Anat Sci Int DOI 10.1007/s12565-014-0246-x
ORIGINAL ARTICLE
An applied anatomical study on the external laryngeal nerve loop and the superior thyroid artery in the neck surgical region Wei-Tian Lu • Shan-Quan Sun • Juan Huang Yuan Zhong • Jin Xu • Sheng-Wei Gan • Lu Guo • Ting-Ting Mo
•
Received: 10 February 2014 / Accepted: 14 June 2014 Ó Japanese Association of Anatomists 2014
Abstract This study was conducted to investigate the topographic relationship between the external laryngeal nerve (ELN) loop and the superior thyroid artery (STA), in order to provide the anatomical foundations for protecting the ELN during surgery. In the present study, 48 adult human cadavers were dissected and analyzed. For the 21 (21.9 %) low-position ELN loops observed, the neurovascular relationship between the STA and the nerve was classified into four types: (1) the artery overlapped the nerve; (2) the artery passed through the ELN loop; (3) the muscular branch of the ELN loop and the laryngeal branch of the STA coursed together; and (4) the branches of the STA and the ELN loop were interlaced. Our study suggested that the patterns of ELN loops are so complicated that they have not been statistically defined in any previous study, which should be kept in mind when attempting to protect the nerve from injury. Also, because of the variable
W.-T. Lu S.-Q. Sun (&) J. Huang J. Xu S.-W. Gan Institute of Neuroscience, Chongqing Medical University, 1 Yixueyuan Road, Yuzhong District, Chongqing 400016, China e-mail: [email protected] W.-T. Lu S.-Q. Sun J. Huang J. Xu S.-W. Gan Department of Anatomy, Chongqing Medical University, Chongqing 400016, China Y. Zhong The General Morphology Lab of Experimental Teaching Management Center, Chongqing Medical University, Chongqing 400016, China L. Guo T.-T. Mo National Class Preclinical Medicine Experimental Teaching Demonstration Center, Chongqing Medical University, Chongqing 400016, China
morphology of the ELN loop and its complicated topographic relationship to the STA, the vessels should be individually isolated and then ligated during thyroidectomy. When ligating the laryngeal branch of the STA during larynx surgery, special attention should be paid to avoiding damage to the muscular branch of the ELN/ELN loop. Keywords External laryngeal nerve Gross anatomy Neck surgery Superior thyroid artery Thyroidectomy
Introduction Thyroidectomy was considered professional butchery due to its high mortality rate during the early nineteenth century. However, due to improvements in the associated surgical technique, the mortality rate from thyroid surgery has decreased greatly since then (Hannan 2006). Nevertheless, complications do still occur after thyroidectomy (Fewins et al. 2003; Cernea et al. 2010). Among those complications, nerve injury is one of the most frequent and serious. Injury to the external laryngeal nerve (ELN) can result in transiently or permanently impaired phonation, which is a disastrous outcome for professional teachers and singers (Kochilas et al. 2008). Although the incidence of ELN injuries has decreased significantly due to the application of and improvements in modern techniques and instruments (Friedman et al. 2002; Dedivitis and Guimaraes 2005), cases of ELN damage are still reported from time to time (Jansson et al. 1988; Dackiw et al. 2002; Page et al. 2004). Upon analyzing the factors involved in ELN injury, insufficient knowledge of the anatomy of the ELN was thought to be the main reason for ELN damage. Therefore, a study of the morphologic and topographic
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anatomy of the ELN has been proposed as a key step towards preventing ELN damage during thyroidectomy and neck surgery (Jansson et al. 1988; Furlan et al. 2003). According to the literature, the ELN is a linear nerve trunk (Olthoff et al. 2007; Oliveira and Silva 2007). Based on a study of 60 adult cadavers, Sun and Chang (1991) reported that the superior laryngeal nerve (SLN) and its branches often connected with one or more branches from the cervical sympathetic chain (CSC) to form an SLN loop. SLN loops were subsequently divided into 5 types and 17 subtypes based on morphological variations. Furlan (2002) proposed an alternative SLN/ELN loop classification based on the number of nervous connections between the SLN/ ELN and the CSC, and confirmed that Sun’s results were repeatable and that SLN loops could be observed in different racial groups. Later, Huang et al. (2012) identified an additional 18 SLN loop subtypes based on variations in features and branching patterns, thus extending our knowledge of the SLN loop and its branches. In previous studies, the incidence of a CSC-ELN loop was found to be 73.3 % (Sun and Chang 1991), 92.5 % (Sun and Dong 1997), 59.0 % (Furlan 2002), and 82.0 % (Huang et al. 2012). Therefore, from a statistical point of view, the ELN is more likely to be looped than linear. Meanwhile, a study by Huang et al. (2012) showed that the relationship between the ELN loop and the superior thyroid artery (STA) is variable and complicated, making surgery in this region more challenging. Regretfully, the ELN is still described as linear in the literature and the concept of an ELN loop is rarely recognized by surgeons. Although there have been some works on the surgical anatomy of the STA (Ozgur et al. 2009; Vazquez et al. 2009), studies focusing on the neurovascular relationship between the STA and the ELN loop are scarce, which is one of the reasons why such nerve injuries continue to occur. Given this situation, the purpose of the present study was to conduct a morphologic and topographic study of the ELN loop and the STA during cadaveric dissection in order to provide the anatomical foundations for protecting the ELN during surgery.
