A case report of an absence of the left inferior thyroid artery with compensating the thyroid ima artery

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Abstract Here, we report an anatomical variation of the left inferior thyroid artery in a male cadaver during routine neck dissection. The left inferior thyroid artery was absent and replaced by the thyroid ima artery. The thyroid ima artery formed a U-shaped course and gave branches to the lower part of the thyroid gland. In addition, the thyroid ima artery arose from the brachiocephalic trunk. Furthermore, the branch of the thyroid ima artery ascended parallel to the left recurrent laryngeal nerve. There was no anatomical variation of the right inferior thyroid artery.
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A case report of an absence of the left inferior thyroid artery with compensating the thyroid ima artery | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article A case report of an absence of the left inferior thyroid artery with compensating the thyroid ima artery Fa-Bao Xu, Wen-Bo Yue, Chun Yang This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-7454738/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 13 Oct, 2025 Read the published version in Surgical and Radiologic Anatomy → Version 1 posted 12 You are reading this latest preprint version Abstract Here, we report an anatomical variation of the left inferior thyroid artery in a male cadaver during routine neck dissection. The left inferior thyroid artery was absent and replaced by the thyroid ima artery. The thyroid ima artery formed a U-shaped course and gave branches to the lower part of the thyroid gland. In addition, the thyroid ima artery arose from the brachiocephalic trunk. Furthermore, the branch of the thyroid ima artery ascended parallel to the left recurrent laryngeal nerve. There was no anatomical variation of the right inferior thyroid artery. Inferior thyroid artery Thyroid ima artery Brachiocephalic trunk Anatomical variation Recurrent laryngeal nerve Figures Figure 1 Introduction The thyroid gland is an important endocrine organ situated in the midline of the anterior neck, typically extending from the fifth to the seventh cervical vertebrae. Being highly vascularized, it achieves blood supply primarily via the superior thyroid artery (STA) and the inferior thyroid artery (ITA). According to the anatomical textbooks, the STA is the first branch of the external carotid artery. On the other hand, the ITA arises from the thyrocervical trunk, which originates from the first part of the subclavian artery (SA). During the normal course of ITA, it ascends anterior to the anterior scalene muscle, turns medially at the level of transverse process of the sixth cervical vertebra, then descends anterior to the longus colli muscle, and ultimately reaches the inferior lobe of the thyroid gland. In addition to the typical origins, there are well documented anatomical variations of STA and ITA. A recent review has analyzed the variation of STA and ITA, highlighting the importance of understanding such anatomical variations for surgical practice [ 1 ]. Several case reports recently have further presented other anatomical variations of inferior thyroid artery [ 2 – 5 ]. Here, we reported an unusual variation for the absence of left ITA that was replaced by thyroid ima artery (TIMA) originating from the brachiocephalic trunk (BCT), which has not been demonstrated in the previous studies and case reports. Case Presentation A unilateral variation of the ITA was observed during neck dissection in a 64-year-old male cadaver at the anatomical laboratory of Capital Medical University. The specimen was embalmed with formalin before anatomical dissection. The whole dissection procedure was performed with great care for the adjacent organs, including nerves, glands, muscles, etc. During the routine dissection of the neck, the bilateral blood supply of the thyroid gland was exposed. A variation in the left inferior thyroid artery (LITA) was observed. The LITA was missing, and the TIMA emerged and originated from the BCT (Fig. 1 A). Measurements were obtained in ImageJ. The diameter of the TIMA was 2.54 mm. After its course in a main trunk (15. 93 mm in length), it ran downwards (6.67 mm in length), diagonally (4.18 mm in length), and then upwards (5.08 mm in length), forming a U-shape till its bifurcation into the lower part of the thyroid gland (1 in Fig. 1 ). Furthermore, the TIMA gave off three branches (Fig. 1 B and E). The first branch of TIMA (1.67 mm in diameter) descended inferiorly before entering into the adipose tissue in anterior mediastinum (branch 4 in Fig. 1 A and B). The second branch of TIMA (1.53 mm in diameter) traveled superiorly and entered into the lower portion of the right lobe of thyroid gland (branch 2 in Fig. 1 A and B). The third branch of TIMA (2.08 mm in diameter) (branch 6 in Fig. 1 A and B) travelled medially and superiorly and subdivided into two additional branches (branches 7 and 8 in Fig. 1 A and B) before entering into the thyroid isthmus. The branch 7 traveled superiorly and laterally and entered into the left lobe of thyroid gland. The branch 8 further subdivided into two additional branches (branches 9 and 10 in Fig. 1 A and B). The branch 9 terminated in the thyroid isthmus and the branch 10 traveled superiorly and terminated in the lower portions of the thyroid gland that closely to the entry point of the branch 6. As shown in Fig. 1 C, the branch of the