|Year : 2020 | Volume
| Issue : 2 | Page : 119-123
The incidence and grade of tubercle of zuckerkandl and its relationship to the course of recurrent laryngeal nerve in thyroid surgery
Ashwin Gajendran Vedhapoodi1, Vivek Mariappan2, Suresh Kumar Narayanan2, S Mohamed Siddique2, Venugopal Mohan Kumar2
1 Department of ENT, Government Stanley Medical College, Chennai, Tamil Nadu, India
2 Department of ENT, Madras Medical College, Chennai, Tamil Nadu, India
|Date of Submission||06-Sep-2020|
|Date of Acceptance||14-Sep-2020|
|Date of Web Publication||8-Dec-2020|
17/9, Second Main Road, New Colony, Chromepet, Chennai - 600 044, Tamil nadu
Source of Support: None, Conflict of Interest: None
Aim of the Study: The aim is to study the incidence and grade of Zuckerkandl’s tubercle (ZT) and the course of recurrent laryngeal nerve (RLN) with respect to the grade of ZT. Settings and Design: A prospective observational anatomical study. Materials and Methods: The relationship of ZT to RLN was studied, and the size of the ZT was measured and graded according to Pelizzo’s grading system in all cases of routine thyroidectomy in 36 patients (45 sides) from December 2018 to November 2019. Results: ZT was present in 32 (71.11%) of the sides, more commonly on the right side in 24 (88.89%) with a P value of 0.001. Among the total thyroidectomy, bilateral ZT was present in 7 cases (77.78%). In the 45 sides Grade 0 was noted in 13/45 (28.89%), Grade I 14/45 (31.11%), Grade II 9/45 (20%), and Grade III 9/45 (20%) with a P value of 0.001. ZT more than 0 but less than 1 cm was the most common occurrence (Grade I and II). In the 32 sides which had ZT, 23/32 (71.88%) were Type A (posterior) and 9/32 (28.12%) were type D (lateral) with a P value of 0.01. Conclusions: The identification and meticulous dissection of ZT ensures completeness of thyroidectomy. As the size of the ZT increases, the nerve often runs posterior and medial to surface of ZT. The site of ZT can be considered an eloquent area in thyroid surgery as it lies in proximity to the RLN and superior parathyroid gland.
Keywords: Anatomical landmark, recurrent laryngeal nerve, thyroidectomy, tubercle of Zuckerkandl
|How to cite this article:|
Vedhapoodi AG, Mariappan V, Narayanan SK, Siddique S M, Kumar VM. The incidence and grade of tubercle of zuckerkandl and its relationship to the course of recurrent laryngeal nerve in thyroid surgery. J Head Neck Physicians Surg 2020;8:119-23
|How to cite this URL:|
Vedhapoodi AG, Mariappan V, Narayanan SK, Siddique S M, Kumar VM. The incidence and grade of tubercle of zuckerkandl and its relationship to the course of recurrent laryngeal nerve in thyroid surgery. J Head Neck Physicians Surg [serial online] 2020 [cited 2021 Jan 23];8:119-23. Available from: https://www.jhnps.org/text.asp?2020/8/2/119/302632
| Introduction|| |
Thyroid surgery is one of the common head and neck procedures. The surgeon must be aware of the intricacy and the variations of the gland and the surrounding vital structure, especially the recurrent laryngeal nerve (RLN) and parathyroid glands with its vascular supply. The tubercle of Zuckerkandl was first described by Emil Zuckerkandl, an Austrian anatomist, as a posterior extension of the lateral lobes of the thyroid containing thyroid tissue itself. Pelizzo et al. in 1998 described Zuckerkandl’s tubercle (ZT) as a reliable landmark for RLN. The surgical importance of ZT includes its complete excision during thyroidectomy and its close relationship to the RLN.
