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Effect of In Ovo Exposure to an Organochlorine Mixture Extracted from Double Crested Cormorant Eggs (Phalacrocorax auritus) and PCB 126 on Immune Function of Juvenile Chickens

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Abstract

Organochlorine (OC) contaminants including polychlorinated biphenyls (PCBs) and p, p’-dichlorodiphenyldichloroethylene (DDE) have been associated with immune modulation in wild fish-eating birds from the Great Lakes. The objective of this study was to evaluate the immune function of juvenile chickens after in ovo exposure to PCB 126 or an environmentally relevant OC mixture extracted from eggs of double crested cormorants (Phalacrocorax auritus) from Green Bay, Lake Michigan, USA. Fertile white leghorn chicken (Gallus domesticus) eggs were injected before incubation with 0.55–1.79 ng TCDD equivalents (TEQ)/egg PCB 126 and 1.2–4.9 ng TEQs/egg of cormorant egg extract into the air cell in two separate experiments. After hatching, the immune function was tested using in vivo phytohemagglutinin (PHA) skin response in 11-day-old chicks, antibody titers to immunization with sheep red blood cells (SRBC) in 28-day-old chicks, and, at necropsy, thymus and bursal mass and cellularity. PCB 126 decreased antibody titers at all doses and decreased the thymus and bursa index but not cellularity at 1.79 ng TEQ/egg. The cormorant egg extract caused no significant alterations in immune function even though it has been demonstrated as immunotoxic in chicken embryos. However, twofold to threefold increases in total anti-SRBC titers in 28-day-old chicks exposed to 1.2 or 2.4 ng TEQ/egg of cormorant extract were similar to elevations in anti-SRBC titer observed in Caspian tern (Sterna caspia) chicks from a highly OC-contaminated site in Saginaw Bay, Lake Huron. Posthatch exposure to OC through fish consumption in addition to in ovo OC exposure might be associated with the immune modulation reported in wild birds. Chicks in this study might have begun to compensate for embryonic immunotoxicity by the ages at which we studied them.

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Acknowledgments

The authors thank Jen Rutkiewicz and Kathy Bryant for assistance in blood sampling and necropsy. The authors would also like to thank Diane Nicks (USGS, CERC) and John Meadows (USGS, CERC) for preparation of the doses of the DCCO extract and Tim Kubiak (US Fish and Wildlife Service), T.J. Miller (US Fish and Wildlife Service), and Ken Stromborg (US Fish and Wildlife Service) for their contributions in collection and development of the DCCO extract. Additionally, the authors thank the anonymous peer reviewers for their constructive reviews of the manuscript. Funding was from the Michigan Great Lakes Protection Fund and the Environmental Protection Agency.

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Authors and Affiliations

  1. Department of Animal and Avian Sciences, University of Maryland, Building 142, College Park, MD, 20742, USA

    E. T. Lavoie

  2. Department of Forestry and Natural Resources, Institute of Environmental Toxicology, Clemson University, 261 Lehotsky Hall, Clemson, SC, 29634, USA

    F. Wiley & W. W. Bowerman

  3. Biology Department, Calvin College, 1726 Knollcrest Circle SE, Grand Rapids, MI, 49546, USA

    K. A. Grasman

  4. US Geological Survey, Columbia Environmental Research Center, 4200 New Haven Road, Columbia, MO, 65201, USA

    D. E. Tillitt

  5. Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI, 48824, USA

    J. G. Sikarskie

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  1. E. T. Lavoie
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  2. F. Wiley
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  3. K. A. Grasman
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  4. D. E. Tillitt
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  5. J. G. Sikarskie
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  6. W. W. Bowerman
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Correspondence to E. T. Lavoie.

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Lavoie, E.T., Wiley, F., Grasman, K.A. et al. Effect of In Ovo Exposure to an Organochlorine Mixture Extracted from Double Crested Cormorant Eggs (Phalacrocorax auritus) and PCB 126 on Immune Function of Juvenile Chickens. Arch Environ Contam Toxicol 53, 655–661 (2007). https://doi.org/10.1007/s00244-006-0150-z

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