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Anat. Histol. Embryol. 36, 241–249 (2007) ISSN 0340–2096

doi: 10.1111/j.1439-0264.2006.00733.x

Faculty of Veterinary Medicine, Agricultural University of Wrocław, Wrocław, Poland

Topography and Arterial Supply of the Thyroid and the Parathyroid Glands in Selected Species of Falconiformes

T. Radek 1 and T. Piasecki 2 *

Addresses of authors: 1 Department of Anatomy and Histology, Faculty of Veterinary Medicine, Agricultural University of

Wrocław, ul. Kozuchowska_

Clinic of Infectious Diseases, Faculty of Veterinary Medicine, Agricultural University of Wrocław, pl. Grunwaldzki 45, 50-366 Wrocław, Poland; *Corresponding author: e-mail: piatom@op.pl

With 8 figures and 4 tables

Received November 2005; accepted for publication June 2006

1-3, 51-631 Wrocław, Poland; 2 Department of Epizootiology and Veterinary Administration with

Summary

Birds of two suborders, Accipitres and Falcones were the subjects of the study. The thyroids were always located asymmetrically. In Accipitridae the larger left gland was usu- ally situated significantly more cranially than the right one. In common kestrel, the size of bilateral thyroids was similar while their mutual relationships were individually variable. The location of the parathyroid glands in common kestrel was relatively constant. Seven topographical patterns of the loca- tion of the parathyroid gland were noted in Accipitridae. In birds of both the suborders, the thyroid might be supplied by three (groups of) arteries: the cranial thyroid, the caudal thy- roid and the middle thyroid arteries. The aforementioned vessels were derived from the common carotid and the oe- sophagotracheobronchial artery. In common kestrel, the thy- roid vessels might also branch from the ascending oesophageal artery, which passes along the thyroid, while in common buzzard and other Accipitridae – from the common trunk of the comes nervi vagi and the ascending oesophageal artery. The parathyroid glands were supplied by one to three para- thyroid arteries. The vessels for the cranial parathyroid gland mostly originated from the caudal thyroid artery, while for the caudal one – from the oesophagotracheobronchial artery. The average number of thyroid and parathyroid arteries in com- mon buzzard was significantly higher than those in common kestrel.

Introduction

The bilateral avian thyroid is situated right inside the thoracic inlet or slightly cranially to it. It is placed on the surfaces of the common carotid and the jugular vein, usually rostrally to the syrinx and laterally to the oesophagus and the trachea (Raether, 1964; Cotofan et al., 1970; Feder, 1971; Epple, 1993; Orosz, 1997). The mutual relationships between the cranial (IV) and the caudal (III) parathyroid glands and their location against the surrounding organs are variable and species-specific (Abdel-Magied and King, 1978; Hess et al., 1990; Epple, 1993; Orosz, 1997). Moreover, they exhibit, higher than the thyroid, individual intra-species changeability (Abdel-Magied and King, 1978). Nevertheless, the avian parathyroid glands are mostly situated next to each other on the surface of the jugular vein, among the trachea and the ultimobranchial glands (Epple, 1993; Orosz,

1997).

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The evident interspecies differences in either the origins or the numbers of thyroid and parathyroid arteries reflect the species-specific changeability of four vessels branching from the common carotid: the oesophagotracheobronchial and the ascending oesophageal artery, the comes nervi vagi and the vertebral trunk (Bhaduri et al., 1957; Raether, 1964; Cotofan et al., 1970; Baumel, 1993). The purpose of the study was the morphological and topographical analysis of glandular arteries and their parent vessels in common buzzard, rough-legged buzzard, western marsh harrier, sparrow hawk and common kestrel. The litera- ture still lacks the information on the morphology of the arterial system and the endocrine glands in Falconiformes. Accordingly, the results described in the present paper might improve the knowledge on this branch of the comparative avian anatomy.

