Organochlorine-associated immunosuppression in prefledgling Caspian terns and herring gulls from the Great Lakes: An ecoepidemiological study

Environmental Health Perspectives

Volumn 104, Issue SUPPL. 4, 1996, Pages 829-842

  Grasman, Keith A ^a,d   Fox, Glen A ^b   Scanlon, Patrick F ^a   Ludwig, James P ^c  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b ENVIRONMENT CANADA   (Canada)

^c SERE Group   (Canada)

^d WRIGHT STATE UNIVERSITY   (United States)

Author keywords

Biomarkers; Fish eating birds; Great Lakes; Immunosuppression; Immunotoxicology; Larus argentatus; Organochlorines; PCBs; Sterna caspia

Indexed keywords

BIOLOGICAL MARKER; ERYTHROCYTE ANTIBODY; ORGANOCHLORINE DERIVATIVE; PHYTOHEMAGGLUTININ; POLYCHLORINATED BIPHENYL; RETINOL;

ANTIBODY TITER; BIRD; CANADA; CELLULAR IMMUNITY; CHICKEN; CONCENTRATION RESPONSE; CONFERENCE PAPER; CONTAMINATION; CONTROLLED STUDY; EGG; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; IMMUNOTOXICITY; LAKE; LEUKOCYTE COUNT; LYMPHOCYTE FUNCTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SKIN TEST; SPECIES DIFFERENCE; T LYMPHOCYTE; WILDLIFE;

AVES; CLUPEA HARENGUS; GALLUS GALLUS; LARIDAE; LARUS ARGENTATUS; OVIS ARIES; STERNA CASPIA;

EID: 0029740181     PISSN: 00916765     EISSN: None     Source Type: Journal    
DOI: 10.1289/ehp.96104s4829     Document Type: Conference Paper

References (92)

