Considerations on the origin of the inferior thyroid artery emerging from the subclavian artery determined by CT examination

The specialized literature has a low degree of information regarding the origin of the inferior thyroid artery (ITA). Our study was performed on computed tomography angiographies (CTAs), and the following aspects were observed: the origin of the ITA from the subclavian artery (SCA) or thyrocervical trunk (TCT), taking note of the distance of the origin of the ITA in relation to the origin of the SCA or the corresponding TCT, as well as the origin of the ITA, comparing right to left and according to gender. Our study was realized on a total of 108 ITA (64 on the right side and 44 on the left, with 48 in male subjects and 60 in females), analyzed on CTA. From the 108 arteries, we found the origin of ITA directly from the SCA in 31.48% of cases, and in 68.52% from the TCT. The distance between the origin of the right SCA and the origin of the corresponding ITA, was between 29.1 and 53.1 mm, while on the left side, the same distance was between 43.7 and 68.1 mm. The distance between the right TCT and the origin of the right SCA, was between 22.5 and 75.0 mm, and for the left side, it’s between 48.7 and 56.8 mm. The inferior thyroid artery is one of the arteries most susceptible to variations in terms of origin and size. With differences between the two sides (right and left), as well as differences related to gender.


Introduction
The specialized literature has very few studies on the origin of ITA based on the use of CT angiography. The inferior thyroid artery can have its origin in the subclavian artery, in two forms: directly from SCA or from a thyrocervical trunk, with several variants.
From the trunk can emerge four terminal arterial branches: the inferior thyroid artery, the ascending cervical artery, the anterior transverse of the neck, and the suprascapular artery.
It is called Farabeuf's thyrobicervicoscapular trunk, or Henle's thyrocervical trunk, giving rise to the inferior thyroid artery, ascending cervical artery, and anterior transverse of the neck [7,16], or the inferior thyroid artery, cervical ascending artery, and suprascapular artery.
ITA is the most medial branch of the trunk, with a significant caliber, it goes vertically and superiorly until it reaches the spinous process of the C 6 vertebra, at a distance of 1-1.5 cm from the anterior tubercle of its transverse process (Chassaignac tubercle). After Paturet [9], it arises from the superior surface of the SCA, at the level of its prescalenic portion according to several authors [3,9,13], anteriorly and laterally of the vertebral artery, near or even at the origin of the internal thoracic artery according to Testut [16].
According to Lippert, ITA can be absent in 3% of cases, being supplied by the superior thyroid artery. Lippert also found that ITA has its origin medially from the anterior scalene muscle in 95% of cases. [7] The artery describes near the origin the first curvature with its convexity superiorly, placing the artery infero-medially, afterward it straightens after it describes a second curvature with its convexity inferiorly, which makes the artery go medially, coming in rapport with the trachea. Frequently, at the level of the middle cervical ganglion, the artery crosses the cervical sympathetic chain which forms a nervous surrounding around the artery [3,9].

Material and methods
Our study was realized on a number of 108 inferior thyroid arteries (64 on the right side and 44 on the left; 48 on male subjects and 60 on female subjects) analyzed on angiographies by computed tomography (CTA) made on a LightSpeed VCT64 Slice CT General Electric installation. The study has the accord of the local Ethics Commission (34490/08.08.2019) within the institution of "Sf. Apostol Andrei" Clinical County Emergency Hospital from Constanța and respects the principles of the General Regulation on Personal Data Protection (EU) 679/2016. The research was conducted in accordance with the Helsinki Declaration and in compliance with all relevant national regulations regarding patient studies. Also, informed consent was obtained from the patients.
The origin of the ITA from the SCA or TCT was examined, taking note of the distance of the origin of the ITA or the corresponding TCT in relation to the origin of the SCA, as well as the origin of the ITA, comparing right to left and according to gender.

