Abstract
The thyroid gland is a highly vascularized organ in vertebrates. However, the information on the vascular pattern of this gland in pigs remains limited. This study elucidates the morphoanatomy and arterial supply of the gland in three breeds: Landrace (L), Large White (W), and Crossbreed (LWD). Two hundred twelve pigs were used and dissected to observe the arteries supplying blood to the gland. As a result, the gland was classified into three types based on its appearance: pear-shaped, butterfly-shaped, or partially separated. Moreover, the arteries supplying the gland were observed and then compared among breeds. The arterial supply of the thyroid gland on the cranial side consisted of branches from the cranial laryngeal artery, cranial thyroid artery, superficial cervical artery, and common carotid artery. Otherwise, the caudal side was supplied by the caudal thyroid artery, superficial cervical artery, bicarotid trunk, internal thoracic artery, and external thoracic artery. Furthermore, significant differences were identified between L and LWD, as well as between W and LWD, in the pattern of arterial origin on the cranial right side of the thyroid gland. Similarly, on the left side, significant differences were observed not only between L and W but also between W and LWD. On the caudal side, significant differences were found between L and W, as well as between W and LWD. These anatomical variations provide important insights for research and clinical applications involving the thyroid gland in pigs.
Keywords: artery, breed, pig, thyroid gland, variation
INTRODUCTION
The thyroid gland is a brownish-red, spindle-shaped, richly vascularized organ located in the lower neck, extending from the ventral to the lateral aspect of the tracheal ring [5, 9, 29]. This gland is found in all vertebrates, typically bilobed and situated on the ventrolateral surface of the trachea, connected by an isthmus [49]. Moreover, the thyroid gland is positioned near the cervical lymph nodes and major blood vessels, which are covered by the sternothyroid and sternocleidomastoid muscles [5, 9, 38]. In pigs, the thyroid gland is a thick, compact glandular tissue located ventral to the trachea, connected by bands of connective tissue that contain blood vessels [21, 42, 52]. The thyroid gland in a pig is identified as violaceous, with a pear-shaped to butterfly-like appearance, and, conversely, arises as a single unit macroscopically [5, 16]. Furthermore, this organ is responsible for metabolism-related functions, producing thyroid hormones that are controlled by thyroid-stimulating hormone (TSH) from the anterior pituitary gland [6, 45]. The thyroid gland secretes triiodothyronine (T3), thyroxine (T4), and calcitonin, which are crucial for organismal development and homeostasis [23]. The hormones T3 and T4 are essential for maintaining normal metabolic activity levels. Calcitonin decreases bone resorption by lowering blood calcium levels [36, 37]. To regulate hormone production within the body, the thyroid gland secretes hormones directly into the bloodstream via blood vessels, as it lacks ducts [36].
The thyroid gland is a vascularized organ with an extensive arterial supply and variable arterial anatomy [11]. In general (human), the thyroid gland is supplied by two paired arteries, the right and left superior thyroid artery, which arise from the external carotid artery (ECA), and the right and left inferior thyroid artery, which commonly arise from the thyrocervical trunk (TT) of the subclavian artery [13, 14, 16, 50]. The middle thyroid artery, also known as the thyroidea ima artery, arises from the anterior surface of the common carotid artery (CCA), a feature rarely observed in humans but present in budgerigars, guinea pigs, and rabbits [30, 39, 51]. The thyroid gland is highly vascularized and closely associated with variations in vascular anatomy, including the presence of aberrant vessels and atypical vascular patterns [22]. Variations of the thyroid artery primarily involve the origins of the superior and inferior thyroid arteries, as well as the absence or replacement of their branches [51]. Some angiographic literature reports that different anatomical patterns of origin of the thyroid artery can be observed [4, 40]. In some cases, the thyroid ima artery can replace the inferior thyroid artery [13]. Particularly, the right inferior thyroid artery is replaced by an artery branching off the right internal thoracic artery (ITA). On the other hand, the left inferior thyroid artery was replaced by an artery branching off the vertebral artery between the transverse processes of the second and third cervical vertebrae [50]. In pigs, the aortic arch branches into the left subclavian artery and the brachiocephalic artery. The brachiocephalic artery then bifurcates into the right subclavian artery and the bicarotid trunk, which subsequently divides into the right and left CCA (RCCA-LCCA) [17]. In animals, the terms used to describe the arterial supply of the thyroid gland differ somewhat from those used in humans [12]. The superior and inferior thyroid arteries are referred to as the cranial and caudal thyroid arteries (CrTA and CdTA), respectively [39, 44]. In pigs, the CdTA is known to appear from the left and right sides of the caudal portion of the thyroid gland [52]. Along with other anatomical similarities between pigs and humans, this characteristic contributes to the established use of pigs as animal models in both veterinary and human medical research [17, 18, 31].
