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Clinically Oriented Anatomy, Embryology, and Histology

Dorothea Liebermann-Meffert
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Anatomy

Dimensions of Normal Esophagus

The esophagus is the musculomembranous tube that serves as a passage for food between the pharynx and the gastrointestinal tract. It is the narrowest tube of the gastrointestinal tract, spanning the interval between the cricopharyngeal constriction and the most voluminous part of the gut, the stomach. Its length, defined as the distance between the cricoid bone and the gastric orifice, ranges from 24 to 34 cm, with an average of 27.6 cm in adult human cadavers.[1] To discern the precise localization of the cricoid bone, however, is difficult, and clinicians use the incisors as a landmark; this adds up the esophageal lengths to 39 to 48 cm in clinical examinations (Figure 1).[1]

Figure 1 
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Classical division of the esophagus and projection to the related organs. The relationships to the cervical and thoracic vertebrae as radiologic landmarks are indicated on the left of the figure. The distances from the incisors and from the cricoid cartilage to the end of the esophagus are also indicated. The curves of the esophagus (arrows 1, 2, 3) are shown. UES, upper esophageal sphincter; LES, lower esophageal sphincter.

Three minor deviations are present. The first one changes from the median position at the pharyngoesophageal junction (Figures 2 and 3) toward the left at the base of the neck (see Figure 3). The second deviation is at the level of the seventh thoracic vertebra, where the esophagus shifts slightly to the right of the spine. The third and most prominent angulation occurs after traversing the diaphragmatic crura and above the esophagogastric junction, where the terminal esophagus turns to the left (see Figure 1). As a result, the esophagogastric junction takes position lateral to the xiphoid process of the sternum and to the left of the 12th vertebral body. This means the fundus and the proximal stomach lie anterolateral to the spine, with the greater curvature facing the posterior subdiaphragmatic space and the anterior gastric wall facing the left abdominal wall. This topographic relationship is inadequately shown in standard anatomic or surgical textbooks but is well seen on CT in textbooks of radiology.[2] Figures 2 and 3 demonstrate the intimate contact between the wall of the esophagus and the trachea, possessing no limiting tissue.

Figure 2 
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Diagram (caudal view) of the positional anatomy of the esophagus known from computed tomographic representations at the cervical level (top), upper chest (middle), and esophagogastric junction (bottom).
Figure 3 
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Cross section through the esophagus (1), trachea (2), and thyroid gland (3) in a human at a cervical level. Macroscopic (formaldehyde fixed) specimen (left) and histologic (hematoxylin and eosin stained) specimen (right) are viewed from cranial aspects. The positional close contact between the esophagus and trachea and the lack of a distinct structural partition are recognizable. (SPECIMENS COURTESY OF THE AUTHOR.)

At rest, the esophageal tube is collapsed. The configuration is flat in the upper and middle regions and rounded in the lower esophageal portion; mean diameters are 2.5 to 1.6 cm and 2.5 to 2.4 cm, respectively.[1],[3] The esophagus possesses two functional and anatomic narrowings, the one at the entry into the tube and the other at its end. These are called the upper and lower esophageal sphincters (UES and LES).

Surrounding Tissues, Compartments, and Anchors of the Esophagus

The esophagus is wrapped in a thin, continuous adventitial sheath, the fibroareolar lamina, that binds together the muscles, vessels, and bony constituents of the neck and chest. Unlike the digestive tube, however, the esophagus has no mesentery and no serosal coating. Its position within the loose, areolar connective tissue of the mediastinum provides transverse and longitudinal mobility to the esophagus. Respiration may induce movement over a few millimeters, and swallowing may cause movement as much as the height of one vertebral body.[4]

Cranially, the carotid sheath—a portion of the deep cervical fascia—separates to form the pretracheal (previsceral) fascia anteriorly and the prevertebral (retrovisceral) fascia posteriorly. Slit-shaped spaces between the layers of these fasciae form communicating compartments between the neck and chest (Warwick and Williams, 1978).[5] The pretracheal space surrounds the vascular structures of the anterior mediastinum but is limited distally by the fibrous tissue of the pericardium. The prevertebral space may extend from the base of the skull down to the diaphragm but is frequently obliterated below the level of the tracheal bifurcation.