Materials and methods Forty-eight adult cadavers (33 male, 15 female; 96 sides) fixed with 4 % formalin were examined in this study. Bodies that had undergone neck surgery were excluded. The ELN, STA, and surrounding adjacent structures, including the thyroid gland, cricothyroid muscle (CTM), inferior pharyngeal constrictor muscle (IPCM), and thyroid cartilage, were carefully dissected. All of the structures were dissected using a 6-power magnifying glass. Data on the basic shape, connected formation, course, and branches
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of the nerve connection between the SLN, internal laryngeal nerve (ILN), ELN, and CSC were observed and recorded. The distance from the lowest point of the ELN loop to the superior thyroid pole was measured. The morphology of the ELN loop and its relationship to the STA were noted. All dissections were performed using a standard surgical procedure. This study was approved by the Human Ethics Committee of Chongqing Medical University.
Results ELN loop and its branches The ELN loops (76 sides) were subdivided into three types based on the distance from the superior thyroid pole to the lowest point of the loop (Sun and Chang 1991): type I (55 sides), 1 cm above the superior thyroid pole; type II (16 sides), less than 1 cm above the superior thyroid pole (Figs. 1a1, b1, 2a1, b1, 3a1, b1, 4a1, b1); type III (5 sides), below the superior thyroid pole (Fig. 4c1, d1). All ELN loops presented glandular and cricothyroid muscle branches (GB and CTB, respectively). In some sides, the ELN loop exhibited branches that entered the IPCM (Fig. 4c1, d1) or the larynx (Fig. 3a1, b1). STA and its branches Before entering the thyroid gland, the STA presented anterior and posterior glandular branches (Figs. 1a1, 2a1, b1, 3b1). In 6 sides, the STA showed several medial branches that entered the isthmus or the muscles (Figs. 1a1, b1, 2a1, b1, 4b1–d1). In 5 sides, the STA exhibited laryngeal branches below the level of the hyothyroid membrane and entered the larynx and adjacent muscles (Fig. 3a1, b1). Relationship of the ELN loop to the STA Because type I ELN loops were far from the superior thyroid pole, these loops were not observed for surgical implications. For the 21 low-position ELN loops (type II and III) observed, the neurovascular relationship between the STA and the nerve was classified into four types: (1) the branch of the STA overlapped with the branches of the ELN loop (Figs. 1a1, b1, 5); (2) the glandular branch of the STA passed through the ELN loop (Figs. 2a1, b1, 5); (3) the laryngeal branch of the STA and the CTB of the ELN loop were enclosed by a fibrous sheath, forming a neurovascular bundle, which entered the CTM (Figs. 3a1, b1, 5); and (4) the branches of the STA and the ELN loop were interlaced (Figs. 4a1–d1, 5).
