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Ann Thorac Surg 1999;67:217-223
© 1999 The Society of Thoracic Surgeons

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Original Articles

Recurrent and superior laryngeal nerves: a new look with implications for the esophageal surgeon

^a University Hospital, Klinikum rechts der Isar, Technische Universität, München, Germany

Accepted for publication June 24, 1998.

Address reprint requests to Professor Dr. med Liebermann-Meffert, Department of Surgery, Klinikum r.d.Isar, Ismaningerstr.22, D 81675 München, Germany

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Background. Injury to the recurrent laryngeal nerve (RLN) is an unwelcome and not unfrequent complication of operations on or near the upper thoracic or cervical esophagus. Because anatomic information useful to the surgeon is difficult to come by, the aim of this study was to reinvestigate and display the RLNs and superior laryngeal nerves in humans.

Methods. Postmortem en bloc specimens were studied: 23 by macroscopic dissection and 11 by large field serial histology. The nerves and their branches and supply areas were photographed at each step of dissection from the lateral (the surgeon’s approach) and from the posterior aspect.

Results. The RLNs were 2- to 3-mm thick compact slack cords, sinuously passing upward within the lateral peritracheal, and less frequent periesophageal, loose connective tissue, the left RLN being closer to the tracheoesophageal groove than the right. Both RLNs gave off 8 to 14 branches, equally distributed to the esophagus and trachea. These were 2.5- to 1-cm long when stretched. The primarily identical pattern became unpredictable underneath the thyroid gland, an area that covered approximately 3 cm of the proximal esophagus. The RLN, still fairly robust (> 1 mm) dipped, being firmly attached, into the larynx laterocaudad to the cricopharyngeus muscle. As the RLN and superior laryngeal nerves supply the same laryngeal muscles and mucosa, this twofold innervation may compensate for some sequelae of RLN injury.

Conclusions. Displaying the RLNs, an important step in a variety of neck operations, dissection of the RLNs branches close to the esophagus and intestinocervical anastomosis as low as possible, will certainly reduce RLN injury.

	Introduction

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Injury to the recurrent laryngeal nerve (RLN) is an unwelcome and not unfrequent complication of operations on or near the upper thoracic or cervical esophagus. Injury to the RLNs in esophageal operations appears to be on the rise [1]. Nobody can say for certain whether the reason is an increase in the overall number of neck and mediastinal operations, an increase in the number and variety of specialists who operate infrequently in less than familiar terrain or simply more honest reporting. Postoperative vocal cord paralysis rates range from less than 1% to as high as 20% to 37% in the literature [2–4]. Suboptimal documentation adds to the confusion. Two things, however, are clear: textbook descriptions and depictions of laryngeal nerve anatomy [5, 6] have not matched the interest in the anatomy, function, and surgical procedure of the visceral occupants of the same area. Indeed, our understanding of the superior and recurrent laryngeal nerves has hardly changed since Gray [7] and Pernkopf [8] contributed their colossal text on gross human anatomy more than half a century ago. Anatomy illustrations usually depict the nerves in unhelpful projections; for example, the esophageal surgeon most often dissects the cervical esophagus from the left lateral approach, whereas the anatomist sees through all obstacles from the front side or sagittal perspective.

Surgeons, for their part, have become complacent, dismissing recurrent nerve palsy as inconvenient hoarseness easily remedied with an injection of Teflon, rather than as a usually avoidable disruption of reflexes that shunt food to the esophagus and air to the lungs.

The purpose of this study was to take a fresh and detailed look at the anatomy of the laryngeal nerves from the viewpoint of the esophagus surgeon who needs to know where the nerves run, exactly what they innervate, and how to avoid injuring them. Therefore, emphasis was laid on photographic display of the most frequent nerve distribution, in particular to that of the "unseen" right RLN.

	Material and methods

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
The innervation of the esophagus and hypopharynx was studied in 34 human corpses. The age of the subjects ranged from 21 to 85 years (mean, 60 years). Eighteen were men and 16 women. Fifteen specimens were obtained from the Anatomical Institute of the Technical University of Munich, 8 from the Institute of Forensic Medicine, Ludwig-Maximilian University Munich, Germany, and 13 from the Institute of Pathology, University Basel, Switzerland. None had previous intrathoracic disease.