1. Koller LD. Effects of environmental contaminants on the immune system. Adv Vet Sci Comp Med 23:267-295 (1979).
2. Luster MI, Blank JA, Dean JH. Molecular and cellular basis of chemically induced immunotoxicity. Annu Rev Pharmacol Toxicol 27:23-49 (1987).
3. Wong S, Fournier M, Coderre D, Banska W, Krzystyniak K. Environmental immunotoxicology. In: Animal Biomarkers as Pollution Indicators (Peakall DB, ed). London:Chapman and Hall, 1992;167-280.
4. Holladay SD, Luster MI. Developmental immunotoxicology. In: Developmental Toxicology (Kimmel C, Buckesam J, eds). New York:Raven Press, 1994;93-118.
5. Pruett SB. Immunotoxicity of agrochemicals: an overview of currently available information. Toxicol Ecotoxicol News 1:49-54 (1994).
6. Fox GA. What have biomarkers told us about the effects of contaminants on the health of fish-eating birds in the Great Lakes? The theory and a literature review. J Gt Lakes Res 19:722-736 (1993).
7. Harris HJ, Erdman TC, Ankley GT, Lodge KB. Measures of reproductive success and polychlorinated biphenyl residues in eggs and chicks of Forster's terns on Green Bay, Lake Michigan, Wisconsin - 1988. Arch Environ Contain Toxicol 25:304-314 (1993).
8. Keith JA. Reproduction in a population of herring gulls (Larus argentatus) contaminated by DDT. J Appl Ecol 3 (Suppl):57-60 (1966).
9. Weseloh DV, Teeple SM, Gilbertson M. Double-crested cormorants of the Great Lakes: Egg-laying paramenters, reproductive failure, and contaminant residues in eggs, Lake Huron 1972-1973. Can J Zool 61:427-436 (1983).
10. Peakall DB, Fox GA. Toxicological investigations of pollutant-related effects in Great Lakes gulls. Environ Health Perspect 71:187-193 (1987).
11. Kubiak TJ, Harris HJ, Smith LM, Schwartz TR, Stalling DL, Trick JA, Sileo L, Docherty DE, Erdman TC. Microcontaminants and reproductive impairment of the Forster's tern on Green Bay, Lake Michigan - 1983. Arch Environ Contam Toxicol 18:706-727 (1989).
12. Ludwig JP, Auman HJ, Kurita H, Ludwig ME, Campbell LM, Giesy JP, Tillitt DE, Jones P, Yamashita N, Tanabe S, Tatsukawa R. Caspian tern reproduction in the Saginaw Bay ecosystem following a 100-year flood event. J Gt Lakes Res 19:96-108 (1993).
13. Bowerman WW, Giesy JP, Best DA, Kramer VJ. A review of factors affecting productivity of bald eagles in the Great Lakes region: implications for recovery. Environ Health Perspect 103:51-59 (1995).
14. Fox GA, Collins B, Hayakawa E, Weseloh DV, Ludwig JP, Kubiak TJ, Erdman TC. Reproductive outcomes in colonial fish-eating birds: a biomarker for developmental toxicants in Great Lakes food chains. II: Spatial variation in the occurrence and prevalence of bill defects in young double-crested cormorants in the Great Lakes, 1979-1987. J Gt Lakes Res 17:158-167 (1991).
15. Gilbertson M, Kubiak T, Ludwig J, Fox G. Great Lakes embryo mortality, edema, and deformities syndrome (GLEMEDS) in colonial fish-eating birds: similarity to chick-edema disease. J Toxicol Environ Health 33:455-520 (1991).
16. Bowerman WW, Kubiak TJ, Holt JB, Evans DL, Eckstein RG, Sindelar CR, Best DA, Kozie KD. Observed abnormalities in mandibles of nestling bald eagles, Haliaeetus leucocephalus. Bull Environ Contain Toxicol 53:450-457 (1994).
17. Giesy JP, Ludwig JP, Tillitt DE. Deformities in birds of the Great Lakes region. Environ Sci Technol 28:128-135 (1994).
18. Fox G, Gilman AP, Peakall DB, Anderka FW. Behavioral abnormalities in nesting Lake Ontario herring gulls. J Wildl Manage 42:477-483 (1978).
19. Mora MA, Auman HJ, Ludwig JP, Giesy JP, Verbrugge DA, Ludwig ME. Polychlorinated biphenyls and chlorinated insecticides in plasma of Caspian terns: relationships with age, productivity, and colony site tenacity in the Great Lakes. Arch Environ Contain Toxicol 24:320-331 (1993).
20. Government of Canada. Toxic Chemicals in the Great Lakes and Associated Effects. Ottawa:Government of Canada, 1991.
21. Stow, CA. Great Lakes herring gull egg PCB concentrations indicate approximate steady-state conditions. Environ Sci Tech 29:2893-2897 (1995).
22. Silkworth JB, Grabstein EM. Polychlorinated biphenyl immunotoxicity: dependence on isomer planarity and the Ah gene complex. Toxicol Appl Pharmacol 65:109-115 (1982).
23. Silkworth JB, Antrim L, Kaminsky LS. Correlations between polychlorinated biphenyl immunotoxicity, the aromatic hydrocarbon locus, and liver microsomal enzyme induction in C57BL/6 and DBA/2 mice. Toxicol Appl Pharmacol 75:156-165 (1984).
