Arterial blood supply of the internal neck organs: anatomy, topography, clinical significance in endocrine surgery
https://doi.org/10.14341/serg12720
Abstract
BACKGROUND. Current trends of «fast track surgery» give rise to development of new safe techniques of the thyroid and parathyroid surgery, the purpose of which is to minimize the level of postoperative complications, such as vocal cord palsy, hypoparathyroidism, bleeding. In this regard, it is important for the endocrine surgeon to save «dry operating field», which contributes to the clear visualization of such «thin» structures as the recurrent laryngeal nerve, the external branch of the superior laryngeal nerve and the parathyroid glands. Therefore, the key issue of this surgery is to understand the anatomical and topographic features of the blood supply to the internal neck organs (a complex of neck organs consisting of the thyroid and parathyroid glands, larynx, trachea, esophagus).
AIM. To determine the main sources of arterial blood supply of the internal neck organs and their anatomical, topographic features.
MATERIALS AND METHODS. The computed tomography protocols of cervical branches of brachiocephalic arteries were analysed in the study. The thickness of the reconstructed sections in the axial, frontal and sagittal planes was 0.35±0.05 mm. The fact of blood supply was confirmed by the anatomical close of the arterial structure to the internal organ and the presence of intramural arterial branches.
RESULTS. The course of all cervical branches of the subclavian and common carotid artery was traced among 42 patients. It is noted, that only the inferior, superior thyroid arteries and thyroid ima artery supply internal neck organs with the blood. At the same time, the superior thyroid artery was visualized in all angiograms. However, the inferior thyroid artery was absent in 2.4% of cases. The thyroid ima artery was rarely detected (in 4.8% of patients). In 73.2% of cases, the inferior thyroid artery was detected high at the upper third level of the thyroid lobe and then had a descending course. In 23.2% of cases, the artery was formed at the middle third level of the thyroid lobe and was directed horizontally to the gland. Only in 3.6% of cases, the ascending course was determined in the vessel. The inferior thyroid artery was located on the posterior surface of the thyroid lobe, where it formed glandular branches. On the contrary, the branches of the superior thyroid artery were located mainly along the anterolateral surface of the thyroid gland. The average thickness of the inferior thyroid artery was 2.1±0.5 mm, and the superior thyroid artery was 1.6± 0.7 mm.
CONCLUSION. According to the study, arterial blood supply to the internal neck organs is provided mainly by the inferior and superior thyroid arteries. At the same time, the trunk of the inferior thyroid artery is larger than the superior thyroid artery (p=0.032). The inferior thyroid artery forms branches along the posterior surface of the thyroid lobe and from a topographic point of view it is the main source of blood supply to the parathyroid glands. In most cases, the inferior thyroid artery has a descending course, is directed along the posterior surface of the thyroid gland and forms an X-shaped intersection with the recurrent laryngeal nerve.
About the Authors
A. A. Kuprin
Moscow Regional Research and Clinical Institute (MONIKI);
A.K. Eramishanzev city clinical hospital
Russian Federation
Russian Federation
Aleksandr A. Kuprin, MD, PhD
61/2 Schepkina street, Moscow, 129110
eLibrary SPIN: 7950- 8820
V. Y. Malyuga
Moscow Regional Research and Clinical Institute (MONIKI)
Viktor Y. Malyuga, MD
Moscow
eLibrary SPIN: 1303-6923
E. A. Stepanova
Moscow Regional Research and Clinical Institute (MONIKI)
Elena A. Stepanova, MD, PhD
Moscow
eLibrary SPIN: 5965-8784
References
1. Endokrinnaya khirurgiya: rukovodstvo dlya vrachey. Ed. by Kharnas SS. Moscow: GEOTAR-Media; 2010. (In Russ.)
2. Thyroid-info.ru. [Internet]. Istoriia izucheniia shchitovidnoi zhelezy (In Russ.) Available at: https://thyroid-info.ru/about/istoriya-izucheniya-shchitovidnoy-zhelezy. Accessed 17.08.22.
3. Ross DS, Burch HB, Cooper DS, et al. American Thyroid Association guidelines for diagnosis and management of hyperthyroidism and other causes of thyrotoxicosis. Thyroid. 2016;26(10):1343-1421. doi: https://doi.org/10.1089/thy.2016.0229
4. Bondarenko VO. Vozvratnyy gortannyy nerv v khirurgii shchitovidnoy i parashchitovidnoy zhelez. Moscow: Atlas; 2006. (In Russ.)