Which Structures Stabilize the Esophagus?

Insignificant tiny membranes of different extension attach the cranial half of the muscular esophagus to the trachea (Figure 4 and 5), the pleura, and the retroperitoneum. The membranes contain elastic and/or collagen fibers (see Figure 4) and occasional, small smooth muscle bundles or striated muscle fibers.[3],[6] The bundles run toward the posterior end in the retrovisceral fascia or blindly within the connective tissue network of the mediastinum. The membranes are all delicate, ranging from 30 to 1000 μm in thickness and 0.5 to 3 cm in craniocaudal length.[6] They are definitely much smaller than the coarse “bronchoesophageal” or “pleuroesophageal” muscle cords depicted by Netter.[7] They, however, can be viewed during mediastinoscopic dissection when the esophagus is exposed from the neck.

Figure 4 
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Histologic cross section through one of the membranes (1) that connect the human esophagus (2) and the trachea (3), viewed from cranial aspect. The finger-shaped insertion of the membrane into the esophageal muscle can be seen. (SPECIMEN COURTESY OF THE AUTHOR.)
Figure 5 
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Diagram of the anchoring structures of the esophagus viewed from the left. The inferior laryngeal constrictor muscles (1) that insert on the sphenoid bone and the longitudinal muscle of the esophagus that inserts lateral on the cricoid cartilage through the cricopharyngeal tendon (2) are shown. Bundles of elastic, collagen, and muscle fibers connect the esophageal wall with the trachea (3), pleura, and retrovisceral fascia (4). The attachment by the phrenoesophageal membrane (5) is rather mobile, whereas the posterior gastric ligaments (8) and the lesser omentum (6) yield a tight adherence. LES, lower esophageal sphincter; UES, upper esophageal sphincter.

Elastically attached by the phrenoesophageal membrane (PEM), the distal esophagus traverses the diaphragm through the esophageal hiatus (see Figure 5). At the central margin of the diaphragm, the subdiaphragmatic and the endothoracic aponeuroses blend into the PEM (Figure 6). This structure can be recognized by its well-defined lower edge and the slightly yellow color of the enclosed fat pad (see Figure 6).

Figure 6 
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The phrenoesophageal membrane (PEM) of a human autopsy specimen viewed in situ from the anterolateral aspect. This structure also became known as Laimer’s or Allison’s membrane. As shown in the photograph, the lower sheath of the membrane is inserted onto the gastric fundus (3). At the top the diaphragm is held up with a forceps. Diaphragmatic decussating fibers (1) and a submembranous pad of adipose tissue (2) are seen. The diagram shows how the PEM wraps the esophagogastric junction with a wide membranous collar (dotted lines). (FROM DURANCEAU A, LIEBERMANN-MEFFERT D: EMBRYOLOGY, ANATOMY, AND PHYSIOLOGY OF THE ESOPHAGUS. IN ORRINGER MB, ZUIDEMA GD [EDS]: SHACKELFORD’S SURGERY OF THE ALIMENTARY TRACT, VOL 1. THE ESOPHAGUS, 3RD ED. PHILADELPHIA, WB SAUNDERS, 1991, P 3.)

The PEM splits into two sheaths. One sheath extends craniad for 2 to 4 cm through the hiatus, where its fibers penetrate the esophageal musculature to insert on the submucosa. The second sheath passes down across the cardia and is separated from the muscular wall of the gastroesophageal junction by areolar connective or fat tissue.[6] At the level of the gastric fundus, the fibers of the PEM blend into the serosa and the gastric musculature (see Figure 6), the gastrohepatic ligament, and the dorsal gastric mesentery (see Figures 5 and 6). The PEM wraps the gastroesophageal junction completely like a loose collar. This guarantees sufficient plasticity for the LES to move in relation to the diaphragm. Stability is provided by the inelastic gastric ligaments that attach the cardia and the posterior fundus wall to the upper retroperitoneal fasciae.