Because of the hidden position of the RLNs in the posterior mediastinum behind the trachea, this study required the specimens to be dissected from the posterior aspect en bloc. Each visceral package contained the neck and thoracic organs from the tongue to the diaphragm, and from the sternum to the spine. We then removed the heart and lungs, leaving the great vessels, tracheal bifurcation, and the main bronchi intact. Although we focused our attention on the inferior (recurrent) and superior laryngeal nerves (SLNs), we made notes of the surrounding structures and relationships, the layout being entered schematically on standard sketches. The proximity of the RLNs to the esophagus, the trachea, and the larynx and their distribution pattern was also noted at each step of preparation.

We used different techniques to display the structures.

Macroscopic preparation
Twenty-three specimens were fixed as follows: First, while still in situ, a mixture of alcohol, glutaraldehyde, and low percentage formaldehyde solution was injected into the large vessels. Then the specimens were dissected en bloc and submerged in 10% alcohol, which was changed daily for 3 weeks, then monthly. This fixation solution had the advantage of being essentially free from odor, irritant, or toxic substances enabling us to work close to the specimen without offending the eyes and the nose. Shrinkage of the viscera and other soft tissues was 5%, which was less than that of the histologically processed specimens (22%) and that previously reported for the isolated stomach using a different fixation technique [9].

During the stepwise preparation we measured the length and thickness of the vagus nerve and the RLN from the turning point up to the entry into the larynx using a slide gauge.

Six specimens were subjected to a protracted and painstaking dissection of the inferior (recurrent) and SLN. We identified the distance and number of branches leaving the RLNs to enter the esophagus, trachea, and larynx using for small branches and difficult areas up to 40 times magnification. Several high power spot lights were required. Each step of preparation was related to anatomic and surgical landmarks and photographed with either Leitz-reprovit-camera (Leica Camera AG, Solus, Germany) or a Hasselblad (Hasselblad, Göteborg, Sweden) camera using Kodak (Kodak Germany Kodak AG, Stuttgart, Germany) TMx 100° films. We then traced the structures on the photographs using transparent bigraph paper and looked for patterns of innervation.

In similar intention we opened the pharynx musculature and the larynx from the dorsal aspect and meticulously followed the terminal branches of the inferior and superior laryngeal nerves to their terminations in the esophagus, hypopharynx, cricopharynx, larynx, and trachea. The superior laryngeal nerve was traced from its bifurcation into internal and external divisions above and behind the course of the carotid arteries.

The time required for each of the two investigators to dissect and photograph the material was 204 hours (mean) for each of the six specimens.

In six further en bloc specimens we applied increasing traction on the RLNs. First on the esophagus toward lateral in three specimens using a rubber band while the RLNs were still in their connective tissue surroundings, and in the other three we exerted pull on the RLNs after their complete exposure.

Histologic evaluation
The 11 specimens used were fixed en bloc in 5% formaldehyde solution at pH 4 for 3 weeks. Then they were transversely cut in 1-cm thick consecutive segments from the cricoid cartilage to the area 3 cm caudal to the tracheal bifurcation. After photographic documentation of the macroscopic cut surfaces histologic "large field slides" were prepared from the complete cut surface and stained with hematoxylin-eosin and with van Gieson dye. After being photographically magnified threefold, each slide was covered with a transparent millimeter paper sheet on which the structures were traced. Special attention was given to the location of the recurrent nerves in relation to the esophagus and the trachea; the distance from each was precisely measured.

Representation
The most common pattern of the distribution of the RLNs and the SLNs and the often unseen right RLN are shown as examples in the photographs.

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Recurrent laryngeal nerve origins
Without argument, the vagi originating in the medulla oblongata were the longest and the broadest of the cranial nerves. They lay in the carotid sheath, keeping a distance of 1 to 2 cm from the esophagus and trachea during their descent to the mediastinum, from where their offshoot, the recurrent laryngeal nerves, returned to the neck. The left RLN arose at the level of the ligamentum arteriosum where it looped around the aorta from front to back. Here the surrounding connective tissue was relatively dense containing a network of collagen fibers, fine lymphatic and blood vessels, and nerve fibers. This confined the ability of the nerve to follow greater pull at this location. On the right side the nerve took a similar dive around the proximal portion of the subclavian artery, whereas the branches of the vagus innervated the esophagus and trachea further down (Fig 1 ).

