries and Aquatic Sciences 52 (Suppl. 1), 8489.CrossRefGoogle Scholar
Delak, M. & Radakovic, M. (1978) [Finds of chlorinated hydrocarbons with pesticidal properties in Fasciola hepatica and in the liver of cattle]. Veterinarski Arhiv 48, 1722 (in Serbo-Croatian).Google Scholar
Dimov, V.B., Neychev, H.O., Tsocheva, N.T., Poljakova-Krusteva, O.T. & Krusteva, L.P. (1985) Phagocytic and microbicidal activity of peritoneal-exudative cells from rats upon the combined effect of Fasciola hepatica and diethylnitrosamine. Dokladi na Bolgarskata Akademiya na Naukite 38, 12451247.Google Scholar
Doenhoff, M.J., Hassounah, O.A. & Lucas, S.B. (1985) Does the immunopathology induced by schistosome eggs potentiate parasite survival? Immunology Today 6, 203206.CrossRefGoogle ScholarPubMed
El-Ansary, A. (2003) Biochemical and immunological adaptation in schistosome parasitism. Comparative Biochemistry and Physiology 136B, 227243.CrossRefGoogle Scholar
El-Bassiouni, E.A., Mostafa, M.H., El-Sewedy, S.M., El-Meligy, S., Abdel-Aziz, T. & Abdel-Rafee, A. (1984) Hepatic microsomal enzymes in Schistosoma mansoni infected mice: II. Effect of duration of infection and lindane administration on aminopyrine demethylase and aniline hydroxylase. Journal of Environmental Science and Health B (Pesticides, Food Contaminants, and Agricultural Wastes) 19, 193207.Google ScholarPubMed
El-Gohary, M., Yassin, A.-E. & Shalaby, M.A. (2003) The effect of chronic lead exposure on the course of schistosomiasis in hamsters and the protective effect of the antioxidant preparation ‘Antox’. Human and Experimental Toxicology 22, 481490.CrossRefGoogle ScholarPubMed
El-Khafif, N., Sabry, H., Yehia, H. & Mansy, S. (2001) Ultrastructural study of the combined effect of lead toxicity and schistosomiasis on the liver and kidney in mice. New Egyptian Journal of Medicine 25, 4048.Google Scholar
Evans, D.W., Irwin, S.W.B. & Fitzpatrick, S. (2001) The effect of digenean (Platyhelminthes) infections on heavy metal concentrations in Littorina littorea. Journal of the Marine Biological Association of the United Kingdom 81, 349350.CrossRefGoogle Scholar
Flavell, D.J. & Lucas, S.B. (1983) Promotion of nitrosodimethylamine-initiated bile duct carcinogenesis in the hamster by the human liver fluke. Opisthorchis viverrini. Carcinogenesis 4, 927930.CrossRefGoogle ScholarPubMed
Foley, A.M., Schroeder, B.A., Redlow, A.E., Fick-Child, K.J. & Teas, W.G. (2005) Fibropapillomatosis in stranded green turtles (Chelonia mydas) from the Eastern United States (1980–98): trends and associations with environmental factors. Journal of Wildlife Diseases 41, 2941.CrossRefGoogle ScholarPubMed
Gabrashanska, M. & Tsocheva, N. (1992) Trace-elements content in the tissues of Fasciola hepatica on the background of diethylnitrosamine intoxication. Dokladi na Bolgarskata Akademiya na Naukite 45(10): 111113.Google Scholar
Gentile, J.M. (1985) Schistosome related cancers–a possible role for genotoxins. Environmental Mutagenesis 7, 775785.CrossRefGoogle ScholarPubMed
Giesy, J.P. & Smith, D.H. (1985) Cadmium partitioning and related effects in parasitized and non-parasitized mosquitofish (Gambusia affinis: Poeciliidae). Verhandlungen Internationale Vereinigung für Theoretische und Angewandte Limnologie 22, 24052412.Google Scholar
Gorchilova, L., Polyakova-Krusteva, O. & Vinarova, M. (1986) [Electron microscope study of the tegument and intestinal wall of Fasciola hepatica isolated from experimentally infected rats with chronic diethylnitrosamine intoxication]. Khelmintologiya 22, 914 (in Bulgarian).Google Scholar
Granath, W.O. Jr. Yoshino, T.P. (1985) Biomphalaria glabrata (Gastropoda): effect of urethane on the morphology and function of hemocytes, and on susceptibility to Schistosoma mansoni (Trematoda). Journal of Invertebrate Pathology 45, 324330.CrossRefGoogle ScholarPubMed
