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Associations between Altered Immune Function and Organochlorine Contamination in Young Caspian Terns (Sterna caspia) from Lake Huron, 1997–1999

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Abstract

Previous studies of laboratory animals and wildlife species have demonstrated the immunotoxicity of organochlorines. This study confirmed that associations between organochlorines and suppressed T cell function and enhanced antibody production in young Caspian terns from the Great Lakes, first observed in the early 1990s, continued into the late 1990s. These associations were based on measurement of organochlorines in plasma of individuals and pooled egg samples. During 1997–99, immune function, hematological variables, and organochlorine contamination were measured in prefledgling Caspian terns at two Lake Huron colonies: Channel Shelter Island (Confined Disposal Facility) at the mouth of the Saginaw River in southern Saginaw Bay and Elm Island in the North Channel. Elevated organochlorine exposure, reproductive effects, and decreased recruitment have been documented previously in the Saginaw Bay colony. Concentrations of polychlorinated biphenyls (PCBs) in eggs and plasma and 1,1-dichloro-2,2-bis(p)chlorophenyl)ethylene (DDE) in plasma were consistently higher in Saginaw Bay compared to the North Channel. The mean phytohemagglutinin (PHA) skin test, a measure of T lymphocyte function, was 42% lower in Saginaw Bay. Regression analyses showed strong negative associations between the PHA response and plasma PCBs and, to a slightly lesser degree, DDE. Despite interyear differences, total antibody titers following immunization with sheep red blood cells were higher in Saginaw Bay than the North Channel. Titers were positively associated with plasma PCBs and DDE. Plasma PCBs and DDE were negatively correlated with the percentage of monocytes and positively correlated with the percentage of basophils.

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References

  • Aguilar, A. and Borrell, A. (1994). Abnormally high polychlorinated biphenyl levels in striped dolphins (Stenella coeruleoalba) affected by the 1990-1992 Mediterranean epizootic. Sci. Total Environ. 154, 237-47.

    Google Scholar 

  • Andersson, L., Nikolaidis, E., Brunstrom, B., Bergman, A. and Dinker, L. (1991). Effects of polychlorinated biphenyls with Ah receptor affinity on lymphoid development in the thymus and the bursa of Fabricius of chick embryos in ovo and in mouse thymus anlagen in vitro. Toxicol. and Appl. Pharmacol. 107, 183-8.

    Google Scholar 

  • Badesha, J.S., Maliji, G. and Flaks, B. (1995). Immunotoxic effects of prolonged dietary exposure of male rats to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Eur. J. Pharmacol. Environ. Toxicol. Pharmacol. Sect. 293, 429-37.

    Google Scholar 

  • Clark, D.A., Gauldie, J., Szewczuk, M.R. and Sweeney, G. (1981). Enhanced suppressor cell activity as a mechanism of immunosuppression by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Proc. Soc. Exp. Biol. Med. 168, 290-9.

    Google Scholar 

  • Clark, D.A., Sweeney, G., Safe, S., Hancock, E., Kilburn, D.G. and Gauldie, J. (1983). Cellular and genetic basis for suppression of cytotoxic T cell generation by haloaromatic hydrocarbons. Immunopharmacology 6, 143-53.

    Google Scholar 

  • De Waal, E.J., Schuurman, H.-J., Van Loveren, H. and Vos, J.G. (1997). Differential effects of 2,3,7,8-tetrachlorodi-benzo-p-dioxin, bis ( tri-N-butyltin) oxide and cyclosporin on thymus histopathology. Crit. Rev. Toxicol. 27, 381-430.

    Google Scholar 

  • Dewailly, E., Ayotte, P., Bruneau, S., Gringas, S., Belles-Iles, M. and Roy, R. (2000). Susceptibility to infections and immune status in Inuit infants exposed to organochlorines. Environ. Health Perspect. 108, 205-11.

    Google Scholar 

  • Edelman, A.S., Sanchez, P.L., Robinson, M.E., Hochwald, G.M. and Throbecke, G.J. (1986). Primary and secondary wattle swelling response to phytohemagglutinin as a measure of immunocompetence in chicks. Avian Dis. 30, 105-11.

    Google Scholar 

  • Fan, F., Wierda, D. and Rozman, K. (1996). Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on humoral and cell-mediated immunity in Sprague-Dawley rats. Toxicology 106, 221-8.

    Google Scholar 

  • Fox, G.A., Trudeau, S., Won, H. and Grasman, K.A. (1998). Monitoring the elimination of persistent toxic substances from the Great Lakes: chemical and physiological evidence from adult herring gulls. Environ. Monitoring Assessment 53, 147-68.

