• Users Online: 304
  • Home
  • Print this page
  • Email this page
Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 


 
 Table of Contents  
REVIEW ARTICLE
Year : 2018  |  Volume : 5  |  Issue : 2  |  Page : 91-95

Review of surgical anatomy of tubercle of Zuckerkandl and its importance in thyroid surgery


Department of Anatomy, Azeezia Institute of Medical Sciences, Kollam, Kerala, India

Date of Web Publication9-Apr-2018

Correspondence Address:
S Viveka
Department of Anatomy, Azeezia Institute of Medical Sciences, Kollam - 691 537, Kerala
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/cjhr.cjhr_107_17

Rights and Permissions
  Abstract 


Background and Objectives: Tubercle of Zuckerkandl (TZ) is the posterior or posterolateral extension of thyroid gland. Recurrent laryngeal nerve (RLN) is related to TZ either on its posterior or posteromedial aspect in the deeper fascial plane. The objective of this review is to report separately the prevalence of TZ as noted by anatomists and surgeons. Materials and Methods: An extensive search for articles with TZ either in the title or keywords was done using PubMed, ScienceDirect, Google Scholar, SciELO, EMBASE, and Web of Science databases. The search terms were restricted to TZ, Zuckerkandl tubercle, posterolateral extension of thyroid, RLN, and thyroid surgeries. Results: Out of 39 records, 25 studies, reported total number of sides where TZ was studied with prevalence percentages (n = 4231 sides). This included 6 cadaveric studies and 19 surgical studies. Combined pooled prevalence of TZ was found to be 76.5%. Prevalence in cadaveric and surgical studies was 84% and 69%, respectively. Overall, 15 studies reports RLN is related to posterior or posteromedial to TZ. Conclusions: The prevalence of TZ is 76.5%. When present, it is a useful guide for locating, dissecting, and preserving RLN. Cadaveric studies report a higher prevalence of 84%, while surgical studies report an average of 69% TZ. Most surgical studies report higher right-sided prevalence.

Keywords: Recurrent laryngeal nerve, thyroid surgeries, tubercle of Zuckerkandl


How to cite this article:
Viveka S. Review of surgical anatomy of tubercle of Zuckerkandl and its importance in thyroid surgery. CHRISMED J Health Res 2018;5:91-5

How to cite this URL:
Viveka S. Review of surgical anatomy of tubercle of Zuckerkandl and its importance in thyroid surgery. CHRISMED J Health Res [serial online] 2018 [cited 2018 Apr 26];5:91-5. Available from: http://www.cjhr.org/text.asp?2018/5/2/91/229578




  Introduction Top


Posterolateral extension of thyroid lobe is the tubercle of Zuckerkandl (TZ). This is named after eminent anatomist Emil Zuckerkandl (described it in 1902), who is known for his work on neural crest cells (in relation to aorta), temporal bone pneumatization, and fascial covering of kidney. However, Otto Madelung was the first one to describe the posterolateral extension of thyroid gland in 1867. Thyroid parenchyma condenses and forms a small outward posterolateral projection at the level of cricothyroid junction. This is referred as TZ [Figure 1]. While the endodermal outgrowth from the junction of anterior two-third and posterior one-third of tongue descends downward, forming thyroglossal duct, it later divides to the right and left lobes. Adding to these cells, the 4th pharyngeal cleft and ultimobranchial body also contribute to developing thyroid. Such fusion is said to form TZ. Microscopic analysis of component cells of TZ reveals that it has a higher concentration of C cells in addition to thyroid follicles.[1],[2] Superior parathyroid gland being relatively more constant in position is located posterior to TZ.
Figure 1: Schematic diagram showing posterior extension of thyroid gland - tubercle of Zuckerkandl

