Morphology of the Pattern of Branching of the Aortic Arch in Syrian Hamsters (Mesocricetus Auratus)

The branching patterns of the aortic arches of 28 adult male and female Syrian hamsters (SH) were thoroughly examined under a stereomicroscope for the rst time by using latex injection and corrosion casting to determine their general arrangements and morphological variations as well as their differences and similarities to other rodents and rabbits. Three major arteries, namely, the brachiocephalic trunk (BC), left common carotid artery (CC) and left subclavian artery (SA), originating from the aortic arch (AR), were uniformly noted in SH. The BC was consistently divided into the right SA and the right CA. SA in SH normally releases the internal thoracic, deep cervical, dorsal scapular, vertebral, supercial cervical and supreme intercostal arteries. The costocervical trunk typically consisted of supreme intercostal and internal thoracic arteries and a common trunk for dorsal scapular and deep cervical arteries. To comprehend the comparative morphology of the pattern of branching of AR more completely, our results were compared with previous studies in rodents and rabbits. (1) The general morphology of the great arteries from AR in SH was similar to that in mole rats, rats, mice, porcupines, and gerbils but was essentially different from that in rabbits, guinea pigs, red squirrels, ground squirrels, pacas and chinchillas. (2) The typical pattern of the branching of the subclavian arteries in SH was similar to that in guinea pigs, rats, and rabbits but was different from that of the reported rodents regardless of the origins of the bronchoesophageal and internal thoracic arteries and the composition of the costocervical trunk.


Introduction
Hamsters belong to the order Rodentia, suborder Myomorpha, and family Cricetidae. Approximately 90% of the hamsters used in research are of Syrian origin (Lossi et al. 2016). Syrian hamsters exhibit characteristics that make them desirable models for cardiovascular research (Suckow et al. 2012).
The aortic arch in domestic mammals gives rise to vessels that supply the head, forelimb and cranial region of the thorax as well as the thoracic region (Nickel et al. 1981). The branching pattern of the aortic arch has been described in various rodents, including rats (Green 1963; Hebel and Stromberg 1976; Popesko et al. 1992b The twenty-ve Syrian hamsters (13 males and 12 females) were used for latex injection. The animal was placed in dorsal recumbency before administration of the anaesthesia. The animals were intraperitoneally anaesthetized with a combination of ketamine (Bremer Pharma GMBH, Germany), acepromazine (Alfasan, Netherlands), and xylazine (Alfasan, Netherlands) according to https://www.mcgill.ca/research/ les/research/112-_hamster_anesthesia. Under anaesthesia, the thoracic cavity was opened and ipped over. Then, to prevent coagulation of the blood, heparin sodium (5000 IU/ml, Alborz Darou, Iran) was injected into the apex cordis. The animals were exsanguinated by cutting the caudal vena cava and the vessels were immediately perfused with sodium chloride (0.9%) via a cannula, which was inserted into the apex cordis to remove blood cloths during exsanguination; an average amount of 20 ml of sodium chloride solution for the each specimen seemed adequate.
Subsequently, red (Sahar colour, Tehran, Iran) coloured latex (1-Stop Solution, Kuala Lumpur, Malaysia) was hand injected into the apex cordis for about 5 second until the tips of the thoracic limbs were seen to be lled. Later, the apex was ligatured. The amount of latex used to obtain good visualization of the arteries of the aortic arch ranged from 1-2 ml for each hamster. The injected specimens were xed by immersion in 10% natural formalin solution which contained 4% formaldehyde. Three Syria hamsters (two males and one female) were examined by a corrosion cast technique. Vinyl resin (Rhodopas AX 90/10; Rhone-Poulenc; Courbevoie; France) in a 10% ketone solution was injected similar to the latex injection. The internal casts of the arterial branches of the aortic arch were obtained by macerating the specimens in 10% sodium hydroxide bath (Verli et al. 2007). All dissections were examined under a binocular stereomicroscope (Nikon, SMZ800, Japan). The dissection data were documented by digital images obtained with Samsung Mobil (South Korea, Galaxy J5, 2015). In the photographs, a part of a steel ruler was used as a scale bar and distance between the two lines was 1 mm. For the nomenclature of the aortic arch and its branches, Nomina Anatomica Veterinaria (2017) was applied.

