Identification of valid anatomical landmarks to locate and protect recurrent laryngeal nerve during thyroid surgery: A cadaveric study
Creators: name: ASGHAR, ADIL
Publisher: name: Open Science Framework
Year: 2022
Subjects: subject: Medicine and Health Sciences

description: Title: Identification of valid anatomical landmarks to locate and protect recurrent laryngeal nerve during thyroid surgery: A cadaveric study Abstract: Purpose: Recurrent laryngeal nerve (RLN) is the most crucial structure in terms of intricacy, anatomic variations of the nerve may further make thyroid surgery cumbersome. The present study was undertaken to provide comprehensive knowledge about the soundness of Berry’s ligament (BL), tracheoesophageal groove (TEG) and inferior thyroid artery (ITA) and the posterior border of the thyroid gland as anatomical landmarks to identify the nerve intraoperatively. Methods: Thirty adult cadavers were dissected to identify the RLN in the neck and to locate it in relation to the aforementioned anatomical landmarks. Results: The RLN/BL relationship: RLN was most often located superficial to the BL (88.3%), followed by deep to the BL in 8.4%, and piercing the BL in 3.3 % of cases respectively. The RLN/TEG relationship: the RLN was located inside the TEG in most of the cases (71.7%), followed by RLN lying outside the TEG in 28.3%. When located outside the groove, it was most commonly found lateral to the TEG (64.7%). RLN/ITA relationship: the nerve was passing deep to the artery in most of the cases (65%), followed by superficial (30%) and rarely (5%) in-between the branches. RLN/posterior border of thyroid relationship: In 57 (95%) cases, RLN was coursing in the area posterior to the posterior border of the gland with an average distance of 6.31 mm ranging between 3.12 mm to 10.30 mm. Conclusions: Both the BL and TEG are potentially crucial for safeguarding of RLN. Although in results, BL turns out to be more consistent than TEG, we propose the utilization of both these anatomical landmarks together for complication-free neck surgeries. Whereas, Posterior border of thyroid turns out to be the single most consistent landmark for identification of RLN. Keywords: Groove; Landmark; Ligament; Nerve injury; Thyroidectomy Introduction: The recurrent laryngeal nerve (RLN) is a branch of the vagus. RLN may have variations during the course from thorax to larynx and it is highly vulnerable during thyroid surgery. It has been observed that RLN enters larynx after dividing into two or more branches. The prevalence of RLN injury is 0.1-8% during thyroid surgery. During surgery, RLN damage is associated with its improper identification and difficult isolation due to adhesion. The course of injury to the recurrent laryngeal nerve is a critical but avoidable complication of thyroidectomy and other neck surgeries. This complication may be avoided by prior identification of the nerve with the assistance of important anatomical landmarks found along its course [10, 14]. A reliable landmark and method for identifying the RLN are imperative to avert postoperative complications such as hoarseness of voice and vocal cord paralysis. Intraoperatively, RLN can be identified by several techniques, such as palpation, intraoperative nerve monitoring (IONM), and direct inspection felicitated by crucial anatomical landmarks such as Berry’s ligament (BL), the Tracheoesophageal Groove (TEG), Inferior thyroid artery (ITA) and Zukerkandl’s tubercle. A volatile relationship exists among these parameters [12]. The lucid identification of these landmarks improves the sensitivity of IONM. BL is a fibrous structure that anchors the thyroid gland to the first three tracheal rings and the most common site of injury to the RLN, where the nerve penetrates into the larynx [1, 2]. Few authors have proposed BL as a reliable anatomical landmark to locate the RLN intraoperatively [5, 21], however, this has yet to be widely accepted and implemented as standard practice [2]. Previous reports revealed capacious variations in the location of the RLN with respect to the BL, the nerve coursing superficial to the BL ranges from zero to 100 % [4, 6, 21] while the penetrating pattern varies between zero [4, 6, 9, 13, 16, 21] to 31.6% [20]. A further thorough cognizance of the frequency with which nerves penetrate