TIMA ascended parallel to the left recurrent laryngeal nerve. The distance between them was approximately 5.26 mm. This relationship differs from the classic anterior, posterior, or inter-arterial courses described between the recurrent laryngeal nerve and the ITA. In order to further confirm the variation of LITA, the left thyrocervical trunk and its branches were also dissected. The left thyrocervical trunk, a branch of the left subclavian artery (LSCA), gave off several branches, including transverse cervical artery (Fig. 1 D, 13), suprascapular artery (Fig. 1 D, 14), and others. After further dissection and tracking, the branches of the left thyrocervical trunk did not give off any branches to supply the lower part of the thyroid gland. The right inferior thyroid artery originated from the right thyrocervical trunk, which was normal without variation. The course of RITA was also observed to be normal with no variation. The anatomical relation of RITA and right recurrent laryngeal nerve on the right side was normal without variation. Discussion Anatomical variations in humans are indispensable parts of human gross anatomy, and play a key role in understanding human diversity. The primary significance of individual variations is to enhance diagnostic accuracy and therapeutic efficacy, particularly in surgery intervention [ 6 ]. Consequently, studies or case reports of anatomical variations have gained considerable scientific interest. Many articles have documented anatomical variations of ITA [ 1 – 5 ]. As far as we know, the current case represents a distinctive variation of an absence of LITA and compensation by TIMA arising from the BCT, which is worthy of our attention and further study. It has been demonstrated that anatomical variations of ITA may be absent, exhibit duplication, arise from different levels, or be replaced with other arteries [ 1 , 7 , 8 ]. Specifically, a case study had reported the hypoplastic RITA and absence of LITA [ 9 ]. An absence of bilateral ITAs was also described during a neck region dissection [ 10 , 11 ]. A recent case report also provided evidence of absence of ITA bilaterally [ 5 ]. In such cases, it is TIMA that compensates for the missing ITA. However, Sherman and colleagues reported a case that LITA was absent, but TIMA was not found [ 8 ]. We here described a case that the LITA was absent and replaced by the TIMA originating from the BCT. Notablly, a particular case report by Weiglein and colleagues has documented that the absence of RITA was compensated by a TIMA branching off the right internal thoracic artery and the absence of LITA was compensated by a branch from the vertebral artery [ 11 ]. These findings highlight the necessary to increase awareness of the arteries serving a compensatory role for blood supply to the thyroid gland when the ITA is absent. Clinically, a deep knowledge of vascularization of thyroid gland is essential for surgical practices on the neck. A 2022 review article has described abnormal originations of the ITA [ 1 ]. The majority of ITA originates from the thyrocervical trunk; it can also anomalously originate from the common carotid artery, followed by the subclavian artery, the vertebral artery or the suprascapular artery [ 1 , 3 – 5 , 12 ]. TIMA, an uncommon variance, typically compensates for ITA absence and originates from the brachiocephalic trunk, the right common carotid artery, the right internal thoracic artery, and the aortic arch [ 1 , 13 – 16 ]. Notably, Sannomiya, et al. reported a rare double TIMA without classic thyroid arteries variations [ 17 ]. Niida and Yamasaki proposed a classification of TIMA according to its anatomical origin. The classification divides the double TIMA variants into three subtypes: type 1 originating from brachiocephalic trunk and common carotid artery; type 2 originating from brachiocephalic trunk and aortic arch; type 3 originating from right internal thoracic artery and left internal thoracic artery [ 17 , 18 ]. Although the TIMA is often present as a compensatory variation for the absence of ITA, Esen et al. reported concurrent presence of TIMA and ITA in 7/15 cases (46%), indicating that they are unnecessarily mutually exclusive [ 7 ]. A recent report described a presence of multiple branches of TIMA over the trachea during a cadaver dissection; such TIMA and its branching pattern leads to a high risk for abnormal bleeding during tracheotomy or cricothyroidotomy [ 19 , 20 ]. This anatomical variation underscores the values of the preoperative CT angiography or arteriogrphic investigation to optimize patient outcomes [ 7 , 9 ]. Ultrasound-guided percutaneous dilatational tracheostomy (US-PDT) could facilitate prevention of vascular puncture. Thus, US-PDT can be used as an alternative to fIber-optic bronchoscopy dilatational tracheostomy [ 21 ]. Additionally, TIMA could be safely and effectively embolized for the management of Graves’ disease and thyroid storm [ 22 ]. Some evidence indicated that the variation of TIMA may be due to the regression and persistence of vascular structures of thyroid gland in embryonic stage. Thyroid gland is supplied by many arteries during its development [ 16 , 23 ]. Finally, most of them disappear, leaving behind STA and ITA as the regular arteries supplying thyroid gland in adult. A recent study analyzed the prevalence of TIMA with a meta-analysis [ 24 ]. A higher prevalence of TIMA was present in human fetuses (14.8%) than adults (3.3%). Therefore, Yurasakpong and colleagues