Abstract

Thyroid hyperplasia (goiter) is a common clinical presentation found in captive elasmobranchs throughout the world. Thyroid hyperplasia is typically observed as a progressive swelling of the thyroid gland, which can expand to as much as 300 times its normal size. This condition, if left untreated, can result in difficulty swallowing, followed by death. The husbandry management of thyroid hyperplasia has been centered on iodide replacement, either as an addition to the water or as an oral supplement.

The thyroid gland in elasmobranchs is an encapsulated organ located in loose connective tissue between the ventral side of the coracohyal and the medial side of the coracomandibular muscles. The tissue of the thyroid gland is comprised of follicles with a highly vascular blood capillary system. Each follicle is formed of epithelial cells surrounding a fluid-filled lumen. The lumen contains a colloidal suspension of an iodide-rich protein called thyroglobulin, which is engulfed by follicle cells under stimulation by the thyroid stimulating hormone (TSH) and converted by hydrolysis into T₄ (thyroxine) before being secreted into the blood stream. Serum T₄ then goes through hepatic deiodination and is converted to T₃ (triiodothyronine), the active thyroid hormone. In mammals, both T₄ and T₃ are secreted by the thyroid gland. The complete thyroidal system is regulated by feedback mechanisms associated with the physiological state of the animal. The function of the thyroid can be loosely monitored by observing thyroid hormone concentrations.

Thyroid hormones concentrations were monitored in the whitetip reef shark (Triaenodon obesus) as an experimental window into thyroid physiology. Sharks with goiters had lower concentrations of serum T₄ and serum T₃, and thus were hypothyroid. No significant male/female differences were detected. Serum T₄ concentrations in the goitered sharks ranged from 0.93 to 0.99 ng/ml. Serum T₄ concentrations in "healthy" captive sharks ranged from 1.34 to 8.77 ng/ml. Serum T₃ concentrations in goitered sharks ranged from 0.22 to 0.33 ng/ml compared to a range of 0.52 to 0.83 ng/ml in "healthy" captive sharks. The "healthy" whitetip reef sharks were maintained at the Waikiki Aquarium.

Water chemistry is the most significant factor causing goiter formation in captive elasmobranchs. Goiters are thought to result from low aquatic iodide concentrations, impaired iodide uptake, or impaired secretion of T₄ from the thyroid gland. Generally, examination of aquarium seawater reveals low iodide and high nitrogen, particularly nitrate. In the facility where goiters were occurring, water iodide concentration was measured at less than 0.006 mg/l (natural seawater = 0.013 mg/l). Interestingly, iodine (iodide + iodate) concentration in this system was 0.06 mg/l and natural seawater is also 0.06 mg/l. At the Waikiki Aquarium, where no goiters occur, iodide concentration was 0.08 mg /l and iodine concentration was 0.24 mg/l. This suggests that the iodide concentration is a possible causal factor in the formation of goiters. However, other water chemistry compounds such as a bacterium, phenols, disulfide, or other potential goitrogens may also effect the thyroid gland and may accumulate in seawater systems. Nitrate concentrations were also quite different between the two facilities. In the goitered water system, the concentration was 1.55 mg/l compared to 0.34 mg/l at the Waikiki Aquarium. Aquarium water chemistry is rarely investigated thoroughly, and little comparative information exists for facilities with chronic goiters.

A review of captive elasmobranch thyroid hyperplasia cases from the Lower Animal Tumor Registry reveals an interesting pathology dichotomy. Three cases of diffuse hyperplastic goiter were found to have mostly small follicles with little to no colloid. Two cases of diffuse colloid goiter had an enlargement of follicles, which were filled with colloid, and three cases of multinodular colloid goiters were also found. Multinodular goiter is characterized by the following: nodularity created by islands of colloid-filled or hyperplastic follicles; random irregular scarring; non-uniform colloid accumulation, and focal hemorrhages and hemosiderin deposition. Colloid goiters that are left untreated are typically transformed over time into multinodular colloid goiters. Diffuse hyperplastic goiters and diffuse colloid goiters may have different origins, making detailed studies necessary.

The absence of water chemistry samples in the majority of pathology cases makes diagnosis of thyroid hyperplasia extremely difficult. It appears that the majority of goiters examined are not simply due to an iodine deficiency and subsequent TSH hypersecretion. A similar conclusion has been suggested for cases of human goiters in which thyroid hyperplasia occurs despite an adequate supply of iodine in the diet. The thyroid gland is greatly influenced by stress during capture from the wild, stocking density, species composition, food intake and type, water temperature, water chemistry, goitrogenic agent(s), age, and reproductive state. Additional water-chemistry and goiter studies are needed to delineate the etiology of thyroid hyperplasia.

Acknowledgements

The authors would like to thank M. Atkinson, S. Atkinson, B. Ron, A. Skillman, G. Wong, and B. Rasmussen for their work on the first two phases of this project. We would also like to thank the University of Hawaii Sea Grant College Program for partial funding under institutional grant no. NA36RG0507, and the Hawaii Institute of Marine Biology (Director G. Grau) for providing laboratory space and equipment to run the thyroid hormone assays. The Registry of Tumors in Lower Vertebrates is supported by NCI Contract N01CB-77021 to George Washington University. We thank Karen Clinton for slide preparation and Ruth LeBlanc for record transcription.