the BL will bring down the complications, as traction-related injuries are commonly linked with RLNs taking a piercing course [1, 13]. The TEG is a deep sulcus formed by the concourse of the trachea anteriorly and oesophagus posteriorly. It provides a fairly safe haven for the RLN as it ascends towards the larynx [20] and can also be used as a landmark for identifying the nerve [25]. During surgery, the TEG needs to be inspected routinely for the presence of the nerve, otherwise, it might be overlooked unwittingly [23]. Previous studies also revealed that the location and relationship of the RLN to the TEG have varied widely. The reported presence of an RLN coursing within the TEG has ranged from 24.9% to 100% [8, 17]. ITA is another crucial landmark for recognizing the RLN intraoperatively. The anatomical relationship between the RLN and the ITA is volatile (Fig. 1). RLN is related to the ITA differently on both sides. On the right side, RLN crosses ITA at the anterior aspect but, the same crosses ITA at the posterior aspect on the left side. The clear visualization of the relationship between artery and nerve is the necessity of precise surgical technique to avoid the damage of neurovascular structures. The fourth landmark is the posterior border of the thyroid lobe, which points toward the tracheoesophageal groove. Usually, RLN travels in the area posterior to this landmark, but in a few instances, it can course anteriorly making itself vulnerable to injury during partial thyroidectomy. RLN may have a very intimate relationship with the thyroid capsule along the posterior border. This relationship is a possible indicator in calculating the safe zone in deciding the line of incision in subtotal thyroidectomy or near-total thyroidectomy (Fig 2). Although, the distance between the RLN and posterior border of the thyroid is crucial, very little is mentioned in the literature. The high variability of the data published to date, forbidden us from making solid opinions regarding the robustness of these soft tissue structures as valid and reliable anatomical landmarks for the RLN identification. The lofty incidence of RLN injury, and the need to safeguard the structure during surgery, has persuaded substantial research during recent years. However, a reliable and uniform technique for identifying and safeguarding the nerve has yet to be conceived [12]. With such a background, the aim of the current work was to evaluate the reliability of the BL, TEG, ITA and posterior border of the thyroid gland as anatomical landmarks for identifying the RLN. Reliable landmarks would help to alleviate the frequency of iatrogenic injury and long-term postoperative complications. Methods: A total of 30 formalin-fixed adult cadavers (25 male and 5 female) aged between 45 to 75 years were dissected bilaterally at the dissection hall of Anatomy department, to investigate the anatomical relationship of the RLN to the BL, TEG, ITA and the posterior border of the thyroid gland. The dissection of the neck was done as per Cunningham’s practical manual for dissection. A wooden block with slight concavity in the middle was placed underneath the nape of the neck, so as to keep the neck in extended and fixed position without undue movement during dissection. A midline vertical incision was given thereafter, starting from the symphysis menti and continuing downwards up to the sternal notch. Then the incision was extended laterally from the sternal notch up to the tip of the acromion along the anterior border of subcutaneous clavicle. Subplatysmal flaps of the skin along with the superficial facia and subcutaneous fatty tissue were then raised and reflected laterally for better exposure of the anterior triangle of neck. The strap muscles (sternohyoid, sternothyroid and omohyoid) lying in front of the thyroid gland were identified, transacted transversely through middle of the muscle belly and reflected upward and downward. The dissection was carried out until the thyroid gland was clearly visible. Structures surrounding the gland (muscles, fatty and connective tissues) were kept away from the area of dissection by applying mechanical traction with the help of metallic hook or forceps. The RLN was visualized by applying slight medial traction on the trachea. Once, the area was clearly visible, the