Click here to view


Nerve injuries are most dreaded complications of thyroid surgeries. Anatomists and surgeons define, delineate, and dissect meticulously the related neck anatomy to denote the nerves in relation to thyroid. External branch of superior laryngeal nerve is related to the superior pole of thyroid gland. To avoid injury to this nerve, superior vascular pedicle of thyroid is ligated very close to the gland. Recurrent laryngeal nerve (RLN) is related to the inferior pole of thyroid gland. The capsular branches of inferior thyroid artery are ligated and transected. The main trunk of inferior thyroid artery is never ligated as it would lead to compromise of blood supply to parathyroid glands. The quality control of thyroidectomies and methods to minimize nerve injury advocates visual identification of the RLN, careful exposure, and preservation of RLN.[3],[4] During thyroidectomy surgeries, before the dorsal mobilization of thyroid lobe, inferior thyroid artery, and RLN are located distal to the artery at the esophagotracheal sulcus and RLN is traced till its entry into the larynx.[5]

Even though the posterolateral projection of thyroid was described in the 18th century, Gilmour reported the relation of TZ with RLN in 1938.[6] It has been underutilized anatomical landmark during thyroid surgeries until 1998 when Pelizzo et al. reported a constant relation of TZ with RLN.[7] Pelizzo et al. have described TZ as an arrow pointing RLN.[7] Since then, the prevalence, relation with RLN, and embryological basis of TZ are being evaluated with much vigor and clarity. Recently, there is surge in interest, both among surgeons and anatomists in identifying TZ and reporting its prevalence. Even though many studies have affirmatively concluded about this posterolateral extension of thyroid, we cannot exclude the possibility of thyroid gland (being soft tissue) occupying a gap at the entry point of RLN into the larynx. The depression created by the entry of RLN into the larynx may be occupied by the posterior or posterolateral extension of thyroid gland and appear as TZ. If such gap-filling posterior extension occurs, there could be differences in prevalence noted in studies carried out during thyroid surgeries and those done with cadaveric (fixed) specimens. Such pressure extension, if present, leads to overestimation of the prevalence of TZ in cadaveric studies. The objective of this review is to report separately the prevalence of TZ as noted by anatomists and surgeons. Studies focusing on differential reporting of fresh cadaveric prevalence and formalin fixed cadavers are also reported.


  Materials and Methods Top


Study source and duration

During October 2017, an extensive search for articles with TZ either in title or keywords was done using PubMed, ScienceDirect, Google Scholar, SciELO, EMBASE, and Web of Science databases.

Search criteria

To include all relevant studies, a comprehensive search for all articles related to thyroid surgeries was carried out and all articles with reference to TZ were included. The search terms were restricted to TZ, Zuckerkandl tubercle, posterolateral extension of thyroid, RLN, and thyroid surgeries. Only articles in English (both originals and translations) were included in the review.

Study selection

All articles irrespective of the date of publication were included in the review. Original research and case reports were included in this study.

Data collection and data items

Studies were categorized into two types, surgical studies and cadaveric studies. Data regarding the total number of cases (sides) studied, percentage of cases where TZ was noted, and any special comments either in results section or conclusion section are noted.

Synthesis of results

As this review is about the prevalence of TZ and relation to RLN, only the reported prevalence percentages were taken from the individual studies along with the total number of sides studied. Average of reported mean represented the pooled prevalence of TZ.


  Results Top


A total of 1550 records were found with keywords used for searching. Out of which, 1511 records are not directly related to TZ and were excluded from the study. A total of 39 records analyzed. Out of which 14 studies were not direct study of TZ in relation to thyroid surgeries and RLN. They were excluded from the study. One review article was excluded from data collection.

Characteristics of included studies

Out of 39 records, 25 studies, reported total number of sides where TZ was studied with prevalence percentages. This included 6 cadaveric studies and 19 surgical studies [Table 1].
Table 1: Characteristics of studies included in this review

Click here to view


Pooled prevalence of tubercle of Zuckerkandl

A total of 514 sides were included from 6 cadaveric studies. The prevalence of TZ ranges from 59% to 100%. Average prevalence is 84% (432 sides). From 19 surgical studies, a total of 3777 sides of thyroid were examined during thyroid surgeries. The prevalence of TZ was 69%. Four studies particularly mention that TZ prevalence was more on the right side.[22],[28],[29],[33] Page et al. have found TZ in only 7% of the sides out of 79 sides studied and all were right sided.[29] Combined pooled prevalence of TZ was 76.5% from 4271 thyroid lobes.