Materials and Methods

Twenty-eight specimens of birds belonging to the two species (Mielczarek and Cichocki, 1999) were subjected to compar- ative, descriptive and morphometric study: (i) common buzzard (Buteo buteo – Accipitres, Accipitridae family, six females and five males), and (ii) common kestrel (Falco tinnunculus – Falcones, Falconinae family, seven females and 10 males). Additionally, descriptive studies were performed in three single representatives of other species from the Accipitridae family: rough-legged buzzard (Buteo logopus, one male), western marsh harrier (Circus aeruginosus, one female) and sparrow hawk (Accipiter nisus, one female). All the specimens obtained between 1993 and 1998 were from the Wrocław Zoological Garden. The arterial system of birds was accessed via the left heart ventricle or through the brachial artery and injected with colored latex (latex injection kit ZPK 580; Griffing & George, West Sussex, UK). Subsequently, the specimens were fixed in 10% formaldehyde and dissected under 16–25 · magnification using a Technival 2 microscope. The skin and the bilateral sternotracheal muscles were removed to expose the right and the left glands, the topography of which was described in relation to the common carotid, the jugular vein, the trachea and the oesophagus. Moreover, the topography of the arteries derived from the common carotid was established (Fig. 1). Subsequently, the measurements of the thyroid and the parathyroid glands were taken. Moreover, the distance

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242 Fig. 1. Diagram illustrating the measurements taken bilaterally in all the specimens studied. Example of

Fig. 1. Diagram illustrating the measurements taken bilaterally in all the specimens studied. Example of the right glands in common kestrel (A) and in common buzzard (B): a – brachiocephalic trunk, b – sub- clavian artery, c and c* – common carotid and internal carotid, respectively, d – oesophagotracheobronchial artery, e – ascending oesophageal artery, f – vertebral trunk, g – comes nervi vagi, nv – vagal nerve and its distal ganglion, pth – parathyroid glands, th – thyroid, vj – jugular vein; 1 – length of the thyroid, 2 – width of the thyroid, 3 – length of both the parathyroid glands, 4 – width of the parathyroid glands, 5 – distance between the bifurcation of the brachiocephalic trunk and the caudal extremity of the thyroid.

between the caudal extremity of the thyroid and the bifurca- tion of the brachiocephalic trunk into the common carotid and the subclavian artery was determined (Fig. 1). Morphometry was carried out with the aid of an electronic scaled calliper (mm ) 2 ). Mean values from three independent measurements were calculated for each parameter to ensure the reproduci- bility of results obtained. Empiric or mean measurement values enabled the drawing of the schemes of the species-specific topographical relations among the thyroid, the parathyroid glands, the glandular arteries and their parent vessels in Falconiformes (Fig. 2). The bilateral asymmetry of the thyroid location in common kestrel and common buzzard was expressed with the Van Valen (1962) coefficient figured out from 1 ) R 2 formula. The following criteria were considered in the course of morphological and topographical analysis of the thyroid and the parathyroid arteries: (i) origin, number and ramification pattern, (ii) topography before entering the glands, described in relation to the surrounding organs, and (iii) the region in which they drained the glandular parenchyma. All the measurement results were subjected to statistical analysis. The statistical significance of differences in bilateral measurements taken in common buzzard or in common kestrel was tested using Student’s t-test, whereas the importance of bilateral or inter-species differences in the average number of thyroid or parathyroid arteries observed was verified with the chi-squared test (P £ 0.05 for both the tests employed).

Results

In birds of both the suborders, the thyroid was located inside the cranial thoracic inlet, cranially from the syrinx. Its medial surface adjoined the common carotid and the jugular vein. Moreover, the right gland adhered to the oesophagus, whereas the left one to the trachea. Mean