predicted that TIMA may function as a normal developmental artery and its persistence beyond the fetal stage would result in its classification as an anatomical variant. Similar to the previous description [ 25 ], the TIMA in this case supplies blood to thyroid gland and adipose tissue in anterior mediastinum (the remnant of thymus gland), which supporting the hypothesis of Yurasakpong et al. Vascular endothelial growth factor (VEGF), a signaling protein for angiogenesis, has been reported to be highly expressed in the developing thymus and thyroid gland of zebrafish [ 26 ]. This biological characteristic suggests a further investigation into the potential relationship between VEGF dynamics and the regression and persistence mechanisms of TIMA. In addition, during embryogenesis, the pharyngeal arch arteries are transient embryonic blood vessels that remodel to form the critical segments of the aortic and its branches. The factors regulating angiogenesis of pharyngeal arch arteries such as Tmem88 (a Wnt signaling modulator expressed in pharyngeal mesoderm) [ 27 ] might be linked to the regression and persistence of TIMA. Therefore, future investigations are needed to detect the genetic factors related to the development of TIMA. In summary, anatomical variations play a pivotal role in the clinical practice of medicine, particularly in surgical disciplines. Descriptive studies based on cadaver dissection, imaging examination and surgical procedures, can provide more evidence of variation. An increasing number of studies have documented the variations of arteries for the thyroid gland. However, the case here stands out as a distinctive instance of the missing LITA being replaced by the TIMA arising from the BCT. Such anatomical variation occurrence underscores the importance of anatomical study and is essential for medical practice, which can have profound implications for surgical interventions and clinical outcomes. Declarations Author contributions Fa-Bao Xu and Wen-Bo Yue performed dissection and identify the structures. Fa-Bao Xu prepared the figure. Chun Yang wrote the manuscript. Fa-Bao Xu and Chun Yang reviewed and edited the manuscript. Funding This study was funded by Beijing Association of Higher Education (grant number MS2023268). Acknowledgments The authors sincerely thank those who donated their bodies to science so that anatomical research could be performed. Results from such research can potentially increase mankind's overall knowledge that can then improve patient care. Therefore, these donors and their families deserve our highest gratitude. Conflict of Interest The authors declare that they have no conflict of interest. References Branca, J.J.V., A. Lascialfari Bruschi, A.M. Pilia, D. Carrino, G. Guarnieri, M. Gulisano, A. Pacini, and F. Paternostro (2022) The Thyroid Gland: A Revision Study on Its Vascularization and Surgical Implications. Medicina (Kaunas) 58(1). Hvizdošová, N., J. Vecanová, S. Matéffy, and I. Hodorová (2022) Combined unusual origin and course of the right vertebral artery and right inferior thyroid artery: a case report. Surg Radiol Anat 44(10): p. 1355-1359. Westrych, K., K. Ruzik, N. Zielinska, F. Paulsen, G.P. Georgiev, Ł. Olewnik, and P. Łabętowicz (2022) Common trunk of the internal thoracic artery, inferior thyroid artery and thyrocervical trunk from the subclavian artery: a rare arterial variant. Surg Radiol Anat 44(7): p. 983-986. Bunea, M.C., L.M. Rusali, I.C. Bratu, S. Tudorache, and P. Bordei (2023) Considerations on the origin of the inferior thyroid artery emerging from the subclavian artery determined by CT examination. Surg Radiol Anat 45(6): p. 721-727. Novakov, S.S. and S.D. Delchev (2021) Two cases of variations in inferior thyroid arterial pattern and their clinical implications. Folia Morphol (Warsz) 82(2): p. 396-399. Alraddadi, A. (2021) Literature Review of Anatomical Variations: Clinical Significance, Identification Approach, and Teaching Strategies. Cureus 13(4): p. e14451. Esen, K., A. Ozgur, Y. Balci, S. Tok, and E. Kara (2018) Variations in the origins of the thyroid arteries on CT angiography. Jpn J Radiol 36(2): p. 96-102. Sherman, J.H. and G.L. Colborn (2003) Absence of the left inferior thyroid artery: clinical implications. Clin Anat 16(6): p. 534-7. Krudy, A.G., J.L. Doppman, and M.F. Brennan (1980) The significance of the thyroidea ima artery in arteriographic localization of parathyroid adenomas. Radiology 136(1): p. 51-45. Yilmaz, E., H.H. Celik, B. Durgun (1993) A. Atasever, and S. Ilgi, Arteria thyroidea ima arising from the brachiocephalic trunk with bilateral absence of inferior thyroid arteries: a case report. Surg Radiol Anat 15(3): p. 197-9. Weiglein, A.H., A rare variant of thyroid gland vascularization. Surg Radiol Anat 18(3): p. 233-5. Yang, L., X. Hu, and J. Lu (2024) A Rare Case of Anatomical Variation of Inferior Thyroid Artery Originated From the Brachiocephalic Trunk During Retrosternal Goiter Excision. Ear Nose Throat J p. 1455613241239529. Fujimoto, Y., F. Suwa, and K. Kimura (1974) A case of the left superior thyroid artery arising from the left common carotid artery and the A. thyroidea ima. Okajimas Folia Anat Jpn 51(5): p. 219-30. Tohno, S., Y. Tohno, H. Matsumoto, S. Fujimoto, T. Fujimoto, N. Futamura, and K. Furuta (1989) A case of the thyroidea ima artery arising from the aortic arch. Kaibogaku Zasshi 64(5): p. 490-4. Lovasova, K., D. Kachlik, M. Santa, and D. Kluchova (2017) Unilateral occurrence of five different thyroid arteries-a need