Bilateral Subclavian Arteries Passing in Front of the Scalenus Anterior

Home , Costocervical trunk, Subclavian artery, Suprascapular artery, Thyrocervical trunk

Anatomical Science International (2007) 82, 180Ð185 doi: 10.1111/j.1447-073x.2006.00162.x

CaseBlackwell Publishing Asia Report Bilateral subclavian arteries passing in front of the scalenus anterior muscles* Mamoru Uemura, Akimichi Takemura and Fumihiko Suwa Department of Anatomy, Osaka Dental University, Osaka, Japan

Abstract Herein, we present a very rare case of bilateral subclavian arteries passing in front of the scalenus anterior muscles in a cadaver. This abnormality was observed in a 73-year-old Japanese male cadaver during a dissection session for students in 2004 at Osaka Dental University. The bilateral scalenus anterior muscle originated from the anterior tubercle of the transverse processes of the fifth and sixth cervical vertebrae and inserted into the scalene tubercle of the first ribs. The right scalenus minimus muscle was observed, but no left scalenus minimus muscle was observed. The aortic arch was a type A according to Adachi’s classification. The origin of the internal thoracic artery was distal to that of the thyrocervical trunk. The bilateral brachial plexuses was formed by the union of the ventral rami from the fifth cervical to the first thoracic nerves and passed between the scalenus anterior and the scalenus medius muscles. To our knowledge, such a case has not been reported previously. Key words: abnormalities, gross anatomy, scalenus anterior muscle, scalenus minimus muscle, subclavian artery.

Introduction acute cardiac insufficiency. The length and diameter of the blood vessels and size of the muscles were Herein, we present for the first time a very rare case measured with calipers. We investigated the incidence of bilateral subclavian arteries passing in front of the of this case in 318 cadavers (636 sides) studied in scalenus anterior muscles in a cadaver; this was dis- dissection sessions for students at our facilities in covered during a dissection session for students in the period 1994–2004. 2004 at Osaka Dental University. There are few reports The protocol for the present research did not include of the abnormalities concerning the course of the any specific issue that needed to be approved by subclavian artery. To our knowledge, no case of bilateral the ethics committees of our institutions. The present subclavian arteries passing in front of the scalenus work conformed to the provisions of the Declaration anterior muscles has been reported. Adachi (1928) of Helsinki in 1995 (as revised in Edinburgh 2000). and seven others (Mori, 1941; Komatsu et al., 1984; Inuzuka, 1989; Takafuji & Sato, 1991; Okamoto et al., Results 1997; Kodama, 2000; Yuda et al., 2000) have reported 14 cases of a unilateral subclavian artery passing in Right side front of the scalenus anterior muscle. Right subclavian artery Case Report The brachiocephalic trunk (16.2 mm in diameter) bifurcated into the right subclavian artery (12.0 mm The present case was observed in a 73-year-old in diameter) and the right common carotid artery Japanese male cadaver. The cause of death was an (8.1 mm in diameter). The right subclavian artery arose from the brachiocephalic trunk at a level with the middle of the third thoracic vertebra, ran super- *This study was presented at the 110th Annual Meeting of olaterally and sequentially branched first into the the Japanese Association of Anatomists (Toyama, Japan) right vertebral artery (4.0 mm in diameter), the right 29–31 March 2005. costocervical trunk (2.0 mm in diameter) and the Correspondence: Mamoru Uemura, Department of Anatomy, Osaka Dental University, 8-1 Kuzuhahanazono-cho, right thyrocervical trunk (3.2 mm in diameter) supe- Hirakata-shi, Osaka 573-1121, Japan. riorly, and then into the right internal thoracic artery Email: [email protected] (3.0 mm in diameter) inferiorly. In addition, the artery Received 6 June 2006; accepted 20 July 2006. passed in front of the right scalenus anterior muscle © 2006 Japanese Association of Anatomists and behind the right subclavian vein, and shifted Subclavian A. & scalenus anterior M. 181

