Clinical and anatomical features of blood supply of parathyroid glands: autopsy case series
https://doi.org/10.14341/serg9637
Abstract
Hypoparathyroidism is the most common complication after surgery on the thyroid gland. All authors confirm the fact that the main cause of hypoparathyroidism is a violation of the blood supply of parathyroid glands, as well as their damage or even accidental removal during surgery. Having analyzed the real cases, and based on our own experience, we came to the conclusion that in order to prevent complications, we will need to study the types of blood supply of the parathyroid glands in details. To this end, we have performed 46 unilateral microdissections and X-ray angiography studies of the arterial supply at 23 organocomplexes of the neck. 42 upper and 43 lower parathyroid glands were detected. It has been established that the main feeding vessel of parathyroid glands is the inferior thyroid artery (type I). The association of glands with the inferior thyroid artery was revealed in 71.8% of cases. A mixed variant of blood supply (simultaneously from the superior and inferior thyroid arteries) was revealed in 14.1% cases (type II). Only 10.6% of the gland were fed isolated from the superior thyroid artery (type III). In addition, in 8.7% cases in the preparations there was no inferior thyroid artery. In 3.5% cases, the connections of the lower parathyroid glands with the thyroid arteries were not reliably detected. Most probably, their feeding was provided at the expense of small collaterals from surrounding organs (type VI).
About the Authors
Viktor Y. MalyugaDistrict City Hospital №2
Russian Federation
MD, PhD
Aleksandr A. Kuprin
A.K. Eramishanzeva City Clinical Hospital
Russian Federation
MD, PhD
References
1. Halsted WS, Evans HM. The parathyroid glandules. Their blood supply, and their preservation in operation upon the thyroid gland. Ann Surg. 1907;46(4):489-506. doi: 10.1097/00000658-190710000-00001.
2. Song CM, Jung JH, Ji YB, et al. Relationship between hypoparathyroidism and the number of parathyroid glands preserved during thyroidectomy. World J Surg Oncol. 2014;12:200. doi: 10.1186/1477-7819-12-200.
3. Wang YH, Bhandari A, Yang F, et al. Risk factors for hypocalcemia and hypoparathyroidism following thyroidectomy: a retrospective Chinese population study. Cancer Manag Res. 2017;9:627-635. doi: 10.2147/CMAR.S148090.
4. Нурутдинов Р.М. Профилактика и лечение осложнений при операциях на щитовидной железе: Дис. … канд. мед. наук. – М.; 2010. [Nurutdinov RM. Profilaktika i lechenie oslozhneniy pri operatsiyakh na shchitovidnoy zheleze. [dissertation] Moscow; 2010. (In Russ.)]
5. Dolapci M, Doganay M, Reis E, Kama NA. Truncal ligation of the inferior thyroid arteries does not affect the incidence of hypocalcaemia after thyroidectomy. Eur J Surg. 2000;166(4):286-288. doi: 10.1080/110241500750009096.
6. Zhu J, Tian W, Xu Z, et al. Expert consensus statement on parathyroid protection in thyroidectomy. Ann Transl Med. 2015;3(16):230. doi: 10.3978/j.issn.2305-5839.2015.08.20.
7. Kolly A, Sarathi V, Bothra S, et al. Hypocalcemia: What a surgeon should know. World Journal of Endocrine Surgery. 2017;9(2):72-77. doi: 10.5005/jp-journals-10002-1215.
8. Abou-Amra M, Abdel-Rahman YO. Effect of bilateral truncal inferior thyroid artery ligation on parathyroid function. AAMJ. 2011;9(2).
9. Maralcan G, Başkonuş I, Borazan E, et al. The effects of inferior thyroid arteries ligation type on post-thyroidectomy clinical hypocalcemia in nontoxic multinodular goiter. Endokrinolojide Diyalog. 2010;7(4):137-140.