of terminological systematization: a case report. Surg Radiol Anat 39(8): p. 925-929. Moriggl, B. and W. Sturm (1996) Absence of three regular thyroid arteries replaced by an unusual lowest thyroid artery (A. thyroidea ima): a case report. Surg Radiol Anat 18(2): p. 147-50. Sannomiya, T., K. Yamaki, Y. Doi, K. Aida, H. Tanaka, Y. Hyakutake, and M. Yoshizuka (1996) A rare case of the double thyroid ima artery. Kurume Med J 43(2): p. 177-80. Niida, S. and M. Yamasaki (1984) The anatomical consideration of the double thyroid ima artery. Kaibogaku Zasshi 59(1): p. 9-17. Totlis, T., K. Natsis, V. Achlatis, T. Pettas, and M. Piagkou (2023) Thyroidea ima artery multiple branching pattern over the trachea. Surg Radiol Anat 45(7): p. 813-817. Kamparoudi, P., D. Paliouras, A.S. Gogakos, T. Rallis, N.C. Schizas, A. Lazopoulos, F. Chatzinikolaou, P. Sarafis, P. Serchan, N. Katsikogiannis, E. Sarika, P. Zarogoulidis, I. Karapantzos, and N. Barbetakis (2016) Percutaneous tracheostomy-beware of the thyroidea-ima artery. Ann Transl Med 4(22): p. 449. Sarıtaş, A. and M.M. Kurnaz (2019) Comparison of Bronchoscopy-Guided and Real-Time Ultrasound-Guided Percutaneous Dilatational Tracheostomy: Safety, Complications, and Effectiveness in Critically Ill Patients. J Intensive Care Med 34(3): p. 191-196. Bonnici, M., C. Nevin, and S. Boo (2023) Thyroid ima artery embolization for the treatment of Graves' disease and thyroid storm. Radiol Case Rep 18(8): p. 2641-2644. Mariolis-Sapsakos, T., V. Kalles, I. Papapanagiotou, V. Bonatsos, N. Orfanos, I.G. Kaklamanos, and E. Manolis (2014) Bilateral aberrant origin of the inferior thyroid artery from the common carotid artery. Surg Radiol Anat 36(3): p. 295-7. Yurasakpong, L., C. Nantasenamat, S. Janta, P. Eiamratchanee, J. Coey, A. Chaiyamoon, N. Kruepunga, T. Senarai, M.F. Langer, K. Meemon, and A. Suwannakhan (2022) The decreasing prevalence of the thyroid ima artery: A systematic review and machine learning assisted meta-analysis. Ann Anat 239: p. 151803. Benedict, T., S. Kuo, N.A.J. Adams, T. Ach, R. Michaels, and A.J. Zachwieja (2024) A thyroidea ima artery variation providing collateral circulation to the mediastinum. Surg Radiol Anat 46(4): p. 507-512. Alt, B., O.A. Elsalini, P. Schrumpf, N. Haufs, N.D. Lawson, G.C. Schwabe, S. Mundlos, A. Grüters, H. Krude, and K.B. Rohr (2006) Arteries define the position of the thyroid gland during its developmental relocalisation. Development 133(19): p. 3797-804. Zhang, M., J. Liu, A. Mao, G. Ning, Y. Cao, W. Zhang, and Q. Wang (2023) Tmem88 confines ectodermal Wnt2bb signaling in pharyngeal arch artery progenitors for balancing cell cycle progression and cell fate decision. Nat Cardiovasc Res 2(3): p. 234-250. Additional Declarations No competing interests reported. Cite Share Download PDF Status: Published Journal Publication published 13 Oct, 2025 Read the published version in Surgical and Radiologic Anatomy → Version 1 posted Editorial decision: Revision requested 03 Sep, 2025 Reviews received at journal 02 Sep, 2025 Reviews received at journal 29 Aug, 2025 Reviewers agreed at journal 28 Aug, 2025 Reviewers agreed at journal 27 Aug, 2025 Reviewers agreed at journal 26 Aug, 2025 Reviews received at journal 26 Aug, 2025 Reviewers agreed at journal 26 Aug, 2025 Reviewers invited by journal 26 Aug, 2025 Editor assigned by journal 26 Aug, 2025 Submission checks completed at journal 26 Aug, 2025 First submitted to journal 25 Aug, 2025 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-7454738","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":509207572,"identity":"de0c43f5-4af8-46fd-bc47-880a6eac718d","order_by":0,"name":"Fa-Bao Xu","email":"","orcid":"","institution":"Capital Medical University","correspondingAuthor":false,"prefix":"","firstName":"Fa-Bao","middleName":"","lastName":"Xu","suffix":""},{"id":509207573,"identity":"0ec603e8-ab65-4f98-9d66-096a71a1ee68","order_by":1,"name":"Wen-Bo Yue","email":"","orcid":"","institution":"Capital Medical University","correspondingAuthor":false,"prefix":"","firstName":"Wen-Bo","middleName":"","lastName":"Yue","suffix":""},{"id":509207574,"identity":"e7fa4ce2-c099-4f3e-803f-496d28979744","order_by":2,"name":"Chun Yang","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA40lEQVRIie3PIQvCQBTA8TcGS8PVs6gf4WAgiH6YtzLLFMFiPMsZZN3mV1g0Pj1wZWJdMCiCGAwaV0Q2+6ZN8P7h3QvvFw5Ap/vVDJFPMo446X1HTH5M/K8IWPWT3FRf83inrtlKDZvT+DJBi8CZzbGcJEO/EyZqzIn8FO0DsGQXlRMK2q4hlRcBbVNkF+BsUEH2tzdZirUcIVcfkDRwzzkRpCxA/IDU01vbCGXfi2hrMiTfrvxLbR+490x2veUiPj2yZ6/hzMJy0iKwWLExKh679DyvKcC8F5sjKo91Op3uT3sBvVRXF4i7WiQAAAAASUVORK5CYII=","orcid":"","institution":"Capital Medical University","correspondingAuthor":true,"prefix":"","firstName":"Chun","middleName":"","lastName":"Yang","suffix":""}],"badges":[],"createdAt":"2025-08-25 14:23:31","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-7454738/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-7454738/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1007/s00276-025-03741-6","type":"published","date":"2025-10-13T15:57:44+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":90485644,"identity":"57f59da3-c9b1-458e-a120-7b043a88c37d","added_by":"auto","created_at":"2025-09-03 08:49:12","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":344956,"visible":true,"origin":"","legend":"\u003cp\u003eThe distribution of the three main branches and several sub-branches of the thyroid ima artery. The white dotted circle indicated the left brachiocephalic vein (cut) (A).The artery divided into three main branches (branches 4-6) and the branch 6 further bifurcates into two additional branches (branches 7 and 8) (B). The branch 8 further subdivided into two additional branches (branches 9 and 20) (B). The relation of the branch of the TIMA and the left recurrent laryngeal nerve (C). Dissection of the left subclavian artery and its branches (D). A line diagram showing the absence of the LITA and characteristic of the TIMA (E). 