Marked lateral deviation of the phrenic nerve due to variant origin and course of the thyrocervical trunk: a cadaveric study

The right SCA originated at the point of 19.7 mm from the origin of the brachiocephalic artery, and at the first portion ramified the vertebral artery (37.2 mm from the origin of the SCA, with a 4.1 mm diameter) and the IFTA (39.2 mm from the origin of the SCA, with a 2.6 mm diameter) (Fig. 1). At the second portion ramified the costocervical artery (41.6 mm from the origin of the SCA, with a 3.0 mm diameter) and at the third portion ramified the TCT cranially (64.6 mm from the origin of the SCA, with a 4.8 mm diameter) and the ITA caudally (74.2 mm from the origin of the SCA, with a 3.2 mm diameter) (Figs. 1, 2). The right TCT ramified trifurcated for the suprascapular artery (4.7 mm from the origin of the TCT, with a 2.1 mm diameter), transverse cervical artery (6.1 mm from the origin of the TCT, with a 3.4 mm diameter) and ascending cervical artery (10.3 mm from the origin of the TCT, with a 1.4 mm diameter) (Fig. 2). The right PN arose independently from the fourth cervical nerve and descended passing the lateral side of the TCT toward the thorax. Therefore, the PN was pulled obviously laterally by the TCT. After passing the outside of the TCT, the nerve was bent at an angle of 60° and inserted to the thorax (Figs. 1, 2). The right ASM originated from the anterior tubercles of C5 and C6 and inserted to the first rib (61.9 mm laterally from the axis of the sternum). The diameter of the insertion was 15.6 mm and the thickness was 3.0 mm. The right lung collapsed with a pleural effusion because of some unknown reasons. Therefore, we could not observe the diaphragmatic elevation, which is one of the common symptoms of the diaphragm paralysis. The thickness of the diaphragm was 1.5 mm examined at 30 mm from the origin of the sternum: it was thinner than the left side (2.7 mm) measured at the symmetric point.

The left SCA arose directly from the aortic arch. At the first portion ramified the vertebral artery (42.6 mm from the origin of the SCA, with a 11.2 mm diameter) and the TCT (47.5 mm from the origin of the SCA, with a 7.1 mm diameter) (Fig. 1). At the second portion ramified the costocervical artery (74.1 mm from the origin of the SCA). At the third portion, there were no arteries from the SCA. The left TCT ramified into three branches, the IFTA (4.4 mm from the origin of the TCT, with a 3.9 mm diameter), the ITA (5.2 mm from the origin of the TCT, with a 3.1 mm diameter), the common trunk of the transverse cervical artery and suprascapular artery (8.2 mm from the origin of the TCT, with a 2.2 mm diameter) and the ascending cervical artery (21.9 mm from the TCT, with a 1.6 mm diameter) (Fig. 1). The left PN arose from C3 to C5 and descended passing the lateral side of the TCT. The left ASM originated from the anterior tubercles of C3 to C6 and was inserted in the first rib (58.3 mm laterally from the axis of the sternum). The diameter of the insertion was 17.5 mm and the thickness was 5.6 mm. Many tumors and a plural effusion were observed in this side.

The transverse septum, which is a rudiment of the diaphragm, is located in the front of the third to fourth neck somite in the fourth week of intrauterine life. The transverse septum gradually shifts to the caudal side from the fifth week, and at this time it is accompanied by nerve fibers. As a result, the phrenic nerves originate from the anterior branch of C3–5 [5]. By the beginning of the eighth week, the dorsal part of the diaphragm is located at the level of the first lumbar [8].

In the seventh week of intrauterine life, the entire right SCA is formed from the right fourth aortic arch artery, the short portion of the right dorsal aorta and the right seventh intersegmental artery. On the other hand, the left SCA is formed from the left seventh intersegmental artery [9]. At around the same time, in the cervical region, the dorsal intersegmental arteries of either side are joined by a series of anastomoses to form the longitudinal channels. These longitudinal channels develop the branches of the SCA—the vertebral artery, ITA, supreme intercostal artery, deep cervical artery and ascending cervical artery [5]. The TCT is formed by the fusion of the IFTA, ascending cervical artery, transverse cervical artery and suprascapular artery [10].

From the fifth week, the myotomes rapidly start to develop. The scalene muscle is derived from the hypaxial portions of the cervical myotomes [2]. In the end of the seventh week of intrauterine life, they develop into the primordium of the scalene muscle. After a while, this muscle reaches the surface of the first rib, which develops an insertion point.

In our peculiar case, we speculate that the right anterior scalene muscle was inserted immediately lateral to the IFTA, and therefore the IFTA remained as an independent branch of the SCA, without making the normal TCT with the other arteries. The other three arteries were thought to fuse together as usual to form the TCT outside of the ASM accompanying the PN.

Kaufman et al. reported three patients with diaphragm paralysis caused by the TCA compression of the phrenic nerve. These arteries originated from the TCT in the first portion of the SCA. They named this condition as ‘Red Cross syndrome’. One of the three patients suffered from severe dyspnea when she turned her head to the affected side. Vascular decompression surgery on the patients had good outcomes [6].

In our case, unlike the Kaufman’s report, the root of TCT arising from the third portion of the SCA compressed the PN. We were not able to demonstrate the right PN and diaphragm paralysis. In addition to that, unfortunately, we could not reveal the symptoms during his lifetime. However, based on the change of posture and the movement of the neck and upper limb, the phrenic nerve might be pulled more by the ipsilateral TCT. This might have caused temporary dyspnea similar to Kaufman’s report.

Hamada et al. described that it is necessary to be aware of the supraclavian triangle blow Erb’s point during neck dissection procedures [4]. In the present case, these variations of the arteries and the PN originating and existing more laterally than usual could increase the risk of arterial and nerve puncture during internal jugular or subclavian venous catheter placement, neck surgery and brachial plexus block. The surgeons should check preoperative examinations including imaging tests, such as contrast-enhanced CT and MRI, in order not to damage these arteries and nerves. In addition, the use of an ultrasound-imaging device during such clinical procedures would improve the safety.

In conclusion, we encountered some rare variations, such as the right TCT and ITA originating from the third portion of the SCA and the ipsilateral phrenic nerve having been pulled and displaced laterally by the TCT, in an 88-year-old Japanese male cadaver. We studied these rare variations and considered the embryological and clinical analysis.

At an early stage of embryonic development, the branches of the SCA are formed from the longitudinal channels linking to the cervical intersegmental arteries. It was presumed that during this period, there was interference in the insertion of the ASM, which caused the TCT to displace remarkably laterad than usual. It is quite possible that this caused some episodes of dyspnea. This might have caused temporary dyspnea in this case. Recently many image diagnostic technologies, such as multiple directed computed tomography, have been developed and are often used. However, it is still possible that rare variations, like this case, may be overlooked and can only be recognized by intimate regional examination. These rare variations should be kept in mind due to this study.