Guth, D.J., Blankespoor, H.D. & Cairns, J. (1977) Potentiation of zinc stress caused by parasitic infection of snails. Hydrobiologia 55, 225229.CrossRefGoogle Scholar
Hashem, M. & Boutros, K. (1961) The influence of bilharzial infection on the carcinogenesis of the bladder. An experimental study. Journal of the Egyptian Medical Association 44, 598606.Google ScholarPubMed
Heinonen, J., Kukkonen, J.V.K. & Holopainen, I.J. (1999) The effects of parasites and temperature on the accumulation of xenobiotics in a freshwater clam. Ecological Applications 9, 475481.CrossRefGoogle Scholar
Heinonen, J., Kukkonen, J.V.K. & Holopainen, I.J. (2000) Toxiceokinetics of 2,4,5-trichlorophenol and benzo(a)pyrene in the clam Pisidium amnicum: effects of seasonal temperatures and trematode parasites. Archives of Environmental Contamination and Toxicology 39, 352359.CrossRefGoogle ScholarPubMed
Heinonen, J., Kukkonen, J.V.K. & Holopainen, I.J. (2001) Temperature- and parasite-induced changes in toxicity and lethal body burdens of pentachlorophenol in the freshwater clam Pisidium amnicum . Environmental Toxicology and Chemistry 20, 27782784.Google ScholarPubMed
Heinonen, J., Penttinen, O.-P., Holopainen, I.J. & Kukkonen, J.V.K. (2003) Sublethal energetic responses by Pisidium amnicum (Bivalvia) exposed to pentachlorophenol at two temperatures. Environmental Toxicology and Chemistry 22, 433438.CrossRefGoogle ScholarPubMed
Hicks, R.M., James, C. & Webbe, G. (1980) Effect of Schistosoma haematobium and N-butyl-N-(4-hydroxybutyl) nitrosamine on the development of urothelial neoplasia in the baboon. British Journal of Cancer 42, 730755.CrossRefGoogle ScholarPubMed
Hira, P.R. & Webbe, G. (1972) The effect of sublethal concentrations of the molluscicide triphenyl lead acetate on Biomphalaria glabrata (Say) and on the development of Schistosoma mansoni in the snail. Journal of Helminthology 46, 1126.CrossRefGoogle ScholarPubMed
Hoole, D. (1997) The effects of pollutants on the immune response of fish: implications for helminth parasites. Parassitologia 39, 219225.Google ScholarPubMed
Hoole, D., Lewis, J.W., Schuwerack, P.M.M., Chakravarthy, C., Shrive, A.K., Greenhough, T.J. & Cartwright, J.R. (2003) Inflammatory interactions in fish exposed to pollutants and parasites: a role for apoptosis and C reactive protein. Parasitology 126, S71S85.CrossRefGoogle ScholarPubMed
Ibrahim, W.L.F., Furu, P., Ibrahim, A.M. & Christensen, N.O. (1992) Effect of the organophosphorous insecticide, chlorpyrifos (Dursban), on growth, fecundity and mortality of Biomphalaria alexandrina and on the production of Schistosoma mansoni cercariae in the snail. Journal of Helminthology 66, 7988.CrossRefGoogle ScholarPubMed
Iida, H. (1985) Experimental study of the effects of Clonorchis sinensis infection on induction of cholangiocarcinoma in Syrian golden hamsters administered 0.03% N-2-fluorenylacetamide (FAA). Japanese Journal of Parasitology 34, 716.Google Scholar
Jacobson, K.C., Arkoosh, M.R., Kagley, A.N., Clemons, E.R., Collier, T.K. & Casillas, E. (2003) Cumulative effects of natural and anthropogenic stress on immune function and disease resistance in juvenile Chinook Salmon. Journal of Aquatic Animal Health 15, 112.2.0.CO;2>CrossRefGoogle Scholar
Kakizoe, Y. (1985) The influence of Schistosoma mansoni infection on carcinogenesis of mouse livers initiated by N-2-fluorenylacetamide. Kurume Medical Journal 32, 169178.CrossRefGoogle ScholarPubMed
Karnaukhov, V.N., Milovidova, N.Y. & Kargopolova, I.M. (1977) On a role of carotenoids in tolerance of sea molluscs to environment pollution. Comparative Biochemistry and Physiology 56A, 189193.CrossRefGoogle Scholar
