INTRODUCTION
Aberrant right subclavian artery (ARSA), also named the arteria lusoria, is an embryologically derived rare variations of aortic arch branching that arises directly from the aortic arch as fourth branch. The reported incidence of ARSA ranges from 0.2% to 1.6% in Japanese [2, 9, 10, 13, 14, 23, 26] and 0.2% to 4.4% of population in other countries [1, 3–5, 7, 11, 12, 15, 19–22, 24, 25, 27, 28]. The retro-oesophageal right subclavian artery (RRSA) is one of the variations of ARSA. RRSA, is an embryological variation that can be detected as the terminal branch of the arch of the aorta passing dorsal to the oesophagus and taking a course toward the right axilla as the usual subclavian artery. The RRSA has been thought to be part of the right dorsal aorta that is normally eliminated by birth. It has been reported that ~80% of ARSA crosses behind the oesophagus [3, 12] as RRSA. Here we report a case of RRSA encountered in student dissection at Kumamoto University School of Medicine during the period from 2018 to 2022. According to previous studies, the general idea about the origin of RRSA is that it develops from the regression of the embryotic fourth aortic arch and a portion of the right dorsal aorta cranial to the seventh intersegmental artery, accompanied with the persistence of the normally regressed segment of the right dorsal aorta caudal to the seventh intersegmental artery. However, the pattern of elimination and persistence of the components of the aortic arch complex is not always the same, showing some inconformity with the influential idea [13]. Thus, the traditional view of the process of RRSA development should be reconsidered based upon detailed observations and analysis of the regional anatomy including branches of RRSA and surrounding structures. Because the incidence of RRSA is very low, it is worth examining how morphological details of the newly found case in the present study can be related to findings in previous observations. Moreover, close observations of this anomaly can give useful knowledge for certain clinical applications such as possible defect of the right recurrent nerve that often accompanies the RRSA and thus requires careful manipulations of cervical structures during surgery.
MATERIALS AND METHODS
The RRSA was found in a donated cadaver of a 62-year-old Japanese male, who had died from kidney cancer, during routine medical student gross anatomy dissection at Kumamoto University School of Medicine. The incidence was 0.7% (1/141 bodies studied from 2018 to 2022). The cadaver was injected with 10% formalin solution from the radial artery by gravity flow and preserved in 30% alcohol. This anomalous case was observed carefully and sketched in detail, and three-dimensional photographs were taken. The protocol for this study did not include any specific issue needed to be approved by Ethics Committee of Kumamoto University Graduate School of Medical Sciences, and the study conformed to the provisions of the Declaration of Helsinki in 1995 (as revised in Fortaleza 2013).
RESULTS
The origin of the RRSA
The RRSA arose from the right side of the most distal part of the arch of the aorta as its fourth branch, following bifurcations of the right common carotid, left common carotid, and left subclavian artery (Figs. 1–6). The RRSA emerged from the arch of the aorta at the level of the third thoracic vertebra. The diameter of the RRSA in its proximal part and that of the left subclavian artery were 2 cm and 1 cm, respectively (Figs. 3, 4). The RRSA was initially directed to the right and upward, passing through the space between the oesophagus and the vertebral column of the level from the second to the third thoracic vertebrae. Thereafter, the RRSA extended to the right side of the oesophagus (Figs. 5, 6). There was no Kommerell diverticulum that was previously described in the proximal part of RRSA [10, 29]. We considered this case as Adachi’s G-type [2].
Branches of the RRSA
The right vertebral artery and the right costocervical trunk were branches of the RRSA in the present case. The right vertebral artery entered the cervical foramen transversarium of the sixth cervical vertebra, whereas the left vertebral artery arising from the left subclavian artery entered the fifth cervical foramen transversarium (Figs. 3, 4). Both of the thyrocervical trunk and the internal thoracic artery branched off from the RRSA just before it passed through the scalene space (Fig. 4). The right dorsal scapular artery branched from the RRSA at the position deep to the scalenus anterior muscle. The artery then passed under the C7 nerve root, became located dorsal to the C5–C6 nerve root (superior trunk of the brachial plexus), and reached the position medial to the border of the levator scapulae and serratus anterior muscles before entering the deep muscle layer (Figs. 2, 4). The suprascapular artery branched from the RRSA in the so-called third part of the subclavian artery at the inferior edge of the first costa (Fig. 2). This artery passed anterior to the C5–C6 nerve root and posterior to a thin branch accompanying the superior trunk, then it entered the suprascapular notch. The RRSA followed the expected path as a right axillary artery.
The highest posterior intercostal artery arising from the thoracic aorta
The suprema intercostal artery branched from the costocervical trunk on both sides and bifurcated into the first and second intercostal arteries. The third and fourth posterior intercostal arteries arose from the thoracic aorta as a common trunk of the highest posterior intercostal artery on both sides (Figs. 3, 4).
The right bronchial artery arising from the thoracic aorta
The bronchial arteries branched from the right anterior part of the thoracic aorta, located distal to the RRSA branching point, at the level of the fourth thoracic vertebra. It then extended toward the anterior hilum of the lung, along with the right main bronchus. Another bronchial artery that was also directed to the hilum of the right lung originated from the caudal common trunk that arose from the anterior surface of the thoracic aorta at the position 3.5 cm distal to the bifurcation of the first bronchial artery. Then, this caudal common trunk bifurcated into two branches (rostral and caudal). The rostral branch further divided into two distal branches, which were directed toward to the hilum of the left lung, taking the course along the ventral and dorsal walls of the left main bronchus. The caudal branch of the common trunk also bifurcated into two distal branches. The rostral bronchial artery that above mentioned extended to the right direction, passing between the left main bronchus and the oesophagus and further along the dorsal wall of the right main bronchus. It finally reached the hilum of the right lung. The other branch descended anteriorly and passed through the oesophageal hiatus. Finally, it connected with a branch of the left gastric artery.