An accurate understanding of the thyroid gland’s anatomical topography and landmarks is crucial for veterinarians, medical clinicians, and surgeons, as it facilitates access to invasive medical procedures and surgical interventions [21, 42]. The pig model has been demonstrated to be cost-effective for head and neck surgical training and more accurate in simulating human cervical and laryngeal tissues [1, 2]. Understanding the normal anatomy structure and variation in vascularization is important for clarifying misidentifications during surgery [2, 10, 49]. Surgical procedures such as thyroidectomy, neck dissection, and laryngectomy require specialized skills and techniques [26]. Injuries to the recurrent and superior laryngeal nerves, the parathyroid glands, and uncontrolled bleeding from the vascular supply may pose a significant risk [1, 20, 26, 29]. Identification of uncommon variations in the thyroid arteries helps minimize potential complications. Variation in the arterial branches of the thyroid gland exists not only in humans but also in animals [30]. Anatomical and physiological aspects related to thyroid vascularization in pigs remain poorly understood [2, 49]. Investigating the origin variation of thyroid arteries is important based on gross anatomical findings [14]. Hence, this study provides a comprehensive understanding of the anatomy of the thyroid gland in pigs, including its arterial variations, in relation to broader comparative anatomical knowledge across species and to surgical procedures relevant to both veterinary and biomedical sciences.
MATERIALS AND METHODS
Samples and data collections
Systemic heparinization of the dead bodies of 212 pigs (4–25 weeks of age) was used in this study, obtained from a commercial company and a university farm (Miyazaki, Japan). Animals consisted of three breeds: 75 Landrace (L) (females only), 76 Large White (W) (females only), and 61 Crossbreeds (LWD, LW hybrid crossed with Duroc) (29 males, 24 females, and eight unknown). Samples were injected through the thoracic aorta or bicarotid trunk and or left subclavian artery in a cranial direction with a green-colored latex (Showa Denko Chloroprene type 842A, Showa Denko Co., Ltd., Tokyo, Japan). The specimens were kept at room temperature for a day to harden the latex and then macroscopically dissected to observe the arteries supplying blood to the thyroid gland. The research was conducted in the Anatomy Laboratory, Department of Veterinary Sciences, University of Miyazaki, Japan. The Institutional Animal Care and Use Committee of the University of Miyazaki approved this research (No. 2023-033).
Gross anatomical identification
The gross anatomical evaluation consisted of identifying the morphology of the thyroid gland and its vascular structures. An investigation of the arteries supplying the thyroid was conducted and confirmed by journals and anatomy books. The anatomical features were identified based on the Veterinary Anatomical Nomenclature, Sixth Edition [44]. The morphological classification of the thyroid gland, based on that of goats by Pankowski et al. [34], with modifications.
Photograph and schematic drawing
Photographs were captured with a Nikon D300 digital camera, without any specific brightness or contrast adjustments (in automatic mode). Furthermore, schematic drawings were visualized using an iPad Pro (11-inch) 3rd generation with Procreate version 5.3.7 Build 439f120050 (Savage Interactive Pty Ltd., Hobart, Tasmania, Australia).
Statistical analyses
The obtained data were analyzed using Fisher’s exact test and the Holm correction was applied to adjust for multiple comparisons. The statistical software EasyR (EZR) version 1.64 was used for the statistical analysis. A P-value <0.05 was considered statistically significant. Detailed data and analysis are shown in the supplementary data.
RESULTS
Anatomical and topographical view of the thyroid gland
The thyroid gland of the pig was positioned in the ventral midline of the trachea, approximately located in the 6th to 13th tracheal ring. The size of these glands was about 2–5 cm in length and 1.5–3 cm in width. The thyroid gland in the pig appeared as a single unit with an indistinct isthmus. The lobes, right and left, were closed together and merged with the isthmus, and have thin tissue as the cover of the gland. Based on gross anatomical investigation, the thyroid gland was classified into three morphological types: pear-shaped, butterfly-like, and partially separated (Fig. 1). The pear-shaped type was described as a single unit gland with indiscernible lobes, whereas the butterfly-like type was depicted as wider lobe sides with the pointed tip craniolaterally. On the other hand, the partially separated type showed almost complete separation between the right and left lobes.