Comments on Surgical Relevance and Consequences

The basis for stripping the esophagus is the mobile localization of the esophagus within the mediastinum: the mobility, which is due to the nonexistence of coarse esophagus attaching or supplying fiber structures, is the reason why we can subject the esophagus to a blunt pull-through from the mediastinum, provided that there are no contraindications such as periesophageal tumor invasion.[1],[8]

When the esophagus must be resected, stomach or bowel is used as conduit. The shortest distance between the cricoid cartilage and the celiac axis required for esophageal replacement was found to be the orthotopic route in the posterior mediastinum (= 30 cm). The retrosternal (= 32 cm) and subcutaneous routes (= 34 cm) proved to be longer.[9],[10] This should allow tension-free construction of a gastroesophageal anastomosis in the neck. Although the whole stomach can serve as conduit to replace the esophagus, it is advisable to use a nonreversed gastric tube ( tubularized gastric conduit) so that the blood circulation of the gastric substitute will not be compromised.[9],[11],[12]

Inelastic collagenous fiber elements replace the elastic fibers of the PEM with advancing age.[13] This loss of elasticity of the PEM in conjunction with a wide hiatus results in herniation, that is, displacement of the gastroesophageal junction and cardia into the thoracic cavity. Eliska suggested that abnormal anchorage of the PEM in youth and pathologic accumulation of adipose tissue in the connective tissue space between the PEM and the cardia musculature may also contribute to the development of a hiatal hernia.[13]

Mittal[14] has attributed sphincter function to the diaphragm and the PEM and its insertions. I could not confirm this claim after creating hernias in cats using long-term experiments.[15] Dissection of the diaphragmatic membranes and ligaments and positioning of the cardia within the chest by suturing the diaphragm to the middle of the stomach had no long-term effect on either the pressure values or the characteristics of the LES.[15]

A second peculiarity is the localization of the esophagus within fascial compartments. This feature allows infections to spread from anterior esophageal lesions of the esophagus through the pretracheal space to the pericardium.

The cervical region is vulnerable because of the proximity between the esophagus and the trachea (see Figure 3). Special care must be taken not to injure the trachea when developing the plane of dissection between the esophagus and the trachea. The lack of an esophagotracheal partition also paves the way for fistula formation,[3] for example, a tracheoesophageal fistula secondary to chemotherapy[16] and irradiation. This invariably leads to empyema and often death.

The retrovisceral space, however, is clinically more important. For example, oropharyngeal infections can easily descend through spaces within the different sheaths of the deep cervical fascia. Necrotizing mediastinitis resulting from peritonsillar or dental abscesses or even wisdom tooth extraction has been reported and may involve a mortality rate of nearly 40%.[17],[18] Most instrumental perforations occur in the posterior hypopharynx above the narrowing of the cricopharyngeal sphincter, below which there is no barrier to the spread of infection into the mediastinum. Noninstrumental or spontaneous perforation (Boerhaave’s syndrome) and leakage from an esophageal anastomosis behave in a similar way with rapid and disastrous dissemination of sepsis.

Vascular Structures and Nerves Supplying the Esophagus

Arterial Supply

The history of the arterial supply of the esophagus has been quoted extensively by Siewert and Liebermann-Meffert.[19] This publication gives a good review and its reading is recommended. The following description is based on new studies of my group[1],[11],[19] that we performed to answer special questions in regard to foregut surgery.

Cervical Esophagus

Branches deriving from the right and left superior and inferior thyroid arteries supply the wall of the pharynx, esophagus, and trachea (Figure 7). Compared with the thyroid arteries the vessels to the esophagus are small.[1],[19] Their equal distribution contrasts to Shapiro and Robillard’s claim in 1950 that a greater number of vessels supply predominantly the right side of the esophagus.[20]

Figure 7 
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Vascular corrosion casts of the arteries of the neck and mouth viewed from the anterior position. Top, Aorta (1), the common carotid artery (2), a network of the thyroid arteries (3), esophageal arteries (4), the left superior thyroid artery (5), and the arteries of the tongue (6). Note that there is not any vascular anastomosis between both sides of the tongue. Bottom, Vascular casts of the aortic arch (1), a bunch of bronchoesophageal arteries (2), and a network of esophageal vessels (3). The stump seen at the lateral aorta had supplied the thoracic wall. (SPECIMENS COURTESY OF THE AUTHOR.)