5. Chandrasekhar SS, Randolph GW, Seidman MD, et al. Clinical practice guideline: improving voice outcomes after thyroid surgery. Otolaryngol Head Neck Surg. 2013;148(6):S1-S37. doi: https://doi.org/10.1177/0194599813487301
6. Noussios G, Chatzis I, Konstantinidis S, et al. The Anatomical Relationship of Inferior Thyroid Artery and Recurrent Laryngeal Nerve: A Review of the Literature and Its Clinical Importance. J Clin Med Res. 2020;12(10):640-646. doi: https://doi.org/10.14740/jocmr4296
7. Kuprin AA, Malyuga VY, Britvin TA, Abuladze IO. Extralaryngeal branching of the recurrent laryngeal nerve. Autopsy case series. Endocrine surgery. 2020;14(4):4-18. (In Russ.) doi: https://doi.org/10.14341/serg12706
8. Mokrysheva NG, Krupinova JA, Voronkova IA. Parathyroid glands: the normal development, anatomy and histological structure. Endocrine surgery. 2018;12(4):178-187. (In Russ.) doi: https://doi.org/10.14341/serg10039
9. Zhu J, Tian W, Xu Z, et al. Expert consensus statement on parathyroid protection in thyroidectomy. Ann Transl Med. 2015;3(16):230. doi: https://doi.org/10.3978/j.issn.2305-5839.2015.08.20
10. Ostroverkhov GE, Bomash YuM, Lubotskiy DN. Operativnaya khirurgiya i topograficheskaya anatomiya. Uchebnik dlya studentov meditsinskikh vuzov. 5 izdaniye. Moscow: MIA; 2013. (In Russ.)
11. Prives MG, Lysenkov NK, Bushkovich VI. Anatomija cheloveka. Uchebnik dlja studentov medicinskih vuzov. 12 izdanie. Saint Petersburg: SPbMAPO; 2006. (In Russ.)
12. Romanchishen AF, Gostimskiy AV, Karpatskiy IV. Khirurgicheskaya anatomiya kapsuly i fastsial’nogo vlagalishcha shchitovidnoy zhelezy. Meditsina: teoriya i praktika. 2017;2(4):10-18. (In Russ.)
13. Magklara E-P, Pantelia E-T, Solia E, et al. Vertebral artery variations revised: origin, course, branches and embryonic development. Folia Morphologica. 2021;80(1):1-12. doi: https://doi.org/10.5603/fm.a2020.0022
14. Shahoud JS, Kerndt CC, Burns B. Anatomy, Thorax, Internal Mammary (Internal Thoracic) Arteries. StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing. 2021 Jul 26.
15. Paliouras D, Rallis T, Gogakos AS, et al. Surgical anatomy of the internal thoracic arteries and their branching pattern: a cadaveric study. Ann Transl Med. 2015;3(15):212. doi: https://doi.org/10.3978/j.issn.2305-5839.2015.09.03
16. Terminologia Anatomica [Internet]. Available at: https://ifaa.unifr.ch/ Accessed 17.08.22.
17. Bergman RA, Afifi AK, Miyauchi R. Illustrated Encyclopedia of Human Anatomic Variation. Anatomy Atlases: Opus II: Cardiovascular System: Arteries: Head, Neck, and Thorax. Thyroidea Ima (of Neubauer) Artery [Internet]. Available at: https://anatomyatlases.org. Accessed 17.08.22.
18. Esen K, Ozgur A, Balci Y, et al. Variations in the origins of the thyroid arteries on CT angiography. Jpn J Radiol. 2018;36(2):96-102. doi: https://doi.org/10.1007/s11604-017-0710-3
19. Singh R. Variations in the origin and course of the suprascapular artery: case report and literature review. J Vasc Bras. 2018;17(1):61-65. doi: https://doi.org/10.1590/1677-5449.008117
20. Ogawa R, Murakami M, Vinh VQ, Hyakusoku H. Clinical and Anatomical Study of Superficial Cervical Artery Flaps: Retrospective Study of Reconstructions with 41 Flaps and the Feasibility of Harvesting Them as Perforator Flaps. Plast Reconstr Surg. 2006;118(1):95-101. doi: https://doi.org/10.1097/01.prs.0000220880.28359.86
21. Arslan M, Acar HI, Comert A, Tubbs RS. The cervical arteries: an anatomical study with application to avoiding nerve root and spinal cord blood supply. Turk Neurosurg. 2017;118(1):95-101. doi: https://doi.org/10.5137/1019-5149.JTN.19469-16.1
22. Alabduladhem TO, Lasrado S. Anatomy, Head and Neck, Costocervical Trunk Arteries. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing. 2021 Jan.