Fig. 1.
Gross anatomy of the morphological differentiation of the thyroid gland in pigs. (a) Topographic view of the thyroid gland with different shapes (b). Schematic drawing of the thyroid classified as (i) pear, (ii) butterfly-like, and (iii) partially separated. Scale bar=1 cm.
Gross anatomical classification of the thyroid gland in pigs showed that the butterfly-like shaped thyroid gland was the most common compared to the pear-shaped and partially separated (Table 1). This type of thyroid was dominant, accounting for 50% of the total 168 samples (L:57, W:66, and LWD:45 cases), whereas the other types account for 38.7% and 11.3%, respectively. In detail, between breeds, pear-shaped was the most common in LWD at 48.9%, followed by L (35.1%) and W (34.8%). A total of 65.2% the butterfly-like shape was found in W, whereas 45.6% in L and 33.3% in LWD. Lastly, the partially separated type was observed at 19.3% in L and 17.8% in LWD, but no cases were observed in W.
Table 1. Gross anatomy classification of the thyroid gland in the pigs.
| Thyroid types | Breeds | Total (168) | ||||||
|---|---|---|---|---|---|---|---|---|
| L (57) | W (66) | LWD (45) | ||||||
| Case | (%) | Case | (%) | Case | (%) | Case | (%) | |
| Pear-shaped (i) | 20 | 35.1 | 23 | 34.8 | 22 | 48.9 | 65 | 38.7 |
| Butterfly-like (ii) | 26 | 45.6 | 43 | 65.2 | 15 | 33.3 | 84 | 50.0 |
| Partially separated (iii) | 11 | 19.3 | 0 | 0.0 | 8 | 17.8 | 19 | 11.3 |
L=landrace, W=large white, LWD=crossbreed.
A topographical view of the thyroid gland’s vascularization in pigs showed that several arteries surround the gland (Fig. 2). From the heart, the blood circulated through the systemic loop cranially via the aorta, then passed through the brachiocephalic trunk to the bicarotid trunk (BT) after branching with the right subclavian artery (RSCA). On the other hand, the left subclavian artery (LSCA) branched separately from the aorta. The BT then arose into the common carotid artery (CCA) alongside the thyroid gland. Moreover, the subclavian artery (SCA) branched into the internal thoracic arteries (ITA) and the superficial cervical arteries (SpCA-LSpC). These arterial branches were observed on both the right and left sides, with corresponding left–right directional designations used throughout the description.
Fig. 2.
Gross anatomy of the thyroid arterial vascularization in the pig. (a) Topographic view of the thyroid vascularization. (b) Illustrative drawing depicting the vascular supply surrounding the thyroid region. T: thyroid gland, TC: thyroid cartilage, TR: trachea, BT: bicarotid trunk, BCT: brachiocephalic trunk, RCCA: right common carotid artery, LCCA: Left common carotid artery, RSpCA: right superficial cervical artery, LSpCA: left superficial cervical artery, RITA: right internal thoracic artery, LITA: left internal thoracic artery, RSCA: right subclavian artery, and LSCA: left subclavian artery. Scale bar=1 cm.
Arterial vascularization of the thyroid gland
The frequencies and percentages of the artery supplying the thyroid gland in different pig breeds are presented in Table 2. On that table, classification is based on the number of arteries supplying that organ from the cranial and caudal sides, whether the left or right side, unilaterally or bilaterally. In some cases, the arterial supply to the thyroid gland was unilateral, from only the right or left side for cranial and caudal vascularization. Overall, the thyroid gland supplied by two arteries was the most common pattern, observed in 44.8% of cases, followed by those supplied by one artery (30.7%) and three arteries (19.8%). Furthermore, thyroid glands supplied by more than three arteries were rare, occurring in only 4.7% of 212 samples. Across three breeds, the results were also similar, with at least two arteries supplying the thyroid gland in most cases. Furthermore, after examining all the samples, the arterial vascularization of the thyroid gland was classified by origin (cranial or caudal). The cranial side was related to the artery that supplies the thyroid gland from the cranial side, both right and left; vice versa for the caudal side (Figs. 3, 4, 5). Furthermore, the frequencies of the supplying arteries differ by body side (right, median, and left) and are presented in Table 3. Based on our findings, the thyroid gland was supplied by nine arteries originating from the cranial and caudal sides. The cranial side was supplied by four arterial branches: the cranial laryngeal artery (CLA), cranial thyroid artery (CrTA), common carotid artery (CCA), and superficial cervical artery (SpCA). In contrast, the caudal side was supplied by five arterial branches: the superficial cervical artery (SpCA), the caudal thyroid artery (CdTA), the bicarotid trunk (BT), the external thoracic artery (ETA), and the internal thoracic artery (ITA).