Thoracic Esophagus

Down to the level of the tracheal bifurcation, the upper thoracic esophagus receives branches from the thyroid arteries, but the majority of the supplying vessels to the esophagus and tracheal bifurcation are derived from the bunch of arteries arising at the inflection of the aorta.[1],[20] More caudally, most often only one singular artery arises from the anterior aspect of the aorta. Although this vessel clearly supplies the distal part of the trachea and the stem bronchi, small branches also form the esophageal vascularization, as seen in Figures 7-8. In general, these vessels are straight and short, connecting tightly the aorta, the trachea, and the esophagus.[1] At variable localization, one other unpaired artery may arise from the anterior aortic aspect. This vessel, however, courses obliquely down from its origin (Figure 9) to divide—still within the mediastinum—into an ascending and a descending branch.[1],[19]

Figure 8 
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Arterial corrosion cast of thoracoabdominal organs—aorta, esophagus, and stomach—viewed from the anterior aspect. The bronchial artery is shown deriving from the aorta and giving off several smaller branches that form the minute esophageal network. The stump left of the aorta is the residual of the rami intercostalis. (BERACRYL INJECTION INTO THE AORTA BY THE AUTHOR.)

Abdominal Esophagus

The distal esophagus and the gastric cardia are nourished by up to 11 small arteries that originate at intervals from the left gastric artery.[1],[19] These vessels travel straight upward alongside the anterior aspect of the cardia (see Figure 9) and follow the wall through the diaphragm in the longitudinal esophageal axis to subdivide into periesophageal tributaries before they dip into the muscular layers. The posterior wall of the terminal esophagus receives several large vessels derived from the splenic artery and/or from vessels of the dorsal fundus, but previous claims that nutritional vessels arise from phrenic arteries have not been substantiated.[1]

Figure 9 
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Diagram of the most common vascular pattern of blood supply to the esophagus and cardia in the human adult. 1, aorta; 2, esophagus.

Concerning the vascularization as a whole, the esophagus is an organ of shared vasculature with poor “proper” extrinsic support. In fact, apart from the few “vasa propria” that derive from the aorta directly, the esophagus receives its blood via vessels feeding mainly other organs, such as the thyroid gland, trachea, and stomach. Even though the vessels are minute within the periesophageal tissue, previous claims of a poor or missing vascularization in the wall of the midesophagus could not be substantiated because connections within and throughout the submucosa and mucosa form a complete and vast intramural network of fine vessels (Figure 10).[1],[19] And nowhere is the wall of the esophagus avascular.

Figure 10 
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Sample of the submucosal microvascular esophageal blood supply displayed in a scanning electron micrograph. The arteries and veins are small and form a minute polygonal network. (RESIN-INJECTED SPECIMEN BY THE AUTHOR.)

Comments on Surgical Relevance and Consequences

The correctly mobilized esophagus retains an excellent blood supply over a long distance. The vascularization is seldom responsible for a failed anastomosis.[21] This circulation is evidently due to the rich and complete network of vessels within the wall.

Blunt pull-through esophagectomy without thoracotomy for esophageal cancer is relatively safe and causes a minimum of blood loss.[1],[22],[23] When hemorrhage has occurred after stripping of the esophagus, it was from the site of tumor adhesions rather than from the periesophageal vessels.[24] A usually limited bleeding may occur because the major supporting arteries divide into minute branches at some distance from the esophageal wall, and, when torn, benefit from contractile hemostasis.[1]

Venous Drainage

Intraesophageal (Intrinsic) Veins

The intraesophageal veins include the subepithelial plexus, which is located in the lamina propria of the tunica mucosa.[25] The veins are arranged mainly in the longitudinal axis of the esophagus and extend through the whole length of the esophageal submucosa.[26]

The subepithelial plexus receives blood from the adjacent capillaries and drains into the submucous plexus. At the lower end of the esophagus, the systemic and the portal system obviously anastomose; in case of portal venous obstruction the thin-walled superficial veins presumably enlarge to form varices. Vianna and colleagues[26] described a specialized longitudinal venous arrangement prevalent in the lower third of the esophagus and in the cardia. This structure consists of perforating veins deriving from the small communicating veins of the submucous plexus that pierce the muscular wall of the esophagus. The intramural veins receive tributaries from the muscle coats and form the veins on the surface of the esophagus.

