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Topography and Arterial Supply of the Thyroid and the Parathyroid Glands in
Selected Species of Falconiformes
T. Radek1 and T. Piasecki2*
Addresses of authors: 1Department of Anatomy and Histology, Faculty of Veterinary Medicine, Agricultural University of
Wrocław, ul. Ko_zuchowska 1-3, 51-631 Wrocław, Poland; 2Department of Epizootiology and Veterinary Administration with
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
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 common kestrel, the bilateral comes nervi vagi left the
(Table 1) and the parathyroid arteries, as well as the vessels for vertebral trunk or the common carotid at the level of the
the vagal nerve and its distal ganglion, the carotid body and cranial extremity of the thyroid. The further course and the
the ultimobranchial glands ramified laterally from the afore- ramifications of that vessel are illustrated in Fig. 2 (more
mentioned branches or originated directly from the oesoph- frequent pattern) or in Fig. 6 (individual variants). The
agotracheobronchial artery. ascending oesophageal artery usually ramified from the
The origin and course of the comes nervi vagi and the oesophagotracheobronchial artery, caudally to the thyroid or
ascending oesophageal artery were species-specific (Fig. 2). In at the level of its caudal part (Figs 4 and 6). It passed along the
A 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
B 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
Fig. 3. A – Ventral view of the thoracic inlet in common kestrel caudal thyroid artery (Table 2, Fig. 2). In common kestrel, the
(male), B – right thyroid and parathyroid region (most commonly
vessel described originated mostly from the ascending oeso-
observed arterial pattern): 1 – thyroid (the lateral surface of the left one
and the medial surface of the right one), 2 – cranial parathyroid glands, phageal artery (Figs 3 and 8) and, more rarely, from the
2¢ – caudal parathyroid gland, 3 – oesophagus, 4 – trachea, 4¢ – syrinx, oesophagotracheobronchial artery (Table 1). The caudal thy-
5, 5¢ – vagal nerve and its distal ganglion, 6 – brachial plexus, roid artery was the only arterial supply for the left and right
a – brachiocephalic trunk, b – subclavian artery, c – common thyroid in five and two birds, respectively. In such cases the
carotid, c¢ – internal carotid, d – oesophagotracheobronchial artery,
d¢ – tracheal and syringical branches, e – ascending oesophageal artery, caudal thyroid artery passed along the gland, giving rise to the
e¢ – oesophageal branches, f – vertebral trunk, g – comes nervi vagi, caudal, the middle and the cranial thyroid branches.
i – suprascapular artery, j – parathyroid artery, k – caudal thyroid In common buzzard, the caudal thyroid artery mostly
artery, l – middle thyroid artery, m – cranial thyroid artery. 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
medial surface of the thyroid sending the thyroid arteries and, the left one, directly from the common carotid.
directly or indirectly, the parathyroid arteries (Fig. 3). Finally, In both the species analysed, the caudal thyroid artery
it anastomosed with the descending oesophageal artery in the (arteries), originating from the oesophagotracheobronchial
middle of the neck. artery or from the common carotid and in two buzzards – also
In common buzzard and other Accipitridae the comes nervi from the left common trunk of the comes nervi vagi and the
vagi and the ascending oesophageal artery originated bilater- ascending oesophageal arteries (Fig. 5), was Ôthe long vesselÕ.
ally as a common trunk leaving mostly the common carotid Its origin was found caudally to the thyroid. In its course to
(Figs 2 and 6) or less frequently, the oesophagotracheobron- the thyroid, the caudal thyroid artery supplied the parathyroid
chial artery (Fig. 6). The topography of the initial part of the glands, the carotid body and the ultimobranchial glands
trunk described was similar to that of the ascending oesopha- (Figs 3, 5, 7 and 8). The Ôshort arteriesÕ in turn, originated from
geal artery in common kestrel (with the exception of western the ascending oesophageal artery in common kestrel or from
marsh harrier; Fig. 2) and similarly the vessel gave rise to the the common trunk of the comes nervi vagi and the ascending
thyroid and the parathyroid arteries (Figs 2, 5 and 7). The oesophageal artery in common buzzard (Figs 3, 5 and 7). At
bifurcation of the common trunk was found cranially to the the level of the caudal extremity of the thyroid, the caudal
thyroid. The left trunk gave rise to the relatively small, single thyroid artery gave rise to the parathyroid branch(es), which
ascending oesophageal artery, which in the middle of the neck passed caudally, and the cranial thyroid branch. Subsequently,
anastomosed with the descending oesophageal artery. The the caudal thyroid artery (arteries) ramified into the minute
right trunk in turn gave rise to a number of anastomosing subcapsular branches, which drained the caudal and the
oesophageal branches, one of which, branching between the middle two-thirds of the thyroid. The multiple caudal 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 arteries in common buzzard and common kestrel was
common kestrel (Fig. 8). In common buzzard in turn the individual-specific, their average counts on both sides were
thyroid was mostly supplied by all three types of the thyroid significantly lower in the latter species (P £ 0.05). The
arteries (Figs 5 and 7). Although the number of the thyroid 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
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
Acc – common carotid, Otb – oesophagotracheobronchial artery, Cnv+Oea – common trunk of the comes nervi vagi and the ascending
oesophageal artery, Cnv – comes nervi vagi, Oea – ascending oesophageal artery (or rea – the right oesophageal branch).