External laryngeal nerve loop
Fig. 1a–b Type A relationship between the STA and the ELN loop. a1 The STA presents 2 GBs and a CTB. The loop overlaps with the branches of the STA and presents a CTB (triangle). a2 Sketch of a1. b1 The laryngopharyngeal branch of the STA runs across the lowest point of the loop. The loop overlaps with the PB and the LB of the
STA and exhibits a CTB. b2 Sketch of b1. CTB cricothyroid muscle branch, CTM cricothyroid muscle, ELN external laryngeal nerve, GB glandular branch, LB laryngeal branch, PB pharyngeal branch; STA superior thyroid artery, TG thyroid gland
Fig. 2a–b Type B relationship between the STA and the ELN loop. a1 The loop presents a glandular branch (arrowhead) and a CTB (triangle). One GB (arrow) of the STA passes through the loop and enters the TG. a2 Sketch of a1. b1 One GB (arrow) of the STA passes
through the loop (triangle). b2 Sketch of b1. CTB cricothyroid muscle branch, CTM cricothyroid muscle, ELN external laryngeal nerve, GB glandular branch, STA superior thyroid artery, TG thyroid gland
Discussion
frequency, and branching patterns, was more complicated than noted in the previous works. The nerve trunk(s), plus the single ELN, were seen to be single, double, or triple in number. On analyzing all of the papers that have investigated the morphology of ELN/ELN loops (Sun and Chang 1991; Sun and Dong 1997; Furlan 2002; Huang et al. 2012), it seems that the patterns of ELN loops are so complicated that none of the previous studies were able to statistically define them—the statistical results obtained for pattern variations in all of the studies showed statistical randomness. In other words, it can be said that
In this study, the ELN loop appeared in 76 sides (79.2 %). The incidence of connection between CSC and ELN in this study is almost the same as those observed in previous studies (Sun and Chang 1991; Sun and Dong 1997; Furlan 2002; Huang et al. 2012), which further proves that most ELNs are looped. However, the ELN loops found in this study differ from those seen in the previous studies in some aspects. The morphology of the ELN loops, such as their external features, anastomotic
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Fig. 3a–b Type C relationship between the STA and the ELN loop. a1 The STA is pulled laterally. The CTB of the loop (triangle) turns medially and runs between the two LBs (arrow) of the STA, entering the CTM. a2 Sketch of a1. b1 One branch (arrowhead) of the loop
enters the larynx; another CTB hooks the LB of the STA. b2 Sketch of b1. CTB cricothyroid muscle branch, CTM cricothyroid muscle, ELN external laryngeal nerve, LB laryngeal branch, STA superior thyroid artery, TG thyroid gland
‘‘variation is constant’’ for the relationship of the ELN loop to the STA. This indicates that clinical surgeons may accidentally encounter different ELN loop patterns during surgery. Perhaps this is why ELN damage is frequently reported in the literature (Dackiw et al. 2002; Page et al. 2004). Therefore, it is the duty of surgeons to familiarize themselves with both normal and abnormal ELN anatomy in order to avoid nerve injury. Meanwhile, it is also necessary to conduct further investigations of the ELN anatomy in many bodies to improve the reliability of the results of statistical analysis. The STA is the main artery that supplies the thyroid, upper larynx, and neck region (Ozgur et al. 2009). The ELN may be at risk during surgery due to its close proximity to the STA. Therefore, understanding the topographic relationship between the STA and the ELN is important for achieving safe and effective surgery. In order to obtain such topographic data for surgical purposes, in this work we focused on low-position ELN loops. According to our observations, the topographic relationship of the ELN/ELN loop to the STA in the surgical region is much more complicated than noted in previous reports, and ELN/ELN loops can be classified into four types based on this relationship. The branch of the STA may overlap with, accompany, or pass through the ELN loop and its branches. In the present work, apart from the glandular branches, the STA presented several medial branches, including isthmus and muscular branches. These medial branches of the STA can easy overlap with or cross the ELN or ELN loop in such instances. The complicated relationship between the ELN loop and the STA suggests that the superior thyroid vessels, including