Right sidedness of tubercle of Zuckerkandl

Sheahan and Murphy,[28] Page et al.,[29] Yun et al.,[30] Mehanna et al.,[22] Irawati et al.,[17] Gurleyik and Gurleyik,[25] Gil-Carcedo et al.,[24] Mehmood et al.,[20] and Chintamani [36] reported that prevalence of TZ is more on the right side. Overall prevalence on the right side is 65% and on the left side is 52%.

Recurrent laryngeal nerve and tubercle of Zuckerkandl

Overall, 15 studies reports RLN is related to posterior or posteromedial to TZ. Gauger [35] and Mehmood et al.[20] reported RLN is medial to TZ. However, Gurleyik and Gurleyik noted cases where RLN was unusually on the lateral side of TZ.[25]


  Discussion Top


Intraoperative identification and dissection of thyroid gland capsule are very important in the preservation of RLN. RLN is related just posterior to TZ, and this is the crucial site of RLN injury. Just posterior to TZ, RLN can be found buried deep in the fascial planes of ligament of Berry.[7],[17],[18],[20],[23] TZ and inferior thyroid artery is located in a superficial plane. RLN enters larynx behind TZ.[37] Therefore, knowledge about RLN anatomy, branching pattern and variations is very essential.[38] Even though, during thyroid surgeries, it is essential to identify, dissect, and preserve the RLN, 0.1%–0.9% results in iatrogenic injury to nerve. Because of higher anatomical variations including extralaryngeal branching, non-RLN and interlacing of inferior thyroid artery and RLN, nerve visualization is essential to preserve it.[3],[4],[38],[39] RLN is particularly injured in cases where there is extra-laryngeal bifurcation. Gurleyik et al.[40] have reported a rare case where non-RLN pointed by a TZ.

Since the prevalence of TZ is bilaterally asymmetrical (with more prevalence on the right), inquisitive enquiry into the concept of posterior extension of thyroid gland under differential pressure effect prevails. Even though the differential formation of thyroid primordia on the right and left side was suggested as reason for higher right-sided prevalence, the definitive evidence of such developmental process influencing thyroid formation is lacking. It may be viewed as differential pressure effects on right side producing a posterior or posterolateral extension of thyroid gland. Since most of the studies reports unilobed TZ, subtle developmental influence or pressure effect may equally be responsible for the formation of TZ. Dhalapathy Sadacharan has reported a giant TZ extending retrosternally.[19] Such extension is more common with lateral aberrant thyroid. Such report (though isolated) strengthens the uncertainty in the nomenclature of extensions of thyroid gland.

Anatomists' perspective of tubercle of Zuckerkandl

Reports from cadaveric studies have stated the prevalence, location, grading, and distance between TZ and RLN. Pelizzo et al. have classified the TZ into 4 Grades according to the size. Grade 0 – unrecognizable, Grade I – lateral edge of thyroid lobe thickening, Grade II – postero-lateral projection of thyroid gland of <1 cm, and Grade III – posterolateral projection >1 cm.[7] Won et al. have studied the TZ in fresh and fixed cadavers and found no difference in morphology, prevalence, and location. This proves that TZ is not mere gap-filling posterior extension of thyroid gland. Similarly, no study considered under this review mention about any other projections from thyroid gland. Therefore, it is concluded from this extensive surgical and cadaveric review, that TZ is a fixed and most often constant anatomical posterior or posterolateral projection of thyroid gland.

Limitations of the review

Only 39 records with TZ details could be retrieved from the search engines. However, many of the articles relating to TZ published in recent journals (not indexed in the above-mentioned databases) could not be traced.


  Conclusions Top


The prevalence of TZ is 76.5%. When present it is a useful guide for locating, dissecting, and preserving RLN. The prevalence of TZ in cadaveric studies was 84% and from surgical studies was 69%. There is a higher prevalence of TZ in cadaveric studies. Most surgical studies report higher right-sided prevalence.