Table 2. Frequencies and percentages of arteries supplying the thyroid gland in different pig breeds.
| Number of arteries | Breeds | Total (212) | ||||||
|---|---|---|---|---|---|---|---|---|
| L (n=75) | W (n=76) | LWD (n=61) | ||||||
| Case | (%) | Case | (%) | Case | (%) | Case | (%) | |
| 1 | 30 | 40.0 | 19 | 25 | 16 | 26.2 | 65 | 30.7 |
| 2 | 31 | 41.3 | 32 | 42.1 | 32 | 52.5 | 95 | 44.8 |
| 3 | 13 | 17.3 | 18 | 23.7 | 11 | 18.0 | 42 | 19.8 |
| 4 | 1 | 1.3 | 6 | 7.9 | 1 | 1.6 | 8 | 3.8 |
| 5 | 0 | 0.0 | 1 | 1.3 | 1 | 1.6 | 2 | 0.9 |
L=landrace, W=large white, LWD=crossbreed.
Fig. 3.
Topographic lateroventral right view of arterial cranial branches supplying the thyroid gland in pigs. (a). Thyroid with arterial supply from RCLA (shown as 1), (b). Thyroid with arterial supply from RCrTA (shown as 2), (c). The thyroid gland receives arterial supply from the RCCA (shown as 3) and (d). Thyroid with arterial supply from RSpCA (shown as 4). T: thyroid gland, TC: thyroid cartilage, TR: trachea, RCLA: right cranial laryngeal artery, RCrTA: right cranial thyroid artery, RCCA: right common carotid artery, and RSpCA: right superficial cervical artery. Scale bar=1 cm.
Fig. 4.
Topographic ventral view of some arterial caudal branches supplying the thyroid gland in pigs. (a). Thyroid with arterial supply from RSpCA (shown as 1), (b). Thyroid with arterial supply branch from RCdTA (shown as 2), (c). Thyroid with arterial supply from the BT (shown as 3), (d) Thyroid with arterial supply branching from RITA (shown as 4), and (e) Thyroid with arterial supply branching from LETA (shown as 5). TC: thyroid cartilages, TR: trachea, T: thyroid gland, BT: bicarotid trunk, RCCA: right common carotid artery, LCCA: left common carotid artery, RSpCA: right superficial cervical artery, RCdTA: right caudal thyroid artery, RITA: right internal thoracic artery, LETA: left external thoracic artery, RSCA: right subclavian artery, and LSCA: left subclavian artery. Scale bar=1 cm.
Fig. 5.
The schematic drawing of the thyroid arterial branches for thyroid blood supply in pigs. (a) cranial side vascularization (1–4) and (b) caudal side vascularization (5–9). The thyroid artery supply distribution origin from (1) the right-left cranial laryngeal artery (RCLA-LCLA) (2), the right-left cranial thyroid artery (RCrTA-LCrTA), (3) the right-left common carotid artery (CCA), (4) and (6) the right-left superficial cervical artery (RSpCA-LSpCA), (5) the right-left caudal thyroid artery (RCdTA-LCdTA), (7) the bicarotid trunk (BT), (8) the right internal thoracic artery (RITA), and (9) the left external thoracic artery (LETA).