View larger version (149K): [in this window] [in a new window]   Fig 1. Innervation of the distal half of the proximal esophagus (1) and the trachea (2) through the right vagus nerve (5). Turning point (5* ) of the right RLN (3). A pair of tweezers is inserted into the subclavian artery (9) to pull it upward. The structures of the human en bloc specimen are exposed and photographed from the right aspect. Aorta (10).

Recurrent laryngeal nerve main trunk characteristics and course
In our 23 cases all RLNs presented as a singular main cord. On both sides they were easy to discern and palpate as robust cords. The left RLN was a mean of 3.4 mm broad at the offspring and 1.8 mm at the entry into the larynx, the right 3.0 to 1.2 mm, respectively.

Within the somewhat bulky loose connective tissue that covered the esophagus and trachea laterally the RLNs were slack and sinuous (Fig 2 ). Many of the RLNs passed upward along the trachea, then changed sides to become parallel to the respective lateral wall at the upper esophagus. A few were located on the esophagus. They never lay in a straight line in the groove between the trachea and the esophagus, until just before entering the pharynx (Fig 3 ). Owing to the different level of the subclavian artery and the aortic arch as turning points, the right RLN was the shorter of the two. Both RLN were initially farther from the esophagus and the trachea than at the upper end (Fig 4 ). However, the left RLN was significantly more closely applied to the esophagus and trachea throughout its length than was the right nerve (Fig 4).

View larger version (124K): [in this window] [in a new window]   Fig 2. Meandering, sinuous course of the left RLN (3) shown before its dissection from the underlaying peritracheal (2) tissues. The thyroid gland (6) is still in place. Esophagus (1), aorta (10), left common carotid artery (7).

View larger version (17K): [in this window] [in a new window]   Fig 3. Position of the recurrent laryngeal nerve (RLN) in relation to the trachea and esophagus at a level 4 and 1 cm caudal to the cricoid cartilage in the transverse sections of 10 specimens. Shrinkage by fixation was 22%.

View larger version (27K): [in this window] [in a new window]   Fig 4. The lengths of the two recurrent laryngeal nerves between the lower margin of the cricoid cartilage and their turning point as well as the distance from the esophageal wall. The data obtained were measured in 10 histologic serial cross-sections, that is, in normal position undistorted by preparatory manipulation. Reference (0) is the lower margin of the cricoid cartilage.

Two to 3 cm before dipping into the pharynx the RLNs became intimately entangled by the inferior thyroid artery, passing in front, behind, or between the vessel loops at variable angles similar to what is shown in Figures 5 and 6 .

View larger version (97K): [in this window] [in a new window]   Fig 5. The course of the left recurrent laryngeal nerve (3) between the turning point (5*) from the vagus nerve (5) and the entry into the larynx (3*) is photographed from the lateral aspect after removal from the peritracheal tissues. The attachments of the thyroid gland (6) are removed, the gland is shifted posteriorly to display the recurrent laryngeal nerve (3) and the vascular arrangement underneath. Esophagus (1), trachea (2), inferior constrictor muscle of the pharynx wall (11), that is, the lower esophageal sphincter (12). Note the Zenker’s diverticulum on the right (arrow).

View larger version (133K): [in this window] [in a new window]   Fig 6. Posterior aspect of the muscular wall of the esophagus (1) and pharynx (11). The right recurrent laryngeal nerve (3) largely removed from its peritracheal tissue bed is pulled down laterally by tweezers behind its turning point (5*) around the subclavian artery (9). This shows that the ramifications of the recurrent laryngeal nerve enter the lateral wall of the esophagus (1) and trachea (2), by alternating, which was typical. The left cricoid gland (6) is in natural position, the right one (6) is displaced toward posterior. Underneath the lower lobe, the thyroid artery and its vessels (6a) encircle the recurrent laryngeal nerves. The turning point of the left recurrent laryngeal nerve (5*) is seen under the aortic arch (10). Esophagus (1), common carotic artery (7), brachiocephalic trunk (8). Note the venous network on top of the pharyngeal muscle (11), the lower esophageal sphincter (12), and the phrenic nerve (13).

Like the parent nerves, the branches were supported by netlike connective tissue surrounding the trachea and the esophagus and was continuous with the posterior mediastinal space. In the six carefully measured specimens, the left RLN had 2 to 7 branches (mean, 5 branches) and the shorter right RLN actually 5 to 11 branches (mean, 9 branches) to the esophagus; and these alternated with 1 to 5 branches (mean, 3 branches) from the left RLN to the trachea, and 3 to 8 branches (mean, 5 branches) from the right RLN. When placed on traction, the branches ranged in length from 2.5 to 1.8 cm for both esophagus and trachea, becoming shorter toward the cranial end (Fig 6).