Kiesecker, J.M. (2002) Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proceedings of the National Academy of Sciences USA 99, 99009904.CrossRefGoogle ScholarPubMed
Kirichuk, G. & Stadnichenko, A.P. (2004) [The trematode invasion and accumulation of heavy metals by the mollusc Colletopterum ponderosum (Bivalvia: Unionidae: Anodontinae)]. Parazitologiya 38, 359365 (in Russian).Google ScholarPubMed
Kirichuk, G.E., Stadnichenko, A.P. & Pershko, I.A. (2002) [The effect of the trematode invasion and accumulation of heavy metals onto the pond snail (Mollusca: Gastropoda: Lymnaeidae)]. Parazitologiya 36, 295303 (in Russian).Google ScholarPubMed
Kraak, M.H.S. & Davids, C. (1991) The effect of the parasite Phyllodistomum macrocotyle (Trematoda) on heavy metal concentrations in the freshwater mussel Dreissena polymorpha. Netherlands Journal of Zoology 41, 269276.CrossRefGoogle Scholar
Krist, A.C., Jokela, J., Wiehn, J. & Lively, C.M. (2004) Effects of host condition on susceptibility to infection, parasite development rate, and parasite transmission in a snail–trematode interaction. Journal of Evolutionary Biology 17, 3340.CrossRefGoogle Scholar
Krupicer, I., Velebny, S. & Legath, J. (1996) [Effect of emissions from a mercury treating metallurgical works on the intensity of experimental Fasciola hepatica infection in sheep]. Veterinarni Medicina 41, 103106 (in Slovakian).Google Scholar
Lee, J.-H., Rim, H.-J & Bak, U.-B (1993) Effect of Clonorchis sinensis infection and dimethylnitrosamine administration on the induction of cholangiocarcinoma in Syrian golden hamsters. Korean Journal of Parasitology 31, 2130.CrossRefGoogle ScholarPubMed
Leung, K.M.Y., Taylor, A.C. & Furness, R.W. (2000) Temperature-dependent physiological responses of the dogwhelk Nucella lapillus to cadmium exposure. Journal of the Marine Biological Association of the United Kingdom 80, 647660.CrossRefGoogle Scholar
Linzey, D.W., Burroughs, J., Hudson, L., Marini, M., Robertson, J., Bacon, J.P., Nagarkatti, M. & Nagarkatti, P.S. (2003) Role of environmental pollutants on immune functions, parasitic infections and limb malformations in marine toads and whistling frogs from Bermuda. International Journal of Environmental Health Research 13, 125148.CrossRefGoogle ScholarPubMed
Loker, E.S. & Adema, C.M. (1995) Schistosomes, echinostomes and snails: comparative immunobiology. Parasitology Today 11, 120124.CrossRefGoogle Scholar
Mai, K. (1998) Comparative studies on the nutrition of two species of abalone, Haliotis tuberculata, L. and Haliotis discus hannai Ino. VII. Effects of dietary vitamin C on survival, growth and tissue concentration of ascorbic acid. Aquaculture 161, 383392.CrossRefGoogle Scholar
Marcogliese, D.J., Brambilla, L.G., Gagne, F. & Gendron, A.D. (2005) Joint effects of parasitism and pollution on oxidative stress biomarkers in yellow perch Perca flavescens. Diseases of Aquatic Organisms 63, 7784.CrossRefGoogle ScholarPubMed
Marshall, I., McManus, D.P. & James, B.L. (1974) Glycolysis in the digestive gland of healthy and parasitized Littorina saxatilis rudis (Maton) and in the daughter sporocysts of Microphallus similis (Jag.) (Digenea: Microphallidae) Comparative Biochemistry and Physiology 49B, 291299.Google Scholar
Martin, D.J. & Rainbow, P.S. (1998) Haemocyanin and the binding of cadmium and zinc in the haemolymph of the shore crab Carcinus maenas . The Science of the Total Environment 214, 133152.CrossRefGoogle ScholarPubMed
Martins-Souza, R.L., Pereira, C.A.J., Coelho, P.M.Z. & Negrao-Correa, D. (2003) Silica treatment increases the susceptibility of the Cabo Frio strain of Biomphalaria tenagophila to Schistosoma mansoni infection but does not alter the natural resistance of the Taim strain. Parasitology Research 91, 500507.Google Scholar