24. Nagarkatti PS, Sweeney GD, Gauldie J, Clark DA. 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 72:169-176 (1984).
25. Safe S. Polychlorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs): biochemistry, toxicology, and mechanism of action. CRC Crit Rev Toxicol 13:319-395 (1984).
26. Vos JG, Luster MI. Immune alterations. In: Halogenated Biphenyls, Terphenyls, Naphthalenes, Dibenzodioxins, and Related Products (Kimbrough RD, Jensen AA, eds). New York:Elsevier Science Publishers, 1989;295-322.
27. Kerkvliet NI, Baecher-Steppan L, Smith BB, Youngberg JA, Henderson MC, Guhler DR. Role of the Ah locus in suppression of cytotoxic T lymphocyte activity by halogenated aromatic hydrocarbons (PCBs and TCDDs): structure-activity relationships and effects in C57B1/6 mice congenic at the Ah locus. Fundam Appl Toxicol 14:532-541 (1990).
28. Kerkvliet NI, Baecher-Steppan L, Brauner JA, Deyo JA, Henderson MC, Tomar RS, Buler DR. 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 (1990).
29. Davis D, Safe S. Halogenated aryl hydrocarbon-induced suppression of the in vitro plaque-forming response to sheep red blood cells is not dependent on the Ah receptor. Immunopharmacology 21:183-190 (1991).
30. Morris DL, Snyder NK, Gokani V, Blair RE, Holsapple MP. Enhanced suppression of humoral immunity in DBA/2 mice following subchronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol Appl Pharmacol 112:128-132 (1992).
31. Lorr NA, Golemboski KA, Hemendinger RA, Dietert RR, Bloom SE. Distribution and inducibility of a P450I activity in cellular components of the avian immune system. Arch Toxicol 60:560-566 (1992).
32. Vos J, Van Driel-Grootenhuis L. PCB-induced suppression of the humoral and cell-mediated immunity in guinea pigs. Sci Total Environ 1:289-302 (1972).
33. Faith RE, Moore JA. Impairment of thymus-dependent immune functions by exposure of the developing immune system to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). J Toxicol Environ Health 3:451-464 (1977).
34. Nikolaidis E, Brunstrom B, Dencker L. Effects of TCDD and its congeners 3,3′,4,4′-tetrachloroazoxbenzene and 3,3′,4,4′-tetrachlorobiphenyl on lympoid development in the thymus of avian embryos. Pharmacol Toxicol 63:333-336 (1988).
35. Andersson L, Nikolaidis E, Brunstrom B, Bergman A, Dencker L. Effects of polychlorinated biphenyls with Ah receptor affinity on lymphoid development in the thymus and bursa of Fabricius of chick embryos in ovo and in mouse thymus anlagen in vitro. Toxicol Appl Pharmacol 107:183-188 (1991).
36. Fine JS, Gasiewicz TA, Fiore NC, Silverstone AE. Prothymocyte activity is reduced by perinatal 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure. J Pharmacol Exp Therap 255:128-132 (1990).
37. Greenlee WF, Dold KM, Irons RD, Osborne R. Evidence for direct action of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on thymic epithelium. Toxicol Appl Pharmacol 79:112-120 (1985).
38. Lundberg K, Gronvik K-O, Goldschmidt TJ, Klareskog L, Dencker L. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) alters intrathymic T-cell development in mice. Chem-Biol Interact 179-193 (1990).
39. Holladay SD, Lindstrom P, Blaylock BL, Comment CE, Germolec DR, Heindell JJ, Luster MI. Perinatal thymocyte antigen expression and postnatal immune development altered by gestational exposure to tetrachlorodibenzo-p-dioxin (TCDD). Teratology 44:385-393 (1991).
40. Blaylock BL, Holladay SD, Comment CE, Heindel JJ, Luster MI. Exposure to tetrachlorodibenzo-p-dioxin (TCDD) alters fetal thymocyte maturation. Toxicol Appl Pharmacol 112:207-213 (1992).
41. Neubert R, Jacob-Muller U, Helge H, Stahlmann R, Neubert D. Polyhalogenated dibenzo-p-dioxins and dibenzofurans and the immune system. 2: In vitro effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on lymphocytes of venous blood from man and a non-human primate (Callithrix jacchus). Arch Toxicol 65:213-219 (1991).
42. Hinsdill RD, Couch DL, Speirs RS. Immunosuppression in mice induced by dioxin (TCDD) in feed. J Environ Pathol Toxicol 4:401-425 (1980).
43. Thomas PT, Hinsdill RD. Perinatal PCB exposure and its effects on the immune system of young rabbits. Drug Chem Toxicol 3:173-184 (1980).
44. Clark DA, Gauldie J, Szewczuk MR, Sweeney G. Enhanced suppressor cell activity as a mechanism of immunosuppression by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Proc Soc Exp Biol Med 168:290-299 (1981).