23. Rogers L. The Thyroid arteries considered in relation to their Surgical importance. J Anat. 1929;64(1):50-61.
24. Roshan S, Pandey N, Bhivate V, et al. Morphometric study of inferior thyroid artery in cadavers. Int J Anat Res. 2015;3(4):1726-1731. doi: https://doi.org/10.16965/ijar.2015.328
25. Johnsen SL, Kiserud T. Morphometric study of inferior thyroid artery in cadavers. Nor Epidemiol. 2009;19(1):1726-1731. doi: https://doi.org/10.5324/nje.v19i1.10
26. Zhernakova YuV, Kaveshnikov VS, Serebriakova VN. The prevalence of carotid atherosclerosis in spontaneous populations in Tomsk. Sistemic hypertension. 2014;11(4):37-42. (In Russ.)
27. Bokeriia LA, Pokrovskii AV, Sokurenko GIu, et al. Natsional’nye rekomendatsii po vedeniiu patsientov s zabolevaniiami brakhiotsefal’nykh arterii [Internet]. Moscow: Rossiiskoe obshchestvovo angiologov i sosudistykh khirurgov; 2013. 72 p. (In Russ.) Available at: http://www.angiolsurgery.org/recommendations/2013recommendations_brachiocephalic.pdf. Accessed 03.04.2015.
28. Ozgur Z, Govsa F, Celik S, et al. Clinically relevant variations of the superior thyroid artery: an anatomic guide for surgical neck dissection. Surg Radiol Anat. 2009;31(3):151-159. doi: https://doi.org/10.1007/s00276-008-0405-7
29. Levashev YuN, Yablonskiy PK, Pishchik VG. Trachea allotransplantation in the clinic and experiment. Grekov’s Bulletin of Surgery. 2009;168(1):108-111. (In Russ.)
30. Parshin VD, Lyundup AV, Tarabrin EA, Parshin VV. Long-term oucomes of tracheal transplantation: success and unsolved problems. Khirurgiya Zhurnal im NI Pirogova. 2018;19(11):11-19. (In Russ. doi: https://doi.org/10.17116/hirurgia201811111
31. Gupta P, Bhalla AS, Thulkar S, et al. Variations in superior thyroid artery: A selective angiographic study. Indian J Radiol Imaging. 2014;24(01):66-71. doi: https://doi.org/10.4103/0971-3026.130701
32. Malyuga VY, Kuprin AA. Clinical and anatomical features of blood supply of parathyroid glands: autopsy case series. Endocrine Surgery. 2018;12(1):40-54. (In Russ.) doi: https://doi.org/10.14341/serg9637
33. Thomusch O, Machens A, Sekulla C, et al. The impact of surgical technique on postoperative hypoparathyroidism in bilateral thyroid surgery: a multivariate analysis of 5846 consecutive patients. Surgery. 2003;133(2):180-185. doi: https://doi.org/10.1067/msy.2003.61
34. Waseem T, Ahmed SZ, Baig H, et al. Truncal vs Branch Ligation of Inferior Thyroid Arteries in Total Thyroidectomy: Does It Affect Postoperative Hypoparathyroidism? Otolaryngol Head Neck Surg. 2021;164(4):759-766. doi: https://doi.org/10.1177/0194599820957283
35. Henry BM, Vikse J, Graves MJ, et al. Extralaryngeal branching of the recurrent laryngeal nerve: a meta-analysis of 28,387 nerves. Langenbecks Arch Surg. 2016;401(7):913-923. doi: https://doi.org/10.1007/s00423-016-1455-7.
36. Alt B, Elsalini OA, Schrumpf P, et at. Arteries define the position of the thyroid gland during its developmental relocalisation. Development. 2006;133(19):3797-3804. doi: https://doi.org/10.1242/dev.02550
37. Kameda Y. Cellular and molecular events on the development of mammalian thyroid C cells. Dev Dyn. 2016;245(3):323-341. doi: https://doi.org/10.1002/dvdy.24377
38. Nilsson M, Fagman H. Mechanisms of Thyroid Development and Dysgenesis. In: Indian Journal of Radiology and Imaging. 2013;24:123-170. doi: https://doi.org/10.1016/B978-0-12-416021-7.00004-3
39. Surya E, Anitha V. Anomalous origin of left vertebral artery arising from the arch of aorta and its embryological basis. Int J Anat Res. 2014;2(3):537-540.