Misechko, L.E. & Stadnichenko, A.P. (1988) [Intoxication of Lymnaea stagnalis infected by trematode parthenites with copper sulphate]. Parazitologiya 22, 9699 (in Russian).Google Scholar
Miyasato, M. (1984) Experimental study of the influence of Schistosoma japonicum infection on carcinogenesis of mice liver treated with N-2-fluorenylacetamide (2-FAA). Japanese Journal of Parasitology 33, 4148.Google Scholar
Mizinska-Boevska, Y., Tsocheva, N., Polyakova-Krusteva, O. & Krustev, L. (1990a) Electron microscopic study of the peritoneal macrophages of rats with chronic fascioliasis and the carcinogenic effect of diethylnitrosamine. Acta Veterinaria Hungarica 38, 6975.Google ScholarPubMed
Mizinska-Boevska, Y., Tsocheva, N., Krustev, L. & Polyakova-Krusteva, O. (1990b) Ultrastructural and functional changes in rat peritoneal macrophages under toxic influence of diethylnitrosamine against the background of chronic fascioliasis. Helminthologia 27, 2131.Google Scholar
Mizinska-Boevska, Y., Tsocheva, N., Polyakova-Krusteva, O. & Krustev, L. (1991) Functional changes in the liver of rats with fascioliasis treated with diethylnitrosamine. Enzyme cytochemical study. Khelmintologiya 29, 3540 (in Bulgarian).Google Scholar
Moorthy, K.S., Reddy, B.K., Swami, K.S. & Chetty, C.S. (1985) Glucose metabolism in hepatopancreas and gill of Lamellidens marginalis during methyl parathion toxicity. Pesticide Biochemistry and Physiology 24, 4044.CrossRefGoogle Scholar
Morley, N.J. & Lewis, J.W. (2004) Free-living endohelminths: the influence of multiple factors. Trends in Parasitology 20, 114115.CrossRefGoogle ScholarPubMed
Morley, N.J., Crane, M. & Lewis, J.W. (2002) Toxic effects of cadmium and zinc on the transmission of Echinoparyphium recurvatum cercariae. Journal of Helminthology 76, 157163.CrossRefGoogle ScholarPubMed
Morley, N.J., Irwin, S.W.B. & Lewis, J.W. (2003a) Pollution toxicity to the transmission of larval digeneans through their molluscan hosts. Parasitology 126, S5S26.CrossRefGoogle Scholar
Morley, N.J., Crane, M. & Lewis, J.W. (2003b) Cadmium toxicity and snail–digenean interactions in a population of Lymnaea spp. (Gastropoda: Pulmonata). Journal of Helminthology 77, 4955.CrossRefGoogle Scholar
Morley, N.J., Leung, K.M.Y., Morritt, D. & Crane, M. (2003c) Toxicity of anti-fouling biocides to Parorchis acanthus (Digenea: Philophthalmidae) cercarial encystment. Diseases of Aquatic Organisms 54, 5560.CrossRefGoogle ScholarPubMed
Morley, N.J., Crane, M. & Lewis, J.W. (2004a) Influence of cadmium exposure on the incidence of first intermediate host encystment by Echinoparyphium recurvatum cercariae in Lymnaea peregra . Journal of Helminthology 78, 329332.CrossRefGoogle ScholarPubMed
Morley, N.J., Leung, K.M.Y., Morritt, D. & Crane, M. (2004b) Toxicity of anti-fouling biocides to encysted metacercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae) and their snail hosts. Chemosphere 56, 353358.CrossRefGoogle ScholarPubMed
Morley, N.J., Crane, M. & Lewis, J.W. (2005) Changes in survival characterisitcs of Diplostomum spathaceum cercariae emerged from cadmium-exposed Lymnaea stagnalis. Journal of Helminthology 79, 5559.CrossRefGoogle Scholar
Mostafa, M.H., El-Bassiouni, E.A., El-Sewedy, S.M., Akhnouk, S., Tawfic, T. & Abdel-Rafee, A. (1984) Hepatic microsomal enzymes in Schistosoma mansoni-infected mice: I. Effect of duration of infection and lindane administration on dimethylnitrosamine demethylases. Environmental Research 35, 154159.CrossRefGoogle ScholarPubMed
Mostafa, M.H., Helmi, S., Badawi, A.F., Tricker, A.R., Spiegelhalder, B. & Preussmann, R. (1994) Nitrate, nitrite and volatile N-nitroso compounds in the urine of Schistosoma haematobium and Schistosoma mansoni infected patients. Carcinogenesis 15, 619625.CrossRefGoogle ScholarPubMed