Figure 1. Photograph (a) and schematic illustration (b) showing the anterior view of the subclavian arteries (su) and the scalenus anterior muscles (SA). aa, aortic arch; ac, ascending cervical artery; av, axillary vein; ax, axillary artery; bc, brachiocephalic trunk; br, brachial plexus; cc, common carotid artery; bv, brachiocephalic vein; co, costocervical trunk; C5–8, the fifth–eighth cervical nerves; CV4–7, vertebral body of the fourth–seventh cervical vertebrae; ds, descending scapular artery; E, esophagus; ij, internal jugular vein; it, internal thoracic artery; L, lung; LC, longus colli muscle; LO, longus capitis muscle; lt, lower trunk of the brachial plexus; mt, medial trunk of the brachial plexus; ph, phrenic nerve; R, first rib; S, scalenus minimus muscle; SM, scalenus medius muscle; SP, scalenus posterior muscle; sc, superficial cervical artery; ss, suprascapular artery; sv, subclavian vein; T, trachea; T1, the first thoratcic nerve; TV1, vertebral body of the first thoracic vertebra; tc, transverse cervical artery; ty, thyrocervical trunk; ut, upper trunk of the brachial plexus; va, vagus nerve; vc, superior vena cava; ve, vertebral artery; asterisk, diverticulum. towards the right axillary artery (8.0 mm in diameter) right scalenus anterior muscle. It originated from the at the lateral margin of the right first rib. The right anterior tubercle of the transverse process of the axillary artery passed between the seventh cervical seventh cervical vertebra and inserted into the right nerve (C7) and C8 of the brachial plexus. first rib at the posterior region of the scalenus anterior The right vertebral artery entered the transverse muscle tail. It was innervated by C8 (Figs 1,2). foramen of the sixth cervical vertebra. The right costocervical trunk bifurcated into the right deep cervical Right brachial plexus (1.8 mm in diameter) and the right supreme intercostal The right brachial plexus was formed by the union arteries (1.9 mm in diameter). The right thyrocervical of the ventral rami from C5 to the first thoracic nerve trunk sequentially branched into the right descending (Th1). The upper (C5 and C6), middle (C7) and lower scapular (2.0 mm in diameter), the right superficial trunks (C8 and Th1) passed between the scalenus cervical (2.0 mm in diameter), the right ascending anterior and the scalenus medius muscles and cervical (2.2 mm in diameter) and the right inferior towards the axillary fossa and the humerus. No thyroid (2.0 mm in diameter) arteries. The right abnormalities were found in the trunks (upper, suprascapular artery (2.0 mm in diameter) arose from middle and lower) or the cords (medial, lateral and the right axillary artery (Figs 1,2). posterior; Figs 1,2).

Right scalenus anterior muscle and the scalenus Left side minimus muscle The right scalenus anterior muscle (length 71.7 mm; Left subclavian artery width of muscle head 7.7 mm; width of muscle belly The left subclavian artery (18.6 mm in diameter at 11.4 mm; width of muscle tail 8.4 mm) originated the region where it branches from the aortic arch) from the anterior tubercle of the transverse processes arose superolaterally from the superior wall of the of the ﬁfth and sixth cervical vertebrae and inserted aortic arch. A diverticulum was found near its origin. into the scalene tubercle of the right ﬁrst rib. The This artery sequentially branched into the left vertebral muscle was innervated by C6 and C7. artery (4.0 mm in diameter), the left costocervical The right scalenus minimus muscle (length trunk (2.0 mm in diameter) and the left thyrocervical 42.5 mm; width of muscle head 8.6 mm; width of trunk (4.0 mm in diameter) superiorly and the left muscle belly 7.2 mm; width of muscle tail 5.0 mm) internal thoracic artery (3.4 mm in diameter) inferiorly. was observed to be located posterolaterally to the In addition, the artery passed in front of the left

Figure 2. Photograph (a) and schematic illustration (b) showing the anteroinferolateral view of the right subclavian artery (su) and the right scalenus anterior muscle (SA). aa, aortic arch; ac, ascending cervical artery; av, axillary vein; ax, axillary artery; bc, brachiocephalic trunk; br, brachial plexus; cc, common carotid artery; bv, brachiocephalic vein; co, costocervical trunk; C5–8, the fifth–eighth cervical nerves; CV4–7, vertebral body of the fourth–seventh cervical vertebrae; ds, descending scapular artery; E, esophagus; ij, internal jugular vein; it, internal thoracic artery; L, lung; LC, longus colli muscle; LO, longus capitis muscle; lt, lower trunk of the brachial plexus; mt, medial trunk of the brachial plexus; ph, phrenic nerve; R, first rib; S, scalenus minimus muscle; SM, scalenus medius muscle; SP, scalenus posterior muscle; sc, superficial cervical artery; ss, suprascapular artery; sv, subclavian vein; T, trachea; T1, the first thoratcic nerve; TV1, vertebral body of the first thoracic vertebra; tc, transverse cervical artery; ty, thyrocervical trunk; ut, upper trunk of the brachial plexus; va, vagus nerve; vc, superior vena cava; ve, vertebral artery; asterisk, diverticulum.