Study population
The CTA examinations were retrospectively evaluated. Our study was done on the Romanian Caucasian population, on a number of 108 inferior thyroid arteries (64 on the right side and 44 on the left; 48 on male subjects and 60 on female subjects).
The inclusion criterion in the study was disease-free inferior thyroid arteries, while patients after neck surgery and with atherosclerosis or with ima arteries were excluded.
The mean ages of the males and females were 66.5 ± 17.5 and 51.5 ± 30.5 years, respectively.

CTA imaging protocol
CTA examinations were performed with a 128-slice CT scanner (Revolution EVO, General Electric, Boston, Massachusetts, United States of America). Between seventy and ninety milliliters of nonionic contrast were administered using the bolus tracking technique. Scanning was initiated when the contrast attenuation in the aortic arch reached 100-120 Hounsfield units with a tube voltage of 120 kVp and slice thickness of 0.625 mm. 3D volume rendering (VR) images and curved planar reformats were made from the axial images. Scanning was performed from the aortic arch to the vertex.

Results
Of the 108 arteries, the ITA originating directly from the SCA was found in 34 cases (31.48%), 20 cases were on the right side (31.25% of the right arteries) and 14 cases were on the left side (31.82% of left arteries). In the other 74 cases (68.52%), the origin of ITA was from the TCT, 44 of the cases being on the right side (68.75% of right arteries) and 30 cases on the left side (68.18% of left arteries.). In the male gender, from the 48 cases, ITA had its origin directly from the SCA in 18 of the cases (37.50% of male cases), 10 cases were found on the right side (55.56% of right arteries), and 8 on the left side (44.44% of left arteries). In 30 male cases (62.5% of cases), ITA had its origin in the TCT, 16 cases on the right (53.33% of cases), and 14 on the left (63.64% of cases).
For the female gender, in 60 cases, ITA had its origin directly from the SCA in 16 cases (25.67% of female cases), 10 cases on the right (62.50% of cases), and 6 cases on the left (37.50% of cases). In the female gender, from 44 cases (73.33% of cases), ITA had its origin from the TCT, 28 cases on the right side (63.64% of cases), and 16 cases on the left side (25.67% of cases) ( Table 1).
The distance between the origin of the SCA and the origin of the ITA was monitored in a number of 34 cases (31.48% of cases), 20 on the right side (58.82% of cases) and 14 on the left side (41.18%), 18 cases in the male gender (52.94% of cases) and 16 in the female gender (41.06% of cases). The distance between the origin of SCA and the origin of the right ITA emerging from the corresponding SCA, in a total of 20 cases (58.82% of cases), we found it between 29.1 and 53.1 mm. In the male gender, in 10 cases it was between 29.1 and 53.1 mm (Fig. 1), while for the female gender, also in 10 cases, was between 31.8 and 46.9 mm (Fig. 2).
For the left side, the same measurement, on 14 cases (51.18% of cases), the distance was between 43.7 and 68.1 mm. For the male subjects, in 8 cases (57.14% of cases), this distance was between 51.5 and 68.1 mm (Fig. 3), while for the female subjects, in 6 cases (42.86% of cases), it was between 31.8 and 59.3 mm (Fig. 4).

Fig. 1
Distance between the right inferior thyroid artery at its origin, emerging directly from the subclavian artery, and the origin of the subclavian artery, in a male subject Fig. 2 Distance between the right inferior thyroid artery at its origin, emerging directly from the subclavian artery, and the origin of the subclavian artery, in a female subject  The distance between the origin of the right TCT and the origin of the corresponding right SCA, in a total of 44 cases (59.46% of cases), was found to be between 22.5 and 75.0 mm. In the male gender, in 16 cases (37.84% of cases) it was between 28.1 and 75.0 mm (Fig. 5), while for the female gender, in 28 of cases (63.64% of cases), it was between 22.5 and 52.2 mm (Fig. 6).
For the left side, in 30 cases (40.54% of cases), the distance was between 48.7 and 56.8 mm. In the male gender in 14 cases (46.67% of cases), this distance was between 51.1 and 56.83 mm (Fig. 7), while in the female gender, in 16 cases (53.33% of cases) it was between 48.7 and 56.8 mm (Fig. 8).