Extraesophageal (Extrinsic) Veins

The extraesophageal veins drain into locally corresponding large vessels. These are the inferior thyroid veins, which empty into the brachiocephalic veins, the azygos and hemiazygos veins, the left gastric vein, and the splenic vein.

Comments on Surgical Relevance and Consequences

The azygos vein, because of its vicinity to the root of the lung and its lymph nodes, is one of the initial structures affected by the extramural spread of tumors of the midesophagus. In this situation, the azygos vein can be easily damaged during esophageal resection. In particular during blunt pull-through dissection, this vein represents a high risk factor causing fatal bleeding if the tumor is adherent to the venous wall. Collateral circulation may exist between the azygos vein and the hemiazygos vein. The hemiazygos vein, if not ligated, can be a source of severe hemorrhage when resecting the esophagus through a right thoracotomy.[27]

Lymphatic Pathways

Lymphatic drainage comprises two systems: lymph channels and lymph nodes. The details of these systems, in particular the initial pathways, have recently received special attention because of the lymphatic spread of malignant tumors. Lymph capillaries commence in tissue spaces (Figure 11) as a network of endothelial channels or as blind endothelial sacculations (Partsch, 1988).[28]

Figure 11 
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Diagram showing the initial lymphatic network, which is reconstructed from mesentery preparations. The color red indicates the lymphatic channel. Most probably, this pattern equals that of the esophagus. (MODIFIED FROM ZWEIFACH BW, PRATHER JW: MANIPULATION OF PRESSURE IN TERMINAL LYMPHATICS IN THE MESENTERY. AM J PHYSIOL 228:1326, 1975.)

Intraesophageal (Intrinsic) Lymphatics

Because of the considerable technical difficulties to identify by injection or anatomic preparation these slender, normally collapsed structures,[29],[30] the anatomic knowledge of the esophageal initial lymphatics in healthy individuals is still sparse. Some investigators such as Idanov, in 1959,[31] or Rouvière, in 1932,[32]emphasized the existence of a rich lymphatic network in the lamina mucosa and tela submucosa of the esophagus. Their claims have never been substantiated by convincing or reproducible documentation. According to recent studies one may assume that tiny precapillary spaces also exist in all the levels of the esophageal lamina mucosa, similar to descriptions of interstitial tissues; other authors have stressed the almost complete absence of true anatomic lymph capillaries in the upper and middle levels of the lamina mucosa of the human stomach[29] and esophagus.[30] Transmission electron microscopic studies have shown anastomosing lymph capillaries only in the lower mucosal levels and small valve-containing vessels in the tela submucosa of the esophagus. These appeared to form long channels that parallel the organ axis.

Extraesophageal (Extrinsic) Lymphatics

The submucosal lymph channels give off occasional branches to the collecting subadventitial and surface trunks.

Thoracic Duct

The principal lymphatic vessel of the body is the thoracic duct (Figure 12). It begins with the cisterna chyli at level L1-2, emerges through the aortic hiatus of the diaphragm, and travels in more than half of cases as a single trunk craniad with the aorta on its left and the azygos vein on its right. Then the duct turns at the level of T5-6 behind the left mainstem bronchus toward the left and ascends lateroposteriorly to the trachea and esophagus to end at the angle between the left subclavian and jugular veins by draining the lymph into the bloodstream. Anatomic variations are manifold.[31] The close local relationship of the flimsy duct to the esophagus explains its occasional damage during esophageal resection and chylothorax.