Although the incidence of injury to RLN is relatively low in an effort to safeguard the nerve, the blood supply to the parathyroid glands may be damaged or compromised. The superior approach of dissection for identifying the RLN is gaining popularity since it avoids unwarranted dissection in the tracheoesophageal groove, which leads to vascular compromise of the parathyroid glands. The ZT is a constant landmark in this approach for the safe identification of the RLN. The ZT is classified based on its size into four different groups., The running pathway of RLN in relation to ZT can be classified into four types. The objective of this study is to study the incidence and grade of ZT and the course of RLN with respect to the grade of ZT.
| Materials and Methods|| |
A prospective anatomical observational study was conducted during routine thyroidectomy in 36 patients (45 sides) from December 2018 to November 2019 at our institution. All patients undergoing thyroidectomy (total thyroidectomy, hemithyroidectomy) for benign and malignant pathology were included in the study. Revision thyroidectomies were excluded from the study. All procedures followed in the study were in accordance with the ethical standards of the institutional ethical committee and with the Helsinki Declaration of 1975, as revised in 2000. Informed consent was obtained from all the patients. The preoperative fine-needle aspiration cytology (FNAC) was done in all cases. Under general anesthesia and patient in supine and extended neck position, horizontal prominent skin crease incision was made. Standard dissection protocol was followed. Subplatysmal flaps were elevated, and the strap muscles were separated along the midline raphe. The thyroid capsule was identified, and the extracapsular avascular plane was reached [Figure 1]a. The middle thyroid vein if present was identified and ligated. Then, the dissection was proceeded in a superior to inferior direction. The superior thyroid pole was identified, and the branches of superior thyroid artery were dissected and ligated individually close to the gland to avoid injury to the external branch of superior laryngeal nerve. Then, the lateral lobe was medialized to identify the posterolateral border and the ZT. The superior parathyroid gland and the RLN lie in proximity with the ZT and were identified. The superior parathyroid gland was preserved [Figure 1]b. The relationship of ZT to RLN was studied in all cases by a single surgeon, and the size of the ZT was measured (Apex of ZT to groove between ZT and thyroid lateral margin). The dissection was proceeded inferiorly close to the capsule when identifying and preserving the inferior parathyroid gland and ligating the inferior thyroid artery branches close to the gland. Finally, the entire lobe was mobilized after ligating the inferior thyroid venous plexus. The same was carried out on the other side in case of total thyroidectomy, and the entire gland was removed along with the isthmus and pyramidal lobe if present [Figure 1]c.
|Figure 1: (a) Extracapsular avascular plane of Right thyroid lobe (>) Inferior thyroid artery (*) Common Carotid artery. (b) Right superior parathyroid dissection staying close to the capsule. (c) Total thyroidectomy specimen showing bilateral Zuckerkandl’s tubercle (*) Note right is Grade II and Left is Grade I Zuckerkandl’s tubercle|
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The size of ZT was classified according to Pelizzo’s grading system: Grade 0 (unrecognizable), Grade I (<0.5 mm – only thickening), Grade II (0.5–1 cm), and Grade III (>1 cm). The position of the RLN in relation to ZT was studied as A (posterior to ZT surface), B (anterior to ZT surface), C (through parenchyma), and D (lateral – attached to apex or departing from the apex of ZT) [Figure 2] and [Figure 3].
|Figure 2: (a) Left Grade 0 Zuckerkandl’s tubercle – (^) left recurrent laryngeal nerve (*) left superior parathyroid in its mesentry. (b)(*) Right Grade II Zuckerkandl’s tubercle (^) right recurrent laryngeal nerve lying postero-medial to Zuckerkandl’s tubercle (Type A position)|
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|Figure 3: (a) (*) Right Grade I Zuckerkandl’s tubercle (^) right recurrent laryngeal nerve lying postero-lateral to Zuckerkandl’s tubercle (Type D position). (b) (*) Left Grade III Zuckerkandl’s tubercle in the same patient (^) left recurrent laryngeal nerve lying postero-medial to Zuckerkandl’s tubercle (Type A position)|
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The vocal cord status of all patients was documented in all patients, 1 week postoperatively. All the data were compiled and statistical analysis was done by IBM SPSS Statistics for Windows, Version 20.0., IBM Corp., Chicago, IL, USA.
| Results|| |
In this intraoperative anatomical study, a total of 36 patients (45 sides) were studied. There were 12 males and 24 females. The age group ranged from 30 to 56 with a mean age of 43.25 years. The preoperative cytological findings (FNAC) were colloid goiter (28 cases), follicular adenoma (6 cases), and papillary thyroid carcinoma (2 cases). There were 9 total thyroidectomies and 27 hemithyroidectomies, of which 18 were right hemithyroidectomies and 9 were left hemithyroidectomies [Table 1]a and [Table 1]b.