10. Iqbal M, Parveen S. Recurrent laryngeal nerve palsy and hypocalcemia with and without bilateral ligation of inferior thyroid artery in total thyroidectomy. J Surg Pakistan (International). 2015;20(1):19-22.
11. Araujo Filho VJFd, Silva Filho GBe, Brandão LG, et al. The importance of the ligation of the inferior thyroid artery in parathyroid function after subtotal thyroidectomy. Rev Hosp Clin Fac Med Sao Paulo. 2000;55(4):113-120. doi: 10.1590/s0041-87812000000400002.
12. Singh H, Kumar V. Hypocalcemia in thyroid surgery: a prospective study. Int J Sci Study. 2017;4(12):8-11. doi: 10.17354/ijss/2017/86.
13. 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: 10.1067/msy.2003.61.
14. Wu J, Harrison B. Hypocalcemia after thyroidectomy: the need for improved definitions. World J Endocrine Surg. 2010;2(1):17-20.
15. Chaudhary IA, Afridi Z, Samiullah, et al. To ligate or not the inferior thyroid artery to avoid hypocalcaemia after thyroid surgery. J Ayub Med Coll Abbottabad. 2007;19(2):19-22.
16. Dogru O, Kama NA, Sakrak O, et al. The effect of plasma calcium and phosphorus levels on the ligation of inferior thyroid artery. Turk J Surg. 1992;8(4):271-276.
17. Naseem N, Mengal MZ, Maqbool HMA. Comparison of frequency of clinical tetany between truncal ligation and peripheral ligation of inferior thyroid arteries in subtotal thyroidectomy. PJMHS. 2015;9(1):151-153.
18. Кузнецов Н.С., Симакина О.В., Ким И.В. Предикторы послеоперационного гипопаратиреоза после тиреоидэктомии и методы его лечения. // Клиническая и экспериментальная тиреоидология. – 2012. – Т. 8. – №2. – С. 20–30. [Kuznetsov NS, Simakina OV, Kim IV.Predictors of postoperative hypoparathyroidism after thyroidectomy and methods of treatment. Clinical and experimental thyroidology. 2012;8(2):20-30. (In Russ.)] doi: 10.14341/ket20128220-30.
19. Бельцевич Д.Г., Ванушко В.Э., Румянцев П.О., и др. Российские клинические рекомендации по диагностике и лечению высокодифференцированного рака щитовидной железы у взрослых, 2017 год. // Эндокринная хирургия. – 2017. – Т. 11. – №1. – С. 6–27. [BeltsevichDG, Vanushko VE, Rumyantsev PO, et al. 2017 Russian clinical practice guidelines for differentiated thyroid cancer diagnosis and treatment. Endocrine Surgery. 2017;11(1):6-27. (In Russ.)] doi: 10.14341/serg201716-27.
20. Wang JB, Wu K, Shi LH, et al. In situ preservation of the inferior parathyroid gland during central neck dissection for papillary thyroid carcinoma. Br J Surg. 2017;104(11):1514-1522. doi: 10.1002/bjs.10581.
21. Malik V, Watson GJ, Phua CQ, Murthy P. Fluctuation of corrected serum calcium levels following partial and total thyroidectomy. Int J Clin Med. 2011;02(04):411-417. doi: 10.4236/ijcm.2011.24069.
22. Cakmakli S, Aydintug S, Erdem E. Post-thyroidectomy hypocalcemia: does arterial ligation play a significant role? Int Surg. 1992;77(4):284-286.
23. Wade JSH, Goodall P, Dauncey TM, Fourman P. The course of partial parathyroid insufficiency after thyroidectomy. Br J Surg. 1965;52(7):497-503. doi: 10.1002/bjs.1800520705.
24. Nies C, Sitter H, Zielke A, et al. Parathyroid function following ligation of the inferior thyroid arteries during bilateral subtotal thyroidectomy. Br J Surg. 1994;81(12):1757-1759. doi: 10.1002/bjs.1800811215.