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measurements of the left thyroid in common buzzard (5.69 · 3.52 mm ± 0.48 · 0.41 mm) were significantly higher than of the right one (4.98 · 3.23 mm ± 0.53 · 0.28 mm). In common kestrel, in turn, the sizes of the bilateral thyroids were not significantly different (3.24 · 2.29 ± 0.18 · 0.20 mm and 3.26 · 1.86 ± 0.23 · 0.15 mm for left and right gland, respectively). The bilateral thyroids were situated asymmetrically in all the birds studied. In common buzzard, as well as in other Accipitridae, the left gland was placed more cranially than the right one (directional asymmetry, the coefficient of asymmetry in common buzzard ¼ 0.98; Fig. 2). Accordingly, the mean distance between the caudal extremity of the thyroid and the bifurcation of the brachiocephalic trunk was signifi- cantly different when compared bilaterally (9.34 ± 0.90 mm and 6.86 ± 0.75 mm for left and right side, respectively). Analogical differences were found to be insignificant in common kestrel (4.71 ± 0.72 mm and 4.55 ± 0.54 mm for left and right side, respectively). The bilateral asymmetry in gland location appeared relatively weak and fluctuating (the coefficient of asymmetry ¼ 0.47; Fig. 2). A more cranial location of the left thyroid was observed in seven birds, while in another five specimens the right thyroid was situated more cranially (Fig. 3). In the remaining kestrels the bilateral thyroids were located at a similar level. Interspecific and individual variability of the unilateral and the bilateral parathyroid gland topography in relation to the thyroid, the common carotid and the jugular vein is illustrated in Fig. 4. The unilateral parathyroid glands were usually placed next to each other by the caudal end of the thyroid or slightly more caudally. The separate location of each gland was noted infrequently (Figs 4 and 5). The size of the left glands was slightly higher than that of the right ones in all the species studied (2.86 · 1.69 mm and 2.52 · 1.42 mm for the left and the right parathyroid glands of common buzzard and 1.62 · 0.84 and 1.36 · 0.61 mm for the left and the right parathyroid glands of common kestrel, respectively). In the thyroid and parathyroid region, both the common carotids gave rise directly or indirectly to four large vessels: the oesophagotracheobronchial, the comes nervi vagi, the ascend- ing oesophageal arteries and the vertebral trunk. In common kestrel and in common buzzard some topographical relation- ships among the aforementioned vessels and the glands studied were found to be species-specific (Fig. 2). They are presented in Fig. 2, in addition to the patterns observed in the single representatives of other species analysed. The individual variability of thyroid and parathyroid vasculature noted in common buzzard and common kestrel is illustrated in Fig. 6. The oesophagotracheobronchial artery branched from the medial (the right one) or the dorsolateral (the left one) side of the respective common carotid, caudally to the thyroid and the parathyroid glands or at the level of the latter. It usually began as an individual vessel in common buzzard and other Accipitridae (Figs 2, 5, 6 and 7). In most of the kestrels however, it left the carotid as a common trunk with the ascending oesophageal artery (Figs 2 and 3). It passed caudally in all the specimens studied to supply the bronchus and the preventricular part of the oesophagus with its terminal ramifications. In its initial course, the oesophagotracheobronchial artery gave rise to the branches for the trachea, the oesophagus and the syrinx (the single one in Accipitridae – Figs 2 and 7, one to

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Arteries of Thyroid and Parathyroid Glands 243 Fig. 2. Ventral view of thyroid and the parathyroid

Fig. 2. Ventral view of thyroid and the parathyroid glands against the background of the arterial pattern in A – common kestrel (most common pattern), B – common buzzard (most common pattern), C – rough-legged buzzard, D – western marsh harrier and E – sparrow-hawk:

a – brachiocephalic trunk, b – subclavian artery, c – common carotid and internal carotid, d – oesophagotracheobronchial artery, d¢ – tracheal

and syringical branches, e – ascending oesophageal artery, e¢ – oesophageal branches, f – vertebral trunk, g – comes nervi vagi, g* – common

trunk of the comes nervi vagi and the ascending oesophageal artery, i – suprascapular artery, j – parathyroid artery, k – caudal thyroid artery,

l – middle thyroid artery, m – cranial thyroid artery.

three branches in common kestrel – Figs 3 and 8). The thyroid (Table 1) and the parathyroid arteries, as well as the vessels for the vagal nerve and its distal ganglion, the carotid body and the ultimobranchial glands ramified laterally from the afore- mentioned branches or originated directly from the oesoph- agotracheobronchial artery. The origin and course of the comes nervi vagi and the ascending oesophageal artery were species-specific (Fig. 2). In