Acknowledgment

The author would like to thank the Department of anatomy, Azeezia Institute of Medical Sciences.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Ritchie JE, Balasubramanian SP. Anatomy of the pituitary, thyroid, parathyroid and adrenal glands. Surg (Oxford) 2014;32:499-503.  Back to cited text no. 1
    
2.
Nussey S, Whitehead S. The Thyroid Gland. BIOS Scientific Publishers; 2001. Available from: https://www.ncbi.nlm.nih.gov/books/NBK28/. [Last accessed on 2017 Mar 08].  Back to cited text no. 2
    
3.
Hermann M, Alk G, Roka R, Glaser K, Freissmuth M. Laryngeal recurrent nerve injury in surgery for benign thyroid diseases: Effect of nerve dissection and impact of individual surgeon in more than 27,000 nerves at risk. Ann Surg 2002;235:261-8.  Back to cited text no. 3
    
4.
Canbaz H, Dirlik M, Colak T, Ocal K, Akca T, Bilgin O, et al. Total thyroidectomy is safer with identification of recurrent laryngeal nerve. J Zhejiang Univ Sci B 2008;9:482-8.  Back to cited text no. 4
    
5.
Jiang Y, Gao B, Zhang X, Zhao J, Chen J, Zhang S, et al. Prevention and treatment of recurrent laryngeal nerve injury in thyroid surgery. Int J Clin Exp Med 2014;7:101-7.  Back to cited text no. 5
    
6.
Gilmour JR. The gross anatomy of the parathyroid glands. J Pathol Bacteriol 1938;46:133-49.  Back to cited text no. 6
    
7.
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.  Back to cited text no. 7
    
8.
Won SY. Anatomical considerations of the superior thyroid artery: Its origins, variations, and position relative to the hyoid bone and thyroid cartilage. Anat Cell Biol 2016;49:138-42.  Back to cited text no. 8
    
9.
Vinay Chandra PH. Study of the tubercle of Zuckerkandl and its relation to recurrent laryngeal nerve. J Evol Med Dent Sci 2017;6:2639-41.  Back to cited text no. 9
    
10.
Won HS, Liu HF, Kim JH, Lee S, Chung IH, Kim IB, et al. Zuckerkandl's tubercle of the thyroid gland: Its location in the anatomical position, and comparative morphology of the same specimens before and after fixation. Clin Anat 2015;28:472-6.  Back to cited text no. 10
    
11.
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.  Back to cited text no. 11
    
12.
Yalçin B, Poyrazoglu Y, Ozan H. Relationship between Zuckerkandl's tubercle and the inferior laryngeal nerve including the laryngeal branches. Surg Today 2007;37:109-13.  Back to cited text no. 12
    
13.
Musajo FG, Mangiante G, Ischia A, Marchiori L, Benati G, Mainente M, et al. Zuckerkandl tubercle of the thyroid gland (anatomo-surgical study: Preliminary considerations). Chir Ital 1989;41:129-36.  Back to cited text no. 13
    
14.
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.  Back to cited text no. 14
    
15.
Henry BM, Sanna B, Vikse J, Graves MJ, Spulber A, Witkowski C, et al. Zuckerkandl's tubercle and its relationship to the recurrent laryngeal nerve: A cadaveric dissection and meta-analysis. Auris Nasus Larynx 2017;44:639-47.  Back to cited text no. 15
    
16.
Irkorucu O. Zuckerkandl tubercle in thyroid surgery: Is it a reality or a myth? Ann Med Surg (Lond) 2016;7:92-6.  Back to cited text no. 16
    
17.
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.  Back to cited text no. 17
    
18.
Popescu R, Ponoran D, Ignat O, Constantinoiu S. Monitoring the laryngeal nerves during thyroidectomy. Initial 115 cases experience. Chirurgia (Bucur) 2015;110:327-32.  Back to cited text no. 18
    
19.
Sadacharan D, Mahadevan S, Muthukumar S, Ravikumar K. A rare giant tubercle of Zuckerkandl with retrosternal extension encountered during total thyroidectomy. BMJ Case Rep 2015;2015. pii: bcr2015210307.  Back to cited text no. 19
    