Table 3. Number of the parathyroid arteries supplying the single (III types was previously described in hen, duck and goose
or IV) or both the parathyroid glands (III and IV) on left and right side (Raether, 1964; Cotofan et al., 1970) and, more recently, in
in common buzzard and in common kestrel
budgerigar (Radek and Piasecki, 2004). The average number
Right Left of the thyroid arteries on each side was significantly higher in
common buzzard when compared with common kestrel.
Glands Buzzard Kestrel Buzzard Kestrel According to Komárek et al. (1982) and Baumel (1993) the
thyroid is supplied by one artery in most birds. Such a vascular
Cranial parathyroid (IV)
One artery 7 13 5 14 model was demonstrated in Columba (Bhaduri et al., 1957) as
Two arteries 2 4 4 3 well as in Rhea, Spheniscus, Gavia, Podiceps, Cygnus, Fulica,
Three arteries 0 0 1 0 Apus, Trogon and Corvus (Baumel, 1993). The results of
Four arteries 2 0 0 0 present study in Falconiformes and our previous investigations
Five arteries 0 0 1 0
Total 11 17 11 17
in budgerigar (Radek and Piasecki, 2004) suggest that the
Caudal parathyroid (III) single thyroid artery (or the group of multiple arteries)
One artery 4 13 4 14 observed in some birds corresponds to the caudal thyroid
Two arteries 6 4 3 3 artery. The latter was found to be the most stable, considering
Three arteries 0 0 3 0 either the occurrence or the area it supplied: the ultimobran-
Four arteries 1 0 0 0
Six arteries 0 0 1 0 chial glands, the parathyroid glands, the oesophagus and the
Total 11 17 11 17 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
bronchial artery (Figs 3, 5 and 7). Hardly ever they ramified with the one thyroid artery was demonstrated in six common
from the other arteries, like from the common trunk of the kestrels (in three of them, bilaterally) and in one western marsh
comes nervi vagi and the ascending oesophageal artery in harrier. According to Baumel (1993), either the single thyroid
common buzzard (Figs 5 and 7). The average number of the artery or the caudal thyroid artery originates directly from the
parathyroid arteries in common buzzard was significantly common carotid. That regularity was however not proved in
higher than in common kestrel (P £ 0.05). 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,
Discussion galliformes, seagulls and flamingos, thus far (Baumel, 1993),
Seventeen common kestrels and 11 common buzzards were whereas the gland drained by the cranial, the caudal and the
subjected to the study of the topography and the vasculature middle thyroid arteries is characteristic for Anatidae, Gallus
of the thyroid and the parathyroid glands. Comparative and Columba (Cotofan et al., 1970; Baumel, 1993). The
analysis was extended to the results obtained in other three common buzzard, and plausibly also the rough-legged buz-
specimens of Accipitridae – one rough-legged buzzard, one zard, might be enumerated to the latter group on the basis of
western marsh harrier and one sparrow hawk, on the basis of our study. High individual variability in the arterial model of
their similarity to common buzzard in question of the thyroid the thyroid vasculature and the significant asymmetry of
location and in topographical patterns of large vessels origin- relevant vessels was in turn demonstrated in common kestrel.
ating from the bilateral common carotids. It is very likely that the discrepancies in question of the
The bilateral thyroids were located asymmetrically in the thyroid artery models and their origin result exactly from the
Falconiformes studied, as described in house birds (Raether, individual variability in specific avian species. The aforemen-
1964; Breit et al., 1998). The glands on the left side in tioned differences however might easily reflect the diverse
Accipitridae were usually larger and situated more cranially interpretation of the results obtained by various authors. For
than those on the right. The location of thyroid in accipitrids instance, the cranial thyroid artery in Anatidae was reported to
followed the phenomenological criterion of directional asym- originate either from the ascending oesophageal artery (Coto-
metry. In common kestrel in turn, the mutual relationships of fan et al., 1970) or from the comes nervi vagi (Raether, 1964).
