A Review of Thyroid Hyperplasia in Elasmobranchs: Thyroid Hormones, Environmental Condition, and Pathology--A Progress Report
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
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.
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.