relationship of the nerve to the BL (superficial, piercing, or deep) was noted first (Figure 3). The nerve was then traced downwards to the TEG, and the position of the RLN with respect to this groove was recorded (inside or outside, when outside: anterior, anterolateral, lateral, and posterior) (Figure 4). After noting the position of the nerve in relation to the BL, TEG and ITA, its location and distance from the posterior border of the thyroid gland was also measured with the help of a digital vernier callipers (Mitutoyo, Japan) (Figure 3). The distance between RLN and the midpoint of the posterior border was measured. Percentage prevalence of RLN variation was calculated. The mean and standard deviation were computed for the distance between the posterior border of thyroid and RLN with the help of Microsoft excel 2019. Results: The present study was conducted on 30 formalin-fixed adult cadavers aged between 45 and 75 years. Amongst them, 25 (83.3%) were male and 5 (16.7 %) were female. The RLN was recognized reciprocally in all 30 cadavers (n=60). RLN/BL relationship: In 53 (88.3%) cases, the RLN was located superficial to the BL, in 5 cases, the nerve was piercing the ligament (Figure 3) and in 2 cases, coursing deep to it. The relationship was bilaterally symmetrical in 23 (76.7%) cadavers. RLN/TEG relationship: In 43 (71.7%) cases, the RLN was coursing within the groove (Figure 4) while in 17 (28.3%), the nerve was lying outside the groove (Figure 3). When located outside the groove, it was most commonly found lateral to the TEG (11 nerves, 64.7%) (Table 1). The relationship was bilaterally symmetrical in 19 (63.3%) cadavers. RLN/ITA relationship: The most common type of RLN was deep to the ITA (65%), while the second most common was superficial to the ITA (30%). The least common type was between the branches of the ITA, with an incidence of 5%. In addition, there were differences between the left and right sides, with the posterior type being the most common, occurring in 35.73% of the nerves on the left side and 20.78% of those on the right one (Table 3). The relationship was bilaterally symmetrical in 13 (43.3%) cadavers. RLN/ Posterior border of thyroid: In 57 (95%) cases, RLN was coursing in the area posterior border of the gland with an average distance of 4.95±2.23 mm ranging between 2.21mm to 12.1mm. Almost all the nerves were found within the range of 2 to 10 mm except in two cases, where the distance was more than 10.00 mm. In three (5%) cases, nerve was passing anteriorly to lie closely along the lateral surface of the gland. The relationship was bilaterally symmetrical in 23 (76.7%) cadavers. No significant differences were observed between subtypes based on TEG, ITA and BL. The data collected were not statistically sufficient in order to conclude any sex-related difference in the local anatomy of ITA and the RLN The details of descriptive statistics are mentioned in table 1 and Figures (5-7) Distance from most prominent point posterior border of the thyroid (in mm) Relationship Mean SD N Kruskal Wallis H test (P value&lt;0.05) RLN/TEG Inside 4.969 2.353 43 0.619 Outside anterolateral 5.207 1.481 6 Outside lateral 4.748 2.227 11 RLN/ITA Posterior 5.072 2.484 39 0.728 Between two branch 5.28 1.045 3 Anterior 4.638 1.792 18 RLN/BL Posterior 4.11 0.76 5 0.543 Piercing 5.81 0.707 2 Anterior 5 2.345 53 Discussion: Outright comprehension about the surgical anatomy of RLN including its variations is crucial for a holistic approach towards safe thyroid surgery. Full exposure to RLN is a prerequisite to avoid nerve injury. In the distal 2 cm of its course the nerve lies more superficially, hence at this site it is most vulnerable to the iatrogenic lesion [13]. Anatomical landmarks may be of help in identifying the RLN intraoperatively, however, surgeons need to be well versed with their consistency and reliability before using them in the operating theatre. In our cadaveric dissections, the RLN was coursing superficial to the BL in 53 cases (88.3%). This coincides with the prevalence of superficial RLN/BL relationships noted by Asgharpour et al (88.1%) [2]. Henry et al [12] in their meta-analysis also described the superficial RLN/BL relationship as the most common (78.2%) pattern. Piercing pattern of RLN/BL relationship was seen in 8.3% cases, which was in