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Surgical Anatomy of the Extralaryngeal Aspect of the Superior Laryngeal Nerve
Julio C. Furlan, MD, PhD;
Lenine G. Brandão, MD, PhD;
Alberto R. Ferraz, MD, PhD;
Aldo J. Rodrigues, Jr, MD, PhD
Arch Otolaryngol Head Neck Surg. 2003;129:79-82.
ABSTRACT
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Objectives To describe the topography of the superior laryngeal nerve (SLN) and to evaluate the influence of gender, ethnicity, side of the neck, and individual height on the topography of the SLN.
Design Anatomical study of human cadavers.
Subjects Fifty fresh human cadavers (19 female subjects and 31 male subjects; age range, 22-89 years; mean age, 61 years) were randomly selected for this study. The subjects were divided into nonwhite (n = 18) and white (n = 32) ethnic groups. The t test and linear regression were used for statistical analysis of data.
Results All SLNs emerged medially to the vagus nerve. The SLNs mostly divided into internal (ibSLN) and external (ebSLN) branches distally from their origin (94%). The mean ± SE length of the SLN trunk was 16.7 ± 0.9 mm and was affected by gender (P = .01) but not ethnicity (P = .57), side of the neck (P = .96), or individual height (R2 = 0.01; P = .33). The length of the ibSLN reached 44.9 ± 1.0 mm and was unaffected by gender (P = .91), ethnicity (P = .24), side (P = .40), or height (R2<0.01; P = .71). The length of the ebSLN measured 62.6 ± 1.2 mm and was unaffected by gender (P = .69), ethnicity (P = .42), side (P = .26), or height (R2<0.01; P = .85). The mean ± SE angle between the ibSLN and the tracheoesophageal sulcus was 49° ± 1° and was unaffected by gender (P = .35), ethnicity (P = .11), side (P = .26), or height (R2<0.01; P = .96). Only 1 subject demonstrated a bilateral anatomical variation of the ibSLN close to its entrance into the thyrohyoid membrane.
Conclusions The topography of the SLN has a few anatomical variations and is unaffected by gender, ethnicity, side of the neck, and individual height, except that the SLN is longer in males than in females. These findings are important in that they can help in the prevention of SLN injuries during operations such as laryngectomy and neck dissection, as well as in the planning of laryngeal reinnervation and transplantation.
INTRODUCTION
ANATOMICAL KNOWLEDGE of the superior laryngeal nerve (SLN) is crucial for helping anatomists and surgeons to prevent intraoperative injury and to improve rehabilitation or reinnervation techniques in cases of laryngeal paralysis.1 However, "the anatomy of the SLN continues to be misrepresented, and this ‘error' persists in journals as well as the most recently published textbooks," as Kambic et al2 wrote in 1984. Also, anatomy and physiology are mutually collaborative scientific fields, and progress in either one is potentially helpful for the other.
The functions of the internal (ibSLN) and external (ebSLN) branches of the SLN are not well recognized. According to Rueger,3 the current understanding is that the ibSLN and the ebSLN are mixed nerves, as was the popular view before 1850. In fact, sensorial neurons were mostly found within the ibSLN; fewer were observed within the ebSLN.4 Other studies demonstrated that sympathetic fibers may reach the larynx through both branches of the SLN.5 Moreover, not only has ebSLN motor function on cricothyroid muscle,6 but also stimulation of the ibSLN can provoke tonic contraction in the vocal cord and ventricular folds, probably using the nervous connection with the recurrent laryngeal nerve: the so-called Galen anastomosis.7 Finally, other functions such as olfactory acuity and respiratory control have been associated with the SLN.8-9
The focus of this study was to describe the topography of extralaryngeal aspect of the SLN and its branches, as well as to evaluate the influence of gender, ethnicity, side of the neck, and individual height on the topography of the SLN.
METHODS
Fifty fresh human adult cadavers were randomly selected for the study, which was approved by the Ethics Board Committee of the Faculty of Medicine, University of São Paulo, São Paulo, Brazil. Bilateral neck dissections were performed as follows: The cadavers were placed in a supine position on the necropsy table with a rolled pad behind the shoulders to extend the neck. The head was slightly rotated to the contralateral side as in a lateral neck operation. The vagus nerve was carefully dissected from the jugular foramen to the origin of the trunk of the SLN; subsequently, the ebSLN and ibSLN were dissected to their entrances into the larynx (Figure 1). All nerve structures were dissected using a x2.5 magnifying glass.
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Figure 1. Dissection of superior laryngeal nerve on a left lateral view. 1 indicates greater horn of the hyoid bone; 2, internal branch of the superior laryngeal nerve; 3, external branch of the superior laryngeal nerve; 4, vagus nerve; 5, hypoglossal nerve; 6, common carotid artery; and 7, submandibular gland.