Mostafa, M.H., Sheweita, S.A. & O'Connor, P.J. (1999) Relationship between schistosomiasis and bladder cancer. Clinical Microbiology Reviews 12, 97111.CrossRefGoogle ScholarPubMed
Mutafova, T., Tsocheva, N., Polyakova-Krusteva, O. & Krustev, L. (1986) [Effect of diethylnitrosamine on the chromosome structure of rats infected with Fasciola hepatica and on that of the liver fluke]. Khelmintologiya 22, 4250 (in Bulgarian).Google Scholar
Narayanan, R. & Venkateswara Rao, P. (1981) Effect of xiphidiocercarial infection on the activities of glycolytic and oxidative enzymes in Lymnaea luteola. Journal of Parasitology 67, 3134.CrossRefGoogle Scholar
Okwuosa, V.N. & Osuala, F.O.U. (1993) Toxicity of washing soaps to Schistosoma mansoni cercariae and effects of sublethal concentrations on infectivity in mice. Applied Parasitology 34, 6975.Google ScholarPubMed
Pellinen, J., Ruokolainen, M., Makela, P. & Taskinen, J. (1994) Organic halogen compounds, EOX, in mussels from a clean lake and a pulp mill recipient. Chemosphere 29, 15151526.CrossRefGoogle Scholar
Pistl, J., Mikula, I., Krupicer, I. & Snirc, J. (1995) The influence of heavy metal emissions and Fasciola hepatica infestation on the immunogenicity of a Listeria vaccine. Veterinary and Human Toxicology 37, 110112.Google ScholarPubMed
Pokora, Z., Szilman, P. & Pokora, I. (1993) [Histochemical estimation of zinc accumulation in the hepatopancreatic gland cells of the snail Lymnaea stagnalis (L.) after subacute intoxication with zinc acetate, including infection with digenean larvae]. Wiadomosci Parazytologiczne 39, 225232 (in Polish).Google Scholar
Polyakova-Krusteva, O., Tsocheva, N. & Krustev, L. (1988a) [Mortality rate among rats infested with Fasciola hepatica and given multiple injections of diethylnitrosamine]. Veterinarna Sbirka 86(6): 4345 (in Bulgarian).Google Scholar
Polyakova-Krusteva, O.T., Tsocheva, N.T. & Krustev, L.T. (1988b) Changes in the body weight of rats after Fasciola hepatica and diethynitrosamine treatment. Dokladi na Bolgarskata Akademiya na Naukite 41(7): 129131.Google Scholar
Roberts, M.L., Lewis, J.W., Wiegertjes, G.F. & Hoole, D. (2005) Interaction between the blood fluke, Sanguinicola inermis and humoral components of the immune response of carp, Cyprinus carpio . Parasitology 131, 261271.CrossRefGoogle ScholarPubMed
Russo, J. & Lagadic, L. (2000) Effects of parasitism and pesticide exposure on characteristics and functions of hemocyte populations in the freshwater snail Lymnaea palustris (Gastropoda, Pulmonata). Cell Biology and Toxicology 16, 1530.CrossRefGoogle ScholarPubMed
Ruus, A., Skaare, J.U. & Ingebrigtsen, K. (2001) Accumulation of the lipophilic environmental contaminant lindane in metacercariae of Bucephaloides gracilescens (Trematoda, Bucephalidae) in the central nervous system of bullrout Myoxocephalus scorpius . Diseases of Aquatic Organisms 48, 7577.CrossRefGoogle ScholarPubMed
Salice, C.J. & Roesijadi, G. (2002) Resistance to cadmium and parasite infection are inversely related in two strains of a freshwater gastropod. Environmental Toxicology and Chemistry 21, 13981403.CrossRefGoogle ScholarPubMed
Schuwerack, P.-M.M., Lewis, J.W., Hoole, D. & Morley, N.J. (2001) Ammonia-induced cellular and immunological changes in juvenile Cyprinus carpio infected with the blood fluke. Sanguinicola inermis Parasitology 122, 339345.Google ScholarPubMed
Schuwerack, P.-M.M., Lewis, J.W. & Hoole, D. (2003) Cadmium-induced cellular and immunological responses in Cyprinus carpio infected with the blood parasite, Sanguinicola inermis . Journal of Helminthology 77, 341350.CrossRefGoogle ScholarPubMed