scalenus anterior muscle and behind the subclavian vical (2.1 mm in diameter) and the left inferior thyroid vein and shifted towards the left axillary artery (1.7 mm in diameter) arteries. The left suprascapular (7.4 mm in diameter) at the lateral margin of the artery (2.0 mm in diameter) arose from the left axillary left first rib. The left axillary artery ran in front of artery (Figs 1,3). the left brachial plexus without passing through the plexus. Left scalenus anterior muscle The left vertebral artery entered the transverse The left scalenus anterior muscle (length 76.6 mm; foramen of the sixth cervical vertebra. The left cos- width of muscle head 12.0 mm; width of muscle belly tocervical trunk bifurcated into the left deep cervical 8.5 mm; width of muscle tail 13.0 mm) originated (1.8 mm in diameter) and the left supreme intercostal from the anterior tubercle of transverse processes of arteries (2.0 mm in diameter). The left thyrocervical the fifth and sixth cervical vertebrae and inserted into trunk sequentially branched into the descending the scalene tubercle of the left first rib. It was inner- scapular (2.0 mm in diameter), the left superficial vated by C6 and C7. No left scalenus minimus mus- cervical (1.7 mm in diameter), the left ascending cer- cle was observed (Figs 1,3).

Figure 3. Photograph (a) and schematic illustration (b) showing the anteroinferolateral view of the left subclavian artery (su) and the left scalenus anterior muscle (SA). aa, aortic arch; ac, ascending cervical artery; av, axillary vein; ax, axillary artery; bc, brachiocephalic trunk; br, brachial plexus; cc, common carotid artery; bv, brachiocephalic vein; co, costocervical trunk; C5–8, the fifth–eighth cervical nerves; CV4–7, vertebral body of the fourth–seventh cervical vertebrae; ds, descending scapular artery; E, esophagus; ij, internal jugular vein; it, internal thoracic artery; L, lung; LC, longus colli muscle; LO, longus capitis muscle; lt, lower trunk of the brachial plexus; mt, medial trunk of the brachial plexus; ph, phrenic nerve; R, first rib; S, scalenus minimus muscle; SM, scalenus medius muscle; SP, scalenus posterior muscle; sc, superficial cervical artery; ss, suprascapular artery; sv, subclavian vein; T, trachea; T1, the first thoratcic nerve; TV1, vertebral body of the first thoracic vertebra; tc, transverse cervical artery; ty, thyrocervical trunk; ut, upper trunk of the brachial plexus; va, vagus nerve; vc, superior vena cava; ve, vertebral artery; asterisk, diverticulum.

Left brachial plexus aortic arch, which was a type A according to the In the left brachial plexus, the same findings were classification of Adachi (1928; Figs 1–3). observed as those on the right side (Figs 1,3). Other findings Discussion The bilateral phrenic nerves originated from C4 and Our discussion of the cases in which the subclavian C5, crossed in front of the scalenus anterior muscle, artery passes in front of the scalenus anterior muscle passed between the subclavian artery and the sub- includes the following sections: reports on and the clavian vein, and then entered into the mediastinum. incidence of the abnormality, the developmental These nerves innervated the diaphragm. The forma- mechanism and the branches of the subclavian artery. tion of the first bilateral ribs was normal. No abnor- Reports on and the incidence of this abnormality malities were observed in the thoracic duct, the right lymphatic duct or the bilateral vagus nerves. The Previous studies have reported 14 cases (two cases brachiocephalic trunk, the left common carotid artery were reported in fetuses) of the subclavian artery and the left subclavian artery arose directly from the passing in front of the scalenus anterior muscle

Table 1. Previous reports of the subclavian artery passing in front of the scalenus anterior muscle