Discussions
In our study, the ITA was present in all the explored cases, Paturet [9] affirms that it can be absent sometimes on one side, and Lippert [7] states that in 3% of the cases it was missing. Chandrakala [4] didn't find it in 3.75% on the right side of the examined cases and in 6.25% on the left side. Bergman [2] found it missing in 8.43% of cases while Sherman [14] didn't find it in 1-6% of the cases. Several authors [3,4,13,16] mention the possibility of the ITA originating directly from the SCA ( Table 2).
For the distance between the origin of the ITA and the origin of the SCA Chandrakala [4] states an average of 15.9 mm, this measurement being smaller than the one in our study with 14.1-38.1 mm for the male gender and with 16.8-31.9 mm for the female gender. The distance between the origin of the TCT and the origin of the SCA, compared to Chandrakala [4], in our study had a higher value with   From the studied literature, only Esen [5] realized his study on CTA, the other authors got their results from cadavers. Comparing the results, we obtained and the ones from the literature we consulted we found differences, sometimes significant ones, regarding the origin of the ITA from the TCT or directly from the SCA. Thus, in relation to the results obtained by Lippert [7], we found the origin of ITA from the TCT is in a smaller proportion with 16.48%, and in a higher proportion with 23.48% when the origin is from SCA. Compared to Bergman's [2] results, we found the origin of ITA from the TCT in a smaller percentage by 21.98% and in a bigger percentage by 23.98% when ITA emerged from the SCA. Dasseler [cited by 12] found the origin of ITA in TCT in a percentage of 80.12%, higher than our study with 11.60%, and the origin of ITA from SCA in a percentage of 16.12%, smaller than our study by 15.46%. In relation to the results supplied by Esen [5], we found the origin of ITA from the TCT in a smaller percentage with 26.25% on the right side and 22.12% on the left side, while in the case of ITA originating from SCA we had a higher percentage by 28.45% on the right side and 29.82% on the left side. According to Roshan's [12] results, the origin of ITA from the TCT had a smaller percentage by 27.25% on the right side and 31.72% on the left side, while the origin of the ITA from the SCA had a higher percentage by 27.25% on the right side and 31.82% on the left.
Compared to Rimi [10], the origin of ITA from TCT found by us is in a smaller proportion by 18.25% on the right and 22.02% on the left side, while the origin of the ITA from the SCA was in a higher ratio compared to our findings by 18.25% on the right and 22.02% on the left side. According to Graves's [6] results, the origin of the ITA from the TCT was in a smaller number of the total quantity of cases by 14.34%, on the right it was by 11.25%, while on the left side it was by 17.52%. The origin of the ITA from the SCA on the total number of cases was higher in our study than Graves [6] by 21.48%, on the right with 18.05% and 29.62% on the left side.
At Adachi [cited by 6] the origin of the ITA from TCT was in a higher number of cases by 25.98%, on the right it was greater by 23.55%, while on the left it was smaller by 28.72%. In all our cases, the origin of the ITA from the  SCA in total was bigger with 26.78%, on the right higher by 24.25%, while on the left with 29.62%. Comparing with Toni's [17] results, we found in all our cases the origin of the ITA from the TCT in a smaller percentage by 25.98%, on the right by 23.55% while on the left by 26.62%. In the cases with the ITA origin from SCA, the number found by us was higher than Toni's [17] by 26.28% total with 26.15% on the right side and 29.62% on the left side. Magoma [8] found the origin of the ITA from TCT in a higher percentage than us by 18.98% on the total of cases, on the right by 20.72% and 17.11% on the left side. The ITA with its origin from SCA was found in a smaller ratio, with the same percentages as the previous ones.
Comparing with Rohlich [cited by 8] we found the origin of the ITA from SCA in a higher percentage with 23.28% for the total number of cases, with 24.05% higher on the right, and 25.22% on the left side. Amanuel [1] finds the origin of ITA in all the cases from the TCT.