1, TIMA; 2, inferior thyroid vein; 3, left brachiocephalic vein; 4-10, main branches and sub-branches of the TIMA; 11, thyrocervical trunk; 12, ascending cervical artery; 13, transverse cervical artery; 14, suprascapular artery; 15, left phrenic nerve; BCT, brachiocephalic trunk; LITA, left inferior thyroid artery; L/RCCA, left/right common carotid artery; LEJV, left external jugular vein; L/RIJV, left/right internal jugular vein; L/RSCA, left/right subclavian artery; lSCV, Left subclavian vein; RLN, recurrent laryngeal nerve; TIMA, thyroid ima artery.\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-7454738/v1/e0ff0b35c6192070e2d1cc01.png"},{"id":93956759,"identity":"55f1be69-7dff-4600-b62b-7bc7072228fe","added_by":"auto","created_at":"2025-10-20 16:12:11","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":694611,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-7454738/v1/27ebe118-13dd-4123-a4c6-745f4844a18d.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"A case report of an absence of the left inferior thyroid artery with compensating the thyroid ima artery","fulltext":[{"header":"Introduction","content":"\u003cp\u003eThe thyroid gland is an important endocrine organ situated in the midline of the anterior neck, typically extending from the fifth to the seventh cervical vertebrae. Being highly vascularized, it achieves blood supply primarily via the superior thyroid artery (STA) and the inferior thyroid artery (ITA). According to the anatomical textbooks, the STA is the first branch of the external carotid artery. On the other hand, the ITA arises from the thyrocervical trunk, which originates from the first part of the subclavian artery (SA). During the normal course of ITA, it ascends anterior to the anterior scalene muscle, turns medially at the level of transverse process of the sixth cervical vertebra, then descends anterior to the longus colli muscle, and ultimately reaches the inferior lobe of the thyroid gland.\u003c/p\u003e\u003cp\u003eIn addition to the typical origins, there are well documented anatomical variations of STA and ITA. A recent review has analyzed the variation of STA and ITA, highlighting the importance of understanding such anatomical variations for surgical practice [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. Several case reports recently have further presented other anatomical variations of inferior thyroid artery [\u003cspan additionalcitationids=\"CR3 CR4\" citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. Here, we reported an unusual variation for the absence of left ITA that was replaced by thyroid ima artery (TIMA) originating from the brachiocephalic trunk (BCT), which has not been demonstrated in the previous studies and case reports.\u003c/p\u003e"},{"header":"Case Presentation","content":"\u003cp\u003eA unilateral variation of the ITA was observed during neck dissection in a 64-year-old male cadaver at the anatomical laboratory of Capital Medical University. The specimen was embalmed with formalin before anatomical dissection. The whole dissection procedure was performed with great care for the adjacent organs, including nerves, glands, muscles, etc.\u003c/p\u003e\u003cp\u003eDuring the routine dissection of the neck, the bilateral blood supply of the thyroid gland was exposed. A variation in the left inferior thyroid artery (LITA) was observed. The LITA was missing, and the TIMA emerged and originated from the BCT (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eA). Measurements were obtained in ImageJ. The diameter of the TIMA was 2.54 mm. After its course in a main trunk (15. 93 mm in length), it ran downwards (6.67 mm in length), diagonally (4.18 mm in length), and then upwards (5.08 mm in length), forming a U-shape till its bifurcation into the lower part of the thyroid gland (1 in Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Furthermore, the TIMA gave off three branches (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eB and E).\u003c/p\u003e\u003cp\u003e\u003c/p\u003e\u003cp\u003eThe first branch of TIMA (1.67 mm in diameter) descended inferiorly before entering into the adipose tissue in anterior mediastinum (branch 4 in Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eA and B). The second branch of TIMA (1.53 mm in diameter) traveled superiorly and entered into the lower portion of the right lobe of thyroid gland (branch 2 in Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eA and B). The third branch of TIMA (2.08 mm in diameter) (branch 6 in Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eA and B) travelled medially and superiorly and subdivided into two additional branches (branches 7 and 8 in Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eA and B) before entering into the thyroid isthmus. The branch 7 traveled superiorly and laterally and entered into the left lobe of thyroid gland. The branch 8 further subdivided into two additional branches (branches 9 and 10 in Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eA and B). The branch 9 terminated in the thyroid isthmus and the branch 10 traveled superiorly and terminated in the lower portions of the thyroid gland that closely to the entry point of the branch 6.