45. Clark DA, Sweeney G, Safe S, Hancock E, Kilburn DG, Gauldie J. Cellular and genetic basis for suppression of cytotoxic T cell generation by haloaromatic hydrocarbons. Immunopharmacology 6:143-153 (1983).
46. Takagi Y, Aburada S, Otake T, Ikegami N. Effect of polychlorinated biphenyls (PCBs) accumulated in the dam's body on mouse filial immunocompetence. Arch Environ Contam Toxcol 16:375-381 (1987).
47. Tomar RS, Kerkvliet NI. Reduced T-helper cell function in mice exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol Let 57:55-64 (1991).
48. Thomas PT, Hinsdill RD. Effect of polychlorinated biphenyls on the immune responses of rhesus monkeys and mice. Toxicol Appl Pharmacol 44:41-55 (1978).
49. Luster MI, Germolec DR, Clark G, Wiegard G, Rosenthal GJ. Selective effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin and corticosterone on in vitro lymphocyte maturation. J Immunol 140:928-935 (1988).
50. House RV, Lauer LD, Murray MJ, Thomas PT, Ehrlich JP, Burleson GR, Dean JH. Examination of immune parameters and host resistance in B6C3F1 mice following adult exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Toxicol Environ Health 31:203-215 (1990).
51. Zile MH. Vitamin A homeostasis endangered by environmental pollutants. Proc Soc Exp Biol Med 201:141-153 (1992).
52. McKinney JD, Faukes J, Jordan S, Chae K, Oatley S, Coleman RE, Briner W. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) as a potent and persistent thryoxine agonist: a mechanistic model for toxicity based on molecular reactivity. Environ Health Perspect 61:41-53 (1985).
53. Brouwer A, Van den Berg KJ. Binding of a metabolite of 3,4,3′,4′-tetrachlorobiphenyl to transthyretin reduces serum vitamin A transport by inhibiting the formation of the protein complex carrying both retinol and thyroxine. Toxicol Appl Pharmacol 85:301-312 (1986).
54. Brouwer A, Van den Berg KJ, Blaner WS, Goodman De WS. Transthyretin (prealbumin) binding of PCBs: a model for the mechanism of interference with vitamin A and thyroid hormone metabolism. Chemosphere 15:1699-1706 (1986).
55. Friedman A, Sklan D. Antigen-specific immune response impairment in the chick as influenced by dietary vitamin A. J Nutr 119:790-795 (1989).
56. Bruns NJ, Webb KE Jr. Vitamin A deficiency: serum cortisol and humoral immunity in lambs. J Anim Sci 68:454-459 (1990).
57. Haddad EE, Mashaly MM. Chicken growth hormone, triiodothyronine, and thyrotropin releasing hormone modulation of the levels of chicken natural cell-mediated cytotoxicity. Dev Comp Immunol 15:65-77 (1991).
58. Spear PH, Bourbonnais DH, Norstrom RJ, Moon TW. Yolk retinoids (vitamin A) in eggs of the herring gull and correlations with polychlorinated dibenzo-p-dioxins and dibenzofurans. Environ Toxicol Chem 9:1053-1061 (1990).
59. Spear PH, Moon TW, Peakall DB. Liver retinoid concentrations in natural populations of herring gulls (Lams argentatus) contaminated by 2,3,7,8-tetrachlorodibenzo-p-dioxin and in ring doves (Streptopelia risoria) injected with a dioxin analogue. Can J Zool 64:204-208 (1985).
60. Friend M, Trainer DO. Polychlorinated biphenyl: interaction with duck hepatitis virus. Science 170:1314-1316 (1970).
61. Vos JG, Kreeftenberg JG, Engel HWB, Minderhoud A, Van Noorle Jansen LM. Studies on 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced immune suppression decreased resistance to infections, endotoxin hypersensitivity, serum zinc concentrations, and effect of thymosin treatment. Toxicology 9:75-86 (1978).
62. Imanishi J, Nomura H, Matsubara M, Kita M, Won S-J, Mizutani T, Kishida T. Effect of polychlorinated biphenyl on viral infections in mice. Infect Immun 29:275-277 (1980).
63. Martineau D, Lagace A, Beland P, Higgins R, Armstrong D, Shugart LR. Pathology of stranded beluga whales (Delphinapterus leucas) from the St. Lawrence Estuary, Quebec, Canada. J Comp Pathol 98:287-311 (1988).
64. Gilmartin WG, DeLong RL, Smith AW, Sweeney JC, De Lappe BW, Risebrough RW, Griner LA, Dailey MD, Peakall DB. Premature parturition in the California sea lion. J Wildl Dis 12:104-115 (1976).
65. Barinaga M. U.S. sea lions join casualties. Nature (London) 336:8 (1988).
66. McGourty C. Seal epidemic still spreading. Nature (London) 334:553 (1988).
67. De Swart RL, Ross PS, Vedder LJ, Timmerman HH, Heisterkamp S, Van Loveren H, Vos JG, Reijnders PJH, Osterhaus ADME. Impairment of immune function in harbor seals (Phoca vitulina) feeding on fish from polluted waters. Ambio 23:155-159 (1994).
