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

Volumn 128, Issue 4, 2004, Pages 445-454

  Sures, B ^a   Knopf, K ^b  

^a UNIVERSITY OF KARLSRUHE   (Germany)

^b LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

Author keywords

Anguilla anguilla; Antibody response; Cadmium; Immunosuppression; Parasites; PCB 126; Pollution

Indexed keywords

3,3',4,4',5 PENTACHLOROBIPHENYL; CADMIUM;

ANGUILLA ANGUILLA; ANGUILLICOLA CRASSUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; EEL; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL MODEL; HOST PARASITE INTERACTION; HUMORAL IMMUNITY; IMMUNOBLOTTING; NEMATODE; NEMATODIASIS; NONHUMAN; PRIORITY JOURNAL; WATER POLLUTANT; WATER POLLUTION; WORM;

ANGUILLA; ANIMALS; ANTIBODIES, HELMINTH; BLOTTING, WESTERN; CADMIUM; ENZYME-LINKED IMMUNOSORBENT ASSAY; NEMATODA; NEMATODE INFECTIONS; POLYCHLORINATED BIPHENYLS; STATISTICS, NONPARAMETRIC; WATER POLLUTANTS, CHEMICAL;

ANGUILLA ANGUILLA; ANGUILLICOLA; ANGUILLIFORMES; ANIMALIA; METAZOA; NEMATODA;

EID: 2442423175     PISSN: 00311820     EISSN: None     Source Type: Journal    
DOI: 10.1017/S003118200300475X     Document Type: Article

References (83)