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common kestrel, the bilateral comes nervi vagi left the vertebral trunk or the common carotid at the level of the cranial extremity of the thyroid. The further course and the ramifications of that vessel are illustrated in Fig. 2 (more frequent pattern) or in Fig. 6 (individual variants). The ascending oesophageal artery usually ramified from the oesophagotracheobronchial artery, caudally to the thyroid or at the level of its caudal part (Figs 4 and 6). It passed along the

244

A

B
B

Fig. 3. A – Ventral view of the thoracic inlet in common kestrel (male), B – right thyroid and parathyroid region (most commonly observed arterial pattern): 1 – thyroid (the lateral surface of the left one and the medial surface of the right one), 2 – cranial parathyroid glands,

2¢ – caudal parathyroid gland, 3 – oesophagus, 4 – trachea, 4 ¢ – syrinx,

5, 5¢ – vagal nerve and its distal ganglion, 6 – brachial plexus,

a – brachiocephalic trunk, b – subclavian artery, c – common

carotid, c¢ – internal carotid, d – oesophagotracheobronchial artery,

d¢

– tracheal and syringical branches, e – ascending oesophageal artery,

e¢

– oesophageal branches, f – vertebral trunk, g – comes nervi vagi,

i – suprascapular artery, j – parathyroid artery, k – caudal thyroid

artery, l – middle thyroid artery, m – cranial thyroid artery.

medial surface of the thyroid sending the thyroid arteries and, directly or indirectly, the parathyroid arteries (Fig. 3). Finally, it anastomosed with the descending oesophageal artery in the middle of the neck. In common buzzard and other Accipitridae the comes nervi vagi and the ascending oesophageal artery originated bilater- ally as a common trunk leaving mostly the common carotid (Figs 2 and 6) or less frequently, the oesophagotracheobron- chial artery (Fig. 6). The topography of the initial part of the trunk described was similar to that of the ascending oesopha- geal artery in common kestrel (with the exception of western marsh harrier; Fig. 2) and similarly the vessel gave rise to the thyroid and the parathyroid arteries (Figs 2, 5 and 7). The bifurcation of the common trunk was found cranially to the thyroid. The left trunk gave rise to the relatively small, single ascending oesophageal artery, which in the middle of the neck anastomosed with the descending oesophageal artery. The right trunk in turn gave rise to a number of anastomosing oesophageal branches, one of which, branching between the

