Assessment of the anatomy and physiology of the thyroid gland of the Indo-Pacific bottlenose dolphin, Tursiops aduncus, using ultrasonography

Abstract

This 3-year study was the first to systematically monitor 18 Tursiops aduncus, at Ocean Park, Hong Kong. At the end of the study, the mean age of the population was 16.0 years (range 3 - 37 years). There were 7 males and 11 females in the initial subject group. Of these, 2 animals died during the study period, 14 animals were sexually mature and 4 were immature. Ages were 3 37 years [mean 16 y]. Body weights were 106.1 185.1 kg [mean 132.3 kg]. Body lengths were 196 244 cm [mean 220.1 cm]. For all the subjects, sonographic examination of the thyroid gland was performed once a week. Blood samples were collected monthly whenever possible for thyroid hormone evaluation, using the corresponding enzyme immunoassay kits. A total of 1384 thyroid ultrasound examinations were performed and 241 blood samples for serum thyroid hormone levels were collected and analyzed. The accuracy of four 2-D ultrasound methods in dolphin thyroid volume measurement was also investigated for the first time, with the standard of reference determined by 3-D ultrasound. The inter- and intra-operator variability of the four 2-D ultrasound and the 3-D ultrasound thyroid volume measurement methods were also evaluated. Results show both 2-D and 3-D ultrasound can be used to evaluate dolphin thyroid volume. Methods A and B are considered to be more accurate and reliable methods for 2-D ultrasound dolphin thyroid measurement, regardless of the dolphin thyroid configuration, due to the difficulty in judging the maximal dimension of the craniocaudal dimension of the thyroid lobe in Methods C and D. Sonographic features of the normal dolphin thyroid gland and adjacent neck structures were also documented for the first time. Possible association between thyroid morphology and serum thyroid hormone levels was evaluated for the first time in bottlenose dolphins. Various degrees of association were demonstrated between thyroid hormone levels and thyroid volume amongst sex, age group and sexual maturity. The most prominent association was identified when the analyses were stratified by age, possibly due to the energy requirements of somatic growth transiting to reproductive development with advancing age. Variations in dolphin thyroid morphology for somatic growth, reproductive development and different body sizes, as well as seasonality, were also evaluated for the first time. Results indicate that thyroid volume varies with age, sex, sexual maturity and body size, due to the differences in energy expenditure within these parameters. In terms of sonographic features, a significant difference was found in the echogenicity of the adult and juvenile thyroid gland. This study was the first to evaluate the possible variations of thyroid morphology in female dolphins during different reproductive events and the estrous cycle. Reproductive event was considered to be a significant predictor for thyroid volume measurement, in which a significantly larger thyroid volume in lactating females was presented compared to estrous and anestrous females which may be due to the high energy requirements and milk production during lactation. Cyclic changes of thyroid volume during the estrous cycle were documented, with the minimum thyroid volume during the follicular phase and the maximum thyroid volume during the luteal phase, possibly related to the influence of female sex steroids. The principal findings of this study have shown that sonography is a non-invasive, readily available, comparatively low cost and real-time imaging tool to assess the anatomy and function of the thyroid gland of bottlenose dolphins. In addition, for the first time, a baseline status of the thyroid gland in bottlenose dolphins was established, which provides a means of sonographic diagnosis in live animals with thyroid abnormalities and guides corrective therapy. Techniques developed may be applied to other marine mammals and provide information about thyroid physiology of other species, allowing optimal captive management. Such techniques may also aid conservation of wild animals in the future.