arterial branches and venous tributaries, should be isolated individually and then ligated to avoid mistaking them for the ELN during surgery. It is worth noting that, in type C, the laryngeal branch of the STA—which arises from the STA below the level of the hyothyroid membrane—is accompanied by the CTB of the ELN or ELN loop (Fig. 3a1, b1). Previous studies have shown that the origin, courses, and branching patterns of the STA may vary, which increases the complexity of the vessels and nerves (Ozgur et al. 2009; Vazquez et al. 2009). Therefore, when ligating the laryngeal branch of the STA in larynx surgery, special attention should be paid to avoiding damage to the muscular branch of the ELN or ELN loop. In addition, 5.2 % of the ELN loops were below the superior thyroid pole in the present study (Fig. 4c1, d1). The ELN loop and its branches were covered by the superior pole and coursed between the gland and the STA. Numerous studies have shown that the position of ELN and its relation to the STA may change due to disease of the thyroid gland, parathyroid gland, or lymph nodes (Moosman and DeWeese 1968; Cernea et al. 1995). Therefore, great caution should be exercised regarding these hidden nerves during operations. The academic debate regarding whether surgeons should identify the ELN during surgery is controversial. Some scholars hold the opinion that the identification of the ELN is not a dangerous procedure and that the nerve is safe while undergoing visual dissection and exploration in most thyroidectomy procedures (Hurtado-Lopez et al. 2005). The present study showed that the relationship between the ELN/ELN loop and the STA is so
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External laryngeal nerve loop
Fig. 4a–d Type D relationship between the STA and the ELN loop. a1 The ECA presents 2 STAs (arrow). The medial part (triangle) of the loop runs posterolateral to the medial STA and enters the CTM. The lateral part (arrowhead) of the loop runs anterior and medial to the lateral STA and enters the TG. a2 Sketch of a1. b1 The loop lies medial to the STA. The lateral part of the loop enters the TG. The CTB (triangle) from the loop passes through the glandular branch of the STA and then runs accompanied by the IB (arrow) of the STA. b2 Sketch of b1. c1 The loop exhibits an anterior IPCM branch (arrow) and a posterior branch which bifurcates into the GB (arrowhead) and the CTB (triangle). The bifurcation of the ELN lies on the surface of
the branch of the STA and is lower than the superior thyroid pole. c2 Sketch of c1. d1 The STA presents an isthmus branch and GB (arrow). The lateral part of the loop enters the TG (arrowhead); the medial part of the loop subdivides into the glandular branch and the IPCM branch (triangle), which runs forwards below the posterior branch of the STA. d2 Sketch of d1. CTB cricothyroid muscle branch, CTM cricothyroid muscle, ECA external carotid artery, ELN external laryngeal nerve, GB glandular branch, IB isthmus branch, IPCM inferior pharyngeal constrictor muscle, STA superior thyroid artery, TG thyroid gland
inconsistent that it is impossible to identify the ELN or ELN loop in some cases. Therefore, individual isolation of the STA together with its branches in the critical surgical region (the plane less than 1 cm above and the plane below the superior thyroid pole) is recommended before ligation. Great caution should be exercised regarding some branches of the STA, especially branches that course medially to the larynx or muscles. Considering the varied and complicated neurovascular relationship involved, we do not recommend systematic detection of
the ELN loop or its branches during surgery. It is difficult and impractical for surgeons to identify all of these structures given the limited surgical field and time. An attempt to dissect the ELN or ELN loop may in some cases increase the chance of nerve damage when dealing with the thyroid vascular pedicle, including the arteries and veins. However, the application of other instruments during surgery, such as intraoperative nerve monitoring (Barczynski et al. 2012), provides extra insurance against ELN or ELN-loop injury.
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Fig. 5 Topographic relationship between the STA and the ELN loop. ELN external laryngeal nerve, STA superior thyroid artery Acknowledgments The authors most gratefully acknowledge the donors of the cadavers used in the present study. This project was funded by the National Basic Research Program of China (2009CB18300). Conflict of interest of interest.
The authors declare that they have no conflict
References Barczynski M, Konturek A, Stopa M, Honowska A, Nowak W (2012) Randomized controlled trial of visualization versus neuromonitoring of the external branch of the superior laryngeal nerve during thyroidectomy. World J Surg 36:1340–1347
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Cernea CR, Nishio S, Hojaij FC (1995) Identification of the external branch of the superior laryngeal nerve (EBSLN) in large goiters. Am J Otolaryngol 16:307–311 Cernea CR, Brandao LG, Hojaij FC, De Carlucci D, Montenegro FL, Plopper C, Vanderlei F, Gotoda R, Dias FL, Lima RA (2010) How to minimize complications in thyroid surgery? Auris Nasus Larynx 37:1–5 Dackiw AP, Rotstein LE, Clark OH (2002) Computer-assisted evoked electromyography with stimulating surgical instruments for recurrent/external laryngeal nerve identification and preservation in thyroid and parathyroid operation. Surgery 132:1100–1106 (discussion 1107–1108) Dedivitis RA, Guimaraes AV (2005) Identification of the external branch of the superior laryngeal nerve during minimally invasive video-assisted thyroidectomy. Braz J Otorhinolaryngol 71:326–328