\u003c/p\u003e\u003cp\u003eAs shown in Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eC, the branch of the TIMA ascended parallel to the left recurrent laryngeal nerve. The distance between them was approximately 5.26 mm. This relationship differs from the classic anterior, posterior, or inter-arterial courses described between the recurrent laryngeal nerve and the ITA.\u003c/p\u003e\u003cp\u003eIn order to further confirm the variation of LITA, the left thyrocervical trunk and its branches were also dissected. The left thyrocervical trunk, a branch of the left subclavian artery (LSCA), gave off several branches, including transverse cervical artery (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eD, 13), suprascapular artery (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eD, 14), and others. After further dissection and tracking, the branches of the left thyrocervical trunk did not give off any branches to supply the lower part of the thyroid gland.\u003c/p\u003e\u003cp\u003eThe right inferior thyroid artery originated from the right thyrocervical trunk, which was normal without variation. The course of RITA was also observed to be normal with no variation. The anatomical relation of RITA and right recurrent laryngeal nerve on the right side was normal without variation.\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eAnatomical variations in humans are indispensable parts of human gross anatomy, and play a key role in understanding human diversity. The primary significance of individual variations is to enhance diagnostic accuracy and therapeutic efficacy, particularly in surgery intervention [\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e]. Consequently, studies or case reports of anatomical variations have gained considerable scientific interest. Many articles have documented anatomical variations of ITA [\u003cspan additionalcitationids=\"CR2 CR3 CR4\" citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. As far as we know, the current case represents a distinctive variation of an absence of LITA and compensation by TIMA arising from the BCT, which is worthy of our attention and further study.\u003c/p\u003e\u003cp\u003eIt has been demonstrated that anatomical variations of ITA may be absent, exhibit duplication, arise from different levels, or be replaced with other arteries [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e, \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. Specifically, a case study had reported the hypoplastic RITA and absence of LITA [\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e]. An absence of bilateral ITAs was also described during a neck region dissection [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e, \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e]. A recent case report also provided evidence of absence of ITA bilaterally [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. In such cases, it is TIMA that compensates for the missing ITA. However, Sherman and colleagues reported a case that LITA was absent, but TIMA was not found [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. We here described a case that the LITA was absent and replaced by the TIMA originating from the BCT. Notablly, a particular case report by Weiglein and colleagues has documented that the absence of RITA was compensated by a TIMA branching off the right internal thoracic artery and the absence of LITA was compensated by a branch from the vertebral artery [\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e]. These findings highlight the necessary to increase awareness of the arteries serving a compensatory role for blood supply to the thyroid gland when the ITA is absent.\u003c/p\u003e\u003cp\u003eClinically, a deep knowledge of vascularization of thyroid gland is essential for surgical practices on the neck. A 2022 review article has described abnormal originations of the ITA [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. The majority of ITA originates from the thyrocervical trunk; it can also anomalously originate from the common carotid artery, followed by the subclavian artery, the vertebral artery or the suprascapular artery [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e, \u003cspan additionalcitationids=\"CR4\" citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e, \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e]. TIMA, an uncommon variance, typically compensates for ITA absence and originates from the brachiocephalic trunk, the right common carotid artery, the right internal thoracic artery, and the aortic arch [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e, \u003cspan additionalcitationids=\"CR14 CR15\" citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e]. Notably, Sannomiya, et al. reported a rare double TIMA without classic thyroid arteries variations [\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e]. Niida and Yamasaki proposed a classification of TIMA according to its anatomical origin. The classification divides the double TIMA variants into three subtypes: type 1 originating from brachiocephalic trunk and common carotid artery; type 2 originating from brachiocephalic trunk and aortic arch; type 3 originating from right internal thoracic artery and left internal thoracic artery [\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e, \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e]. Although the TIMA is often present as a compensatory variation for the absence of ITA, Esen et al. reported concurrent presence of TIMA and ITA in 7/15 cases (46%), indicating that they are unnecessarily mutually exclusive [\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e].