40. Takafuji T, Sato Y. Study on the subclavian artery and its branches in Japanese adults. Okajimas Folia Anat Jpn. 1991;68(2-3):171-185. doi: https://doi.org/10.2535/ofaj1936.68.2-3_171
41. Sherman JH, Colborn GL. Absence of the left inferior thyroid artery: Clinical implications. Clinical Anatomy. 2003;16(6):534-537. doi: https://doi.org/10.1002/ca.10195
42. Ramesh Rao T, Balakrishnan R, Prakashchandra S, Suresh R. Ectopic Thyroid Tissue With a Rare Vascular Variation. Int J Morphol. 2007;25(1). doi: https://doi.org/10.4067/S0717-95022007000100017
Supplementary files
|
|
1. Figure 1. Branches of the thyroid trunk. A — CT angiography of the right thyroid trunk branches (frontal section); B — schematic drawing of the right thyroid trunk. V-a. vertebralis; De — dextra; Si — sinistra. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(352KB)
|
Indexing metadata ▾ | |
|
|
2. Figure 2. Topography of the ITA. A — schematic drawing of the right thyroid trunk; B — CT angiography (frontal section). Right ITA; C — CT angiography (frontal view). Left ITA. 1 — ascending part of the ITA; * — ITA knee; 2 — descending part of the ITA; S — a. subclavia; C — a. carotis communis; MSA, musculus scalenus anterior; De — dextra; Si — sinistra. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(556KB)
|
Indexing metadata ▾ | |
|
|
3. Figure 3. Schematic drawing of the ITA knee location relative to the thyroid gland lobe. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(211KB)
|
Indexing metadata ▾ | |
|
|
4. Figure 4. The ITA knee is located at the level of the upper pole of the thyroid lobe. A — CT angiogram (frontal view); B — CT angiogram (horizontal plane); * — ITA knee. C — a. carotis communis; V — a. vertebralis; MSA — musculus scalenus anterior; MLC, musculus longus colli; De — dextra; Si — sinistra. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(366KB)
|
Indexing metadata ▾ | |
|
|
5. Figure 5. The ITA knee is located at the level of the upper third of the thyroid lobe. A — CT angiogram (sagittal section); B — CT angiogram (horizontal plane). * — ITA knee; C — a. carotis communis; V — a. vertebralis; MSA — musculus scalenus anterior; MLC — musculus longus colli; De — dextra; Si — sinistra. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(294KB)
|
Indexing metadata ▾ | |
|
|
6. Figure 6. The ITA knee is located at the level of the middle third of the thyroid lobe. A — CT angiogram (sagittal section); B — CT angiogram (horizontal plane); * — ITA knee; C — a. carotis communis; V — a. vertebralis; MSA — musculus scalenus anterior; MLC — musculus longus colli; De — dextra; Si — sinistra. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(325KB)
|
Indexing metadata ▾ | |
|
|
7. Figure 7. Descending part of the ITA. A — CT angiography (sagittal section). The descending branch of the ITA goes down along the posterior surface of the thyroid lobe; B — CT angiography (horizontal section). The descending part of the ITA is located in the space between the thyroid gland, the esophagus and the long muscle of the neck. 2 — descending part of the ITA; * — ITA knee; MLC — musculus longus colli; E — esophagus; De — dextra; Si — sinistra. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(311KB)
|
Indexing metadata ▾ | |
|
|
8. Figure 8. Topography of the ITA branches. A, B, C, D — CT angiography (horizontal section). The branches of the ITA are located along the posterior surface of the thyroid gland. Part of the branches are sent to the gap between the thyroid lobe and the trachea. C — a. carotis communis; V — a. vertebralis; S — a. subclavia; E — esophagus; De — dextra; Si — sinistra. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(608KB)
|
Indexing metadata ▾ | |
|
|
9. Figure 9. ITA forms two branches. A — CT angiography (sagittal section). Both branches are directed downward (arrows); B — CT angiography (sagittal section). Ascending and descending branches of ITA (arrows); B — schematic drawing (front view). Options for the location of the branches of the ITA. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(542KB)
|
Indexing metadata ▾ | |
|
|
10. Figure 10. Origin of the STA. A — CT angiography (sagittal section). The origin of the STA is the bifurcation of the common carotid artery; B — CT angiography (horizontal section). The STA originates from the external carotid artery. C — a. carotis communis; Ce — a. carotis externa; Ci — a. carotis interna. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(313KB)
|
Indexing metadata ▾ | |
|
|