25. Canbeyli B, Karaoğlan M, Özenen B, et al. The role of ligation of inferior thyroid artery on hypocalcemia in thyroidectomies. J Tepecik Hosp Turkey. 1991;1(2):115-118.
26. Sut S, Kurt N, Yildirim M, et al. Is the parathyroid function effected by ligation of the inferior thyroid arteries during bilateral subtotal thyroidectomy? Turk J Surg. 1996;12(4): 293-298.
27. Kebsch A, Settmacher U, Lesser T. Bilateral truncal ligation of the inferior thyroid artery during bilateral subtotal thyroidectomy causes a decrease in parathormone without clinically manifest hypoparathyroidism: a randomized clinical trial. Eur Surg Res. 2015;55(3):141-150. doi: 10.1159/000437094.
28. Cocchiara G, Cajozzo M, Amato G, et al. Terminal ligature of inferior thyroid artery branches during total thyroidectomy for multinodular goiter is associated with higher postoperative calcium and PTH levels. J Visc Surg. 2010;147(5):e329-332. doi: 10.1016/j.jviscsurg.2010.08.020.
29. Kosinski B. Evaluation of the effect of ligation of the inferior thyroid arteries during non-radical thyroidectomy in simple goiter on selected parameters of calcium-phosphate metabolism in the body. Ann Acad Med Stetin. 1991;37:179-190.
30. Li ZD, Liu HW, Dong HL, Li SC. Preservation of parathyroid glands and their functions during total thyroidectomy. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi. 2010;45(11):899-903.
31. Kapre M. Preservation of the parathyroids in thyroid surgery. World Articles in Ear, Nose and Throat. 2009;2(1).
32. Nobori M, Saiki S, Tanaka N, et al. Blood supply of the parathyroid gland from the superior thyroid artery. Surgery. 1994;115(4):417-423.
33. Лысенков Н.К., Бушкович В.И., Привес М.Г. Учебник нормальной анатомии человека. – М: Медгиз; 1958. [Lysenkov NK, Bushkovich VI, Prives MG. Uchebnik normal'noy anatomii cheloveka. Moscow: Medgiz; 1958. (In Russ.)]
34. Zhao W, Gao B-L, Yi G-F, et al. Thyroid arterial embolization for the treatment of hyperthyroidism in a patient with thyrotoxic crisis. Clin Invest Med. 2009;32(1):78. doi: 10.25011/cim.v32i1.5091.
35. Johansson K, Ander S, Lennquist S, Smeds S. Human parathyroid blood supply determined by laser-Doppler flowmetry. World J Surg. 1994;18(3):417-420. doi: 10.1007/bf00316825.
36. Testini M, Gurrado A, Lissidini G, Nacchiero M. Hypoparathyroidism after total thyroidectomy. Minerva Chir. 2007;62(5):409-415.
37. Sciume C, Geraci G, Pisello F, et al. Complications in thyroid surgery: symptomatic post-operative hypoparathyroidism incidence, surgical technique, and treatment. Ann Ital Chir. 2006;77(2):115-122.
38. Ander S, Johansson K, Smeds S. Blood supply and parathyroid hormone secretion in pathological parathyroid glands. World J Surg. 2014;20(5):598-602. doi: 10.1007/pl00012250.
39. Ander S, Johansson K, Smeds S. In situ preservation of the parathyroid glands during operations on the thyroid. Eur J Surg. 1997;163(1):33-37.
40. Randolph GW. Surg Thyroid Parathyroid Glands. 2nd ed. Philadelphia: Elsevier Saunders; 2012.
41. Arrangoiz R, Cordera F, Caba D, et al. Parathyroid embryology, anatomy, and pathophysiology of primary hyperparathyroidism. Int J Otorhinolaryngol Head Neck Surg. 2017;06(04):39-58. doi: 10.4236/ijohns.2017.6400.
42. Delattre JF, Flament JB, Palot JP, Pluot M. Variations in the parathyroid glands. Number, situation and arterial vascularization. Anatomical study and surgical application. J Chir (Paris). 1982;119(11):633-641.