Table 3. Number of cases and percentage frequencies of the arteries supplying the thyroid gland in three pig breeds by their body side.
| Arteries supplying the thyroid gland* | Breeds, number, and percentage | Total (n=212) | |||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| L (n=75) | W (n=76) | LWD (n=61) | |||||||||||
| Right | Median | Left | Right | Median | Left | Right | Median | Left | Right | Median | Left | ||
| Arteries supplying to the cranial side | 29 (38.7%) | 21 (28.0%) | 38 (50.0%) | 38 (50.0%) | 30 (49.2%) | 24 (39.3%) | 97 (45.8%) | 83 (39.2%) | |||||
| Branch of the cranial laryngeal artery (CLA) | 3 | 1 | 4 | 2 | 0 | 0 | 7 | 3 | |||||
| Cranial thyroid artery (CrTA) | 3 | 4 | 5 | 17 | 0 | 5 | 8 | 26 | |||||
| Arteries arising from the common carotid artery (CCA) | 0 | 6 | 7 | 13 | 2 | 4 | 9 | 23 | |||||
| Superficial cervical artery (SpCA) | 23 | 11 | 23 | 9 | 29 | 16 | 75 | 36 | |||||
| Absent | 46 (61.3%) | 54 (72.0%) | 38 (50.0%) | 38 (50.0%) | 31 (50.8%) | 37 (60.7%) | 115 (54.2%) | 129 (60.8%) | |||||
| Arteries supplying to the caudal side | 62 (82.7%) | 20 (26.7%) | 61 (80.3%) | 21 (27.6%) | 52 (85.2%) | 13 (21.3%) | 175 (82.5%) | 54 (25.5%) | |||||
| Caudal thyroid artery (CdTA) | 6 (8%) | 5 (6.7%) | 29 (38.2%) | 15 (19.7%) | 11 (18%) | 6 (9.8%) | 46 (21.7%) | 26 (12.3%) | |||||
| Superficial cervical artery (SpCA) | 56 | 14 | 30 | 6 | 39 | 7 | 125 | 27 | |||||
| Bicarotid trunk (BT) | 2 (2.7%) | 4 (5.3%) | 1 (1.6%) | 7 (3.3%) | |||||||||
| Internal thoracic artery (ITA) | 0 | 0 | 2 | 0 | 2 | 0 | 4 (1.9%) | 0 | |||||
| External thoracic artery (ETA) | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 1 (0.4%) | |||||
| Absent | 13 (17.3%) | 55 (73.3%) | 15 (19.7%) | 55 (72.4%) | 9 (14.8%) | 48 (78.7%) | 37 (17.5%) | 158 (74.5%) | |||||
L=landrace, W=large white, LWD=crossbreed. *Some pigs may have two different branches on the right and/or left sides.
Arterial supply of the thyroid gland from the cranial side
The topographic lateroventral right view of arterial cranial branches supplying the thyroid gland in pigs is presented in Fig. 3. Four arterial branches investigated supplying the thyroid gland: the cranial laryngeal artery (CLA), cranial thyroid artery (CrTA), common carotid artery (CCA), and superficial cervical artery (SpCA). The right CLA (RCLA) was depicted through the thyroid gland cranial side after branching from the RCCA (Fig. 3a). Similarly, the right CrTA (RCrTA) was found branch at the peripheral one-third of the CCA length from the cranial alongside the RCLA (Fig. 3b). Not only that, some individuals had an artery arising medially from the CCA length to the thyroid gland (Fig. 3c). Furthermore, a small arterial branch was found arising craniomedially from the right superficial cervical artery and supplying the muscle near the thyroid cartilage (TC) (Fig. 3d). All of these various branches contributed to the arterial vascularization in the cranial part of the pig’s thyroid gland. In the butterfly-shaped thyroid type, the arteries supplied the cranial portion of each thyroid gland’s lobes. In the other thyroid types, the arteries supplied the dorsal part of the gland from the medial side, and in some cases, only portions of the left and right sides.
Arterial supply of the thyroid gland from the caudal side
The topographic ventral view of some arterial caudal branches supplying the thyroid gland in pigs is depicted in Fig. 4. After examining the samples, the arteries supplying the caudal thyroid gland were the SpCA, the caudal thyroid artery (CdTA), the BT, and the external and internal thoracic arteries (ETA and ITA, respectively). In detail, the artery was found to branch from the right SpCA (RSpCA) and supplied the thyroid gland (Fig. 4a). In this study, an arterial vessel directly arose from the CCA and supplied the gland caudally and defined as the CdTA branch at the cardiac one-third of the CCA length (Fig. 4b). This artery arose mostly from the right or left side, and only two samples have both. In addition, a branch from the middle part of the BT also supplied blood to the thyroid gland (Fig. 4c). In a complex way, the artery arose from the thoracic branches, namely the right ITA (RITA) and left ETA (LETA) (Fig. 4d and 4e). Since the caudal form of the thyroid gland was mostly the same for all thyroid types, the arteries were supplied from the caudal into the dorsal part. Furthermore, a schematic illustration of the thyroid arterial vascularization supplying the thyroid gland is presented in Fig. 5 (Fig. 5a and 5b).