68. Ross PS, de Swart RL, Reijnders PJH, Van Loveren H, Vos JG, Osterhaus ADME. Contaminant-related suppression of delayed-type hypersensitivity and antibody responses in harbor seals fed herring from the Baltic Sea. Environ Health Perspect 103:162-167 (1995).
69. Lahvis G, Wells RW, Kuehl DW, Stewart JL, Rhinehart HL, Via CS. Decreased lymphocyte responses in free-ranging bottlenose dolphins (Tursiops truncatus) are associated with increased concentrations or PCBs and DDT in peripheral blood. Environ Health Perspect 103:67-72 (1995).
70. Ludwig JP, Kurita-Matsuba H, Auman HJ, Ludwig ME, Summer CL, Giesy JP, Tillitt DE, Jones PD. Deformities, PCBs, and TCDD-equivalents in double-crested cormorants (Phalacrocorax auritus) and Caspian terns (Sterna caspia) of the upper Great Lakes, 1986-1991: testing a cause-effect hypothesis. J Gt Lakes Res (in press).
71. Dewailly E, Bruneau S, Laliberte C, Belles-Iles M, Weber JP, Ayotte P, Roy R. Breast milk contamination by PCBs and PCDDs/PCDFs in arctic Quebec: preliminary results on the immune status of Inuit infants. Organohalogen Comp 13:403-406 (1993).
72. Fox GA. Practical causal inference for ecoepidemiologists. J Toxicol Environ Health 33:359-373 (1991).
73. Ludwig JP. Present status of the Caspian tern population of the Great Lakes. Michigan Academian 12:69-77 (1979).
74. L'Arrivée L, Blokpoel H. Seasonal distribution and site fidelity in Great Lakes Caspian terns. Colonial Waterbirds 11:202-214 (1988).
75. Grasman KA, Scanlon PF. Effects of acute lead ingestion and diet on antibody and T-cell-mediated immunity in Japanese quail. Arch Environ Contam Toxicol 28:161-167 (1995).
76. Gross WB, Siegel PB. Effects of early environmental stresses on chicken body weight, antibody responses to RBC antigens, feeding efficiency, and response to fasting. Avian Dis 24:569-579 (1980).
77. Gross WB, Siegel PB. Long-term exposure of chickens to three levels of social stress. Avian Dis 25:312-325 (1981).
78. Norstrom RJ, Simon M, Muir DCG, Schweinsburg RE. Organochlorine contaminants in arctic marine food chains: identification, geographical distribution, and temporal trends in polar bears. Environ Sci Technol 22:1063-1071 (1988).
79. Kennedy SW, Lorenzen A, James CA, Collins BT. Ethoxyresorufin-O-deethylase and porphyrin analysis in chicken embryo hepatocyte cultures with a fluorescence multiwell plate reader. Anal Biochem 211:102-112 (1993).
80. Kennedy SW, Lorenzen A, Norstrom RJ. Chicken embryo hepatocyte (CEH) bioassay for measuring cytochrome P4501A-based 2,3,7,8-tetrachlorodibenzo-p-dioxin-equivalent concentrations in environmental samples. Environ Sci Technol 30:706-715 (1996).
81. Norstrom RJ, Simon M, Mulvihill MJ. A gel-permeation/column chromatography cleanup method for the determination of CDDs in animal tissues. Int J Environ Analyt Chem 23:267-287 (1986).
82. Norstrom RJ, Simon M, Muir DCG. Polychlorinated dibenzo-p-dioxins and dibenzofurans in marine mammals in the Canadian north. Environ Pollut 66:1-19 (1990).
83. Kennedy SW, Jones SP. Simultaneous measurement of cytochrome P4501A catalytic activity and total protein concentration with a fluorescence plate reader. Anal Biochem 222:217-223 (1994).
84. Hollander M, Wolfe DA. Nonparametric Statistical Methods. New York:John Wiley and Sons, 1973.
85. Gibbons JR. Nonparametric Statistical Inference. New York:McGraw Hill, 1971.
86. Zar JH. Biostatistical Analysis, 2d ed. Englewood Cliffs, NJ:Prentice Hall, 1984.
87. Edelman AS, Sanchez PL, Robinson ME, Hochwald GM, Throbecke GJ. Primary and secondary wattle swelling response to phytohemagglutinin as a measure of immunocompetence in chicks. Avian Dis 30:105-111 (1986).
88. Schrank CS, Cook ME, Hansen WR. Immune responses of mallard ducks treated with immunosuppressive agents: antibody response to erythrocytes and in vivo response to phytohemagglutinin-P. J Wildl Dis 26:307-315 (1990).
89. Grasman KA. Immunological and hematological biomarkers for contaminants in fish-eating birds of the Great Lakes. PhD Dissertation. Blacksburg, VA:Virginia Polytechnic Institute and State University, 1995.
90. Lochmiller RL, Vestey MR, Boren JC. Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110:503-510 (1993).
91. Stadecker MJ, Lukic M, Dvorak A, Leskowitz S. The cutaneous basophil response to phytohemagglutinin in chickens. J Immunol 118:1564-1568 (1977).
92. Gross WB, HS Siegel. Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis 27:972-979 (1983).