Incidence and grade of tubercle of Zuckerkandl
The tubercle of Zuckerkandl was present in 32 (71.11%) of the sides, more commonly on the right side in 24 (88.89%). It was present in 8 (44.44%) on the left side [Table 2]. Among the 9 patients who underwent total thyroidectomy, bilateral ZT was present in 7 cases (77.78%). In the total of 45 sides, Grade 0 was 13/45 (28.89%), Grade I 14/45 (31.11%), Grade II 9/45 (20%), and Grade III 9/45 (20%). Among the right-sided ZTs, Grade 0 was noted in 3/27 (11.11%), Grade I 10/27 (37.04%), Grade II 6/27 (22.22%), and Grade III 8/27 (29.63%). Among the left side ZTs, Grade 0 was noted in 10/18 (55.56%), Grade I 4/18 (22.22%), Grade II 3/18 (16.67%), and Grade III 1/18 (5.55%) [Table 3].
|Table 3: Relationship of Zuckerkandl's tubercle and recurrent laryngeal nerve (n=32)|
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Relationship between Zuckerkandl’s tubercle and recurrent laryngeal nerve
The main RLN running pathways were studied after excluding 13 sides which were Grade 0 of ZT on both the right and left sides. In the remaining 32 sides which had ZT, 23/32 (71.88%) were Type A (posterior to ZT surface) and 9/32 (28.12%) were type D (lateral – attached to apex or departing from the apex). The Type B (anterior to ZT surface) or Type C (through the parenchyma of ZT) relations were not seen in any of the sides. In the right side ZTs, 20/24 (83.33%) were type A and 4/24 (16.67%) were type D. In left side ZTs, 3/8 (37.50%) were type A and 5/8 (62.50%) were Type D [Table 4]. Overall, it was observed that smaller the ZT, the nerve runs just at the apex or posterolateral to the apex of the ZT. As the size of the ZT increases, the nerve more often runs posterior and medial to the surface of the ZT. Whenever the ZT was present, it was a consistent and reliable marker for the identification of RLN.
|Table 4: Comparison of grade of Zuckerkandl's tubercle to type of recurrent laryngeal nerve|
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There was no vocal cord paresis or palsy postoperatively in any of the 36 patients.
All efforts were taken to preserve the parathyroid glands in all the patients. In one patient with papillary thyroid carcinoma on the left lobe, both the superior and inferior parathyroid glands were removed along with a left side central neck dissection. This patient had a transient hypocalcemia and hypoparathyroidism in the immediate postoperative period, which recovered later with calcium gluconate. None of the other patients had any features of hypoparathyroidism.
| Discussion|| |
Thyroidectomy is a common head and neck procedure and the major concern is the preservation of RLN and parathyroid glands, injury to which will affect the quality of life of the patient.
Otto Wilhelm Madelung in 1867 described ZT as a “posterior horn of the thyroid.”, Emil Zuckerkandl popularized it in 1902 and described it as “processus posterior glandula thyroidea.” In 1998, Pelizzo rediscovered this structure as a constant anatomical surgical landmark for identifying the RLN and graded it according to the size.
Embryologically, the thyroid originates from the medial and lateral anlages. The median anlage is made up of follicular cells and it arises from the epithelial cells of the foramen cecum. It descends along the midline and forms the median thyroid which forms the major part of the gland. The lateral thyroid anlage develops from the 4th or the 5th branchial cleft and forms the ultimobranchial body. It consists of the parafollicular C cells. The lateral thyroid thus formed is the ZT., The ZT is embryologically considered to be arising from the fusion of medial and lateral thyroid anlages.
The classical method of dissection was to trace the RLN by dissecting along the entire cervical RLN in the triangular area bounded by the common carotid artery laterally, inferior thyroid artery superiorly, and the berry’s ligament with the RLN itself medially in the tracheoesophageal groove.,,, However, in 1988, it was Pelizzo et al. who suggested that the ZT is a reliable landmark for the identification of the RLN by the superior approach to dissection.