the bilateral thyroids were variable corresponding to fluctu- The study of Cotofan et al. (1970), lacks the data on the
ating asymmetry (Van Valen, 1962; Watała and Markowski, topography of the comes nervi vagi artery, whereas in that of
1999). Raether (1964) the analogous information on the ascending
Either the topography of the bilateral parathyroid glands in oesophageal artery is missing. Consequently, it is hard to
relation to the thyroid or the unilateral mutual relationships comment on the results of both of these authors. Moreover, it
between the cranial and the caudal glands were similar as should be remembered that the comes nervi vagi and the
described in most birds (Raether, 1964; Cotofan et al., 1970; ascending oesophageal artery might branch as a common
Abdel-Magied and King, 1978; Hess et al., 1990). The high trunk in some avian species (Bhaduri et al., 1957; Baumel,
variability in the topography of the aforementioned glands in 1993; Radek and Piasecki, 2004) and it was so in the accipitrids
the accipitrids studied, reflected in the seven variants of the in the present study. The discrepancies also deal with the origin
parathyroid gland location, among them six occurring in of the caudal thyroid artery in domestic hen. According to
common buzzard, is however worthy of attention. The relevant Abdel-Magied and King (1978), the aforementioned vessel
literature lacks the data on such individual variations in the ramifies from the common carotid and, after giving rise to
parathyroid gland topography in other avian species. some branches to the thyroid, continues as the ascending
The thyroid might be supplied by three single or multiple oesophageal artery. Cotofan et al. (1970) however, revealed
thyroid arteries: the cranial, the caudal and the middle ones. that the caudal thyroid artery originates from the ascending
The occurrence of the multiple vessels of the aforementioned oesophageal as one of two or three thyroid-supplying vessels.
Nevertheless, the results of present study on the separation Feder, F. H., 1971: Zur Topographie und mikroskopischen Anatomie
variants and the number of parathyroid branches in Falconi- der endokrinen Organe beim Wellensittich (Melopsittacus undula-
formes analysed are in general consonant with the relevant tus). Anat. Anz. 128, 338–353.
data for domestic birds (Raether, 1964; Cotofan et al., 1970; Hess, J. B., D. L. Fletcher, R. J. Buhr, and W. M. Britton, 1990:
Localization of chicken parathyroid glands through vital staining.
Abdel-Magied and King, 1978).
Poultry Sci. 69, 133–137.
Komárek, V., L. Malinovský, and L. Lemež, 1982: Anatomie Avium
Domesticarum et Embryologia Galli (M. U. Čihak and P. Popesko,
References
eds). Bratislava: Prı́roda, vol. 3, pp. 38.
Abdel-Magied, E. M., and A. S. King, 1978: The topographical Mielczarek, P., and W. Cichocki, 1999: Polish names for birds. Notatki
anatomy and blood supply of the carotid body region of domestic Ornitologiczne 40, 30–37.
fowl. J. Anat. 126, 535–546. Orosz, S., 1997: Anatomy of the endocrine system. In: Avian Medicine
Baumel, J. J., 1993: Systema cardiovasculare. In: Handbook of Avian and Surgery (W. B. Altman ed.). Philadelphia, London, Toronto:
Anatomy. Nomina Anatomica Avium (J. J. Baumel, ed.). Cam- Saunders Company, pp. 475–479.
bridge, MA: Nuttal Ornithological Club, pp. 425–462. Radek, T., and T. Piasecki, 2004: The topographical anatomy and
Bhaduri, J. L., B. Biswas, and S. K. Das, 1957: The arterial sys- arterial supply of the thyroid and parathyroid glands in budgerigar
tem of the domestic pigeon (Columba livia Gmelin). Anat. Anz. 104, (Melopsittacus undulates). Folia Morphol. 63, 163–171.
1–13. Raether, W., 1964: Schilddrüse, Epithelkörperchen, Ultimobranchialer
Breit, S., H. E. König, and E. Stöger, 1998: Morphological studies on Körper und Paraganglion caroticum ihre Topographie, Blutver-
the thyroid gland of chicken in addition to seasonal changes. Anat. sorgung und Morphologie bei Huhn, Taube, Gans und Ente. Diss.
Histol. Embryol. 27, 271–276. Vet. Gießen.
Cotofan, N., O. Cotofan, and L. Cozariuc, 1970: Cercelari privid Van Valen, L., 1962: A study of fluctuating asymmetry. Evolution 16,
vascularizatia tiroidei si paratiroidei la pasari. Ins. Ionescu Brad Iasi 125–142.
Lucr. Sti. II Zooteh. Med. Vet. 11, 145–152. Watała, K., and J. Markowski, 1999: Fluctuating asymmetry as the
Epple, A., 1993: Glandulae endocrine. In: Handbook of Avian Anat- indicator of biological condition of individual birds and population.
omy. Nomina Anatomica Avium (J. J. Baumel ed.). Cambridge, Przegl. Zool. 43, 53–66.
MA: Nuttal Ornithological Club, pp. 401.