1. AALTONEN, T. M., JOKINEN, E. I., LAPPIVAARA, J., MARKKULA, S. E., SALO, H. M., LEPPÄNEN, H. & LAMMI, R. (2000). Effects of primary- and secondary-treated bleached kraft mill effluents on the immune system and physiological parameters of roach. Aquatic Toxicology 51, 55-67.
2. ANDERSON, D. E., DIXON, O. W., BODAMMER, J. E. & LIZZIO, E. F. (1989). Suppression of antibody-producing cells in rainbow trout spleen sections exposed to copper in vitro. Journal of Aquatic Animal Health 1, 57-61.
3. ARKOOSH, M. R., CASILLAS, E., CLEMONS, E., KAGLEY, A. N., OLSON, R., RENO, P. & STEIN, J. E. (1998a). Effect of pollution on fish diseases: Potential impacts on salmonid populations. Journal of Aquatic Animal Health 10, 182-190.
4. ARKOOSH, M. R., CASILLAS, E., HUFFMAN, P., CLEMONS, E., EVERED, J., STEIN, J. E. & VARANASI, U. (1998b). Increased susceptibility of juvenile chinook salmon from a contaminated estuary to Vibrio anguillarum. Transactions of the American Fisheries Society 127, 360-374.
5. BARAK, N. A. E. & MASON, C. F. (1990). Mercury, cadmium and lead in eels and roach: the effects of size, season and locality on metal concentrations in flesh and liver. Science of the Total Environment 92, 249-256.
6. BARSE, A. M. & SECOR, D. H. (1999). An exotic nematode parasite of the American eel. Fisheries 24, 6-10.
7. BARTON, B. A. & IWAMA, G. K. (1991). Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annual Review of Fish Diseases 1, 3-26.
8. BELPAIRE, C., DE CHARLEROY, D., THOMAS, K., VAN DAMME, P. & OLLEVIER, F. (1989). Effects of eel restocking on the distribution of the swimbladder nematode Anguillicola crassus in Flanders, Belgium. Journal of Applied Ichthyology 5, 151-153.
9. BOLS, N. C., BRUBACHER, J. L., GANASSIN, R. C. & LEE, L. E. J. (2001). Ecotoxicology and innate immunity in fish. Developmental and Comparative Immunology 25, 853-873.
10. BUCHMANN, K., PEDERSEN, L. O. & GLAMANN, J. (1991). Humoral immune response of European eel Anguilla anguilla to a major antigen in Anguillicola crassus (Nematoda). Diseases of Aquatic Organisms 12, 55-57.
11. ELSASSER, M. S., ROBERSON, B. S. & HETRICK, F. M. (1986). Effects of metals on the chemiluminescent response of rainbow trout (Salmo gairdneri) phagocytes. Veterinary Immunology and Immunopathology 12, 243-250.
12. FRIES, L. T. & WILLIAMS, D. J. (1996). Occurrence of Anguillicola crassus, an exotic parasitic swim bladder nematode of eels, in the southeastern United States. Transactions of the American Fisheries Society 125, 794-797.
13. 2+ on the mitogenic response of carp pronephros lymphocytes. Ecotoxicology and Environmental Safety 17, 183-189.
14. GRINWIS, G. C. M., VETHAAK, A. D., WESTER, P. W. & VOS, J. G. (2000). Toxicology of environmental chemicals in the flounder (Platichthys flesus) with emphasis on the immune system: field, semi-field (mesocosm) and laboratory studies. Toxicology Letters 112-113, 289-301.
15. HAENEN, O. L. M. & VAN BANNING, P. (1991). Experimental transmission of Anguillicola crassus (Nematoda, Dracunculoidea) larvae from infected prey fish to the eel Anguilla anguilla. Aquaculture 92, 115-119.
16. HAENEN, O. L. M., VAN WIJNGAARDEN, T. A. M. & BORGSTEEDE, F. H. M. (1994). An improved method for the production of infective third-stage juveniles of Anguillicola crassus. Aquaculture 123, 163-165.
17. HAENEN, O. L. M., VAN WIJNGAARDEN, T. A. M., VAN DER HEIJDEN, M. H. T., HÖGLUND, J., CORNELISSEN, J. B. J. W., VAN LENGOED, L. A. M. G., BORGSTEEDE, F. H. M. & VAN MUISWINKEL, W. B. (1996). Effects of experimental infections with different doses of Anguillicola crassus (Nematoda, Dracunculoidea) on European eel (Anguilla anguilla). Aquaculture 141, 41-57.
18. HAHN, M. E. & STEGEMANN, J. J. (1994). Regulation of cytochrome P4501A1 in teleosts: sustained induction of CYP1A1 mRNA, protein, and catalytic activity by 2,3,7,8-tetrachlorodibenzo-p-dioxin in the marine fish Stenotomous chrysops. Toxicology and Applied Pharmacology 127, 187-198.
19. HOLSAPPLE, M. P., SNYDER, N. K., WOOD, S. C. & MORRIS, D. L. (1991). A review of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced changes in immuno-competence: 1991 update. Toxicology 69, 219-255.
20. HÖGLUND, J. & PILSTRÖM, L. (1995). Mechanical isolation and characterization of antigens from adult Anguillicola crassus. Fish and Shellfish Immunology 5, 51-60.
