Brevetoxicosis in Manatees (Trichechus manatus latirostris) from the 1996 Epizootic: Gross,Histologic,and Immunohistochemical Features

Abstract

In 1996, at least 149 manatees (Trichechus manatus latirostris) died in an unprecedented epizootic along the southwest coast of Florida. At about the same time, a bloom of the brevetoxin-producing dinoflagellates, Gymnodinium breve, was present in the same area. Grossly, severe nasopharyngeal, pulmonary, hepatic, renal, and cerebral congestion was present in all cases. Nasopharyngeal and pulmonary edema and hemorrhage were also seen. Consistent microscopic lesions consisted of catarrhal rhinitis nulm hemorrhage and edema, multiorgan hemosiderosis, and nonsuppurative leptomeningitis. Immunohistochemical staining using a polyclonal primary antibody to brevetoxin (GAB) showed intense positive staining of lymphocytes and macrophages in the lung liver and secondary lymphoid tissues. Additionally, lymphocytes and macrophages associated with the inflammatory lesions of the nasal mucosa and meninges were also positive for brevetoxin. These findings implicate brevetoxicosis as a component of and the likelv primary etiology for the epizootic. The data suggest that mortality resulting from brevetoxicosis may not necessarily be acute but may occur after chronic inhalation and/or ingestion. Immunohistochemical staining with interleukin-1-β-converting enzyme showed positive staining with a cellular tropism similar to GAB. This suggests that brevetoxicosis may initiate apoptosis and/or the release of inflammatory mediators that culminate in fatal toxic shock.

Keywords

Sirenian red tide biotoxin die-off immunoperoxidase pathology

References

1. Baden DG (1996). Analyses of biotoxins (red tide) in manatee tissues. Report no. MR148. Marine and Freshwater Biomedical Sciences Center, National Institute of Environmental Health Sciences, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami, Florida, pp. 1–12.

2. Baden DG (1983). Marine food-borne dinoflagellate toxins. Int. Rev. Cytol. 82: 99–150.

3. Baden DG , Melinek R , Sechet V , Trainer VL , Schultz DR , Rein KD , Tomas CR , Delgado J , and Hale L (1995). Modified immunoassays for polyether toxins: Implications of biological markers, metabolic states, and epitope recognition. J. AOAC Int. 78(2): 499–508.

4. Baden DG and Mende TJ (1982). Toxicity of two toxins from the Florida red tide marine dinoflagellate, Gymnodinium breve. Toxicon 20: 457–461.

5. Barrett AS and Kirschke H (1981). Cathepsin B, H and L. Methods Enzymol. 80: 535–561.

6. Bond JS and Butler PE (1987). Intracellular proteinases. Annu. Rev. Biochem. 56: 333–364.

7. Florida Manatee Recovery Plan (2nd revision) (1995). U.S. Fish and Wildlife Service, Atlanta, Georgia, pp. 1–33.

8. Geng Y and Libby P (1995). Evidence for apoptosis in advanced human atheroma; Colocalization with interleukin-1-converting enzyme. Am. J. Pathol. 147(2): 251–266.

9. Geraci JR (1989). Clinical investigation of the 1987-1988 mass mortality of bottlenose dolphins along the U.S. central and south Atlantic coast. Final report. U.S. Marine Mammal Commission, Washington, D.C., pp. 1–63.

10.

10. Green GD and Shaw E (1981). Peptidyl diazomethyl ketones are specific inactivators of thiol proteinases. J. Biol. Chem. 256: 1923–1928.

11.

11. Gunter G , Williams RH , Davis CC , and Walton Smith FG (1948). Catastrophic mass mortality of marine animals and coincident phytoplankton bloom on the west coast of Florida, November 1946 to August 1947. Ecol. Monogr. 18: 309–324.

12.

12. Hardie EM and Kruse-Elliott K (1990). Endotoxic shock: Part 1. Review of causes. J. Vet. Intern. Med. 4: 258–266.

13.

13. Hemmert WH (1975). The public health implications of Gymnodinium breve red tides, a review of the literature and recent events. In: Proceedings of the First International Conference on Toxic Dinoflagellate Blooms. The Massachusetts Science and Technology Foundation, Wakefield, Massachusetts, pp. 489-497.

14.

14. Huang JM , Wu CH , and Baden DG (1984). Depolarizing action of a red tide dinoflagellate brevetoxin on axonal membranes. J. Pharmacol. Exp. Ther. 229: 615–621.

15.

15. Janeway C and Travers P (1996). Immunobiology. Stamford Press, Singapore, pp. 7:13, 9:15-9:16.

16.

16. Jones TC and Hunt RD (1983). Veterinary Pathology. Lea and Febiger, Philadelphia, Pennsylvania, pp. 191–192, 1638.

17.

17. Layne JN (1965). Observations on marine mammals in Florida waters. Bull. Fl. State Mus. 9: 131–181.

18.

18. Longworth KE , Smith BL , Staub NC , Steffey EP , and Serikov VB (1996). Use of detergent to prevent initial responses to endotoxin in horses. Am. J. Vet. Res. 57(7): 1063–1066.

19.

19. Morris DD , Moore JN , and Crowe N (1992). Effect of experimentally induced endotoxemia on serum interleukin-6 activity in horses. Am. J. Vet. Res. 53: 753–756.

20.

20. O'Shea TJ , Rathbun GB , Bonde RK , Buergelt CD , and Odell DK (1991). An epizootic of Florida manatees associated with a dinoflagellate bloom. Mar. Mammal Sci. 7(2): 165–179.

21.

21. Quick JA and Henderson GE (1974). Effects of Gymnodinium breve red tide on fishes and birds: A preliminary report on behavior, anatomy, hematology and histopathology. Contribution no. 241. Florida Department of Natural Resources Marine Research Laboratory, St. Petersburg, Florida, pp. 85–113.

22.

22. Steidinger KA and Baden DG (1984). Toxic marine dinoflagellates. In: Dinoflagellates, DL Spector (ed). Academic Press, New York, pp. 201–261.

23.

23. Steidinger KA and Haddad K (1981). Biologic and hydrographic aspects of red tides. Bioscience 31: 814–819.

24.

24. Sudarsanam S , Virca DG , March CJ , and Srinivasan S (1992). An approach to computer-aided inhibitor design: Application to cathepsin L. J. Comput.-Aided Mol. Des. 6: 223–233.

25.

25. U.S. Marine Mammal Commission Annual Report to Congress (1996). U.S. Marine Mammal Commission, Bethesda, Maryland, pp. 6-18.