External laryngeal nerve loop Fewins J, Simpson CB, Miller FR (2003) Complications of thyroid and parathyroid surgery. Otolaryngol Clin North Am 36:189–206 Friedman M, LoSavio P, Ibrahim H (2002) Superior laryngeal nerve identification and preservation in thyroidectomy. Arch Otolaryngol Head Neck Surg 128:296–303 Furlan JC (2002) Sympathetic fiber origin of the superior laryngeal nerve and its branches: an anatomic study. Clin Anat 15:271–275 Furlan JC, Cordeiro AC, Brandao LG (2003) Study of some ‘‘intrinsic risk factors’’ that can enhance an iatrogenic injury of the external branch of the superior laryngeal nerve. Otolaryngol Head Neck Surg 128:396–400 Hannan SA (2006) The magnificent seven: a history of modern thyroid surgery. Int J Surg 4:187–191 Huang HX, Sun SQ, Ren ZQ, Wang XL, Tang WJ, Sun YX, Wang KJ (2012) Superior laryngeal nerve loop: patterns and surgical implications. Surg Radiol Anat 34:977–985 Hurtado-Lopez LM, Pacheco-Alvarez MI, Montes-Castillo Mde L, Zaldivar-Ramirez FR (2005) Importance of the intraoperative identification of the external branch of the superior laryngeal nerve during thyroidectomy: electromyographic evaluation. Thyroid 15:449–454 Jansson S, Tisell LE, Hagne I, Sanner E, Stenborg R, Svensson P (1988) Partial superior laryngeal nerve (SLN) lesions before and after thyroid surgery. World J Surg 12:522–527 Kochilas X, Bibas A, Xenellis J, Anagnostopoulou S (2008) Surgical anatomy of the external branch of the superior laryngeal nerve
and its clinical significance in head and neck surgery. Clin Anat 21:99–105 Moosman DA, DeWeese MS (1968) The external laryngeal nerve as related to thyroidectomy. Surg Gynecol Obstet 127:1011–1016 Oliveira LR, Silva AL (2007) Superior laryngeal nerve anatomy in corpses not preserved in formaldehyde: contribution to the operative technique. Acta Cir Bras 22:220–228 Olthoff A, Schiel R, Kruse E (2007) The supraglottic nerve supply: an anatomic study with clinical implications. Laryngoscope 117:1930–1933 Ozgur Z, Govsa F, Celik S, Ozgur T (2009) Clinically relevant variations of the superior thyroid artery: an anatomic guide for surgical neck dissection. Surg Radiol Anat 31:151–159 Page C, Laude M, Legars D, Foulon P, Strunski V (2004) The external laryngeal nerve: surgical and anatomic considerations. Report of 50 total thyroidectomies. Surg Radiol Anat 26:182–185 Sun SQ, Chang RW (1991) The superior laryngeal nerve loop and its surgical implications. Surg Radiol Anat 13:175–180 Sun SQ, Dong JP (1997) An applied anatomical study of the superior laryngeal nerve loop. Surg Radiol Anat 19:169–173 Vazquez T, Cobiella R, Maranillo E, Valderrama FJ, McHanwell S, Parkin I, Sanudo JR (2009) Anatomical variations of the superior thyroid and superior laryngeal arteries. Head Neck 31:1078–1085
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ORIGINAL ARTICLE
An applied anatomical study on the external laryngeal nerve loop and the superior thyroid artery in the neck surgical region Wei-Tian Lu • Shan-Quan Sun • Juan Huang Yuan Zhong • Jin Xu • Sheng-Wei Gan • Lu Guo • Ting-Ting Mo
•
Received: 10 February 2014 / Accepted: 14 June 2014 Ó Japanese Association of Anatomists 2014
Abstract This study was conducted to investigate the topographic relationship between the external laryngeal nerve (ELN) loop and the superior thyroid artery (STA), in order to provide the anatomical foundations for protecting the ELN during surgery. In the present study, 48 adult human cadavers were dissected and analyzed. For the 21 (21.9 %) low-position ELN loops observed, the neurovascular relationship between the STA and the nerve was classified into four types: (1) the artery overlapped the nerve; (2) the artery passed through the ELN loop; (3) the muscular branch of the ELN loop and the laryngeal branch of the STA coursed together; and (4) the branches of the STA and the ELN loop were interlaced. Our study suggested that the patterns of ELN loops are so complicated that they have not been statistically defined in any previous study, which should be kept in mind when attempting to protect the nerve from injury. Also, because of the variable
W.-T. Lu S.-Q. Sun (&) J. Huang J. Xu S.-W. Gan Institute of Neuroscience, Chongqing Medical University, 1 Yixueyuan Road, Yuzhong District, Chongqing 400016, China e-mail: [email protected] W.-T. Lu S.-Q. Sun J. Huang J. Xu S.-W. Gan Department of Anatomy, Chongqing Medical University, Chongqing 400016, China Y. Zhong The General Morphology Lab of Experimental Teaching Management Center, Chongqing Medical University, Chongqing 400016, China L. Guo T.-T. Mo National Class Preclinical Medicine Experimental Teaching Demonstration Center, Chongqing Medical University, Chongqing 400016, China