The incidence of ZT in literature varies widely from 7.04% to 90.5%.,,,,,, The wide heterogeneity could be due the difference in the geographical location, ethnicity, the size of the gland, or the type of tumor (benign, malignant). Among these in the two Indian studies by Irawati et al. and Singh et al., the incidence of ZT was 90.5% and 87.86%, respectively, whereas in our study, it was 71% which is only marginally less compared to those previous studies.
In our study, we observed that the incidence of ZT was more common on the right side 24/27 (88.89%) as compared to the left side 8/18 (44.44%). The right side was common in most of the studies. Mehanna et al. looked at the difference in incidence of ZT on both sides and reported the incidence to be 72.6% on the right and 53.9% on the left side. Various other studies by Gurleyik and Gurleyik - 53/87 (61%), Sheahan - 71/102 (69.6%), Irawati et al. - 93%, and Singh et al. - 85.41%, show that the ZT is more common on the right side.,,,
The incidence of bilateral ZT in our study was 7/9 (77.77%). In the study conducted by Yun et al., the incidence of bilaterality was 91.2% and Irawati et al. reported 80.7%. Pelizzo et al. reported the presence of ZT in 104 Italian patients during lobectomy and found Grade 0 in 24 (23%), Grade I in 9 (8.6%), Grade II in 56 (53.8%), and Grade III in 15 (14.4%) sides. In our study, majority of the sides had Grade I (31.11%) and Grade II (20%) of ZT – 23/45 (51.11%). Majority of the studies have documented Grade I and Grade II ZT as highest occurrence with incidence ranging from 18% to 90%.,,,,,, Grade III of ZT was present in 9/45 (20%) of sides in our study, of which it was more common on the right side 8/9. Pelizzo et al. reported 14.4% and Irawati et al. reported 11% of the sides as grade III, which was almost similar to our study. The positive identification of ZT and its meticulous dissection ensures completeness of thyroidectomy.
The most common relationship of ZT with respect to RLN was type A 23/32 (71.88%), followed by type D 9/32 (28.12%) in our study. The Type B and Type C positions were never encountered in our study. Gauger et al. reported that in 93% of patients, the nerve was located medial to ZT, while in 7% of cases, RLN passed laterally. In another study by Yun et al., the nerve was posterior to ZT in more than 90% of cases, and only in 0.5% of cases, it lied anterior to ZT surface. It was present lateral to ZT in <10% of cases. Gil-Carcedo et al. found RLN posterior to ZT in 95% of cases. The smaller the ZT, the nerve runs just at the apex or posterolateral to the apex of the ZT. As the size of the ZT increases, the nerve more often runs posterior and medial to the surface of the ZT. Whenever the ZT was present, it was a consistent and reliable marker for the identification of RLN.
| Conclusions|| |
The tubercle of Zuckerkandl is a posterolateral extension of lateral lobes of thyroid gland seen in majority of the patients undergoing thyroid surgery. As the size of the ZT increases, the nerve more often runs posterior and medial to the surface of the ZT. Positive identification and meticulous dissection of ZT ensures completeness of the thyroidectomy. The site of ZT can be considered an eloquent area in thyroid surgery as it lies in proximity to the RLN and superior parathyroid gland. Hence, it is a reliable landmark for the RLN and the surgeon must be aware of its variations including grade and position.
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Conflicts of interest
There are no conflicts of interest.
This material has never been published and is not currently under evaluation in any other peer reviewed publication.
The permission was taken from Institutional Ethics Committee prior to starting the project. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent was obtained from all individual participants included in the study.
| References|| |
Zuckerkandl E. Nebst Bermerkungen uber die Epithelkorperchen des Menschen. Anat Hefte 1902;LXI: 61.
Pelizzo MR, Toniato A, Gemo G. Zuckerkandl’s tuberculum: An arrow pointing to the recurrent laryngeal nerve (constant anatomical landmark). J Am Coll Surg 1998;187:333-6.
Gurleyik E, Gurleyik G. Incidence and surgical importance of Zuckerkandl’s tubercle of the thyroid and its relations with recurrent laryngeal nerve. ISRN Surg 2012;2012:450589.
Irawati N, Vaish R, Chaukar D, Deshmukh A, D’Cruz A. The tubercle of Zuckerkandl: An important landmark revisited. Indian J Surg Oncol 2016;7:312-5.