Results
The aortic arch was located at the level of the second intercostal space, and at this level, three great arterial branches, namely, the brachiocephalic trunk and the left common carotid and left subclavian arteries originating from the aortic arch, were uniformly noted on all 25 specimens (100.00%). The short brachiocephalic trunk was the rst branch of the aortic arch, extended cranially and was divided into the right subclavian and right common carotid arteries at the level of the rst intercostal space in 25 specimens (100.00%) (Fig. 1). Both the right and left subclavian arteries normally were given off within the thorax, supreme intercostal, and common trunk for the dorsal scapular and deep cervical arteries, as well as the internal thoracic, vertebral, and super cial cervical arteries.
Type B: the costocervical trunk consisted of a common trunk for the supreme intercostal and internal thoracic arteries and a common trunk for the dorsal and deep cervical arteries on 34/50 sides (68%), including 21/25 right sides (84%) and 13/25 left sides (52%) (Fig. 4).
The supreme intercostal artery was the rst branch arising from the dorsal surface of the subclavian artery. The supreme intercostal artery was usually given off of the rst, second and third dorsal intercostal arteries. Shortly after its emergence from the subclavian artery, the supreme intercostal artery released a long rst dorsal intercostal artery that coursed dorsally to reach the rst intercostal space (Figs. 2, 3, 4).
The common trunk for the dorsal scapular and deep cervical arteries always originated from the subclavian arteries cranial to the origin of the costocervical trunk (when present) or from the supreme intercostal artery. The trunk passed dorsally and left the thoracic cavity from the rst rib. The deep cervical artery was passed cranially to reach the muscles of the neck. The dorsal scapular artery was coursed caudally (Figs. 2, 3, 4).
The vertebral artery arises from the subclavian artery, cranial to the origin of a common trunk for the dorsal scapular and the deep cervical arteries. The vertebral artery began opposite the rst intercostal space and passed dorsally and cranially to enter the transverse foramen of the sixth cervical vertebra (Figs. 2, 3, 4).
The super cial cervical artery was the last branch arising from the dorsal surface of the subclavian artery, cranial to the origin of the vertebral artery, at the level of the rst intercostal space. Immediately, the ascending cervical artery was removed, which was the cervical continuation of the super cial cervical artery. The artery ascended cranially under the ventral cervical muscles. After that, the super cial cervical artery was on the left in the thoracic cavity until it passed dorsocranially between the neck and scapula (Figs. 2, 3, 4).
A relatively large internal thoracic artery originated separately from the ventral surface of the subclavian artery on the 18/50 sides (36%) and was positioned at the origin of the supreme intercostal artery or costocervical trunk (when present) at the level of the rst rib on the right side and at the level of the rst intercostal space on the left side. The artery was then curved ventrally and caudally. The internal thoracic artery originated from a common trunk with the supreme intercostal artery from the subclavian artery on 32/50 sides (64%), including 10/25 right sides (40%) and 6/25 left sides (24%) (Figs. 2, 3, 4).

Discussion
The aortic arch gives off two major arteries, the brachiocephalic trunk and the left subclavian artery in the chinchilla ( However, the right vertebral artery in porcupine (Atalar et al. 2003) and the right and left vertebral arteries in the guinea pig (Cooper and Schiller 1975) may arise from the costocervical trunk.
In the guinea pig, the rst vertebral artery emerges directly from the subclavian artery, but the second vertebral artery may arise with the left dorsal scapular artery by a common trunk from the subclavian artery (Kabak and Hazriroglu 2003).