consonance with the findings of Kaisha et al [14]. During surgical intervention, such a pattern needs scrupulous attention because of the higher risk of lesions, associated with glandular traction [1, 13]. RLN lying deep to the BL was seen least commonly (3.3%). In such a location, its wearisome to visualise the nerve undoubtedly during glandular manipulation, still chances of injuring it are less as in most cases the nerve escapes the area by piercing the larynx at this level. Henry et al [12] noted substantial ethnical and geographical variability in RLN/BL relationship. Most Asian studies [13, 20, 21] have reported a lower prevalence of the superficial relationship (59.3%) than their North American [4], African [18], and European counterparts [6, 16]. Symmetrical RLN patterns with respect to the BL were noted in most cases (76.7%) in our dissections. This information is crucial for surgeons performing total thyroidectomies, as in such instances, when one nerve is identified in a particular location, the same location should be searched first on the contralateral side. In a meta-analysis conducted by Henry et al [12], the RLN/BL relationship was bilaterally symmetrical in 75.5% of cases. Assessment of the bilateral symmetrical behavior of the RLN with respect to the BL and TEG validated that symmetrical behavior of the RLN with respect to the BL (76.7%) was more common than the symmetrical pattern of the course (63.3%) with TEG. That’s why, head &amp; neck surgeons consider the BL as one of the most reliable landmarks in neck surgery to prevent iatrogenic RLN injury [2, 10, 24]. Our findings also support the same notion. So, ‘the rule of thumb’ is no structure should be dissected or ligated until the RLN has been identified and the BL, as a consistent anatomical landmark can be used to locate the nerve intraoperatively. It is also crucial for the surgeons to take the less common piercing pattern or RLN lying deep to the BL into consideration for hassle free procedure. In piercing pattern, where the nerve can be intricately intertwined with the BL, poses a unique peril as in such cases nerve fibres can easily be severed while incising the ligament during thyroidectomy [26]. So, for obvious reasons, such patterns are associated with the highest morbidity of nerve palsy [26]. Serpell [22] highlighted that the substantial variability in the relationship of the nerve to the BL could arise from a lack of appropriate anatomical assessment of the ligament itself [22]. He also noted that the BL comprises two fascial layers, the outer one is false and inner one is true. In a few instances, the RLN can be found in the deeper fibrous layer (the “true” BL) [22] and can lead to fallacious reporting of the penetrating pattern of the BL. Most of the studies reporting variations in RLN/BL relationship have not made any lucid statement pertaining to such variants. In our cadaveric study, we have taken such phenomena into consideration while reporting piercing patterns. Furthermore, Serpell suggested that a meticulous dissection of the RLN posterolaterally helps to reduce nerve traction, allowing for safe BL division and reduction in nerve palsies [22]. Our study results revealed that the reliability of TEG as an identifiable landmark for locating RLN is less established. Only in 71.7 % of cases, the nerve was coursing within the TEG throughout its course. Various authors have studied the location of RLN in relation to the TEG amongst different geographic populations. Armstrong and Hinton, dissected 40 cadavers in USA and found RLN within the groove in 60.0% cases [3]. Chen et al [8] studied 90 Chinese cadavers and located RLN within the groove in all the cases. Lang et al [15] dissected 43 cadavers and found RLN within the grove in 37.2% cases. Henry et al [12] dissected 40 cadaveric necks and found RLN within the groove in 68.1% of cases. As far as the Indian subcontinent is concerned, no such studies done to date to assess RLN/TEG relation. A Meta-analysis conducted by Henry et al [12] showed pooled prevalence of 63.7% of nerves coursing within the TEG. After reviewing available literature, we are of the opinion that, RLN/TEG relationship shows ethnical and geographical differences, Asian studies generally reporting more RLNs coursing in the TEG (75.9%) than European ones (50.9%) [12] The location of the RLN, outside the TEG ranges from anterior, anterolateral, lateral to posterolateral. In our cadavers, it was most commonly (63.3%) located lateral to the TEG, similar to findings of Henry et al [12]. Whereas, the meta-analysis differed with regard to the location of the RLN when it was outside the TEG. Most RLNs outside the TEG (45.7%) were located anteriorly in the meta-analysis [12], ranging from anterior to lateral. The TEG is a valuable landmark for identifying the RLN. It represents an asylum to safeguard the nerve inside the groove. Operating surgeons may easily fail to spot the nerve while lying inside the groove but its presence can be confirmed by simple palpation [7]. This landmark has been proven to be a reliable landmark to identify RLN in laparoscopic procedures of the neck [7]. In a series by Chang, the RLN was identified in 100% of laparoscopic thyroid procedures using the TEG [7]. We advocate that every time an attempt should first be made to identify and locate the RLN in the TEG, subsequently the course of the nerve to be traced upwards up to the level of BL. Once its position is confirmed in relation to the BL, surgical manipulation to be done. We believe that surgeons need to stick to the dictum of “no manipulation until and unless RLN/BL relationship is well established”. However, such a method of identification, can get complicated due to local pathologies (e.g., Large thyroid goitre) or anatomical variations pertaining to the nerve such as extra laryngeal branching of the RLN. Henry et al [11] reported that 76.6% of RLNs branch prior to entering the larynx [11]. In recent years, intraoperative nerve monitoring (IONM) appeared as an alternative to identify RLN intraoperatively, however it has yet to be proven superior to concrete anatomical landmarks [7, 10]. That being said, IONM can be beneficial in cases where pathology does not permit these at-risk structures to be adequately visualized and identified. The use of the BL and TEG in nerve identification is valuable regardless of whether procedures are of primary or secondary nature and can provide valuable surgical information allowing for reduction of iatrogenic nerve injuries. Although the anatomical relationship between RLN and ITA is mostly volatile, still it holds a position amongst head neck surgeons as an important landmark to identify the nerve intraoperatively. The relationship between the artery and the nerve was studied during the past century, and several classification systems were developed. (George Noussiosa). We concluded that the RLN was usually running deep to the ITA, with a prevalence of 65 %. In addition, there were differences between the left and right sides of the thyroid gland, with the deep type being more common on the left, representing an occurrence of 67 %. Uen et al studied 120 cadavers and reported posterior position in 65.8%, 70% being left posterior. Fowler [28], and later, Skandalakis et al [29] concluded that injury to the RLN is more common when the nerve lies anterior to or between the ITA. Surgeons should also take care when performing operations of the thyroid on the right side because of the predominance of the anterior configuration [30]. There are studies suggesting that intraoperative nerve monitoring (IONM) has not proven more effective than direct nerve visualization has [31, 32]. However, when there is an anatomical variant, reoperation of the thyroid gland or obscured pathology IONM should be used to prevent iatrogenic injury of the RLN [33]. Henry et al. (2016) reviwed multiple literatures and documented that symmetrical relationship with ITA only in 36.6% (95% CI 31.5-41.9). The current study found bilateral symmetrical relationship in 63 % of cadaver and the difference may be attributed to population difference or lower sample size. Two systematic reviews published earlier by Henry et al (2016) and Noussios et al (2020) and both have presented relatively different pictures. Henry et al 2016 observed an asymmetrical pattern predominantly (posterior configuration) in relation to ITA in which posterior configurations were common on the left side and anterior configurations were in right sides. Noussios et al (2020) found posterior configuration was more common in both sides. Due to the substantially higher incidence of