Sheweita, S.A., Mubark, J., Doenhoff, M.J., Mostafa, M.H., Margison, G.P., O'Connor, P.J. & Elder, R.H. (2002) Changes in the expression of cytochrome P450 isozymes and related carcinogen metabolizing enzyme activities in Schistosoma mansoni -infected mice. Journal of Helminthology 76, 7178.CrossRefGoogle ScholarPubMed
Stadnichenko, A.P. (1984) Interrelationships between a host (freshwater mollusc) and parasite (trematode). Hydrobiological Journal 20(6): 16.Google Scholar
Stadnichenko, A.P. & Golovacheva, L.D. (1989) [The effect of different concentrations of surface-active substances on the content of dry remainder of hemolymph of Planorbarius corneus (Mollusca, Pulmonata, Bulinidae), infected with parthenites of Notocotylus attenuatus (Trematoda)]. Parazitologiya 23, 449452 (in Russian).Google Scholar
Stadnichenko, A.P. & Golovacheva, L.D. (1990) The influence of different concentrations of surfactants on the physical and chemical properties of the haemolymph of Planorbarius (Mollusca, Bulinidae) infected with trematodes and free from infection. Parazitologiya 24, 238242 (in Russian).Google Scholar
Stadnichenko, A.P. & Kirichuk, G.E. (2000) [The effect of ammonium nitrate on residual nitrogen content in the haemolymph of Planorbarius purpura (Mollusca: Pulmonata: Bulinidae) in normal and trematode-infected individuals]. Parazitologiya 34, 402407 (in Russian).Google Scholar
Stadnichenko, A.P. & Kirichuk, G.E. (2002) [The effect of trematode invasion and chromium sulphate on the crude protein content in the haemolymph of Viviparus viviparus (Mollusca: Gastropoda: Pectinibranchia)]. Parazitologiya 36, 240246 (in Russian).Google ScholarPubMed
Stadnichenko, A.P. & Kotsyuk, R.V. (1990) [Influence of different concentrations of surface-active substances on the daily food intake and duration of the digestive process in Lymnaea stagnalis infected with Echinostoma revolutum parthenitae]. Parazitologiya 24, 528532 (in Russian).Google Scholar
Stadnichenko, A.P., Schabrovetz, T.I. & Kozakevitch, N.N. (1985a) [The effect of trematode infection and extreme conditions of the environment on the ascorbic acid content in the haemolymph of freshwater gastropods (Gastropoda: Pulmonata)]. Parazitologiya 19, 4954 (in Russian).Google Scholar
Stadnichenko, A.P., Misechko, L.E. & Shepel, A.N. (1985b) [Effect of phenol poisoning on the cartinoid pigment contents in the haemolymph of freshwater molluscs (Pulmonata, Lymnaeidae and Bulinidae) infected or uninfected with trematode parthenitae]. Parazitologiya 19, 101104 (in Russian).Google Scholar
Stanichenko, A.P., Shabrovets, T.I. & Kozakievitch, N.N. (1986) [Effect of cuprous sulphate solutions on ascorbic acid content in haemolymph of freshwater molluscs (Gastropda, Pulmonata) in normal conditions and during trematode infection]. Parazitologiya 20, 221224 (in Russian).Google Scholar
Stadnichenko, A.P., Ivanenko, L.D. & Sitnyakovskaya, A.M. (1987) [The effect of phenol and pesticides on the physiochemical properties of the haemolymph of freshwater gastropods infected with trematode parthenitae]. Parazitologiya 21, 716720 (in Russian).Google Scholar
Stadnichenko, A.P., Zelinskaya, A. Yu., Kravchuk, A.D. & Doroshenko, G.V. (1988) [Effect of nitroammophoska solutions on aldolase activity in the haemolymph of the mollusc Planorbarius banaticus in the presence and absence of trematode infection]. Parazitologiya 22, 394397 (in Russian).Google Scholar
Stanichenko, A.P., Slastenko, N.N., Kurkchi, L.N., Tomashevskaya, I.A. & Yanaki, Y.A. (1992) [Trematode invasion and lead nitrate impact upon lung and dermal breath of coil-flats]. Parazitologiya 26, 6771 (in Russian).Google Scholar