morphology of the ELN loop and its complicated topographic relationship to the STA, the vessels should be individually isolated and then ligated during thyroidectomy. When ligating the laryngeal branch of the STA during larynx surgery, special attention should be paid to avoiding damage to the muscular branch of the ELN/ELN loop. Keywords External laryngeal nerve Gross anatomy Neck surgery Superior thyroid artery Thyroidectomy
Introduction Thyroidectomy was considered professional butchery due to its high mortality rate during the early nineteenth century. However, due to improvements in the associated surgical technique, the mortality rate from thyroid surgery has decreased greatly since then (Hannan 2006). Nevertheless, complications do still occur after thyroidectomy (Fewins et al. 2003; Cernea et al. 2010). Among those complications, nerve injury is one of the most frequent and serious. Injury to the external laryngeal nerve (ELN) can result in transiently or permanently impaired phonation, which is a disastrous outcome for professional teachers and singers (Kochilas et al. 2008). Although the incidence of ELN injuries has decreased significantly due to the application of and improvements in modern techniques and instruments (Friedman et al. 2002; Dedivitis and Guimaraes 2005), cases of ELN damage are still reported from time to time (Jansson et al. 1988; Dackiw et al. 2002; Page et al. 2004). Upon analyzing the factors involved in ELN injury, insufficient knowledge of the anatomy of the ELN was thought to be the main reason for ELN damage. Therefore, a study of the morphologic and topographic
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anatomy of the ELN has been proposed as a key step towards preventing ELN damage during thyroidectomy and neck surgery (Jansson et al. 1988; Furlan et al. 2003). According to the literature, the ELN is a linear nerve trunk (Olthoff et al. 2007; Oliveira and Silva 2007). Based on a study of 60 adult cadavers, Sun and Chang (1991) reported that the superior laryngeal nerve (SLN) and its branches often connected with one or more branches from the cervical sympathetic chain (CSC) to form an SLN loop. SLN loops were subsequently divided into 5 types and 17 subtypes based on morphological variations. Furlan (2002) proposed an alternative SLN/ELN loop classification based on the number of nervous connections between the SLN/ ELN and the CSC, and confirmed that Sun’s results were repeatable and that SLN loops could be observed in different racial groups. Later, Huang et al. (2012) identified an additional 18 SLN loop subtypes based on variations in features and branching patterns, thus extending our knowledge of the SLN loop and its branches. In previous studies, the incidence of a CSC-ELN loop was found to be 73.3 % (Sun and Chang 1991), 92.5 % (Sun and Dong 1997), 59.0 % (Furlan 2002), and 82.0 % (Huang et al. 2012). Therefore, from a statistical point of view, the ELN is more likely to be looped than linear. Meanwhile, a study by Huang et al. (2012) showed that the relationship between the ELN loop and the superior thyroid artery (STA) is variable and complicated, making surgery in this region more challenging. Regretfully, the ELN is still described as linear in the literature and the concept of an ELN loop is rarely recognized by surgeons. Although there have been some works on the surgical anatomy of the STA (Ozgur et al. 2009; Vazquez et al. 2009), studies focusing on the neurovascular relationship between the STA and the ELN loop are scarce, which is one of the reasons why such nerve injuries continue to occur. Given this situation, the purpose of the present study was to conduct a morphologic and topographic study of the ELN loop and the STA during cadaveric dissection in order to provide the anatomical foundations for protecting the ELN during surgery.
Materials and methods Forty-eight adult cadavers (33 male, 15 female; 96 sides) fixed with 4 % formalin were examined in this study. Bodies that had undergone neck surgery were excluded. The ELN, STA, and surrounding adjacent structures, including the thyroid gland, cricothyroid muscle (CTM), inferior pharyngeal constrictor muscle (IPCM), and thyroid cartilage, were carefully dissected. All of the structures were dissected using a 6-power magnifying glass. Data on the basic shape, connected formation, course, and branches
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of the nerve connection between the SLN, internal laryngeal nerve (ILN), ELN, and CSC were observed and recorded. The distance from the lowest point of the ELN loop to the superior thyroid pole was measured. The morphology of the ELN loop and its relationship to the STA were noted. All dissections were performed using a standard surgical procedure. This study was approved by the Human Ethics Committee of Chongqing Medical University.