the anterior and between patterns of the RLN/ITA connection on the right side, more caution is required during operations. In bilateral operations, symmetry must not be presumed, and the RLN must be positively recognised on both sides. The significant incidence of RLN/ITA variation must be taken into account while planning, exposing, and performing neck procedures. The midpoint of posterior border of the thyroid gland could be another possible landmark. RLN was located within 2-10 mm from its midpoint. Many authors considered Zukerkandl tubercle as anatomical landmark but it was present only in 63-78% subjects (Gauger et al. 2001, Pelizzo et al 1998). In 93% of cases RLN were located near this landmark at tracheal surface or embedded in gland capsule and in rest, RLN were located lateral to posterior border of gland. (Gauger et al. 2001). We did not find any literature to compare the measured distance. Study results depicting the relationship of the RLN using BL or TEG as landmarks are available, however data showing its anatomical position along the posterior border of the gland is lacking. Such data are very crucial for hassle free thyroid surgery, specifically in deciding the plane of incision in partial thyroidectomy. In the present study, we found that in five percent cases, the nerve can course forward to lie anteriorly along the lateral surface of the gland. Limitations: The small number of female cadavers (5) than that of the males (25) did not allow us to compare our findings between them to study the effect of gender on the study results. Additional research, such as clinical trials need to be conducted to assess the intraoperative viability of the BL and TEG as landmarks for identifying the RLN, only then the true validity of these structures as trustworthy landmarks for at-risk neural structures can be established. Conclusion: Both the BL and TEG are potentially crucial for safeguarding of RLN. Although in results, BL turns out to be more consistent than TEG, we propose the utilization of both these anatomical landmarks together for complication-free neck surgeries. The development of a uniform and consistent procedure, such as identifying the RLN in the TEG and tracing it upwards to the BL for confirmation, will help to preclude iatrogenic injuries and avoid complications. The confirmation of reliable landmarks on which to base those procedures is the first step in that process. Whereas, Posterior border of thyroid turns out to be the single most consistent landmark for identification of RLN. Funding: non funded Conflicts of interest/Competing interests: The authors declare that they have no conflict of interest References: 1. Ardito G, Revelli L, D'Alatri L, Lerro V, Guidi ML, Ardito F (2004) Revisited anatomy of the recurrent laryngeal nerves. Am J Surg 187(2):249-53. doi: 10.1016/j.amjsurg.2003.11.001 2. Asgharpour E, Maranillo E, Sañudo J, Pascual-Font A, Rodriguez-Niedenführ M, Valderrama FJ, Viejo F, Parkin IG, Vázquez T (2012) Recurrent laryngeal nerve landmarks revisited. Head Neck 34(9):1240-6. doi: 10.1002/hed.21882 3. Armstrong WG, Hinton JW (1951) Multiple divisions of the recurrent laryngeal nerve. An anatomic study. AMA Arch Surg 62(4):532-9. doi: 10.1001/archsurg.1951.01250030540011 4. Berlin D and Lahey F (1929) Dissections of the recurrent and superior laryngeal nerves. Surg Gynecol &amp; Obst 49:102-104. 5. Botelho JB, Vieira D, Monteiro de Carvalho D, Batista MB (2012) Anatomic and surgical study of the recurrent laryngeal nerve and its involvement with the ligament of Berry. Rev Col Bras Cir 39(5):364-7. Portuguese. doi: 10.1590/s0100-69912012000500004 6. Cakir BO, Ercan I, Sam B, Turgut S (2006) Reliable surgical landmarks for the identification of the recurrent laryngeal nerve. Otolaryngol Head Neck Surg 135(2):299-302. doi: 10.1016/j.otohns.2006.03.026 7. Chang S, Tang HH, Wang CC, Zhou LD, Li JD, Huang Y, Zeng QJ, Wang ZM (2012) A standard approach to expose the recurrent laryngeal nerve during endoscopic thyroidectomy. J Laparoendosc Adv Surg Tech A 22(3):259-63. doi: 10.1089/lap.2011.0320 8. Chen X, Xie L, Guo X (2002) The regional dissection and clinical application in pars cervicalis of recurrent laryngeal nerve. Sichuan Journal of Anatomy 10(3):150–152. 