Stanichenko, A.P., Ivanenko, L.D., Vasilenko, O.F., Vishnevskaya, A.Y., Zinich, M.M., Kirichuk, G.Y., Myslinskaya, L.N. & Semenij, T.A. (1993) [Trematode invasion and zinc sulphate impact upon physico-chemical properties of haemolymph of coil-flats (Mollusca: Bulinidae)]. Parazitologiya 27, 404409 (in Russian).Google Scholar
Stadnichenko, A.P., Anistratenko, V.V., Grabinskaya, O.V., Martynyuk, O.V., Miroshnichenko, O.A., Oleinik, N.G., Sergeichuk, S.A. & Fasolya, O.I. (1994) [Infection of unionids (Mollusca: Bivavia: Unionidae) with parthenitae of Bucephalus polymorphus (Trematoda) and effect of the parasites on the cardiac rhythm of the host]. Parazitologiya 28, 124130 (in Russian).Google Scholar
Stadnichenko, A.P., Ivanchenko, L.D. & Melnik, A.G. (1995) [Effect of the simultaneous action of temperature and potassium nitrate on the motility of cells of the flame cell epithelium of the branchial apparatus of Anodonta cygnaea (Mollusca: Bivalvia: Anodontinae) infected with trematode parthenites (Trematoda: Bucephalidae)]. Parazitologiya 29, 316320 (in Russian).Google Scholar
Stadnichenko, A.P., Slastenko, N.N., Guzenko, O.V., Svitel'sky, N.M. & Sychevskii, A.S. (1996a) [Effect of trematode invasion and of the action of lead nitrate on the pulmonary and cutaneous respiration of Lymnaea stagnalis (Mollusca: Lymnaeidae)]. Parazitologiya 30, 7680 (in Russian).Google Scholar
Stadnichenko, A.P., Ivanenko, L.D., Gusenko, O.V., Svitel'sky, N.M. & Sychevsky, A.S. (1996b) [Influence of joint effect of trematode infection, environmental temperature and lead nitrate on lung and skin transpirations in a pond snail (Pulmonata: Lymnaeidae)]. Parazitologiya 30, 515520 (in Russian).Google Scholar
Stadnichenko, A.P., Ivanenko, L.D., Kurkchi, L.N., Vyskushenko, D.A., Gradovskaya, R.P. & Zimovetz, I.A. (1999) [Influence of natrium and potassium chlorides on fast behavioural and physiological reactions of pond snails (Mollusca: Gastropoda: Pulmonata) under infection with trematode parthenites]. Parazitologiya 33, 335339 (in Russian).Google Scholar
Stadnichenko, A.P., Hyryn, V., Mokrytskaja, A., Ivanenko, L. & Mostipaka, O. (2003) [The effect of carbophos on the concentration of haemoglobin in haemolymph of Planorbarius purpura (Mollusca: Pulmonata: Bulinidae) uninfected and infected with Trematoda]. Visnyk of L'viv University. Biology Series 33, 163167 (in Ukrainian).Google Scholar
Stefanova, R., Tsocheva, N., Poljakova-Krusteva, O., Krustev, L. & Karamucheva, L. (1990) Content of nucleic acids in liver of Fasciola hepatica infected and diethylnitrosamine treated rats. Dokladi na Bolgarskata Akademiya na Naukite 43(11): 115117.Google Scholar
Sures, B. & Knopf, K. (2004) Individual and combined effects of cadmium and 3,3',4,4',5-pentachlorobiphenyl (PCB 126) on the humoral immune response in European eel (Anguilla anguilla) experimentally infected with larvae of Anguillicola crassus (Nematoda). Parasitology 128, 445454.CrossRefGoogle ScholarPubMed
Sures, B., Jurges, G. & Taraschewski, H. (1998) Relative concentrations of heavy metals in the parasites Ascaris suum (Nematoda) and Fasciola hepatica (Digenea) and their respective porcine and bovine definitive hosts. International Journal for Parasitology 28, 11731178.CrossRefGoogle ScholarPubMed
Tantawy, A.A. (2002) Effect of two herbicides on some biological and biochemical parameters of Biomphalaria alexandrina. Journal of the Egyptian Society for Parasitology 32, 837847.Google ScholarPubMed
Tekwani, B.L., Shukla, O.P. & Ghatak, S. (1988) Altered drug metabolism in parasitic diseases. Parasitology Today 4, 410.CrossRefGoogle Scholar
Tesana, S., Takahashi, Y., Sithithaworn, P., Ando, K., Sakakura, T., Yutanawiboonchai, W., Pairojkul, C. & Ruangjirachuporn, W. (2000) Ultrastructural and immunohistochemical analysis of cholangiocarcinoma in immunized Syrian golden hamsters infected with Opisthorchis viverrini and administered with dimethylnitrosamine. Parasitology International 49, 239251.CrossRefGoogle ScholarPubMed