Figure 12 
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Diagram of the lymphatic pathways and lymph node distribution. During human organogenesis, the lymphatic pathways develop from two different sources, the branchiogenic mesenchyme and the body mesenchyme. As a result, lymph drains toward two different directions (arrows) with a zone of bidirectional flow at the tracheal bifurcation. This feature is consistent with clinical observations. The knowledge of lymph flow and the corresponding lymph node distribution is essential in understanding potential spread of malignancy.

Normally the thoracic duct is collapsed and then appears, like a string of beads, at preparation, because of numerous strong valves. The thoracic duct is 0.5 to 2.0 mm wide (mean, 1.3 mm) at the distal third, 1.0 to 3.0 mm (mean, 1.7 mm) at the middle, and 1.0 to 4.0 mm (mean, 2.3 mm) at the proximal third (threshold, 4.0 mm) as has been shown in 500 lymphograms of healthy individuals by Wirth and Frommhold.[33]

Lymph Nodes of the Esophagus

In noncancer autopsy specimens, we found most of the lymph nodes of the thoracic mediastinum piled up around the tracheal bifurcation (see Figure 12). These were rather large, dark nodes. Anatomically, it was impossible to determine whether they drain the esophagus or the lungs or whether they transport proximally or distally. There is an accumulation of small nodes in the neck and cardia region, but few lymph nodes are normally present in the lateral and ventral mediastinum of the upper third and in the dorsal mediastinum in the lower third of the thorax in healthy individuals. We could not identify the classic chain of lymph nodes along and around the esophagus, as described in textbooks and seen in Netter’s[7] illustration at routine autopsy. This statement is in accordance with that of Wirth and Frommhold,[33] who identified mediastinal lymph nodes in only 5% of 500 normal lymphograms. We found, instead, a greater number of lymph nodes of macroscopic dimensions cranial to the tracheal bifurcation within the tracheoesophageal groove. Considering tumor involvement, the classic lymph node arrangement was elegantly illustrated by Matsubara in 1988.[34]

Comments on Surgical Relevance and Consequences

The initial (terminal) lymphatics (see Figure 12) take up fluid, colloid material from the tissue, cell debris, microorganisms, and eventually tumor cells.[35] The contents are emptied into collecting lymph channels. Paired semilunar valves within the channels determine the direction of flow. They join to form small trunks that convey the fluid and the other absorbed material through the interpositioned lymph nodes. In its passage through the node, noxious material may be filtered off. It is evident that this system of channels provides easy pathways for tumor spread.

Lehnert’s concept that the lymphatics form long channels within the submucosa in which the lymph flows more easily cranially or caudally than through the few channels that pierce the muscular coat supports the clinical observation that the initial submucosal cancer spread follows the longitudinal axis of the organ.[29] Consequently, primary esophageal tumors may extend over a long distance within the esophageal wall before obstructing the lumen.

The absence of lymphatics from the superficial part of the mucosa and the widely anastomosing plexus within the deep layer of the mucosa and the submucosa may explain why the intramural spread of cancer occurs predominantly in the submucosa. Free tumor cells may follow the lymphatic channels over a considerably long distance before passing through the muscular coat into regional lymph nodes.

From the anatomic studies, and the clinical observations, it may be deduced[3],[22],[24],[29],[34],[35] that lymph from areas above the tracheal bifurcation drains mostly craniad toward the thoracic duct whereas lymph from below the carina flows mainly toward the lower mediastinal, left gastric, and celiac lymph nodes. Flow in the area of the tracheal bifurcation normally seems to be bidirectional (see Figure 12), owing to the embryologic development of the two mesenchymal sources.[3],[36],[37] Flow may change under pathologic conditions (tumor invasion). When the lymph vessels become blocked and markedly dilated, either the valves may become incompetent and the flow reversed or a collateral lymphatic circulation may develop; retrograde spread in some malignant tumors may thus be explained. Unfortunately, this possibility also limits the value of establishing normal flow pathways.