The thoracic duct
The thoracic duct ascended between the thoracic aorta and the azygos vein, passed dorsal to the RRSA and ventral to the left vertebral artery/vein (Figs. 3, 4). Finally, it reached the left venous angle by passing through the usual route between the left common carotid artery and the left subclavian artery.
Non-recurrent laryngeal nerve
The recurrent laryngeal nerve is a branch of the vagus nerve. The right recurrent laryngeal nerve loops under the subclavian artery and supplies to larynx. Non-recurrent laryngeal inferior nerve (NRLN) is a very rare anatomic variation that originates from the vagus nerve and directly provides the branch to the larynx. It has been reported that the NRLN is related to vascular anomalies of the branches of the arch of aorta. The right vagus nerve descended with the right common carotid artery and branched directly into the larynx without recurrence (NRLN) in RRSA [8, 17, 18, 30]. In the normal developmental process, the persistence of right fourth aortic arch leads to the recurrence of the laryngeal nerve of this level. In contrast, the laryngeal branch of the vagus nerve becomes directly connected to the larynx when the right fourth aortic arch disappears in RRSA [8, 17, 18, 30]. In this case, the right vagus nerve branched into the NRLN at the level of the sixth cervical vertebra (Figs. 1, 7). On the left side of the present material, a typical recurrent laryngeal nerve was observed. Our observations are consistent to previous finding and support the hypothesis.
DISCUSSION
This study describes the morphology of the RRSA and its associated structures. Because RRSA is a rare anomaly, accumulation of findings in newly found cases will lead to better understanding of the process of forming RRSA. Previous studies have suggested that the proximal part of the RRSA is the persistent of the distal part of the right dorsal aorta, whereas the fourth aortic arch of the right side, which usually remains in the proximal part of the right subclavian artery, is eliminated during the genesis of the RRSA. However, the fourth right aortic arch persists in some RRSA cases [13]. This variability is associated with the morphological variation of the right vertebral artery in two ways: one is the position of branching from the parent artery and the other is the level of the cervical foramen transversarium to which the right vertebral artery is introduced. In the present case, the right vertebral artery arose from the right subclavian artery and entered the foramen at the sixth cervical vertebra as in usual cases. In the previous study focusing this issue [13], three out of five RRSA cases also showed the same pattern (Case No. 2, 3, 4). In these three cases, both the fourth aortic arch and part of right dorsal aorta cranial to the seventh intersegmental artery are thought to be eliminated during the developmental process, and this is in conformity with the traditional view of the process of RRSA genesis. However, in Case No. 1 and 5 of the same study, the right vertebral artery arose from not RRSA but the right common carotid artery [13]. Moreover, the right vertebral artery entered the foramen at the fourth cervical vertebra in both cases; the foramen of the fifth vertebra was also targeted in Case No. 5. The patterns in these two cases can be interpreted as the result of the persistence of the fourth aortic arch and some cranial portion of the right dorsal aorta, which violates the traditional view. The vasculature morphology in the present case corresponds to the pattern in Case No. 2, 3, 4 mentioned above. The observation in another study also revealed a similar pattern regarding the right vertebral artery arising from the RRSA [23]. Because the number of the bodies analysed is rather small, it is uncertain whether disappearance of the fourth aortic arch, as suggested by the present case, is the dominant form of the RRSA. Judging from the previous observations of multiple cases in which the fourth aortic arch persists, it can at least be said that the theory regarding the mechanism of generating the RRSA needs to be modified to explain heterogeneous vasculature patterns in a consistent manner, which might also give perspective to understand the morphogenesis of aortic arches and related arteries in both normal and variant cases.
Because information about the morphology of bronchial arteries in RRSA is limited in previous studies of RRSA, we concentrated on them in this report. It has been reported that 97% of left bronchial arteries originate from the thoracic aorta, whereas the right posterior intercostal artery supplies 89% of the right bronchial artery [6, 16]. In the study of the RRSA, the right posterior intercostal artery was the origin of the right bronchial artery in four out of five cases, whereas the RRSA was the origin of the right bronchial artery in the remaining one case [13]. It was postulated there that branching of the bronchial artery, which can be the visceral branch of the aorta, from the RRSA is compatible with the traditional view that the most proximal part of the RRSA is derived from the dorsal aorta of the right side. It should be noted here that the origin of the right bronchial artery in the present case was neither the posterior intercostal artery nor the RRSA: the right bronchus was targeted by two branches of the thoracic aorta.
CONCLUSIONS
Our report suggests that there is a variability regarding the vascular pattern in structures surrounding the RRSA that can become the origin of the right bronchial artery. This also suggests the necessity of further study to reconsider the mechanism of RRSA development by accumulating findings in this anomaly in future studies.
Acknowledgments
The authors sincerely thank those who donated their bodies to science so that anatomical research could be performed. Results from such research can potentially increase mankind’s overall knowledge that can then improve patient care. Therefore, these donors and their families deserve our highest gratitude.
We would like to thank Dr. Katsushi Kawai for giving us a lot of advice.