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Using a caliper rule, the following segments of the SLN were measured: length of the SLN trunk, length of the ibSLN, and length of the ebSLN. The angle between the ibSLN and the tracheoesophageal sulcus was measured with a caliper as well. The anatomical relationships between the SLN and adjacent structures, such as lingual and facial arteries, were also observed and analyzed.
For every element studied, groups divided into gender, ethnicity (nonwhite and white), side of the neck, and individual height were compared in order to assess their influence on the topography of the SLN. All data were statistically analyzed using the t test and linear regression. Significance was assumed if the P value was less than .05.
RESULTS
Every SLN emerged medially to the vagus nerve and divided into the ibSLN and ebSLN distally from its origin. Most SLNs showed a trunk arising from the inferior (no dose) ganglion of the nerve vagus, just caudal to the jugular foramen of the skull. However, in 6% of the SLNs, the bifurcation occurred at their origin, just below the inferior ganglion of the nerve vagus. The SLN and its branches always assumed an anterior, medial, and caudal direction before reaching the larynx. Their paths of descent initially began posteriorly and proceeded medially to the carotid arteries, and the ibSLN was always located medially to the lingual and facial arteries. Furthermore, the ibSLN was mostly observed in a parallel and medial position to the superior laryngeal artery (89%), but in 11% of the dissections it was located inferiorly and medially to that artery. The ibSLN was adjacent to the wall of pharynx, swung medially caudal to the greater horn of hyoid bone, and passed beneath the thyrohyoid muscle before the nerve pierced the thyrohyoid membrane. The ebSLN descended lying on the inferior pharyngeal constrictor and curved anteriorly and medially close to the lower edge of the thyroid cartilage before the ebSLN innervated the cricothyroid muscle.
The length of the trunk of the SLN ranged from 0 to 41.8 mm (mean ± SE, 16.7 ± 0.9 mm). This element was affected by gender, but not by ethnicity or side of the neck (Table 1). The length of the ibSLN ranged from 21 to 84.9 mm (mean ± SE, 44.9 ± 1.0 mm) and was unaffected by gender, ethnicity, or side of the neck (Table 2). The length of the ebSLN measured between 31.5 and 90.3 mm(mean ± SE, 62.6 ± 1.2 mm) and was unaffected by gender, ethnicity, or side of the neck (Table 3). The angle between the ibSLN and tracheoesophageal sulcus ranged from 18° to 75° (mean ± SE, 49° ± 1°) and was unaffected by gender, ethnicity, or side of the neck (Table 4). Moreover, the length of the trunk of the SLN, the ibSLN, and the ebSLN was not significantly correlated to individual height (Figure 2, Figure 3, and Figure 4, respectively). Also, there was no strong correlation between the individual height and the angle between the ibSLN and the tracheoesophageal sulcus (R2<0.01; P = .96).
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Table 1. Length of Trunk of the Superior Laryngeal Nerve (N = 100)
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Table 2. Length of Internal Branch of the Superior Laryngeal Nerve (N = 100)
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Table 3. Length of External Branch of the Superior Laryngeal Nerve (N = 100)
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Table 4. Angle Between Internal Branch of the Superior Laryngeal Nerve and the Tracheoesophageal Sulcus (N = 100)
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Figure 2. Graphic representation of correlation between individual height and length of trunk of the superior laryngeal nerve (SLN) (linear regression analysis) in 100 dissections.
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Figure 3. Graphic representation of correlation between individual height and length of the internal branch of the superior laryngeal nerve (SLN) in 100 dissections (linear regression analysis).
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Figure 4. Graphic representation of correlation between individual height and length of the external branch of the superior laryngeal nerve (SLN) in 100 dissections (linear regression analysis).
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Only 1 subject had a bilateral anatomical variation of the ibSLN close to its entrance into the thyrohyoid membrane. This variant represented 2% of our dissections and was characterized by a long loop caudal to the hyoid horn, followed by an ascendant pathway up to penetration at the ostium of the thyrohyoid membrane.
COMMENT
Knowledge of the topography of the SLN and its branches is essential for diverse surgical procedures. However, the neuroanatomy of the larynx is still a controversial issue. Most anatomical studies have emphasized the importance of preservation of the ebSLN during thyroidectomy.10 Nevertheless, knowledge of localization and anatomical variations of the ibSLN is a prerequisite for surgeons who perform operations such as sensorial denervation of the larynx for odynophagia or superior laryngeal neuralgia, preservation of the ibSLN during supraglottic laryngectomy and cervical spine procedures, restoration of laryngopharyngeal sensation by neural anastomosis between the greater auricular nerve and the ibSLN, conservation of the ibSLN in the lateral pharyngotomy, and, more recently, laryngeal transplantation.11-17
The classic description of the SLN is a constant and short trunk that divides into the internal and external branches.2, 18-21 However, Kambic et al2 reported that in 5% of their dissections the ebSLN and ibSLN arose from the lower pole of the inferior ganglion of the vagus nerve. Our study demonstrated a 6% incidence of absence of the trunk of the SLN. The internal and external branches of the SLN constantly descend toward and pierce the lateral aspect of the thyrohyoid membrane and cricothyroid muscle, respectively. This pathway was observed in all our dissections and was a consensual finding in other studies.2, 18-22 Nonetheless, both ibSLNs in 1 subject (2% of dissections) were characterized by a long loop caudal to the hyoid horn, followed by an ascendant pathway up to penetration at the ostium of the thyrohyoid membrane. During surgical procedures such as partial laryngectomies, this anatomical variation could result in an injury of the ibSLN owing to its unexpected course.