Frequencies of the supplying arteries differ by body side
Based on Table 3, the arteries supplying the cranial side of the thyroid gland showed almost identical percentages on the right and left sides, with only about 6.6% difference in the total samples. Similarly, the arteries absent on the left side were slightly higher than those on the right. The SpCA was the most common source of blood supply to the thyroid gland across all samples, with a slightly higher percentage on the right than on the left. Moreover, none of the arteries supplied the thyroid gland from the medial side in the cranial part for all breeds. In the details between breeds, L and LWD showed a higher case of arteries supplied by the right side than by the left, whereas W showed the same number on both sides.
On the caudal side, the right-sided arteries were the most common, with 82.5% of all breeds, whereas the left-sided arteries were only 25.5%, both compared to the absence of arteries. Mostly, the thyroid gland was supplied by the RSpCA rather than by the other arteries supplying the caudal side. The CdTA was mostly found on the right side, accounting for 21.7% of all samples. In detail, for CdTA, L showed almost identical values on both sides, whereas W and LWD were around twofold higher on the right side than on the left. On the median side, BT was observed in only 3.3% of cases across all breeds (L: 2.7%; W: 5.3%; LWD: 1.6%; specific to each breed). However, the less common arterial branches were from the thoracic artery, with only 1.9% of ITA and 0.4% of ETA cases in all samples.
Statistical analyzes between breed differences
The statistical analysis of thyroid arterial vascularization among pig breeds is presented in Table 4. Breed differences were observed not only between the L and LWD breeds but also between the W and LWD breeds for the arteries originating from the right side and distributed to the cranial side of the thyroid gland. On the left side, breed differences in cranial thyroid vascularization were observed between the L and W breeds and between the W and LWD breeds. Similarly, the caudal thyroid vascularization on the right side showed differences between the L and W breeds, as well as the W and LWD breeds. However, no breed differences were observed in the arteries that originate from the left as caudal thyroid vascularization.
Table 4. Statistical analysis of thyroid arterial vascularization among pig breeds.
| Part of thyroid arterial vascularization | Breeds comparison | P-value | |
|---|---|---|---|
| Cranial | Right side | L vs. W | 0.064 |
| L vs. LWD | 0.047 | ||
| W vs. LWD | 0.047 | ||
| Left side | L vs. W | 0.014 | |
| L vs. LWD | 0.351 | ||
| W vs. LWD | 0.015 | ||
| Caudal | Right side | L vs. W | 0.000012 |
| L vs. LWD | 0.118 | ||
| W vs. LWD | 0.038 | ||
| Left side | L vs. W | 0.058 | |
| L vs. LWD | 0.503 | ||
| W vs. LWD | 0.487 | ||
L=landrace, W=large white, LWD=crossbreed.
DISCUSSION
Anatomical and topographical view of the thyroid gland
Our investigation revealed that the thyroid glands in pigs appeared as a single, compact mass in the ventromedial region of the trachea, as also reported by Arrangoiz et al. [5] and Aspinal and Capello [6]. The thyroid lobes, dexter and sinister, are closely apposed and encapsulated by a thin fibrous layer [14, 26]. In contrast, in other animals, such as the cat, dog [42], the Rhesus monkey [43], the rabbit [8], the lizard, and mice, and even in humans, the gland is positioned ventrolaterally and consists of two lobes connected via a discernible isthmus [21, 28]. By comparison, the thyroid gland lobes in amphibians and birds are distinctly separated [28]. In cattle, the gland appears spindle-shaped [9], whereas it is roughly triangular in buffalo and oval in goats [37]. Additionally, the thyroid gland of the pig lies on the sixth to thirteenth tracheal rings, similarly to that in dogs [8] and the Rhesus monkey [43], where it begins at the sixth tracheal ring. In contrast to the ruminants (buffalo, sheep, and goats), the glands are located at the first to the sixth-seventh of their tracheal rings [37].