9. Freschi G, Masi C, Pichi Graziani M, Pacifico G, Panconesi R, Corsi A, Seghi P (1994) Anatomic and surgical considerations regarding the recurrent laryngeal nerve in thyroidectomy. Minerva Chir 49(10):943-7. 10. Gremillion G, Fatakia A, Dornelles A, Amedee RG (2012) Intraoperative recurrent laryngeal nerve monitoring in thyroid surgery: is it worth the cost? Ochsner J 12(4):363-6. 11. Henry BM, Vikse J, Graves MJ, Sanna S, Sanna B, Tomaszewska IM, Tubbs RS, Tomaszewski KA (2016) Extralaryngeal branching of the recurrent laryngeal nerve: a meta-analysis of 28,387 nerves. Langenbecks Arch Surg 401(7):913-923. doi: 10.1007/s00423-016-1455-7 12. Henry BM, Sanna B, Graves MJ, Sanna S, Vikse J, Tomaszewska IM, Tubbs RS, Tomaszewski KA (2017) The Reliability of the Tracheoesophageal Groove and the Ligament of Berry as Landmarks for Identifying the Recurrent Laryngeal Nerve: A Cadaveric Study and Meta-Analysis. Biomed Res Int 2017:4357591. doi: 10.1155/2017/4357591 13. Hunt PS, Poole M, Reeve TS (1968) A reappraisal of the surgical anatomy of the thyroid and parathyroid glands. Br J Surg 55(1):63-6. doi: 10.1002/bjs.1800550119 14. Kaisha W, Wobenjo A, Saidi H (2011) Topography of the recurrent laryngeal nerve in relation to the thyroid artery, Zuckerkandl tubercle, and Berry ligament in Kenyans. Clin Anat 24(7):853-7. doi: 10.1002/ca.21192 15. Lang J, Nachbaur S, Fischer K (1986) Laryngeal nerves, branches in the interior of the larynx. Gegenbaurs Morphol Jahrb 132(5):723-36. 16. Leow CK, Webb AJ (1998) The lateral thyroid ligament of Berry. Int Surg 83(1):75-8. 17. Menck J, Grüber J, Lierse W (1990) Vorderer Zugang zur HWS und die Lage des N. Anterior approach to the cervical vertebrae and the location of the recurrent laryngeal nerve. Unfallchirurg 93(8):384-6. 18. Ngo Nyeki AR, Njock LR, Miloundja J, Evehe Vokwely JE, Bengono G (2015) Recurrent laryngeal nerve landmarks during thyroidectomy. Eur Ann Otorhinolaryngol Head Neck Dis 132(5):265-9. doi: 10.1016/j.anorl.2015.08.002 19. Pisanu A, Porceddu G, Podda M, Cois A, Uccheddu A (2014) Systematic review with meta-analysis of studies comparing intraoperative neuromonitoring of recurrent laryngeal nerves versus visualization alone during thyroidectomy. J Surg Res 188(1):152-61. doi: 10.1016/j.jss.2013.12.022 20. Pradeep PV, Jayashree B, Harshita SS (2012) A Closer Look at Laryngeal Nerves during Thyroid Surgery: A Descriptive Study of 584 Nerves. Anat Res Int 2012:490390. doi: 10.1155/2012/490390 21. Sasou S, Nakamura S, Kurihara H (1998) Suspensory ligament of Berry: its relationship to recurrent laryngeal nerve and anatomic examination of 24 autopsies. Head Neck 20(8):695-8. doi: 10.1002/(sici)1097-0347(199812)20:8&lt;695::aid-hed6&gt;3.0.co;2-3 22. Serpell JW (2010) New operative surgical concept of two fascial layers enveloping the recurrent laryngeal nerve. Ann Surg Oncol 17(6):1628-36. doi: 10.1245/s10434-010-0928-0 23. Skandalakis JE, Droulias C, Harlaftis N, Tzinas S, Gray SW, Akin JT Jr (1976) The recurrent laryngeal nerve. Am Surg 42(9):629-34. 24. Uen YH, Chen TH, Shyu JF, Shyr YM, Su CH, Chen JY, Lee CS, Liu JC (2006) Surgical anatomy of the recurrent laryngeal nerves and its clinical applications in chinese adults. Surg Today 36(4):312-5. doi: 10.1007/s00595-005-3151-z. 25. Williams P, Warwick R, Dyson M, Bannister L (1989) Gray’s Anatomy, 37 th edn, Churchill Livingstone, Edinburgh. 26. Yalçin B, Ozan H (2006) Detailed investigation of the relationship between the inferior laryngeal nerve including laryngeal branches and ligament of Berry. J Am Coll Surg 202(2):291-6. doi: 10.1016/j.jamcollsurg.2005.09.025 Gauger, P. G., Delbridge, L. W., Thompson, N. W., Crummer, P., &amp; Reeve, T. S. (2001). Incidence and importance of the tubercle of Zuckerkandl in thyroid surgery. European Journal of Surgery, 167(4), 249-254. Pelizzo, M. R., Toniato, A., &amp; Gemo, G. (1998). Zuckerkandl’s tuberculum: an arrow pointing to the recurrent laryngeal nerve (constant anatomical landmark). Journal of the American College of Surgeons, 187(3), 333-336. Noussios, G., Chatzis, I., Konstantinidis, S., Filo, E., Spyrou, A., Karavasilis, G., &amp; Katsourakis, A. (2020). The Anatomical Relationship of Inferior Thyroid Artery and Recurrent Laryngeal Nerve: A Review of the Literature and Its Clinical Importance. Journal of clinical medicine research, 12(10), 640–646. https://doi.org/10.14740/jocmr4296