21. HÖGLUND, J., ANDERSSON, J., WICKSTRÖM, H. & REIZENSTEIN, M. (1992). The distribution of Anguillicola in Sweden and its association with thermal discharge areas. Irish Fisheries Investigations 36, 143-150.
22. HOOLE, D. (1997). The effects of pollutants on the immune response of fish: implications for helminth parasites. Parassitologia 39, 219-225.
23. KAFAFI, S. A., AFEEFY, H. Y., ALI, A. H., SAID, H. K. & KAFAFI, G. (1993). Binding of polychlorinated biphenyls to the aryl hydrocarbon receptor. Environmental Health Perspectives 101, 422-428.
24. KELLY, C. E., KENNEDY, C. R. & BROWN, J. A. (2000). Physiological status of wild European eels (Anguilla anguilla) infected with the parasitic nematode Anguillicola crassus. Parasitology 120, 195-202.
25. KENNEDY, C. & FITCH, D. J. (1990). Colonization, larval survival and epidemiology of the nematode Anguillicola crassus, parasitic in the eel, Anguilla anguilla, in Britain. Journal of Fish Biology 36, 117-131.
26. KIRK, R. S., LEWIS, J. W. & KENNEDY, C. R. (2000a). Survival and transmission of Anguillicola crassus Kuwahara, Niimi & Itagaki, 1974 (Nematoda) in seawater eels. Parasitology 120, 289-295.
27. KIRK, R. S., KENNEDY, C. R. & LEWIS, J. W. (2000b). Effect of salinity on hatching, survival and infectivity of Anguillicola crassus (Nematoda: Dracunculoidea) larvae. Diseases of Aquatic Organisms 40, 211-218.
28. KNOPF, K. (1999). Untersuchungen zur Immunantwort des Europäischen Aals (Anguilla anguilla) auf den Schwimmblasen-Nematoden Anguillicola crassus. Ph.D. thesis. University of Karlsruhe.
29. KNOPF, K., NASER, K., VAN DER HEIJDEN, M. H. T. & TARASCHEWSKI, H. (2000a). Development of the humoral immune-response in European eel (Anguilla anguilla) experimentally infected with Anguillicola crassus. Diseases of Aquatic Organisms 42, 61-69.
30. KNOPF, K., NASER, K., VAN DER HEIJDEN, M. H. T. & TARASCHEWSKI, H. (2000b). Evaluation of an ELISA and immunoblotting for studying the humoral immune response in Anguillicola crassus infected European eel Anguilla anguilla. Diseases of Aquatic Organisms 43, 39-48.
31. KNOPF, K., WÜRTZ, J., SURES, B. & TARASCHEWSKI, H. (1998). Impact of low water temperature on the development of Anguillicola crassus in the final host Anguilla anguilla. Diseases of Aquatic Organisms 33, 143-149.
32. LAFFERTY, K. D. (1997). Environmental parasitology: What can parasites tell us about human impacts on the environment? Parasitology Today 13, 251-255.
33. LEMAIRE-GONY, S., LEMAIRE, P. & PULSFORD, A. L. (1995). Effects of cadmium and benzo(a)pyrene on the immune system, gill ATPase and EROD activity of European sea bass Dicentrarchus labrax. Aquatic Toxicology 31, 297-313.
34. MACKENZIE, K., WILLIAMS, H. H., WILLIAMS, B., McVICAR, A. H. & SIDDALL, R. (1995). Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 35, 85-144.
35. MAAMOURI, F., GARGOURI, L., OULD DADDAH, M. & BOUIX, G. (1999). Occurrence of Anguillicola crassus (Nematoda, Anguillicolidae) in the Ichkeul lake (Northern Tunisia). Bulletin of the European Association of Fish Pathologists 19, 17-19.
36. MERIAN, E. (1991). Metals and their Compounds in Environment and Life. Occurence, Analysis and Biological Relevance. Verlag Chemie Weinheim, New York.
37. MOLNÁR, K. (1994). Formation of parasitic nodules in the swimbladder and intestinal walls of the eel Anguilla anguilla due to infections with larval stages of Anguillicola crassus. Diseases of Aquatic Organisms 20, 163-170.
38. MOLNÁR, K., BASKA, F., CSABA, G., GLÁVITS, R. & SZÉKELY, C. (1993). Pathological and histopathological studies of the swimbladder of eels Anguilla anguilla infected by Anguillicola crassus (Nematoda: Dracunculoidea). Diseases of Aquatic Organisms 15, 41-50.
39. MOLNÁR, K., SZAKOLCZAI, J. & VETÉSI, F. (1995). Histological changes in the swimbladder wall of eels due to abnormal location of adult and second stage larvae of Anguillicola crassus. Acta Veterinaria Hungarica 43, 125-137.
40. MORAVEC, F. (1992). Spreading of the nematode Anguillicola crassus (Dracunculoidea) among eel populations in Europe. Folia Parasitologica 39, 247-248.
41. MORAVEC, F. (1996). Aquatic invertebrates (snails) as new paratenic hosts of Anguillicola crassus (Nematoda: Dracunculoidea) and the role of paratenic hosts in the life cycle of this parasite. Diseases of Aquatic Organisms 27, 237-239.