Results ELN loop and its branches The ELN loops (76 sides) were subdivided into three types based on the distance from the superior thyroid pole to the lowest point of the loop (Sun and Chang 1991): type I (55 sides), 1 cm above the superior thyroid pole; type II (16 sides), less than 1 cm above the superior thyroid pole (Figs. 1a1, b1, 2a1, b1, 3a1, b1, 4a1, b1); type III (5 sides), below the superior thyroid pole (Fig. 4c1, d1). All ELN loops presented glandular and cricothyroid muscle branches (GB and CTB, respectively). In some sides, the ELN loop exhibited branches that entered the IPCM (Fig. 4c1, d1) or the larynx (Fig. 3a1, b1). STA and its branches Before entering the thyroid gland, the STA presented anterior and posterior glandular branches (Figs. 1a1, 2a1, b1, 3b1). In 6 sides, the STA showed several medial branches that entered the isthmus or the muscles (Figs. 1a1, b1, 2a1, b1, 4b1–d1). In 5 sides, the STA exhibited laryngeal branches below the level of the hyothyroid membrane and entered the larynx and adjacent muscles (Fig. 3a1, b1). Relationship of the ELN loop to the STA Because type I ELN loops were far from the superior thyroid pole, these loops were not observed for surgical implications. For the 21 low-position ELN loops (type II and III) observed, the neurovascular relationship between the STA and the nerve was classified into four types: (1) the branch of the STA overlapped with the branches of the ELN loop (Figs. 1a1, b1, 5); (2) the glandular branch of the STA passed through the ELN loop (Figs. 2a1, b1, 5); (3) the laryngeal branch of the STA and the CTB of the ELN loop were enclosed by a fibrous sheath, forming a neurovascular bundle, which entered the CTM (Figs. 3a1, b1, 5); and (4) the branches of the STA and the ELN loop were interlaced (Figs. 4a1–d1, 5).
External laryngeal nerve loop
Fig. 1a–b Type A relationship between the STA and the ELN loop. a1 The STA presents 2 GBs and a CTB. The loop overlaps with the branches of the STA and presents a CTB (triangle). a2 Sketch of a1. b1 The laryngopharyngeal branch of the STA runs across the lowest point of the loop. The loop overlaps with the PB and the LB of the
STA and exhibits a CTB. b2 Sketch of b1. CTB cricothyroid muscle branch, CTM cricothyroid muscle, ELN external laryngeal nerve, GB glandular branch, LB laryngeal branch, PB pharyngeal branch; STA superior thyroid artery, TG thyroid gland
Fig. 2a–b Type B relationship between the STA and the ELN loop. a1 The loop presents a glandular branch (arrowhead) and a CTB (triangle). One GB (arrow) of the STA passes through the loop and enters the TG. a2 Sketch of a1. b1 One GB (arrow) of the STA passes
through the loop (triangle). b2 Sketch of b1. CTB cricothyroid muscle branch, CTM cricothyroid muscle, ELN external laryngeal nerve, GB glandular branch, STA superior thyroid artery, TG thyroid gland
Discussion
frequency, and branching patterns, was more complicated than noted in the previous works. The nerve trunk(s), plus the single ELN, were seen to be single, double, or triple in number. On analyzing all of the papers that have investigated the morphology of ELN/ELN loops (Sun and Chang 1991; Sun and Dong 1997; Furlan 2002; Huang et al. 2012), it seems that the patterns of ELN loops are so complicated that none of the previous studies were able to statistically define them—the statistical results obtained for pattern variations in all of the studies showed statistical randomness. In other words, it can be said that
In this study, the ELN loop appeared in 76 sides (79.2 %). The incidence of connection between CSC and ELN in this study is almost the same as those observed in previous studies (Sun and Chang 1991; Sun and Dong 1997; Furlan 2002; Huang et al. 2012), which further proves that most ELNs are looped. However, the ELN loops found in this study differ from those seen in the previous studies in some aspects. The morphology of the ELN loops, such as their external features, anastomotic
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Fig. 3a–b Type C relationship between the STA and the ELN loop. a1 The STA is pulled laterally. The CTB of the loop (triangle) turns medially and runs between the two LBs (arrow) of the STA, entering the CTM. a2 Sketch of a1. b1 One branch (arrowhead) of the loop
enters the larynx; another CTB hooks the LB of the STA. b2 Sketch of b1. CTB cricothyroid muscle branch, CTM cricothyroid muscle, ELN external laryngeal nerve, LB laryngeal branch, STA superior thyroid artery, TG thyroid gland
‘‘variation is constant’’ for the relationship of the ELN loop to the STA. This indicates that clinical surgeons may accidentally encounter different ELN loop patterns during surgery. Perhaps this is why ELN damage is frequently reported in the literature (Dackiw et al. 2002; Page et al. 2004). Therefore, it is the duty of surgeons to familiarize themselves with both normal and abnormal ELN anatomy in order to avoid nerve injury. Meanwhile, it is also necessary to conduct further investigations of the ELN anatomy in many bodies to improve the reliability of the results of statistical analysis. The STA is the main artery that supplies the thyroid, upper larynx, and neck region (Ozgur et al. 2009). The ELN may be at risk during surgery due to its close proximity to the STA. Therefore, understanding the topographic relationship between the STA and the ELN is important for achieving safe and effective surgery. In order to obtain such topographic data for surgical purposes, in this work we focused on low-position ELN loops. According to our observations, the topographic relationship of the ELN/ELN loop to the STA in the surgical region is much more complicated than noted in previous reports, and ELN/ELN loops can be classified into four types based on this relationship. The branch of the STA may overlap with, accompany, or pass through the ELN loop and its branches. In the present work, apart from the glandular branches, the STA presented several medial branches, including isthmus and muscular branches. These medial branches of the STA can easy overlap with or cross the ELN or ELN loop in such instances. The complicated relationship between the ELN loop and the STA suggests that the superior thyroid vessels, including