\u003c/p\u003e\u003cp\u003eA recent report described a presence of multiple branches of TIMA over the trachea during a cadaver dissection; such TIMA and its branching pattern leads to a high risk for abnormal bleeding during tracheotomy or cricothyroidotomy [\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e, \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e]. This anatomical variation underscores the values of the preoperative CT angiography or arteriogrphic investigation to optimize patient outcomes [\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e, \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e]. Ultrasound-guided percutaneous dilatational tracheostomy (US-PDT) could facilitate prevention of vascular puncture. Thus, US-PDT can be used as an alternative to fIber-optic bronchoscopy dilatational tracheostomy [\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e]. Additionally, TIMA could be safely and effectively embolized for the management of Graves\u0026rsquo; disease and thyroid storm [\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e].\u003c/p\u003e\u003cp\u003eSome evidence indicated that the variation of TIMA may be due to the regression and persistence of vascular structures of thyroid gland in embryonic stage. Thyroid gland is supplied by many arteries during its development [\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e, \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e]. Finally, most of them disappear, leaving behind STA and ITA as the regular arteries supplying thyroid gland in adult. A recent study analyzed the prevalence of TIMA with a meta-analysis [\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e]. A higher prevalence of TIMA was present in human fetuses (14.8%) than adults (3.3%). Therefore, Yurasakpong and colleagues predicted that TIMA may function as a normal developmental artery and its persistence beyond the fetal stage would result in its classification as an anatomical variant. Similar to the previous description [\u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e], the TIMA in this case supplies blood to thyroid gland and adipose tissue in anterior mediastinum (the remnant of thymus gland), which supporting the hypothesis of Yurasakpong et al. Vascular endothelial growth factor (VEGF), a signaling protein for angiogenesis, has been reported to be highly expressed in the developing thymus and thyroid gland of zebrafish [\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e]. This biological characteristic suggests a further investigation into the potential relationship between VEGF dynamics and the regression and persistence mechanisms of TIMA. In addition, during embryogenesis, the pharyngeal arch arteries are transient embryonic blood vessels that remodel to form the critical segments of the aortic and its branches. The factors regulating angiogenesis of pharyngeal arch arteries such as Tmem88 (a Wnt signaling modulator expressed in pharyngeal mesoderm) [\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e] might be linked to the regression and persistence of TIMA. Therefore, future investigations are needed to detect the genetic factors related to the development of TIMA.\u003c/p\u003e\u003cp\u003eIn summary, anatomical variations play a pivotal role in the clinical practice of medicine, particularly in surgical disciplines. Descriptive studies based on cadaver dissection, imaging examination and surgical procedures, can provide more evidence of variation. An increasing number of studies have documented the variations of arteries for the thyroid gland. However, the case here stands out as a distinctive instance of the missing LITA being replaced by the TIMA arising from the BCT. Such anatomical variation occurrence underscores the importance of anatomical study and is essential for medical practice, which can have profound implications for surgical interventions and clinical outcomes.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAuthor contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eFa-Bao Xu and Wen-Bo Yue performed dissection and identify the structures. Fa-Bao Xu prepared the figure. Chun Yang wrote the manuscript. Fa-Bao Xu and Chun Yang reviewed and edited the manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis study was funded by\u0026nbsp;Beijing Association of Higher Education (grant number MS2023268).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgments\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors sincerely thank those who donated their bodies to science so that anatomical research could be performed. Results from such research can potentially increase mankind's overall knowledge that can then improve patient care. Therefore, these donors and their families deserve our highest gratitude.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflict of Interest\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare that they have no conflict of interest.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eBranca, J.J.V., A. Lascialfari Bruschi, A.M. Pilia, D. Carrino, G. Guarnieri, M. Gulisano, A. Pacini, and F. Paternostro (2022) The Thyroid Gland: A Revision Study on Its Vascularization and Surgical Implications. Medicina (Kaunas) 58(1).