20.
Mehmood Z, Khan U, Bokhari I, Hussain A, Subhan A, Nazeer M, et al. Zuckerkandl tubercle: An important landmark in thyroid surgery. J Coll Physicians Surg Pak 2015;25:495-7.  Back to cited text no. 20
    
21.
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.  Back to cited text no. 21
    
22.
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.  Back to cited text no. 22
    
23.
James YE, Doleagbenou A, Kassegne I, Biramah BT, Keke K, Dosseh ED, et al. Zuckerkandl's tubercle: Incidence and relationship with the inferior laryngeal nerve. Morphologie 2014;98:171-5.  Back to cited text no. 23
    
24.
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.  Back to cited text no. 24
    
25.
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.  Back to cited text no. 25
    
26.
Lee TC, Selvarajan SK, Curtin H, Mukundan S. Zuckerkandl tubercle of the thyroid: A common imaging finding that may mimic pathology. AJNR Am J Neuroradiol 2012;33:1134-8.  Back to cited text no. 26
    
27.
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.  Back to cited text no. 27
    
28.
Sheahan P, Murphy MS. Thyroid tubercle of Zuckerkandl: Importance in thyroid surgery. Laryngoscope 2011;121:2335-7.  Back to cited text no. 28
    
29.
Page C, Cuvelier P, Biet A, Boute P, Laude M, Strunski V, et al. Thyroid tubercle of Zuckerkandl: Anatomical and surgical experience from 79 thyroidectomies. J Laryngol Otol 2009;123:768-71.  Back to cited text no. 29
    
30.
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.  Back to cited text no. 30
    
31.
Gravante G, Delogu D, Rizzello A, Filingeri V. The Zuckerkandl tubercle. Am J Surg 2007;193:484-5.  Back to cited text no. 31
    
32.
Yalçin B, Ozan H. Relationship between the Zuckerkandl's tubercle and entrance point of the inferior laryngeal nerve. Clin Anat 2007;20:640-3.  Back to cited text no. 32
    
33.
Costanzo M, Caruso LA, Veroux M, Messina DC, Marziani A, Cannizzaro MA, et al. The lobe of Zuckerkandl: An important sign of recurrent laryngeal nerve. Ann Ital Chir 2005;76:337-40.  Back to cited text no. 33
    
34.
Cannizzaro MA, Veroux M, Cavallaro A, Palumbo A, Veroux P, Marziani A, et al. Zuckerkandl's tuberculum: Could it be useful in thyroid surgery? Chir Ital 2004;56:611-5.  Back to cited text no. 34
    
35.
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.  Back to cited text no. 35
    
36.
Chintamani. “Friend or foe” of a thyroid surgeon?-The tubercle of Zuckerkandl. Indian J Surg 2013;75:337-8.  Back to cited text no. 36
    
37.
Serpell JW. New operative surgical concept of two fascial layers enveloping the recurrent laryngeal nerve. Ann Surg Oncol 2010;17:1628-36.  Back to cited text no. 37
    
38.
Bhargav PR. Salient anatomical landmarks of thyroid and their practical significance in thyroid surgery: A pictorial review of thyroid surgical anatomy (revisited). Indian J Surg 2014;76:207-11.  Back to cited text no. 38
    
39.
Chiang FY, Lu IC, Chen HC, Chen HY, Tsai CJ, Hsiao PJ, et al. Anatomical variations of recurrent laryngeal nerve during thyroid surgery: How to identify and handle the variations with intraoperative neuromonitoring. Kaohsiung J Med Sci 2010;26:575-83.  Back to cited text no. 39
    
40.
Gurleyik E, Dogan S, Gunal O, Pehlivan M. The rare coincidence: Nonrecurrent laryngeal nerve pointed by a Zuckerkandl's tubercle. Case Rep Med 2012;2012:143049.  Back to cited text no. 40
    


    Figures

  [Figure 1]
 
 
    Tables

  [Table 1]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Materials and Me...
Results
Discussion
Conclusions
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed91    
    Printed1    
    Emailed0    
    PDF Downloaded20    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]