Furthermore, this study classified the thyroid gland in pigs into three morphological variation types: pear-shaped, butterfly-like, and partially separated (as shown in Fig. 1). This classification was based on the findings of Pankowski et al. [34], who described the thyroid lobe in goats as having three distinct shapes. As the most common thyroid type in pigs (as shown in Table 1), the butterfly-like type had a pointed craniolateral tip, short to lateral to the trachea, but sometimes longer. Not only that, but the medial tip of this type of thyroid gland may also be related to the presence of the pyramidal lobe. In humans, the pyramidal lobe is an extension superiorly of the thyroid gland (isthmus) and lies in the median plane of the thyroglossal duct [25]. This “third lobe” has several classification types and variations that are important to consider, especially thyroidectomy surgeries [32]. Moreover, the presence of the isthmus in pig thyroid glands remains unclear macroscopically. Our findings showed that, although the thyroid gland forms a single mass, it can still be separated into two distinct parts that appear bilobed. Similar findings of a bilobed mass after thyroid dissection with an indistinct isthmus, which may require histological confirmation [35]. Other animals, such as buffalo, sheep, and goats, have an isthmus because their thyroids are laterally bilobed [37]. Additionally, the differential thyroid gland form in humans and some mammals may occur during the embryonic period as the first organ to develop in the body, appearing as an outpouching of the primitive foregut in the early weeks [5]. Unfortunately, no research has been conducted on the impact of forms on thyroid gland function, particularly regarding growth, disease, fertility, and production efficiency [34]. The thyroid gland’s morphological variation may be linked to vascularization, an essential factor in organ morphogenesis and structural development [48].
Arterial vascularization of the thyroid gland
As presented in Table 2, the thyroid gland in pigs was supplied by 95.3% by one to three arteries, whereas only 4.7% were supplied by four to five arteries. In contrast, the thyroid gland was supplied by four to five arteries in 95.4% of cases in humans [57]. In this study, we classified the arteries based on reports on the second fetal period of pigs in comparative studies of the thyroid gland [52] and thymic arteries in several mammals, such as rats [53], guinea pigs [54], rabbits [55], and the house musk shrew [56]. However, the terms used to describe the arterial supply in humans differ somewhat from those in animals, reflecting their anatomical positioning. The superior and inferior thyroid arteries, as the main supply for the thyroid in humans, are associated with the cranial and caudal thyroid arteries in animals. In humans, those arteries originate from the external carotid arteries and the thyrocervical trunk (TT) (a branch of the subclavian artery) [30]. In the rhesus monkey, the arterial supply to the thyroid gland primarily originates from the external carotid artery [43]. Additionally, these arteries supply not only the thyroid gland but also the neck region and course alongside the nearby nerves [12]. Understanding the surrounding structures of the thyroid gland is important, as it is closely associated with vital structures in the neck.
The classification of the thyroid gland arterial vascularization in pigs based on the supply route, from the cranial or caudal parts of the gland. The arterial branches supplying the cranial side originated from the cranial laryngeal artery (CLA), cranial thyroid artery (CrTA), common carotid artery (CCA), and superficial cervical artery (SpCA). During pig fetal development, the arteries supplying the thyroid gland originate from the CCA and TT [52]. Among these, the artery branching from the CCA is referred to as the middle thyroid artery and has been reported in humans and rabbits [7, 51, 55]. In comparison, during fetal development in piglets, the cranial blood supply to the thyroid gland was observed on the right in 61.2% of cases, arising from the right TT (RTT) and from the right CCA (RCCA) [52]. On the left side, 83.7% cases observed in fetuses arose from the left CCA (LCCA), the left TT (LTT), and the RTT [52]. However, in this study, the corresponding arteries were observed in about 45.8% of cases on the right and 39.2% on the left (as shown in Table 3). On the other hand, the arteries supplying the caudal area of the thyroid gland originated from the SpCA, the caudal thyroid artery (CdTA), the bicarotid trunk (BT), and the external and internal thoracic arteries (ETA and ITA). Our findings revealed that some samples showed a lower frequency of CdTA on the left than on the right (LCdTA: 12.3%; RCdTA: 21.7%). However, only 2.8% of 72 CdTA cases were observed on both sides. Furthermore, Wustiger and Pospieszny [52] reported that arteries arising from the caudal side were observed in 86.9% of cases on the right and about 70.8% on the left. In the present study, arteries supplying the caudal side from the right side were observed in 82.5% of cases, which is consistent with previous findings [52], whereas those from the left side were observed in only 25.5% of cases. During embryonic development, the number and branching pattern of arteries supplying the thyroid gland are abundant, but these vessels may become vestigial in adulthood. This may explain the lower frequency of arterial observation in this study, suggesting a derived arterial supply to the thyroid gland. The difference between our findings may relate to the age of the pigs observed (about 4–25 weeks old) compared with those in the early developmental stage. Additionally, a high frequency of arteries supplying the caudal side of the thyroid gland originating from the right side was observed across pig breeds. The caudal thyroid artery may be absent in pigs, as it is absent in most cats [15].