Assessing the origin of the ITA by comparing right/left, we discovered that between the emergence from the TCT and the SCA there is a difference of 37.04% in favor of the origin from the TCT. Our study's percentage is smaller by 39.96% compared to Lippert [7], with 26.96% compared to Dasseler [cited by 12], 55.96% compared to Bergman [2] and 34.96% compared to Graves [6]. The same percentage considered right/left, we found it higher by 0.86% on the right side, meaning it's smaller by 3.04% compared to Esen [5] and with 7.52% compared to Rohlich [cited by 8]. Although, our percentage is higher by 0.56% compared to Toni's [17]. Rimi [10] and Adachi [cited by 6] found this percentage higher on the left side compared to our study, being higher by 5.54%, respectively 2.64%.
For the ITA originating from TCT, considered right/left, we found a difference of 0.77% in favor of ITA on the right side, being smaller by 0.03% with Rohlich [cited by 8] and by 3.93% compared to Esen [5], but higher with 0.67% compared to Magoma [8]. He also finds this percentage higher on the left side with 4.93%.
For the ITA originating from the SCA, we found a difference of 0.82% in favor of the left SCA, being higher with 0.72% compared to Toni [17] and Magoma [8] and by 0.20% compared to Rohlich [cited by 8]. Esen [5] and Adachi [cited by 6] find this percentage higher on the right side, compared to our study, where it is smaller by 0.02% compared to Esen [5] and by 3.88% compared to Adachi [cited by 6].
In terms of gender, we found that in all the cases with the origin of the ITA from the TCT it was more common in the female gender than the male gender with 10.87%, on the right side it was more frequent in the female gender by 10.11%, while on the left side it was more common in the male gender by 40%. In all the cases with the origin of the ITA from the SCA, it was more common in the male gender by 11.83% compared to the female gender, on the right side it was more frequent at the female gender by 6.94%, while on the left it was more frequent at the male gender by 7.94%.
Graves [6] finds in the total of studied cases that the origin of the ITA from the TCT is smaller by 3.70% for the female gender in relation to the male gender, while the origin of the ITA from the SCA is higher at the female gender by 6.90% compared to the male gender. Takkallapalli [15] found in the total of studied cases that the origin of the ITA from the TCT is smaller by 6.44% in the male gender compared to the female gender, on the right side being with 0.50% smaller. For the origin of the ITA from SCA Takkallapalli [15] finds that on the right side it's smaller in the female gender with 6.50% compared to the male gender, while on the left side it's smaller by 0.50%.

Conclusions
The differences between our personal results obtained from Romanian Caucasian subjects and the existing data in literature would be due to the number of cases worked on, the method used (by dissection or angiography), as well as some geographical characteristics. We found differences in the origin of the ITA comparing right and left, as well as differences in gender. Most often, the extreme values (minimum and maximum) were found in only one case.
The inferior thyroid artery is one of the arteries most susceptible to variations in origin and size, an aspect also reported by Paturet, which is why a detailed knowledge of the anatomy of the thyroid arteries is crucial for the optimal management of patients during surgery in the neck region [9]. Funding None.

Availability of data and materials
The data presented in this study are available upon reasonable request to the corresponding author.

Conflict of interest
The authors declare that they have no conflict of interest.

Ethical approval
The study has the accord of the local Ethics Commission (34490/08.08.2019) within the institution of "Sf. Apostol Andrei" Clinical County Emergency Hospital from Constanța and respects the principles of the General Regulation on Personal Data Protection (EU) 679/2016. The research was conducted in accordance with the Helsinki Declaration and in compliance with all relevant national regulations regarding patient studies. Also, informed consent was obtained from the patients.