Tewari, A., Joshi, H.V., Raghunathan, C., Sravan Kumar, V.G. & Khambhaty, Y. (2001) Effect of heavy metal pollution on growth, carotenoid content and bacterial flora in the gut of Perna viridis in in situ condition. Current Science 81, 819828.Google Scholar
Thamavit, W., Bhamarapravati, N., Sahaphong, S., Vajrasthira, S. & Angsubhakorn, S. (1978) Effects of dimethylnitrosamine on induction of cholangiocarcinoma in Opisthorchis viverrini-infected Syrian golden hamsters. Cancer Research 38, 46344639.Google ScholarPubMed
Thompson, S.N. (1997) Physiology and biochemistry of snail–larval trematode relationships. pp. 149196 in Fried, B. & Graczyk, T.K. (Eds) Advances in trematode biology. Boca Raton, Florida, CRC Press.Google Scholar
Tsocheva, N. & Gabrashanska, M. (1992) Trace element content of the rat liver after Fasciola hepatica infection and diethylnitrosamine intoxication. Dokladi na Bolgarskata Akademiya na Naukite 45(9): 115117.Google Scholar
Tsocheva, N., Mizinska-Boevska, Y. & Dacheva, R. (1988) Enzymocytochemical changes in the liver of rats with chronic fascioliasis and after toxic effect upon diethylnitrosamine treatment. Khelmintologiya 25, 4144.Google Scholar
Tsocheva, N., Krustev, L. & Polyakova-Krusteva, O. (1990a) Analysis of the changes of some quantitative parameters of the liver of Fasciola hepatica infected and diethynitrosamine treated rats. Helminthologia 27, 261268.Google Scholar
Tsocheva, N., Kuncheva, L., Polyakova-Krusteva, O. & Krustev, L. (1990b) Histoautoradiographic study of Fasciola hepatica infected and diethylnitrosamine treated rats. Helminthologia 27, 117123.Google Scholar
Tsocheva, N., Svilenov, D., Polyakova-Krusteva, O., Krustev, L. & Vinarova, M. (1991a) Pathohistological changes in the spleen of Fasciola hepatica -infected rats treated with diethylnitrosamine. Khelmintologiya 29, 5662.Google Scholar
Tsocheva, N., Dragneva, N., Poljakova-Krusteva, O. & Krustev, L. (1991b) A study of the humoral immune response in Fasciola hepatica -infected and diethylnitrosamine-treated rats. Khelmintologiya 29, 4955.Google Scholar
Tsocheva, N., Poljakova-Krusteva, O.T., Krustev, L.P. & Denkova, R. (1991c) Structural characteristics of hepatocyte lysosomes from rats with chronic fascioliasis and diethylnitrosamine intoxication. Dokladi na Bolgarskata Akademiya na Naukite 44(5): 8386.Google Scholar
Tsocheva, N., Kadiiska, M., Yanev, S., Polakova-Krusteva, O., Krustev, L. & Stoychev, T. (1992a) Changes in some parameters of liver drug metabolism in Fasciola hepatica infected and diethylnitrosamine injected rats. Helminthologia 29, 3942.Google Scholar
Tsocheva, N.T., Kadiiska, M.B., Poljakova-Krusteva, O.T., Krustev, L.P., Yanev, S.S. & Stoytchev, T.S. (1992b) Combined effect of fascioliasis and diethylnitrosamine carcinogenesis on the activity of the rat liver monooxygenase system. Comparative Biochemistry and Physiology 101C, 475479.Google Scholar
Vershinin, A. (1996) Carotenoids in Mollusca: approaching the functions. Comparative Biochemistry and Physiology 113B, 6371.CrossRefGoogle Scholar
Vyskushenko, D.A. (2001) [Influence of copper sulphate on Lymnaea stagnalis heart rate (Mollusca: Gastropoda: Pulmonata) under infection with trematode parthenites]. Parazitologiya 35, 320324 (in Russian).Google Scholar
WHO (1986) The epidemiological association between Schistosoma haematobium infection and bladder cancer. Technical Report Series 186 86, WHO, Geneva.Google Scholar
Yescott, R.E. & Hansen, E.L. (1976) Effect of manganese on Biomphalaria glabrata infected with Schistosoma mansoni . Journal of Invertebrate Pathology 28, 315320.CrossRefGoogle ScholarPubMed