11. Figure 11. Obliterated left STA. CT angiography (frontal section). There is a "break" in the contrast. C — a. Carotis communis; Ci — a. carotis interna; De — dextra; Si — sinistra. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(203KB)
|
Indexing metadata ▾ | |
|
|
12. Figure 12. Location of the glandular branches of the STA. A — CT angiography (horizontal section at the level of the upper poles of the thyroid gland); B — CT angiography (horizontal section slightly below Figure A); C, D — CT angiography (frontal section at the level of the isthmus of the thyroid gland); D — schematic drawing. The anterior isthmus glandular branch is the most permanent and largest glandular branch of the STA. Linea obliqua (TA) — oblique line of the thyroid cartilage — the place of attachment of the prethyroid muscles; C — a. carotis communis; Ce — a. carotis externa, Ci — a. Carotis interna; V — a. vertebralis; De — dextra, Si — sinistra. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(822KB)
|
Indexing metadata ▾ | |
|
|
13. Figure 13. Unpaired thyroid artery (indicated by an arrow). A, B — CT angiography (frontal view). TBC — truncus brachiocephalicus; De — dextra; Si — sinistra. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(297KB)
|
Indexing metadata ▾ | |
|
|
14. Figure 14. Agenesis of the right ITA. A — CT angiography (horizontal section). The right ITA is not contrasted. The right STA is larger than the left STA. B — CT angiography (frontal section). The right STA (1.6 mm) is larger than the left one (0.7 mm). C — a. carotis communis; V — a. vertebralis; De — dextra; Si — sinistra. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(310KB)
|
Indexing metadata ▾ | |
|
|
15. Figure 15. The descending part of the ITA reaches the aortic arch. CT angiography (frontal section). S — a. subclavia. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(197KB)
|
Indexing metadata ▾ | |
|
|
16. Figure 16. Topography of the branches of the STA and ITA. A — CT angiography of the neck (sagittal section). B — schematic drawing. 1, 2 — ОЩЖ; C — a. carotis communis; V — a. vertebralis; MSA — musculus scalenus anterior; MLC — musculus longus colli. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(454KB)
|
Indexing metadata ▾ | |
|
|
17. Figure 17. X-shaped decussation between the ITA and the recurrent laryngeal nerve. A — simulation model (thyroid lobe is not mobilized, side view). B, C, D — intraoperative findings (thyroid lobe is mobilized and retracted anteriorly). Here and in fig. 18, 19: ВОЩЖ — upper PTG; НОЩЖ — lower PTG. a, b — branches of ITA; S — superior — the upper pole of the thyroid gland; I — inferior — lower pole of the thyroid gland | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(1MB)
|
Indexing metadata ▾ | |
|
|
18. Figure 18. Cruciate decussation between the ITA and the recurrent laryngeal nerve. A — simulation model (thyroid lobe is not mobilized, side view). B, C — intraoperative findings (thyroid lobe is mobilized and retracted anteriorly). | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(884KB)
|
Indexing metadata ▾ | |
|
|
19. Figure 19. Neuro-arterial decussation in the ascending direction of the ITA. A — simulation model (thyroid lobe is not mobilized, side view). B — intraoperative findings (thyroid lobe is mobilized and retracted anteriorly). | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(372KB)
|
Indexing metadata ▾ | |
|
|
20. Figure 20. Schematic drawing of the embryogenesis of the thyroid gland, PTG and human vascular structures (right half of the body). A — the beginnings of the thyroid gland, PTG, thymus, vascular system. B — the final position of the organs in an adult. STA repeat the movement of the medial thyroid bud (straight arrow). ITA repeat the movement of the lateral thyroid anlage (arc-shaped arrow). I–VII — pharyngeal arterial arches. Longitudinal communication anastomosis is an embryonic longitudinal vascular anastomosis of the neck, from which the thyroid trunk and ascending cervical artery are formed [39, 40]. T — thymus; УБТ — ultimobranchial bodies; ТВС — truncus brachiocephalicus; C — a. carotis communis. | |
| Subject | ||
| Type | Исследовательские инструменты | |
View
(400KB)
|
Indexing metadata ▾ | |
Review
For citations:
Kuprin A.A., Malyuga V.Y., Stepanova E.A. Arterial blood supply of the internal neck organs: anatomy, topography, clinical significance in endocrine surgery. Endocrine Surgery. 2021;15(3):4-22. (In Russ.) https://doi.org/10.14341/serg12720
Views:
4172
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND 4.0).
Email this article 