Deep cervical artery
No information has been reported regarding the origin of the deep cervical artery in porcupine (Atalar et al. 2003 However, the right deep cervical artery emerged with the internal thoracic artery and costocervical trunk in the mole rat (Aydin et al. 2013). In addition, the deep cervical artery may arise from a common trunk from the subclavian artery in the red squirrel (Aydin 2011) and ground squirrel . In contrast, the deep cervical artery in the Syrian hamster was removed from the dorsal scapular artery by a common trunk.

Super cial cervical artery
The super cial cervical artery in the Syrian hamster originated separately from the subclavian artery, However, the super cial cervical artery, together with the deep cervical and suprascapular arteries, emerge from a short common trunk from the subclavian artery in the red squirrel (Aydin 2011) and ground squirrel ). In addition, the right super cial cervical artery originates from the external thoracic artery by a common trunk from the right subclavian artery in the mole rat (Aydin et al. 2013).
In porcupine (Atalar et al. 2003), the exact origin of the super cial cervical artery is not documented. Consequently, the super cial cervical artery independently originates from the subclavian artery in rodents except in squirrels and mole rats. However, the bronchoesophageal artery in the Syrian hamster was usually detached either from the supreme intercostal artery in 50% of cases or from the internal thoracic artery in 50% of cases. On the other hand, the bronchoesophageal artery in the rat is detached from the internal thoracic artery (Hebel and Stromberg 1976) or from the thoracic aorta (Popesko et al. 1992b). The bronchoesophageal artery may also arise from the costocervical trunk (most frequently), right subclavian artery, or the internal thoracic artery in the guinea pig (Kabak and Hazriroglu 2003). Thus, the general origin of the bronchoesophageal artery exhibited signi cant differences between rodents and rabbits.

Internal thoracic artery
The internal thoracic artery in the Syrian hamster usually originates from a common trunk with the supreme intercostal artery from the subclavian artery, similar to that reported in rabbits (Angell-James 1974), red squirrels (Aydin 2011), and ground squirrels ). However, the right internal thoracic artery together with the deep cervical artery and costocervical trunk may arise from a common trunk from the right subclavian artery, or the left internal thoracic artery originates from the costocervical trunk by a common trunk from the left subclavian artery in the mole rat (Aydin et al. 2013).
On the other hand, the internal thoracic artery arises independently from the subclavian artery in various  (Popesko et al. 2011). In this study, the coscervical trunk was the rst branch arising from the subclavian artery.
The super cial cervical artery in the Syrian hamster was the last branch, usually arising from the dorsal surface of the subclavian artery, similar to that seen in all reported rodents and rabbits.

Conclusions
The following conclusions were reached: (1) Intraspeci c variations were noted in the presence and composition of the costocervical trunk, the origin of the bronchoesophageal artery, and the formation of a common trunk by the internal thoracic artery and supreme intercostal between the right and left subclavian arteries in the Syrian hamster. (2) The origins of the bronchoesophageal and internal thoracic arteries and the composition of the costocervical trunk in the Syrian hamster were different from those of the previously reported rodents and rabbits. (3) The origin of the deep cervical and supreme intercostal arteries in the Syrian hamster was very similar to that in the guinea pig, rat, and rabbit but was different from that of the reported rodents. (4) The origin of the vertebral artery was extremely consistent among rodents and rabbits except in the porcupine. (6) The origin of the dorsal scapular artery in the Syrian hamster was similar to that in the guinea pig and rabbit but was different from that of the reported rodents. (7) The origin of the super cial cervical artery in the Syrian hamster was similar to that in the guinea pig, rat, rabbit, chinchilla, and gerbil but was different from that in the reported rodents. (8) The typical pattern of branching of the subclavian arteries in the Syrian hamster was similar to that in the guinea pig, rat, and rabbit but was different from that of the reported rodents regardless of the origin of the bronchoesophageal and internal thoracic arteries as well as the composition of the costocervical trunk.