    Google Scholar 

  • Fox, L.L. and Grasman, K.A. (1999). Effects of PCB 126 on primary immune organ development in chicken embryos. J. Toxicol. Environ. Health 58, 233-44.

    Google Scholar 

  • Grasman, K.A. and Scanlon, P.F. (1995). Effects of acute lead ingestion and diet on antibody and T-cell-mediated immunity in Japanese quail. Arch. Environ. Contam. Toxicol. 28, 161-7.

    Google Scholar 

  • Grasman, K.A., Fox, G.A., Scanlon, P.F. and Ludwig, J.P. (1996). Organochlorine-associated immunosuppression in prefledgling Caspian terns and herring gulls from the Great Lakes: an ecoepidemiological study. Environ. Health Perspectives 104Suppl. 4, 829-42.

    Google Scholar 

  • Grasman, K.A., Scanlon, P.F. and Fox, G.A. (1998). Reproductive and physiological effects of environmental contaminants in fish-eating birds of the Great Lakes: a review of historical trends. Environ. Monitoring Assessment 53, 117-45.

    Google Scholar 

  • Grasman, K.A., Armstrong, M., Hammersley, D.L., Scanlon, P.F. and Fox, G.A. (2000a). Geographic variation in blood plasma protein concentrations of young herring gulls (Larus argentatus) and Caspian terns (Sterna caspia) from the Great Lakes and Lake Winnipeg. Comp. Biochem. Physiol. C 125, 365-75.

    Google Scholar 

  • Grasman, K.A., Scanlon, P.F. and Fox, G.A. (2000b). Geographic variation in hematological variables in adult and prefledgling herring gulls (Larus argentatus) and possible associations with organochlorine exposure. Arch. Environ. Contam. Toxicol. 38, 244-53.

    Google Scholar 

  • Grasman, K.A. and Whitacre, L.L. (2001). Effects of PCB 126 on thymocyte surface marker expression and immune organ development in chicken embryos. J. Toxicol. Environ. Health 62, 101-116.

    Google Scholar 

  • Hebert, C.E., Norstrom, R.J., Simon, M., Braune, B.M., Weseloh, D.V. and McDonald, C.R. (1994). Temporal trends and sources of PCDDs and PCDFs in the Great Lakes: herring gull egg monitoring, 1981-1991. Environ. Sci. Technol. 28, 1268-77.

    Google Scholar 

  • Hinsdill, R.D., Couch, D.L. and Speirs, R.S. (1980). Immuno suppression in mice induced by dioxin (TCDD) in feed. J. Environ. Pathol. Toxicol. 4, 401-25.

    Google Scholar 

  • Kerkvliet, N.I., Steppan, L.B., Brauner, J.A., Deyo, J.A., Henderson, M.C., Tomar, R.S. and Buhler, D.R. (1990). Influence of the Ah locus on the humoral immunotoxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin: evidence for Ah-receptor-dependent and Ah-receptor-independent mechanisms of immunosuppression. Toxicol. Appl. Pharmacol. 105, 26-36.

    Google Scholar 

  • Lahvis, G., Wells, R., Kuehl, D., Stewart, J., Rhinehart, H. and Via, C. (1995). Decreased lymphocyte responses in free-ai-ranging Bottlenose dolphins (Tursiops truncatus) are associated with increased concentrations of PCBs and DDT in peripheral blood. Environ. Health Perspect. 103Suppl 4, 67-72.

    Google Scholar 

  • Lochmiller, R.L., Vestey, M.R. and Boren, J.C. (1993). Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110, 503-10.

    Google Scholar 

  • Ludwig, J.P., Kurita-Matsuba, H., Auman, H.J., Ludwig, M.E., Summer, C.L., Giesy, J.P., Tillitt, D.E. and Jones, P.D. (1996). Deformities, PCBs, and TCDD-equivalents in double-crested cormorants (Phalacrocorax auritus) and Caspian terns (Hydroprogne caspia) of the upper Great Lakes 1986-1991: testing a cause-effect hypothesis. J. Great Lakes Res. 22, 172-97.

    Google Scholar 

  • Martineau, D., Lagace, A., Beland, P., Higgins, R., Armstrong, D. and Shugart, L.R. (1988). Pathology of stranded beluga whales (Delphinapterus leucas) from the St. Lawrence Estuary, Quebec, Canada. J. Comp. Pathol. 98, 287-311.

    Google Scholar 

  • McGourty, C. (1988). Seal epidemic still spreading. Nature London 334, 553.

    Google Scholar 

  • Mora, M.A., Auman, H.J., Ludwig, J.P., Giesy, J.P., Verbrugge, D.A. and Ludwig, M.E. (1993). Polychlorinated biphenyls and chlorinated insecticides in plasma of Caspian terns: relationships with age, productivity, and colony site tenacity in the Great Lakes. Arch. En¨iron. Contam. Toxicol. 24, 320-31.