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middle and the cranial third of the neck, anastomosed with the right descending oesophageal artery (Fig. 7). The bilateral thyroids might be supplied by three types of thyroid arteries of various origin (Tables 1 and 2). There was at least one cranial thyroid artery on each side in common buzzard (Table 2). It originated from the common trunk of the comes nervi vagi and the ascending oesophageal artery. The left cranial thyroid artery ramified above the bifurcation of the aforementioned trunk and might originate either from the comes nervi vagi or from the ascending oesophageal artery (Fig. 5). The right cranial thyroid artery in turn might be derived either from the common trunk described or from one of its oesophageal branches (Table 1, Fig. 7). Each of the multiple cranial thyroid arteries originated from different of the latter branches (Fig. 2). The cranial thyroid artery (arteries) was demonstrated in 13 specimens of common kestrel, among them in nine specimens bilaterally (Table 2). It usually originated from the ascending oesophageal artery (Table 1; Figs 2 and 3). The origin of the cranial thyroid artery (arteries) was found at the level of the cranial extremity of the thyroid (short vessel) or more cranially (long vessel). In the latter case, before reaching the gland surface, the cranial thyroid artery passed caudally along the common carotid. The cranial thyroid artery gave rise to the thymic branch (Fig. 8) and on the right side in western marsh harrier, also the oesophageal one (Fig. 2). On the surface of the thyroid the cranial thyroid artery ramified into minute, medial and lateral branches, which drained the cranial, and in some specimens also the middle one-third of the gland. In all the birds studied, there was at least one bilateral caudal thyroid artery (Table 2, Fig. 2). In common kestrel, the vessel described originated mostly from the ascending oeso- phageal artery (Figs 3 and 8) and, more rarely, from the oesophagotracheobronchial artery (Table 1). The caudal thy- roid artery was the only arterial supply for the left and right thyroid in five and two birds, respectively. In such cases the caudal thyroid artery passed along the gland, giving rise to the caudal, the middle and the cranial thyroid branches. In common buzzard, the caudal thyroid artery mostly branched from the common trunk of the comes nervi vagi and the ascending oesophageal artery. The right vessel might either originate from the oesophagotracheobronchial artery, whereas the left one, directly from the common carotid. In both the species analysed, the caudal thyroid artery (arteries), originating from the oesophagotracheobronchial artery or from the common carotid and in two buzzards – also from the left common trunk of the comes nervi vagi and the ascending oesophageal arteries (Fig. 5), was the long vessel . Its origin was found caudally to the thyroid. In its course to the thyroid, the caudal thyroid artery supplied the parathyroid glands, the carotid body and the ultimobranchial glands (Figs 3, 5, 7 and 8). The short arteries in turn, originated from the ascending oesophageal artery in common kestrel or from the common trunk of the comes nervi vagi and the ascending oesophageal artery in common buzzard (Figs 3, 5 and 7). At the level of the caudal extremity of the thyroid, the caudal thyroid artery gave rise to the parathyroid branch(es), which passed caudally, and the cranial thyroid branch. Subsequently, the caudal thyroid artery (arteries) ramified into the minute subcapsular branches, which drained the caudal and the middle two-thirds of the thyroid. The multiple caudal thyroid

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Arteries of Thyroid and Parathyroid Glands 245 Fig. 4. Topographical patterns (A–H) of parathyroid glands in

Fig. 4. Topographical patterns (A–H) of parathyroid glands in individual species.

(A–H) of parathyroid glands in individual species. Fig. 5. Left thyroid and parathyroid region in common

Fig. 5. Left thyroid and parathyroid region in common buzzard (fe- male): 1 – thyroid (lateral surface), 2 – cranial parathyroid gland (medial surface), 2¢ – caudal parathyroid gland (lateral surface),

3 – oesophagus, 4 – trachea, 5, 5¢ – vagal nerve and its distal ganglion,

vj – jugular vein, c – common carotid, d, d* – oesophagotracheo-

bronchial artery and its tracheal branch, e – ascending oesophageal artery, f – vertebral trunk, g, g* – comes nervi vagi and the common

trunk of the comes nervi vagi and the ascending oesophageal artery,

h – cervical ascending cutaneous artery, i – suprascapular artery,

j – parathyroid artery, k – caudal thyroid artery, l – middle thyroid artery, m – cranial thyroid artery.

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arteries originated, each separately, from the same or from various of the aforementioned larger vessels. At least one middle thyroid artery was observed bilaterally in eight common buzzards and in five common kestrels. It was however absent or present unilateral only in the remaining specimens (Table 2). Instead of the single one, the middle thyroid artery might appear as a double vessel and in common buzzard even as a triple vessel. The artery described belonged to the short vessels . It originated at the level of one-third of the thyroid, from the ascending oesophageal artery in common kestrel, or from the common trunk of the comes nervi vagi and the ascending oesophageal artery in common buzzard, and entered the glandular parenchyme nearly directly (Table 1, Figs 2, 3, 5 and 7). The origins, the courses and the parental vessels for the arteries of rough-legged buzzard, sparrow hawk and western marsh harrier are presented in Fig. 2. The bilateral thyroids might be supplied by one to three single or multiple thyroid arteries (Table 1, Fig. 2). In the first variant, observed in six common kestrels (in one bird – bilaterally) and on the right side in western marsh harrier, the gland was supplied by the caudal thyroid artery (arteries) (Fig. 2). In another one the thyroid was drained by two types of vessels: the cranial and the caudal thyroid artery (arteries) or the latter accompanied by the middle thyroid artery

246

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246 Radek and Piasecki Fig. 6. Individual variations of main arteries in left and right thyroid

Fig. 6. Individual variations of main arteries in left and right thyroid and parathyroid region of common kestrel and common buzzard:

a

– brachiocephalic trunk, b – subclavian artery, c – common carotid, d – oesophagotracheobronchial artery, d ¢ – tracheosyringical branch,

e

– ascending oesophageal artery, e¢ – oesophageal branches, e* – descending oesophageal artery, f – vertebral trunk, g, g* – comes nervi vagi and

the common trunk of the comes nervi vagi and the ascending oesophageal artery, h – cervical ascending cutaneous artery, i – suprascapular artery.