Innervation

The vegetative (autonomous) nervous system regulates the function of the esophagus. It is subdivided into two parts, the sympathetic and the parasympathetic nervous system. The nerve fascicles may carry parasympathetic and sympathetic components that exert antagonistic influences on the esophagus and control the striated and smooth muscle, glands, and blood vessels.[38],[39]

Sympathetic Nervous System

The sympathetic innervation comes from the cervical and the thoracic sympathetic chain (see Figure 13). The sympathetic pathways are concerned with the movement of the esophageal tract, contraction of the sphincters, relaxation of the muscular wall, increase in glandular and peristaltic activity, and vasoconstriction.

Figure 13
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Diagram of the topographic relationships between the esophagus and its innervation. This shows the situation from the anterior aspect. The dimensions are out of scale.

The sympathetic trunks are two ganglionated nerve cords that extend from the base of the skull down to the sacrum. They are located lateral to the spine (see Figure 13) and possess 11 to 12 thoracic paravertebral ganglia on each side. The sympathetic innervation of the proximal esophagus is derived from the cervical and upper thoracic ganglia.[38] Besides the direct approach to the organ, the fibers form a profuse, delicate network between and around the esophagus.[38]

Parasympathetic Nervous System

The parasympathetic innervation comes from the vagus nerve (see Figure 13). The esophageal branches of the vagus nerve provide motor innervation to the muscular coats and secretomotor innervation to the glands. The vagus nerve is the paired 10th cranial nerve. Its motor fibers arise in the dorsal vagal nucleus, and its sensory fibers derive from the superior and inferior ganglion of the vagus nerve in the neck. The nerve fibers that innervate the upper part of the esophagus and pharyngoesophageal “striped” musculature arise in the nucleus ambiguus.[38] Unlike those of the “smooth” muscles, which receive motor input via preganglionic autonomic fibers and synapse on neurons of the myenteric ganglia, the nerve endings of the striped muscle make direct synaptic contacts through motor end plates.[40]From their origin in the medulla, the vagus nerves descend as a paired trunk and pass through the corresponding jugular foramen. The branches are shown on Figure 13.

CERVICAL ESOPHAGUS. By giving off branches to the pharynx, larynx, and trachea (Figures 14 and 15; see also Figure 13), these fibers form the cervical plexus that also innervates the proximal esophagus.[40] The bilateral superior laryngeal nerves (SLNs) originate from the vagal trunks of the respective side, that is, from the ganglion nodosum (see Figure 13). Both nerves descend alongside the carotid arteries before dividing into branches that enter the pharynx to innervate the muscles of the pharynx, hypopharynx, and larynx.[41],[42]

Figure 14
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Vagal innervation of the upper esophagus by the inferior (recurrent) laryngeal nerve. Posterior aspect of the muscular wall of the esophagus (1) and pharynx (2) is shown. The left (7) and the right recurrent laryngeal nerves are exposed. Laterally on both sides the turning points around the arch of the aorta (6) and the subclavian artery (5) are displayed. The ramifications of the recurrent laryngeal nerves alternatively enter the lateral wall of the esophagus (1) and trachea. The thyroid gland (3) and the common carotid artery (4) are shown. (FROM LIEBERMANN-MEFFERT D, ET AL: RECURRENT AND SUPERIOR LARYNGEAL NERVES: A NEW LOOK WITH IMPLICATIONS FOR THE ESOPHAGEAL SURGEON. ANN THORAC SURG 67:212, 1999. COPYRIGHT 1999, WITH PERMISSION FROM THE SOCIETY OF THORACIC SURGEONS.)
Figure 15
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Vagal innervation of the upper half of the esophagus. The specimen obtained from autopsy shows the neck area from the posterior aspect. The meandering left inferior (recurrent) laryngeal nerve (1) wriggles, being loosely adherent to the periesophageal connective tissue from the aorta (2), cranially to dip under the lower lobe of the thyroid gland (4). It will endure some stretching. Common carotid artery (3). (FROM LIEBERMANN-MEFFERT D, ET AL: RECURRENT AND SUPERIOR LARYNGEAL NERVES: A NEW LOOK WITH IMPLICATIONS FOR THE ESOPHAGEAL SURGEON. ANN THORAC SURG 67:212, 1999. COPYRIGHT 1999, WITH PERMISSION FROM THE SOCIETY OF THORACIC SURGEONS.)