43. Emedicine.medscape.com [Internet]. Kochhar A, Patel AA. Gest TR, editors. Parathyroid Gland Anatomy [updated 2013 Sep 17; cited 2018 Jun 25]. Available from: https://emedicine.medscape.com/article/1949105-overview#showall.
44. Bonjer HJ, Bruining HA. The technique of parathyroidectomy. In: Clark O, Duh Q, Kebebew E, et al, editors. Textbook of Endocrine Surgery. Philadelphia: Saunders; 1997. p. 277-283.
45. Wang C-A. The anatomic basis of parathyroid surgery. Ann Surg. 1976;183(3):271-275. doi: 10.1097/00000658-197603000-00010.
Supplementary files
|
1. Table 1. Types of blood supply to the liver | |
Subject | ||
Type | Исследовательские инструменты | |
View
(104KB)
|
Indexing metadata ▾ |
|
2. Fig. 1. I type. Right lobe SHCHZH: 1, 2 - small branches from the main trunk of NCHA, heading into the pre-tracheal tissue; 3, 4, 5 - branches of the first-order NCHA. RLN is the recurrent laryngeal nerve. a - X-ray angiogram in a direct projection. Contrasted with NSCHA. The artery has many branches. Three main (3, 4, 5) are sent to the thyroid tissue, others, smaller (1, 2) - into the pre-tracheal cell space. Marked with metal tips, NOVES and NOUCH (circled) are in the basin of the NCHA. Contrasted small twigs are sent to the LEL. b - microdissection. The TSS are in a typical place. Vascular "legs" are visualized, reaching the LEL from the branches of the first order NCHA (3, 4, 5). The main stem of the ULN (RLN) is located in front of the NSHA. c is a circuit. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(399KB)
|
Indexing metadata ▾ |
|
3. Fig. 2. I type. The left part of the thyroid gland: 1, 2 - branches of the first-order NCHA. RLN is the recurrent laryngeal nerve. a - X-ray angiogram in a direct projection. Contrasted with NSCHA. The artery has two main branches of the first order (1, 2), directed to the thyroid tissue. Marked with metal tips, NOVES and NOUCH (circled) are in the basin of the NCHA. Contrast small branches, going to the TERMINAL. Arrow - incisura thyreoidea superior. b - microdissection. The spine is located in a typical place, intimately belonging to the upper branch of the first order of NCHA (2). The BAP is located in the pre-tracheal tissue, to which a third-order branch from the lower branch of the NCHA (1) is directed. The division of VLN (RLN) occurs at the level of the NSAHA behind its branches. c is a circuit. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(417KB)
|
Indexing metadata ▾ |
|
4. Fig. 3. X-ray angiogram in the direct projection: 1 - posterior anastomosis between NSHA and VSTA; 2 - anterior anastomosis between NSHA and VST. OCA - common carotid artery (partially contrasted). A contrast is introduced into the left NSCHA. Two anastomoses are clearly visualized, located along the posterior (1) and anterolateral surface (2) of the thyroid lobe. II type of blood supply was identified in our work in 12 (14.1%) of the LTR (9 STICKS, 3 NOSHES). | |
Subject | ||
Type | Исследовательские инструменты | |
View
(143KB)
|
Indexing metadata ▾ |
|
5. Fig. 4. IIa type. The left share SHCHZH. 1, 2, 3 - first-order branches of the first order. RLN is the recurrent laryngeal nerve. a - X-ray angiogram in a direct projection. Contrasted on the left. The artery has three branches of the first order (1, 2, 3), directed to the thyroid tissue. Marked with a metal tip, the NOISE (circumscribed) is located in the course of the posterior anastomosis. The posterior branch of the VHA (3) forms an anastomosis with the upper branch of the NCHA (black arrows). The inter-lobe anastomosis between the left and right OVH (white arrows) is contrasted. b - microdissection. Anterior anastomosis (arrows) was prepared. The branch is in a typical place and receives twigs from the upper third of the anastomosis. The NOSHCH is localized at the lower pole of the thyroid gland and is blood-sucked from the lower branch of the NCHA. VGN is located behind the NSA and is parallel to the posterior anastomosis. c is a circuit. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(426KB)