(arteries). The situation described occurred predominantly in common kestrel (Fig. 8). In common buzzard in turn the thyroid was mostly supplied by all three types of the thyroid arteries (Figs 5 and 7). Although the number of the thyroid

arteries in common buzzard and common kestrel was individual-specific, their average counts on both sides were significantly lower in the latter species (P £ 0.05). The bilateral differences in number of the vessels studied were

Table 1. Number of birds in which the thyroid arteries originated from the particular parental vessels

Right side

Left side

Arteries

Acc

Otb

Cnv+Oea

Cnv

Oea (rea)

Acc

Otb

Cnv+Oea

Cnv

Oea (rea)

Buteo buteo

Cranial thyroid

0

0

4

4

5

0

0

6

5

6

Caudal thyroid

1

5

8

0

0

4

0

10

0

1

Middle thyroid

0

0

8

0

1

0

0

5

0

5

Falco tinnunculus

Cranial thyroid

1

0

0

0

11

0

0

0

1

9

Caudal thyroid

0

9

0

0

10

3

8

0

1

15

Middle thyroid

0

0

0

0

11

0

0

0

0

6

Arteries of Thyroid and Parathyroid Glands

A

B
B

Fig. 7. A – lateral view of right cervical area in common buzzard (female), B – right thyroid and parathyroid region (most common arterial pattern): 1 – thyroid, 2 – parathyroid glands, 3 – oesophagus,

4, 4¢ – trachea and syrinx, 5, 5¢ – vagal nerve and its distal ganglion,

6 – brachial plexus, a – brachiocephalic trunk, b – subclavian artery,

c – common carotid, d – oesophagotracheobronchial artery,

d ¢ – tracheosyringical branch, e – ascending oesophageal artery,

e ¢ – oesophageal branches, e* – descending oesophageal artery,

f – vertebral trunk, g, g* – comes nervi vagi and the common trunk of

the comes nervi vagi and the ascending oesophageal artery, h – cervical ascending cutaneous artery, h* – cervical descending cutaneous artery,

i – suprascapular artery, j – parathyroid artery, k – caudal thyroid artery, l – middle thyroid artery, m – cranial thyroid artery.

however not demonstrated in any of the aforementioned species (Table 1). The cranial and the caudal parathyroid glands were usually supplied by one to two arteries (Fig. 2). In five common buzzards however (left side ¼ 3, right side ¼ 1, both sides ¼ 1), one or both the parathyroid glands were drained by three to six vessels (Table 3). Among the parathyroid arteries observed, the vessels sup- plying only one gland [the cranial (IV) or the caudal (III) parathyroid artery] and the common artery for both the glands of one side were distinguished. The common parathyroid artery was demonstrated on the left side in 21 specimens (23 vessels) and on the right side – in 18 birds (19 vessels). The three types of course and ramification were observed for the common parathyroid artery. The aforementioned vessel mostly reached the unilateral glands at their contact point (11 vessels in 11 birds and nine vessels in eight birds on left and right side, respectively). In the other variant, however, the common artery drained one of the glands sending its terminal branches to another (eight vessels in six birds, and seven vessels in seven birds on left and right side, respectively).