    Google Scholar 

  • Morris, D.L., Jordan, S.D. and Holsapple, M.P. (1991). Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on humoral immunity. I. Similarities to Staphylococcus aureus Cowan strain I (SAC) in the in vitro T-dependent antibody response. Immunopharmacology 21, 159-70.

    Google Scholar 

  • Nagarkatti, P.S., Sweeney, G.D., Gauldie, J. and Clark, D.A. (1984). Sensitivity to suppression of cytotoxic T cell generation by 2,3,7,8-tetrachlorodibenzo-p-dioxin TCDD is dependent on the Ah genotype of the murine host. Toxicol. Appl. Pharmacol. 72, 169-76.

    Google Scholar 

  • Pekarik, C. and Weseloh, D.V. (1998). Organochlorine contaminants in herring gull eggs from the Great Lakes, 1974-1995: change point regression analysis and short-term regression. Environ. Monitoring Assessment 53, 77-115.

    Google Scholar 

  • Ross, P., De Swart, R., Addison, R., Van Loveren, H., Vos, J. and Osterhaus, A. (1996). Contaminant-induced immunotoxicity in harbour seals: wildlife at risk? Toxicology 112, 157-69.

    Google Scholar 

  • Sagerup, K., Henriksen, E.O., Skorpin, A., Skaare, J.U. and Gabrielsen, G.W. (2000). Intensity of parasitic nematodes increases with organochlorine levels in the glaucous gull. J. Appl. Ecol. 37, 532-9.

    Google Scholar 

  • Schrank, C.S., Cook, M.E. and Hansen, WR. (1990). Immune responses of mallard ducks treated with immunosuppressive agents: antibody response to erythrocytes and in vivo response to phytohemagglutinin-P. Journal Wildlife Disease 26, 307-15.

    Google Scholar 

  • Smialowicz, R., Andrews, J., Riddle, M., Rogers, R., Luebke, R. and Copeland, C. (1989). Evaluation of the immunotoxicity of low level PCB exposure in the rat. Toxicology 56, 197-211.

    Google Scholar 

  • Smialowicz, R.J., DeVito, M.J., Riddle, M.M., Williams, W.C. and Birnbaum, L.S. (1997). Opposite effects of 2,29,4,49,5,59-hexachlorobiphenyl and 2,3,7,8-tetrachlorodibenzo-p-dioxin on the antibody response to sheep erythrocytes in mice. Fundam. Appl. Toxicol. 37, 141-9.

    Google Scholar 

  • Stadecker, M.J., Lukic, M., Dvorak, A. and Leskowitz, S. (1977). The cutaneous basophil response to phytohemagglutinin in chickens. J. Immunol. 118, 1564-8.

    Google Scholar 

  • Stow, C.A. (1995). Great Lakes herring gull egg PCB concentrations indicate approximate steady-state conditions. Environ. Sci. Technol. 29, 2893-7.

    Google Scholar 

  • Vos, J.G. and Luster, M.I. (1989). Immune alterations. In R.D. Kimbrough and A.A. Jensen (eds) Halogenated Biphenyls, Terphenyls, Naphthalenes, Dibenzodioxins, and Related Products, pp. 295-322. New York: Elsevier Science Publishers.

    Google Scholar 

  • Won, H.T., Mulvihill, M.J. and Wakeford, B.J. (2000). Multiresidue methods for the determination of chlorinated pesticides and polychlorinated biphenyls (PCBs) in wildlife tissues by gas chromatography/mass spectrometry. Technical Report Series No. 335E. Hull, Quebec: Canada Canadian Wildlife Service.

    Google Scholar 

  • Wong, S., Fournier, M., Coderre, D., Banska, W. and Krzystyniak, K. (1992). Environmental immunotoxicology. In D.B. Peakall (ed) Animal Biomarkers as Pollution Indicators, pp. 167-280. London: Chapman and Hall.

    Google Scholar 

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Authors and Affiliations

  1. Department of Biological Sciences, Wright State University, Dayton, OH, 45435, USA

    Keith A. Grasman

  2. Canadian Wildlife Service, National Wildlife Research Centre, Hull, PQ, K1A 0H3, Canada

    Glen A. Fox

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  1. Keith A. Grasman
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  2. Glen A. Fox
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Grasman, K.A., Fox, G.A. Associations between Altered Immune Function and Organochlorine Contamination in Young Caspian Terns (Sterna caspia) from Lake Huron, 1997–1999. Ecotoxicology 10, 101–114 (2001). https://doi.org/10.1023/A:1008950025622

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