42. MORAVEC, F. & KONECNY, R. (1994). Some new data on the intermediate and paratenic hosts of the nematode Anguillicola crassus Kuwahara, Niimi & Itagaki, 1974 (Dracunculoidea), a swimbladder parasite of eels. Folia Parasitologica 41, 65-70.
43. MORAVEC, F. & ŠKORIKOVÁ, B. (1998). Amphibians and larvae of aquatic insects as new paratenic hosts of Anguillicola crassus (Nematoda: Dracunculoidea), a swimbladder parasite of eels. Diseases of Aquatic Organisms 34, 217-222.
44. MORAVEC, F. & TARASCHEWSKI, H. (1988). Revision of the genus Anguillicola Yamaguti 1935 (Nematoda: Anguillicolidae) of the swimbladder of eels, including descriptions of two new species, A. novaezelandiae sp. n. and A. papernai sp. n. Folia Parasitologica 35, 125-146.
45. MURAD, A. & HOUSTON, A. H. (1988). Leucocytes and leucopoitic capacity in goldfish, Carassius auratus exposed to sublethal levels of cadmium. Aquatic Toxicology 13, 141-154.
46. NAGASAWA, K., KIM, Y. G. & HIROSE, H. (1994). Anguillicola crassus and Anguillicola globiceps (Nematoda: Dracunculoidea) parasitic in the swimbladder of eels (Anguilla japonica and A. anguilla) in East Asia. Folia Parasitologica 41, 127-137.
47. NIELSEN, M. E. & BUCHMANN, K. (1997). Glutathione-s-transferase is an important antigen in the eel nematode Anguillicola crassus. Journal of Helminthology 71, 319-324.
48. O'NEILL, J. G. (1981). Effects of intraperitoneal lead and cadmium on the humoral immune response of Salmo trutta. Bulletin of Environmental Contamination and Toxicology 27, 42-48.
49. QUABIUS, E. S., NOLAN, D. T., SEGNER, H. & WENDELAAR BONGA, S. E. (2002). Confinement stress and starvation modulate the induction of EROD activity after dietary exposure to PCB 126 in the Mozambique tilapia (Oreochromis mossambicus). Fish Physiology and Biochemistry 25, 109-119.
50. REGALA, R. P., RICE, C. D., SCHWEDLER, T. E. & DOROCIAK, I. R. (2001). The effects of tributyltin (TBT) and 3,3′4,4′5- pentachlorobiphenyl (PCB-126) mixtures on antibody-responses and phagocyte oxidative burst activity in channel catfish, Ictalurus punctatus. Archives of Environmental Contamination and Toxicology 40, 386-391.
51. RICE, C. D. & SCHLENK, D. (1995). Immune function and cytochrome P4501A activity after acute exposure to 3,3′4,4′,5- Pentachlorobiphenyl (PCB 126) in channel catfish. Journal of Aquatic Animal Health 7, 195-204.
52. RICE, C. D., ROSZELL, L. E., BANES, M. M. & ARNOLD, R. E. (1998). Effects of dietary PCBs and nonyl-phenol on immune function and CYP1Y activity in channel catfish, Ictalurus punctatus. Marine Environmental Research 46, 351-354.
53. ROBOHM, R. A. (1986). Paradoxical effects of cadmium exposure on antibacterial antibody responses in two fish species: inhibition in cunners (Tautogolabrus adspersus) and enhancement in striped bass (Morone saxatilis). Veterinary Immunology and Immunopathology 12, 251-262.
54. SAFE, S. (1994). Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs) and related compounds. Environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Critical Reviews in Toxicology 21, 51-88.
55. SANCHEZ-DARDON, J., VOCCIA, I., HONTELA, A., CHILMONCYK, S., DUNIER, M., BOERMANS, H., BLAKELY, B. & FOURNIER, M. (1999). Immunomodulation by heavy metals tested individually or in mixtures in rainbow trout (Oncorhynchus mykiss) exposed in vivo. Environmental Toxicology and Chemistry 18, 1492-1497.
56. SCHULTE, S., MENGEL, K., GÄTKE, U. & FRIEDBERG, K. D. (1994). No influence of cadmium on the reproduction of specific antibodies in mice. Toxicology 93, 263-268.
57. SPITZBERGEN, J. M., SCHAT, K. A., KLEEMAN, J. M. & PETERSON, R. (1986a). Interactions of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) with immune responses of rainbow trout. Veterinary Immunology and Immunopathology 12, 263-280.
58. SPITZBERGEN, J. M., SCHAT, K. A., KLEEMAN, J. M. & PETERSON, R. (1986b). Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) or Aroclor 1254 on the resistance of rainbow trout, Salmo gairdneri T, to infectious haematopoietic necrosis virus. Journal of Fish Diseases 11, 73-83.
59. SURES, B. (2001). The use of parasites as bioindicators in aquatic ecosystems: a review. Aquatic Ecology 35, 245-255.
60. SURES, B. (2002). Charakterisierung aquatischer Wirt-Parasit- Interaktionen aus ökologischer und (öko-)toxikologischer Sicht. Habilitationsschrift, Universität Karlsruhe.