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Table 2. Number of birds with the single or multiple cranial, caudal and middle thyroid arteries

 

Right arteries

Left arteries

Common buzzard (n ¼ 11)

Common kestrel (n ¼ 17)

Common buzzard (n ¼ 11)

Common kestrel (n ¼ 17)

Cranial thyroid artery One artery Two arteries Three arteries Four arteries Five arteries Six arteries Absent Caudal thyroid artery One artery Two arteries Three arteries Four arteries Middle thyroid artery One artery Two arteries Three arteries Absent

3

4

2

0

1

1

0

6

4

1

0

5

0

3

3

7

2

9

3

5

1

2

2

0

0

2

0

0

0

0

0

0

0

5

0

7

14

5

6

3

4

10

0

1

1

0

1

0

7

3

4

4

1

2

0

5

0

6

2

11

7 3 4 4 1 2 0 5 0 6 2 11 Fig. 8. Left thyroid

Fig. 8. Left thyroid and parathyroid region in common kestrel (female). One of rare arterial patterns: 1 – thyroid, 2, 2 ¢ – cranial and caudal parathyroid glands, 3 – oesophagus, 4, 4¢ – trachea and syrinx, 5 – vagal nerve, 6 – brachial plexus, 7 – ultimobranchial gland,

a – brachiocephalic trunk, b – subclavian artery, c – common carotid

artery, d – oesophagotracheobronchial artery, d¢ – tracheal branch,

e – ascending oesophageal artery, f – vertebral trunk, g – comes nervi vagi, g* – common trunk of the comes nervi vagi and the ascending

oesophageal artery, i – suprascapular artery, k – caudal thyroid artery, l

– middle thyroid artery, m – cranial thyroid artery, n – thymic branch.

Finally, the common parathyroid artery might divide into the branches for the cranial (IV) and the caudal (III) parathyroid before reaching their surface (in four and three birds on left and right side, respectively). Moreover, in two common kestrels the parathyroid glands of one side were supplied by the double common parathyroid arteries (in one bird bilater- ally and on the left side in another). On the left side they both ramified as described for the second variant, whereas on the right, one of the arteries followed the first variant, while another, the third pattern. The parathyroid arteries usually originated from the caudal thyroid or the oesophagotracheo-

248

Table 3. Number of the parathyroid arteries supplying the single (III or IV) or both the parathyroid glands (III and IV) on left and right side in common buzzard and in common kestrel

Glands

Right

Buzzard

Kestrel

Left

Buzzard

Kestrel

Cranial parathyroid (IV) One artery

7

13

5

14

Two arteries

2443

Three arteries

0010

Four arteries

2000

Five arteries

0010

Total Caudal parathyroid (III)

11

17

11

17

One artery

4

13

4

14

Two arteries

6433

Three arteries

0030

Four arteries

1000

Six arteries

0010

Total

11

17

11

17

bronchial artery (Figs 3, 5 and 7). Hardly ever they ramified from the other arteries, like from the common trunk of the comes nervi vagi and the ascending oesophageal artery in common buzzard (Figs 5 and 7). The average number of the parathyroid arteries in common buzzard was significantly higher than in common kestrel (P £ 0.05).

Discussion

Seventeen common kestrels and 11 common buzzards were subjected to the study of the topography and the vasculature of the thyroid and the parathyroid glands. Comparative analysis was extended to the results obtained in other three specimens of Accipitridae – one rough-legged buzzard, one western marsh harrier and one sparrow hawk, on the basis of their similarity to common buzzard in question of the thyroid location and in topographical patterns of large vessels origin- ating from the bilateral common carotids. The bilateral thyroids were located asymmetrically in the Falconiformes studied, as described in house birds (Raether, 1964; Breit et al., 1998). The glands on the left side in Accipitridae were usually larger and situated more cranially than those on the right. The location of thyroid in accipitrids followed the phenomenological criterion of directional asym- metry. In common kestrel in turn, the mutual relationships of the bilateral thyroids were variable corresponding to fluctu- ating asymmetry (Van Valen, 1962; Watała and Markowski,

1999).