Reference Age Sex Side Position

Unilateral side Adachi (1928) 60 years Female Left * Adachi (1928) 53 years Male Left * Mori (1941) 6 months (fetus) Male Left * Mori (1941) 8 months (fetus) Male Left * Komatsu et al. (1984) 73 years Female Left * Komatsu et al. (1984) 44 years Male Right * Inuzuka (1989) 95 years Female Left C8–Th1 Takafuji and Sato (1991) 79 years Male Left * Okamoto et al. (1997) * * Left * Okamoto et al. (1997) * * Right * Kodama (2000) * * * C7–C8 Kodama (2000) * * * C8–Th1 Kodama (2000) * * * C8–Th1 Yuda et al. (2000) 92 years Female Left * Bilateral sides Present study 73 years Male Right C7–C8 Left **

The position refers to the level of the axillary artery passing through the brachial plexus (*not reported; **the axillary artery ran in front of the left brachial plexus without passing through the plexus).

(Adachi, 1928; Mori, 1941; Komatsu et al., 1984; Table 2. Incidence of the subclavian artery passing in front of Inuzuka, 1989; Takafuji & Sato, 1991; Okamoto et al., the scalenus anterior muscle 1997; Kodama, 2000; Yuda et al., 2000; Table 1). All Incidence Adult these cases reported this abnormality occuring unilat- Reference (cases/total) or fetus erally. In the present study, we report this abnormality ± occurring on bilateral sides of the body for the first Adachi (1928) 0.6 0.4% (2/328) Adult Mori (1941) 1.7 ± 1.2% (2/116) Fetus time. No such reports have been published previously. Takafuji and Sato (1991) 0.7% (1/144) Adult During the course of our investigation, 318 cadavers Kodama (2000) 0.7% (3/428) Adult (636 sides) were studied in dissection sessions for Yuda et al. (2000) 0.2 ± 0.5% (1/482) Adult students (1994–2004); the incidence ratio was found Present study 0.3% (2/636) Adult to be only 0.3%. We investigated 14 cases in which this abnormality was observed on one side only (either the right or the left side; three uncertain cases were excluded). The incidence of this abnormality on in these reports were divided into three groups as the left side was 81.8% (nine of 11 cases), whereas follows: (i) abnormality of the scalenus anterior muscle; on the right side it was 18.2% (two of 11 cases). (ii) abnormality of the brachial plexus and the interseg- That is, the incidence of this abnormality was greater mental artery; and (iii) abnormality of the scalenus on the left side than on the right side. anterior muscle, the brachial plexus and the first rib. We investigated 14 cases each of males or females (five uncertain cases were excluded). The incidence Abnormality of the scalenus anterior muscle in males was 55.6% (five of nine cases), whereas in Adachi (1928) and Mori (1941) suggested that pass- females it was 44.4% (four of nine cases); there was ing of the subclavian artery in front of the scalenus little difference in the incidence of this abnormality anterior muscle was due to the abnormality of this between the sexes. muscle. Komatsu et al. (1984) and Yuda et al. (2000) The incidence of the unilateral subclavian artery suggested that this was caused by the dorsal shift passing in front of the scalenus anterior muscle has of the region to which the scalenus anterior muscle been reported to be less than 0.7% in adults (Table 2). was inserted. Komatsu et al. (1984) reported two such cases in Developmental mechanism the unilateral side and compared the abnormal sides The previous reports (14 cases) discussed the devel- with the normal sides on the region to which the opmental mechanism of the subclavian artery passing scalenus anterior muscle was inserted. They reported in front of the scalenus anterior muscle. The hypotheses that this region had shifted dorsally. We could not