Gravante G, Delogu D, Rizzello A, Filingeri V. The Zuckerkandl tubercle. Am J Surg 2007;193:484-5.
Yun JS, Lee YS, Jung JJ, Nam KH, Chung WY, Chang HS, et al
. The Zuckerkandl’s tubercle: A useful anatomical landmark for detecting both the recurrent laryngeal nerve and the superior parathyroid during thyroid surgery. Endocr J 2008;55:925-30.
Sturniolo G, D’Alia C, Tonante A, Gagliano E, Taranto F, Lo Schiavo MG. The recurrent laryngeal nerve related to thyroid surgery. Am J Surg 1999;177:485-8.
Mirilas P, Skandalakis JE. Zuckerkandl’s tubercle: Hannibal ad Portas. J Am Coll Surg 2003;196:796-801.
Clifton-Bligh R, Delbridge LW. Thyroid Physiology. In: Clark OH, Duh WH, Siperstein C, editors. Textbook of Endocrine Surgery. 2nd
ed. Philadelphia: W. B. Saunders; 2003. p. 3-7.
Weller GL Jr. Development of the thyroid, parathyroid and thymus glands in man. Contrib Embryol Carnegie Inst Wash 1933;24:93-142.
Mansberger AR Jr., Wei JP. Surgical embryology and anatomy of the thyroid and parathyroid glands. Surg Clin North Am 1993;73:727-46.
Singh P, Sharma K, Agarwal S. Per operative study of relation of Zuckerkandl tubercle with recurrent laryngeal nerve in thyroid surgery. Indian J Otolaryngol Head Neck Surg 2017;69:351-6.
Lahey RF. Routine dissection and demonstration of the recurrent laryngeal nerve in subtotal thyroidectomy. Surg Gynecol Obstet 1938;66:775-7.
Simon MM. Pitfalls to be avoided in thyroidectomy; a triangle for localization and protection of the recurrent nerve. J Int Coll Surg 1951;15:428-42.
Lekacos NL, Tzardis PJ, Sfikakis PG, Patoulis SD, Restos SD. Course of the recurrent laryngeal nerve relative to the inferior thyroid artery and the suspensory ligament of Berry. Int Surg 1992;77:287-8.
Sasou S, Nakamura S, Kurihara H. Suspensory ligament of berry: Its relationship to recurrent laryngeal nerve and anatomic examination of 24 autopsies. Head Neck 1998;20:695-8.
Page C, Cuvelier P, Biet A, Boute P, Laude M, Strunski V. Thyroid tubercle of Zuckerkandl: Anatomical and surgical experience from 79 thyroidectomies. J Laryngol Otol 2009;123:768-71.
Kaisha W, Wobenjo A, Saidi H. Topography of the recurrent laryngeal nerve in relation to the thyroid artery, Zuckerkandl tubercle, and Berry ligament in Kenyans. Clin Anat 2011;24:853-7.
Sheahan P, Murphy MS. Thyroid tubercle of Zuckerkandl: Importance in thyroid surgery. Laryngoscope 2011;121:2335-7.
Mehanna R, Murphy MS, Sheahan P. Thyroid tubercle of zuckerkandl is more consistently present and larger on the right: A prospective series. Eur Thyroid J 2014;3:38-42.
Gauger PG, Delbridge LW, Thompson NW, Crummer P, Reeve TS. Incidence and importance of the tubercle of Zuckerkandl in thyroid surgery. Eur J Surg 2001;167:249-54.
Rajapaksha A, Fernando R, Ranasinghe N, Iddagoda S. Morphology of the tubercle of Zuckerkandl and its importance in thyroid surgery. Ceylon Med J 2015;60:23-4.
Pradeep PV, Jayashree B, Harshita SS. A closer look at laryngeal nerves during thyroid surgery: A descriptive study of 584 nerves. Anat Res Int 2012;2012:490390.
Hisham AN, Aina EN. Zuckerkandl’s tubercle of the thyroid gland in association with pressure symptoms: A coincidence or consequence? Aust N Z J Surg 2000;70:251-3.
Gil-Carcedo E, Menéndez ME, Vallejo LA, Herrero D, Gil-Carcedo LM. The Zuckerkandl tubercle: Problematic or helpful in thyroid surgery? Eur Arch Otorhinolaryngol 2013;270:2327-32.
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4]