Either the topography of the bilateral parathyroid glands in relation to the thyroid or the unilateral mutual relationships between the cranial and the caudal glands were similar as described in most birds (Raether, 1964; Cotofan et al., 1970; Abdel-Magied and King, 1978; Hess et al., 1990). The high variability in the topography of the aforementioned glands in the accipitrids studied, reflected in the seven variants of the parathyroid gland location, among them six occurring in common buzzard, is however worthy of attention. The relevant literature lacks the data on such individual variations in the parathyroid gland topography in other avian species. The thyroid might be supplied by three single or multiple thyroid arteries: the cranial, the caudal and the middle ones. The occurrence of the multiple vessels of the aforementioned

Radek and Piasecki

types was previously described in hen, duck and goose (Raether, 1964; Cotofan et al., 1970) and, more recently, in budgerigar (Radek and Piasecki, 2004). The average number of the thyroid arteries on each side was significantly higher in common buzzard when compared with common kestrel. According to Koma´rek et al. (1982) and Baumel (1993) the thyroid is supplied by one artery in most birds. Such a vascular model was demonstrated in Columba (Bhaduri et al., 1957) as well as in Rhea, Spheniscus, Gavia, Podiceps, Cygnus, Fulica, Apus, Trogon and Corvus (Baumel, 1993). The results of present study in Falconiformes and our previous investigations in budgerigar (Radek and Piasecki, 2004) suggest that the single thyroid artery (or the group of multiple arteries) observed in some birds corresponds to the caudal thyroid artery. The latter was found to be the most stable, considering either the occurrence or the area it supplied: the ultimobran- chial glands, the parathyroid glands, the oesophagus and the distal ganglion of vagal nerve (Raether, 1964; Cotofan et al., 1970; Abdel-Magied and King, 1978; Baumel, 1993; Radek and Piasecki, 2004). In the present study, the arterial model with the one thyroid artery was demonstrated in six common kestrels (in three of them, bilaterally) and in one western marsh harrier. According to Baumel (1993), either the single thyroid artery or the caudal thyroid artery originates directly from the common carotid. That regularity was however not proved in our study. The thyroid was supplied by two or three arteries (or their groups) in the birds studied. The dual arterial supply of the thyroid has been described in some Columbidae, galliformes, seagulls and flamingos, thus far (Baumel, 1993), whereas the gland drained by the cranial, the caudal and the middle thyroid arteries is characteristic for Anatidae, Gallus and Columba (Cotofan et al., 1970; Baumel, 1993). The common buzzard, and plausibly also the rough-legged buz- zard, might be enumerated to the latter group on the basis of our study. High individual variability in the arterial model of the thyroid vasculature and the significant asymmetry of relevant vessels was in turn demonstrated in common kestrel. It is very likely that the discrepancies in question of the thyroid artery models and their origin result exactly from the individual variability in specific avian species. The aforemen- tioned differences however might easily reflect the diverse interpretation of the results obtained by various authors. For instance, the cranial thyroid artery in Anatidae was reported to originate either from the ascending oesophageal artery (Coto- fan et al., 1970) or from the comes nervi vagi (Raether, 1964). The study of Cotofan et al. (1970), lacks the data on the topography of the comes nervi vagi artery, whereas in that of Raether (1964) the analogous information on the ascending oesophageal artery is missing. Consequently, it is hard to comment on the results of both of these authors. Moreover, it should be remembered that the comes nervi vagi and the ascending oesophageal artery might branch as a common trunk in some avian species (Bhaduri et al., 1957; Baumel, 1993; Radek and Piasecki, 2004) and it was so in the accipitrids in the present study. The discrepancies also deal with the origin of the caudal thyroid artery in domestic hen. According to Abdel-Magied and King (1978), the aforementioned vessel ramifies from the common carotid and, after giving rise to some branches to the thyroid, continues as the ascending oesophageal artery. Cotofan et al. (1970) however, revealed that the caudal thyroid artery originates from the ascending oesophageal as one of two or three thyroid-supplying vessels.

2007 Blackwell Verlag

Arteries of Thyroid and Parathyroid Glands

Nevertheless, the results of present study on the separation variants and the number of parathyroid branches in Falconi- formes analysed are in general consonant with the relevant data for domestic birds (Raether, 1964; Cotofan et al., 1970; Abdel-Magied and King, 1978).

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