© 2006 Japanese Association of Anatomists Subclavian A. & scalenus anterior M. 185 observe a dorsal shift of this region in the present The brachial plexus did not shift downward from case, because the bilateral subclavian arteries the trunks. Therefore, we concluded that the sug- passed in front of the scalenus anterior muscles. gestion of Okamoto et al. (1997) was not relevant for Takafuji and Sato (1991) suggested that the mech- the present case. anism of the abnormality was caused by the disap- Branches of the subclavian artery pearance of the primordium of the scalenus anterior muscle and the remain of the primordium of the According to anatomical textbooks (Hirasawa & scalenus minimus muscle. Therefore, the subclavian Okamoto, 1982), the branches of the subclavian artery artery passed in front of the scalenus muscle (devel- are the vertebral artery, the internal thoracic artery, oping scalenus minimus muscle). In the present the thyrocervical trunk and the costocervical trunk, case, we were able to observe the scalenus anterior, sequentially. medius, posterior and minimus muscles in the right In six of 14 cases, the features of the branching side. Therefore, we concluded that the suggestion of of the subclavian artery were reported by Adachi Takafuji and Sato (1991) was not applicable. (1928), Komatsu et al. (1984), Inuzuka (1989), and Yuda et al. (2000). They observed that the internal thoracic Abnormality of the brachial plexus and the artery arose from the subclavian artery and the origin intersegmental artery of the internal thoracic artery was distal to that of In four of 14 cases, a positional relationship between the thyrocervical trunk. In the present case, we the axillary artery and the brachial plexus was reported observed the same features. Therefore, we thought by Inuzuka (1989) and Kodama (2000; Table 1). that these features were specific to the case of the In the present case, it was observed that in the subclavian artery passing in front of the scalenus left side the axillary artery ran in front of the brachial anterior muscle. plexus without passing through the plexus (type C A more detailed investigation of the features of the according to Adachi’s (1928) classification). To our branching of the subclavian artery is necessary to knowledge, this phenomenon has never been reported gather evidence that would clarify the developmental previously. Inuzuka (1989) suggested that this was mechanism. caused by the dorsal shift of the region to which the scalenus anterior muscle was inserted and an abnor- References mality of the intersegmental artery. Kodama (2000) hypothesized that this was caused by the abnormal Adachi B (1928) Das Arteriensystem der Japaner, Bd 1. course of the subclavian artery. In two of three cases Kenkyusha, Tokyo (in German). reported by Kodama (2000), this abnormality was Hirasawa K, Okamoto M (1982) Artery. In: Anatomy 2 Angiology thought to be attributed to an inferior shift of the and Neurology. Kanehara Shuppan, Tokyo, 43–54 (in Japanese). remaining intersegmental artery, because the axillary Inuzuka N (1989) A case of the scalenus anterior muscle artery passed between C8 and Th1 of the brachial passing behind the left subclavian artery. Okajimas Folia plexus. In the third case reported by Kodama (2000), Anat Jpn 66, 229–40. and as was observed in the right side of the body Kodama K (2000) Artery. In: Anatomic Variations in Japanese in the present case, the axillary artery passed between (Sato T, Akita K, eds). University of Tokyo Press, Tokyo, 211– 24 (in Japanese). C7 and C8 of the brachial plexus as it does normally. Komatsu S, Handa Y, Ichie M, Naito A, Shimada Y, Shimizu Y We suggest that this abnormality is unrelated to the (1984) Two cases of the anterior scalenus muscle passing position of the remaining intersegmental artery and behind the subclavian artery. Acta Anat Nippon 59, 421 the brachial plexus. (Abstract; in Japanese). Mori Y (1941) Über die A. subclavia und ihre Äste bei japanischen Abnormality of the scalenus anterior muscle, the Feten. Acta Anat Nippon 17, 229–55 (in Japanese with a brachial plexus and the first rib German abstract). Okamoto et al. (1997), who reported two cases, Okamoto K, Wakebe T, Saeki K, Nagashima S (1997) A case of advocated that this abnormality was caused by a the subclavian artery passing in front of the scalenus anterior shift in the position of the region to which the scale- muscle. Acta Anat Nippon 72, 559 (Abstract; in Japanese). nus anterior muscle was inserted, the inferior shift of Takafuji T, Sato Y (1991) Study on the subclavian artery and its branches in Japanese adults. Okajimas Folia Anat Jpn 68, the root composition of brachial plexuses to the lower 171–86. side and aplasia of the first rib. Yuda K, Kodama J, Nakamura T, Nagato T, Yanagisako M, Toh In the present case, the root composition of bilateral H (2000) A case of the left subclavian artery passing in front brachial plexuses was C5–Th1, which was normal. of the scalenus anterior muscle. J Fukuoka Dent Coll 27, The bilateral first ribs did not have aplasia. 113–17 (in Japanese).