61. SURES, B. (2003). Accumulation of heavy metals by intestinal helminths in fish: facts, appraisal and perspectives. Parasitology 126 (Suppl.), S53-S60.
62. SURES, B. & STREIT, B. (2001). Eel parasite diversity and intermediate host abundance in the River Rhine, Germany. Parasitology 123, 185-191.
63. SURES, B., KNOPF, K. & KLOAS, W. (2001). Induction of stress by the swimbladder nematode Anguillicola crassus in European eels, Anguilla anguilla, after repeated experimental infection. Parasitology 123, 179-184.
64. SURES, B., KNOPF, K. & TARASCHEWSKI, H. (1999b). Development of Anguillicola crassus (Dracunculoidea, Anguillicolidae) in experimentally infected Balearic congers Ariosoma balearicum (Anguilloidea, Congridae). Diseases of Aquatic Organisms 39, 75-78.
65. SURES, B., TARASCHEWSKI, H. & JACKWERTH, E. (1994). Lead content of Paratenuisentis ambiguus (Acanthocephala), Anguillicola crassus (Nematodes) and their host Anguilla anguilla. Diseases of Aquatic Organisms 19, 105-107.
66. SURES, B., KNOPF, K., WÜRTZ, J. & HIRT, J. (1999a). Richness and diversity of parasite communities in European eels Anguilla anguilla of the River Rhine, Germany, with special reference to helminth parasites. Parasitology 119, 323-330.
67. SZÉKELY, C. (1994). Paratenic hosts for the parasitic nematode Anguillicola crassus in Lake Balaton, Hungary. Diseases of Aquatic Organisms 18, 11-20.
68. SZÉKELY, C. (1995). Dynamics of Anguillicola crassus (Nematoda: Dracunculoidea) larval infection in paratenic host fishes of Lake Balaton, Hungary. Acta Veterinaria Hungarica 43, 401-422.
69. SZÉKELY, C. (1996). Experimental studies on the infectivity of Anguillicola crassus third stage larvae (Nematoda) from paratenic hosts. Folia Parasitologica 43, 305-311.
70. TARASCHEWSKI, H., MORAVEC, F., LAMAH, T. & ANDERS, K. (1987). Distribution and morphology of two helminths recently introduced into European eel populations: Anguillicola crassus (Nematoda, Dracunculoidea) and Paratenuisentis ambiguus (Acanthocephala, Tenuisentidae). Diseases of Aquatic Organisms 3, 167-176.
71. TESCH, F. W. (1999). Der Aal. Blackwell Wissenschafts-Verlag, Berlin, Wien.
72. THOMAS, K. & OLLEVIER, F. (1992). Paratenic hosts of the swimbladder nematode Anguillicola crassus. Diseases of Aquatic Organisms 13, 165-174.
73. THUVANDER, A. (1989). Cadmium exposure of rainbow trout, Salmo gairdneri Richardson: effects on immune functions. Journal of Fish Biology 35, 521-529.
74. VAN BANNING, P. & HAENEN, O. L. M. (1990). Effects of the swimbladder nematode Anguillicola crassus in wild and farmed eel, Anguilla anguilla. In Pathology in Marine Science. Proceedings of the 3rd International Colloquium on Pathology in Marine Aquaculture, Gloucester Point, Virginia, 2-6 October 1988 (ed. Perkins, F. O. & Cheng, T. C.), pp. S317-S330. Academic Press Inc., New York.
75. VAN DER HEIJDEN, M. H. T., ROOIJAKKERS, J. B. M. A., BOOMS, G. H. R., ROMBOUT, J. H. W. M. & BOON, J. H. (1995). Production, characterization and applicability of monoclonal antibodies to European eel (Anguilla anguilla L., 1758) immunoglobulin. Veterinary Immunology and Immunopathology 45, 151-164.
76. VAN LOVEREN, H., ROSS, P. S., OSTERHAUS, A. D. M. E. & VOS, J. G. (2000). Contaminant-induced immunosuppression and mass mortalities among harbor seals. Toxicology Letters 112-113, 319-324.
77. WAKELIN, D. (1996). Immunology and genetics of zoonotic infections involving parasites. Comparative Immunology and Microbiology 4, 255-265.
78. WENDELAAR BONGA, S. E. (1997). The stress response in fish. Physiological Reviews 77, 591-625.
79. WEYTS, F. A. A., COHEN, N., FLIK, G. & VERBURG-VAN KEMENADE, B. M. L. (1999). Interactions between the immune system and the hypothalamo-pituitary- interrenal axis in fish. Fish and Shellfish Immunology 9, 1-20.
80. WÜRTZ, J. & TARASCHEWSKI, H. (2000). Histopathological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus. Diseases of Aquatic Organisms 39, 121-134.
81. WÜRTZ, J., TARASCHEWSKI, H. & PELSTER, B. (1996). Changes in gas composition in the swimbladder of the European eel (Anguilla anguilla) infected with Anguillicola crassus (Nematoda). Parasitology 112, 233-238.
82. ZELIKOFF, J. T. (1993). Metal pollution induced immunomodulation in fish. Annual Reviews on Fish Disease 2, 305-325.
83. ZELIKOFF, J. T. (1998). Biomarkers of immunotoxicity in fish and other non-mammalian sentinel species: predictive value for mammals? Toxicology 129, 63-71.