In our specimens, both the ibSLN and the ebSLN were always located medially to the carotid arteries. This seems to be the most common description of their relationship,19 even though Kambic et al,2 for instance, reported that the ebSLN "descends from behind the internal carotid artery." However, anatomical variations of this topographic relationship, such as an anterior position of the SLN on the internal carotid artery, have been reported.21 Also, in our study, the ibSLN was always located medially to the lingual and facial arteries. Droulias et al19 reported that the ibSLN passed laterally to the lingual artery in 22 of 24 specimens. The ibSLN has been described as always accompanied by the superior laryngeal artery, and this nerve mostly remains cranial to that artery.18-19,22 Our findings showed that most ibSLNs (89%) were in a parallel and medial position to the superior laryngeal artery, whereas they were located inferiorly and medially to the superior laryngeal artery in 11% of dissections.
The length of SLN trunk was, on average, 16.7 mm, and it was 0 mm in 6 of 100 dissections. Male subjects had a statistically longer SLN trunk than female subjects (P = .01). There was no statistically significant difference regarding ethnicity (P = .57), side of the neck (P = .96), and individual height (R2 = 0.01; P = .33). Durham and Harrison18 mentioned a limit of 20 mm for the length of the SLN trunk, and Kambic et al2 reported that the SLN trunk was approximately 15 mm long, but in 5% of the dissections, the 2 branches of the SLN originated from the ganglion itself. In our study, the length of the ibSLN was, on average, 44.9 mm, and there was no statistically significant difference with regard to gender (P = .91), ethnicity (P = .24), side of the neck (P = .40), and individual height. Moreover, the length of the ebSLN measured, on average, 62.6 mm and was unaffected by gender (P = .69), ethnicity (P = .42), side of the neck (P = .26), and individual height (R2 = 0.01; P = .85). Thomassin21 described an ebSLN that was 65 mm long, whereas Kambic et al2 mentioned an average of 80 mm for the ebSLN. Also, in our specimens, there was no considerable difference between the right and left sides of the neck in the course of the SLN and its branches, whereas Kambic and colleagues usually found differences between the 2 sides in their dissections. Finally, the angle between the ibSLN and the tracheoesophageal sulcus was, on average, 49°, and, to our knowledge, no previous study has cited this parameter. Also, to our knowledge, this is the first study to statistically analyze the influence of gender, ethnicity, side of the neck, and individual height on the length of the trunk of the SLN, the ibSLN, and the ebSLN, as well as the angle between the ibSLN and the tracheoesophageal sulcus.
CONCLUSIONS
The topography of the SLN has a few anatomical variations and is unaffected by gender, ethnicity, side of the neck, and individual height, except that the SLN is longer in males than in females. These findings are important in that they can help the surgeon to prevent SLN injuries during operations such as laryngectomy, neck dissection, thyroidectomy, anterior cervical spine approach, and parathyroidectomy, as well to plan laryngeal reinnervation and transplantation.
Moreover, this study reinforced the need for further investigation with focus on the anatomy of the SLN and its branches. Greater awareness by anatomists and surgeons regarding misrepresentation of the anatomy of the SLN and its branches would be beneficial to reduce risk of iatrogenic injury to those nerves.
AUTHOR INFORMATION
Corresponding author: Julio C. Furlan, MD, PhD, Mount Sinai Hospital, 600 University Ave, Suite 1521, Toronto, Ontario, Canada M5G 1X5 (e-mail: juliofurlan{at}idirect.com).
Accepted for publication August 29, 2002.
This study was presented at the annual meeting of the American Head and Neck Society, Boca Raton, Fla, May 11-13, 2002.
The dissections were performed at the Obit Verifying Service of the Faculty of Medicine, University of São Paulo, São Paulo, Brazil.
We thank Margaret Allen for her assistance with the preparation of the manuscript for this article.
From the Division of Head and Neck Surgery, Department of Surgery, Clinical Hospital of the Faculty of Medicine (Drs Furlan, Brandão, and Ferraz), and the Department of Anatomy, Faculty of Medicine (Dr Rodrigues), University of São Paulo, São Paulo, Brazil. Dr Furlan is now with the Department of Surgery, Mount Sinai Hospital, University of Toronto, Toronto, Ontario.
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