\u003c/li\u003e\n\u003cli\u003eHvizdo\u0026scaron;ov\u0026aacute;, N., J. Vecanov\u0026aacute;, S. Mat\u0026eacute;ffy, and I. Hodorov\u0026aacute; (2022) Combined unusual origin and course of the right vertebral artery and right inferior thyroid artery: a case report. 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Eiamratchanee, J. Coey, A. Chaiyamoon, N. Kruepunga, T. Senarai, M.F. Langer, K. Meemon, and A. Suwannakhan (2022) The decreasing prevalence of the thyroid ima artery: A systematic review and machine learning assisted meta-analysis. Ann Anat 239: p. 151803.\u003c/li\u003e\n\u003cli\u003eBenedict, T., S. Kuo, N.A.J. Adams, T. Ach, R. Michaels, and A.J. Zachwieja (2024) A thyroidea ima artery variation providing collateral circulation to the mediastinum. Surg Radiol Anat 46(4): p. 507-512.\u003c/li\u003e\n\u003cli\u003eAlt, B., O.A. Elsalini, P. Schrumpf, N. Haufs, N.D. Lawson, G.C. Schwabe, S. Mundlos, A. Gr\u0026uuml;ters, H. Krude, and K.B. Rohr (2006) Arteries define the position of the thyroid gland during its developmental relocalisation. Development 133(19): p. 3797-804.\u003c/li\u003e\n\u003cli\u003eZhang, M., J. Liu, A. Mao, G. Ning, Y. Cao, W. Zhang, and Q. Wang (2023) Tmem88 confines ectodermal Wnt2bb signaling in pharyngeal arch artery progenitors for balancing cell cycle progression and cell fate decision. Nat Cardiovasc Res 2(3): p. 234-250.\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"surgical-and-radiologic-anatomy","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"sara","sideBox":"Learn more about [Surgical and Radiologic Anatomy](http://link.springer.com/journal/276)","snPcode":"276","submissionUrl":"https://submission.nature.com/new-submission/276/3","title":"Surgical and Radiologic Anatomy","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"Inferior thyroid artery, Thyroid ima artery, Brachiocephalic trunk, Anatomical variation, Recurrent laryngeal nerve","lastPublishedDoi":"10.21203/rs.3.rs-7454738/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-7454738/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eHere, we report an anatomical variation of the left inferior thyroid artery in a male cadaver during routine neck dissection. The left inferior thyroid artery was absent and replaced by the thyroid ima artery. The thyroid ima artery formed a U-shaped course and gave branches to the lower part of the thyroid gland. In addition, the thyroid ima artery arose from the brachiocephalic trunk. Furthermore, the branch of the thyroid ima artery ascended parallel to the left recurrent laryngeal nerve. There was no anatomical variation of the right inferior thyroid artery.\u003c/p\u003e","manuscriptTitle":"A case report of an absence of the left inferior thyroid artery with compensating the thyroid ima artery","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-09-03 08:49:08","doi":"10.21203/rs.3.rs-7454738/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2025-09-03T19:18:03+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-09-02T15:35:27+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-08-29T12:08:13+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"149794851706361472476200095928188165130","date":"2025-08-28T22:05:39+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"252230091651917713678106456472016703626","date":"2025-08-27T06:02:56+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"313362779415190244482007523774967933719","date":"2025-08-26T22:03:58+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-08-26T21:32:09+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"53794344922086979937864507202181220052","date":"2025-08-26T21:28:07+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2025-08-26T21:25:54+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2025-08-26T20:17:00+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2025-08-26T04:52:12+00:00","index":"","fulltext":""},{"type":"submitted","content":"Surgical and Radiologic Anatomy","date":"2025-08-25T14:11:29+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"surgical-and-radiologic-anatomy","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"sara","sideBox":"Learn more about [Surgical and Radiologic Anatomy](http://link.springer.com/journal/276)","snPcode":"276","submissionUrl":"https://submission.nature.com/new-submission/276/3","title":"Surgical and Radiologic Anatomy","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"074b1c6b-5a69-4806-9ad7-1c38704eb6be","owner":[],"postedDate":"September 3rd, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2025-10-20T16:09:23+00:00","versionOfRecord":{"articleIdentity":"rs-7454738","link":"https://doi.org/10.1007/s00276-025-03741-6","journal":{"identity":"surgical-and-radiologic-anatomy","isVorOnly":false,"title":"Surgical and Radiologic Anatomy"},"publishedOn":"2025-10-13 15:57:44","publishedOnDateReadable":"October 13th, 2025"},"versionCreatedAt":"2025-09-03 08:49:08","video":"","vorDoi":"10.1007/s00276-025-03741-6","vorDoiUrl":"https://doi.org/10.1007/s00276-025-03741-6","workflowStages":[]},"version":"v1","identity":"rs-7454738","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-7454738","identity":"rs-7454738","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}

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last seen: 2026-05-20T01:45:00.602351+00:00
unpaywall
last seen: 2026-05-22T02:00:06.705733+00:00
License: CC-BY-4.0