arterial branches and venous tributaries, should be isolated individually and then ligated to avoid mistaking them for the ELN during surgery. It is worth noting that, in type C, the laryngeal branch of the STA—which arises from the STA below the level of the hyothyroid membrane—is accompanied by the CTB of the ELN or ELN loop (Fig. 3a1, b1). Previous studies have shown that the origin, courses, and branching patterns of the STA may vary, which increases the complexity of the vessels and nerves (Ozgur et al. 2009; Vazquez et al. 2009). Therefore, when ligating the laryngeal branch of the STA in larynx surgery, special attention should be paid to avoiding damage to the muscular branch of the ELN or ELN loop. In addition, 5.2 % of the ELN loops were below the superior thyroid pole in the present study (Fig. 4c1, d1). The ELN loop and its branches were covered by the superior pole and coursed between the gland and the STA. Numerous studies have shown that the position of ELN and its relation to the STA may change due to disease of the thyroid gland, parathyroid gland, or lymph nodes (Moosman and DeWeese 1968; Cernea et al. 1995). Therefore, great caution should be exercised regarding these hidden nerves during operations. The academic debate regarding whether surgeons should identify the ELN during surgery is controversial. Some scholars hold the opinion that the identification of the ELN is not a dangerous procedure and that the nerve is safe while undergoing visual dissection and exploration in most thyroidectomy procedures (Hurtado-Lopez et al. 2005). The present study showed that the relationship between the ELN/ELN loop and the STA is so
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External laryngeal nerve loop
Fig. 4a–d Type D relationship between the STA and the ELN loop. a1 The ECA presents 2 STAs (arrow). The medial part (triangle) of the loop runs posterolateral to the medial STA and enters the CTM. The lateral part (arrowhead) of the loop runs anterior and medial to the lateral STA and enters the TG. a2 Sketch of a1. b1 The loop lies medial to the STA. The lateral part of the loop enters the TG. The CTB (triangle) from the loop passes through the glandular branch of the STA and then runs accompanied by the IB (arrow) of the STA. b2 Sketch of b1. c1 The loop exhibits an anterior IPCM branch (arrow) and a posterior branch which bifurcates into the GB (arrowhead) and the CTB (triangle). The bifurcation of the ELN lies on the surface of
the branch of the STA and is lower than the superior thyroid pole. c2 Sketch of c1. d1 The STA presents an isthmus branch and GB (arrow). The lateral part of the loop enters the TG (arrowhead); the medial part of the loop subdivides into the glandular branch and the IPCM branch (triangle), which runs forwards below the posterior branch of the STA. d2 Sketch of d1. CTB cricothyroid muscle branch, CTM cricothyroid muscle, ECA external carotid artery, ELN external laryngeal nerve, GB glandular branch, IB isthmus branch, IPCM inferior pharyngeal constrictor muscle, STA superior thyroid artery, TG thyroid gland
inconsistent that it is impossible to identify the ELN or ELN loop in some cases. Therefore, individual isolation of the STA together with its branches in the critical surgical region (the plane less than 1 cm above and the plane below the superior thyroid pole) is recommended before ligation. Great caution should be exercised regarding some branches of the STA, especially branches that course medially to the larynx or muscles. Considering the varied and complicated neurovascular relationship involved, we do not recommend systematic detection of
the ELN loop or its branches during surgery. It is difficult and impractical for surgeons to identify all of these structures given the limited surgical field and time. An attempt to dissect the ELN or ELN loop may in some cases increase the chance of nerve damage when dealing with the thyroid vascular pedicle, including the arteries and veins. However, the application of other instruments during surgery, such as intraoperative nerve monitoring (Barczynski et al. 2012), provides extra insurance against ELN or ELN-loop injury.
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Fig. 5 Topographic relationship between the STA and the ELN loop. ELN external laryngeal nerve, STA superior thyroid artery Acknowledgments The authors most gratefully acknowledge the donors of the cadavers used in the present study. This project was funded by the National Basic Research Program of China (2009CB18300). Conflict of interest of interest.
The authors declare that they have no conflict
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