|
Indexing metadata ▾ |
|
6. Fig. 5. IIb type. The left share SHCHZH. RLN is the recurrent laryngeal nerve. a is microdissection. Anterior anastomosis is located under the capsule on the anterolateral surface of the thyroid (arrows). STI situated on the anterior anastomosis in the region of the lower third of the anastomosis. b - scheme. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(206KB)
|
Indexing metadata ▾ |
|
7. Fig. 6. X-ray angiograms of two organocomplexes with anomaly of development of the left NSHA (direct projection). OCA is a common carotid artery. The arrows indicate the direction of the contrast. a, b - at the first stage of the study, it was not possible to identify and cannulate the left NSA. Two organocomplexes with cannulated and contrasted left VSCH. The arrows indicate the spread of contrast to the opposite side with the staining of the right VSTA and NCHA. Left NSA is absent. TSS marked with metal tips. The nutrition is carried out on the side of atresia due to the UPH. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(245KB)
|
Indexing metadata ▾ |
|
8. Fig. 7. Type III. a - X-ray angiogram in a direct projection. Cannulated and contrasted right and left VSTA (both NSCHA when searching at the first stage of the work are not identified). NSChA is not contrasted on both sides. Marked with metal tips, NOVES and NOUCHES (circled) are located in the basin of the VCHA. b, c - microdissection. The left share SHCHZH. NCHA is absent. The abscess is located on the anterior surface of the thyroid gland under the capsule and is mainly supplied by the anterior branch of the VCHA, which runs along the anterior surface of the thyroid. The spine is located in a typical place and is also blood-sucked by branches of the VL. d - scheme. The left share SHCHZH. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(491KB)
|
Indexing metadata ▾ |
|
9. Fig. 8. Intraoperative picture of anomaly of development of left NSA. Both TSS (circumcised) are located at the level of the shield-aperture articulation (in midposition) and are blood flowing. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(198KB)
|
Indexing metadata ▾ |
|
10. Fig. 9. X-ray angiogram in a direct projection. Contrast is introduced in both NSCH. The contrast retrogradno falls in the right and left VSCH and unpaired thyroid artery (arrows). Marked (highlighted) only STICK. NOSHL were low in pre-tracheal tissue and before angiography were not found and not labeled. Their connection with the thyroid arteries with microdissection was not revealed. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(202KB)
|
Indexing metadata ▾ |
|
11. Fig. 10. Intraoperative finding of unpaired thyroid artery (arrows). BAPTIZH intimately adjoins the trunk of this artery (IV type of blood supply). SHCHZH - the lower pole of the thyroid gland. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(175KB)
|
Indexing metadata ▾ |
|
12. Table 2. Number of branches of the first and second-order branches | |
Subject | ||
Type | Исследовательские инструменты | |
View
(94KB)
|
Indexing metadata ▾ |
|
13. Table 3. Order of the branches of the NCHA feeding the LNS | |
Subject | ||
Type | Исследовательские инструменты | |
View
(93KB)
|
Indexing metadata ▾ |
|
14. Fig. 11. A typical picture of the blood supply of the thyroid gland and the liver. 1 - anterior anastomosis, 2 - posterior anastomosis. I-IV - types of blood supply of the TSS. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(110KB)
|
Indexing metadata ▾ |
Review
For citations:
Malyuga V.Y., Kuprin A.A. Clinical and anatomical features of blood supply of parathyroid glands: autopsy case series. Endocrine Surgery. 2018;12(1):40-54. (In Russ.) https://doi.org/10.14341/serg9637

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND 4.0).