At extreme lateral stretch, either on the esophagus or the trunk of the RLNs, these branches tore off exactly at the site of the entering in the esophagus muscle or tracheal membrane, respectively.

The cranial 2 to 4 cm of the esophagus and the RLNs were overlain by the thyroid glands. In the area of the lower lobe the thyroid arteries and veins became convoluted and the number, location, size, and length of these vessels varied greatly. In the 23 specimens, for example, there were 20 singular, 17 double, and 8 multiple branches of the thyroid artery and in one case it was even lacking. Both sides were counted.

Before they dipped into the larynx, the RLNs divided to give off the last branch. This branch passed straight upward across the thyroid gland. Three times of the six cases the fascicles appeared to terminate within the parenchyma of the lower lobe of the thyroid gland.

Entry landmark of the RLN into the laryngopharynx, the cricopharyngeal band
Each RLN entered the pharynx just posterior to the inferior cornu of the thyroid cartilage (Figs 5 and 6). At this place the RLNs were firmly attached to the surrounding. An unexpected but common finding was a strong, transverse, 1-cm broad ligament or membrane overlying the cricopharyngeal muscle to which it was more or less firmly attached (Fig 6) by collagen and elastic fiber strands. These mingled with the muscle sheet beneath to form one anatomic unit with the cricopharyngeal muscle, which is the upper esophageal sphincter. It was caudal to its most lateral extremity on either side to the cricoid cartilage that the RLN entered the pharynx (Fig 6).

Branching of the recurrent laryngeal nerve within the pharynx and larynx
In the laryngopharynx the RLNs continued cranially in the dense sparse connective tissue of the groove that is lateral to the posterior cricoarytenoid muscle and between the cricoid and thyroid cartilages (Fig 7 ). They gave off branches to the posterior cricoarytenoid muscle, cricopharyngeal and inferior constrictor muscles, to the mucous membrane, and the flimsy submucosa (Fig 7). Finally, 0.6- to 1.0-mm thick fascicles entered the lateral cricoarytenoid muscle, the transverse and oblique arytenoid muscles, and the thyroarytenoid and aryepiglottic muscles. Therefore, all of the laryngeal muscles except the cricothyroid were innervated by the RLNs.

View larger version (160K): [in this window] [in a new window]   Fig 7. The posterior wall of the pharynx (11) and hypopharynx has been cut open and the pharynx musculature (11) is pulled aside with tweezers to show the lumen. On the right, the mucosa (20) has been partly removed and the terminal recurrent laryngeal nerve (3) is seen passing upward to the epiglottis (14). The recurrent laryngeal nerve branches that supply the laryngeal muscles and the mucosa (20) are exposed. The cricoesophageal membrane (19), which is the tendon of origin of the longitudinal esophageal muscle, is displayed. Inferior thyroid artery (6).

A substantial connection between the SLN and RLN was found in only two of the six specimens, both of them on the left side.

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
The conditions operating on the upper esophagus place the respiratory, swallowing, and speech functions at risk. Temporary nerve paralysis is an unpleasant experience to both patient and surgeon, but permanent bilateral abductor paralysis is a real calamity, a major catastrophe to the individual [10–14].

This study was undertaken to provide a useful guide for surgeons operating on the esophagus and airway, a guide to avoid damage to the recurrent nerves. It represents the effort of surgeon–anatomists to probe the course and terminal points of laryngeal nerves using the tools and techniques of microsurgery. The lessons of these dissections meld with those of several decades of operating and for one of us (CAH) deliberately exposing the recurrent nerve over 600 times without knowingly incurring, save in instances of malignancy-permanent recurrent nerve damage. The results have been based on clinical criteria.

At the level of the aortic arch and above, the recurrent nerves and their branches get in the way of the probing instruments or fingers. Avulsion of the nerves during blunt dissection appears not to play an essential role in RLN damage; experimental traction in our study has demonstrated their disruption only at the weakest point, at the entry into the muscular wall.