Beneficial’s understanding of the thyroid gland vascularization in pigs
Pigs are widely acknowledged as a valuable animal model for research due to their anatomical and physiological similarities to humans and their cost-effectiveness in biomedical research [17,18,19, 41]. Both conventional and miniature pigs are frequently used in studies involving vascular and endocrine systems, providing one of the closest approximations to human anatomy for vascular surgical research [17, 19]. Understanding the arterial vascularization of the thyroid gland is beneficial for clinicians, researchers, and surgeons, particularly in procedures involving the cervical region. Detailed knowledge of thyroid vascular anatomy can improve surgical planning and reduce complications during thyroidectomy, tracheostomy, neck dissection, and laryngectomy [1, 2]. The thyroid anatomical landmark is pivotal for determining the surgical dissection and minimizing nerve and artery injuries. Major injury to the blood vessel may cause bleeding complications with a higher risk of death [20]. In particular, the recurrent laryngeal nerve injury can cause swallowing and breathing difficulties [33].
Because the thyroid gland is highly vascularized, understanding the topography, branching patterns, and possible vascular variations is essential in anatomical, radiological, and surgical studies [22, 47]. Variations in thyroid arteries, including differences in branching patterns or the absence of specific vessels, may increase the risk of unexpected bleeding during surgery and dissection [24]. In addition, vascular variations are often associated with differences in nerve innervation, further increasing the risk of injury [3, 27]. Therefore, anatomical investigations of thyroid vascularization contribute not only to surgical safety but also to a broader understanding of developmental and morphological variation.
Statistical analyses of breed differences
Statistical analysis in the present study demonstrated breed-related differences in the arterial supply of the thyroid gland. Significant differences were observed in the arteries supplying the cranial region of the thyroid gland on both the left and right sides among L, W, and LWD breeds. In contrast, differences in the caudal region were identified only on the right side between the L and W breeds. Among the evaluated breeds, W pigs are among the most widely used as an animal model for human medical research [2]. These breed-specific vascular differences highlight the importance of considering anatomical variability when using pigs as experimental models in surgical and translational studies [46].
This study provides additional insight into the vascular anatomy of the porcine thyroid gland and highlights anatomical variations that should be considered in both experimental and clinical applications. Although angiography is more commonly used to investigate vascular anomalies than gross anatomical dissection, previous angiographic studies have also demonstrated thyroid vascular variations [7, 12]. Awareness of these arterial variations is essential for clinicians and researchers to minimize unexpected complications during diagnostic, interventional, and surgical procedures.
Furthermore, the findings underscore the need for additional investigations into the embryological and developmental basis of thyroid vascularization, as well as vascular variation in other organs. Variability in thyroid morphology, including differences in gland shape, may also have functional implications that remain insufficiently understood and warrant further study. Overall, this study contributes to the broader understanding of comparative anatomy and physiology across species and supports the continued use of pigs as valuable models for advancing both veterinary and human medical research, particularly in the context of evolving surgical techniques and digital medical technologies.
Conclusions
The vascular supply to the thyroid gland of pigs may differ among breeds. These differences between breeds include the arteries supplying the cranial and caudal parts. These new insights into the arterial vascularization of the thyroid gland identify anatomical variations that should be considered in veterinary and medical studies using pigs as an animal model.
CONFLICT OF INTEREST
The authors declare no potential conflicts of interest regarding the research, authorship, and publication of this article.
Supplementary Material
Acknowledgments
The University of Miyazaki supported this research. The author would like to thank all the laboratory members for their support.
Funding Statement
The University of Miyazaki supported this research.
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