When preparing the left RLN one might expect difficulties at the level of its upward turn around the aortic arch because it is embedded in firm connective tissue. A second danger point is the neck area. In the neck where twigs of the RLN are in close proximity to the upper esophagus, where they are interwoven with the vascular system of the thyroid gland in an unpredictable manner, and where great anatomic variations prevail [10–14], logic dictates constructing a cervical anastomosis as low as feasible even in the chest. In addition the cranial course of the right RLN and its distance from the esophageal wall supports constructing the cervical anastomosis as low as feasible. Knowledge of the nerve anatomy is clearly important. Experts know the corridors that the nerves traverse and keep out of trouble by avoiding them [10–14]; even so it may be safer to expose and identify the nerves and keep sharp dissection close to the esophagus where injury to the main trunk is less likely. The RLNs are ordinarily of sufficient caliber to be felt when pushed against the rigid trachea. This palpation under tension maneuver appears to be safe [10] and effectively exposes an additional 2.5 cm of nerve.

Usually, the surgeon approaches the cervical esophagus from its left aspect. The ipsilateral RLN is easy to identify, but the contralateral RLN is out of sight. It is this right RLN that is especially vulnerable to inclusion by the dissector or right angle clamp. One must be certain that the instrument hugs exclusively the muscle. Mass ligation is also risky. The same goes for passing a rubber or plastic traction band around the esophagus as it is routinely done, or placing a self-retaining retractor in a way that puts the ipsilateral RLN on tension. The plate of such a retractor was thought to be responsible for a 38% incidence of nerve palsy in Orringer’s early series of transhiatal esophagectomies [4]. When the search for the RLN is exasperating one has to consider the possibility of an anomalous nonrecurrent nerve. The failure to do so usually results in a traumatic and futile dissection.

Although the branches of the RLNs are commonly more than 1 mm in diameter, we suggest the use of a two to three power optical loupe or a mediastinoscope to uncover the critical nerves. Optical enhancement enables the surgeon to see the nerve striations that distinguish them from blood vessels and connective tissue strands. Mediastinoscopy allows dissection to be kept as close as possible to the esophageal wall and thereby avoid nerve damage. The RLNs are especially vulnerable just below the point where the nerve passes under the inferior constrictor muscles to become intralaryngeal [10]. The inferior horn of the thyroid cartilage is a palpable landmark in operations on the cricopharyngeal muscle or when correcting a Zenker’s diverticulum. It is a less useful reference point when operating from the front. Then the inferior thyroid artery may be exposed and 1 or 2 cm below this vessel the nerve almost always can be identified. Inadvertent partial division of this artery or one of its branches may trap the unwary surgeon into blind or hasty application of a clamp or ligature.

Having entered the larynx, branches of the RLN are directed both to the larynx and pharynx where thin overlaying mucosa and submucosa give poor protection to the RLN from mechanical or chemical trauma. Even with careful insertion of nasogastric or intratracheal tubes, or during endoscopic maneuvers, RLN palsy may occur. The thin connective tissue bed and the apparently strong fixation may render the RLNs in the pharynx more vulnerable to compression, avulsion, and even moderate pull than in the neck or chest. The same is true for the SLN.

A further new finding of this study was the double innervation of the larynx by terminal twigs of both RLNs and SLNs to the aryepiglotticus, lateral cricothyroideus, arytenoideus, and obliquus muscles. The implication of the double innervation of the laryngeal muscles is that it allows variable compensation for a single nerve being damaged. Only the posterior cricoarytenoid muscles appear to be innervated by the RLN alone.

We postulate that up-to-date knowledge of how to expose and protect the recurrent nerves is important for surgeons operating in the neck or upper chest and that understanding the detailed anatomy should diminish the likelihood of RLN injury.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
We thank Professor Dr.med. Laurenz. J. Wurzinger, Anatomisches Institut der TU München, Professor Dr.med. Wolfgang Eisenmenger, chairman of the Institut für Forensische Medizin der LMU München, Germany, and to Professor Dr.med. Michael Mihatsch, chairman of the Institut für Pathologie der Universität Basel, Switzerland for providing the corpses. We also express our gratitude to our photographer, Carmen Borchart, Photodivision, Chirurgische Klinik, Klinikum rechts der Isar, TU München.

	References

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Clement A. Hiebert Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Liebermann-Meffert, D. M.I. Articles by Siewert, J. R. Search for Related Content PubMed PubMed Citation Articles by Liebermann-Meffert, D. M.I. Articles by Siewert, J. R.