Of the inferior (recurrent) laryngeal nerves (RLNs), the right one arises from the vagus nerve in front of the subclavian artery and turns posteriorly around the artery (see Figures 13 and 14) before ascending obliquely to the right lateral aspect of the trachea behind the common carotid artery. The left RLN originates from the vagus nerve in front of the aortic arch, surrounds the aorta posteriorly, and ascends, maintaining a meandering course (see Figure 16). Both the RLNs approach the esophagus during their lateral ascent and give off an equal number of nerve branches (6 to 12) to the esophagus as well as to the trachea (see Figure 14). When approaching the pharyngoesophageal junction (see Figure 14), both the right and the left RLNs have obtained an intimate proximity with the wall of the esophagus and trachea.[41],[42] This proximity is particularly pronounced when the proximal RLNs become positioned underneath the medial plane of the thyroid glands. There they entangle the thyroid vessels before they enter the larynx from lateral and caudal to the cricopharyngeal muscle band.[41]

Figure 16
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Vagal innervation of the midesophagus (1) shown from an anterior aspect. The specimen obtained from autopsy displays elegantly the loosely adherent vagal network of the midesophagus, when pulled up by the forceps (3). Caudad to the tracheal bifurcation (2) large dark lymph nodes are a frequent finding. (SPECIMEN COURTESY OF THE AUTHOR.)

The terminal branches of the RLNs are most often 1.0 to 1.5 mm thick and divide into several branches to innervate all the laryngeal muscles, including the vocal and epiglottic muscles.[41],[42],[43] The observation of a nonrecurrent laryngeal nerve is an unfrequent event.[44] The situation is almost never found on the right side (31 [0.1%] of 6000 cases of thyroid surgery done by Toniato and associates[44] and none on the left). This corresponds to the data presented by Hiebert and colleagues.[43]

THORACIC ESOPHAGUS. At the level of the tracheal bifurcation, the ongoing main vagal trunks pass posterior to the roots of the lung and divide into multiple small branches to form pulmonary and esophageal plexuses. Caudal to the tracheal bifurcation, the esophageal vagal trunks break up into a network of fascicles (Figure 15). The left vagus builds up mainly the anterior plexus, and the right vagus, the posterior plexus. At a variable distance from the cardia, the fibers of both the anterior plexus and the posterior plexus reorganize into two thick trunks that travel down on the anterior and posterior esophageal wall (Figure 16). Both vagal trunks may now contain fibers from the upper contralateral side.

ABDOMINAL ESOPHAGUS AND STOMACH. Together with the esophagus, the vagus nerves pass through the diaphragmatic hiatus, where they are barely distinguishable under the phrenoesophageal membrane. The posterior vagus nerve often divides into smaller branches that lie 2 to 4 cm distant from the end of the esophagus and to its right. The anterior vagus nerve runs at the left side to the anterosuperior surface of the stomach.

Intramural Innervation

Branches from the periesophageal, parasympathetic, and sympathetic plexus enter the wall of the esophagus together with the blood vessels. They form the intrinsic innervation, which is composed of fine nerve fibers and numerous groups of ganglia. The ganglia lie either between the longitudinal and the circular layers of the tunica muscularis, in which case they are called myenteric or Auerbach’s plexus, or in the tela submucosa, in which case they are called the submucous or Meissner plexus. The one regulates the contraction of the muscle coats; the other regulates the peristalsis of the muscularis mucosae and the secretion. Both are interconnected by a meshwork of fibers.[45] The number of ganglia is fairly uniform within the esophageal wall.[46] Near the junctional zone, however, the nerve fascicles become thicker and ganglia accumulate.[45]

Comments on Surgical Relevance and Consequences

During esophageal resection and goiter operations, the RLNs are at high risk. Injuries involving the SLNs and RLNs cause clinical pictures of a variety of transient or even lasting motor and sensory disorders of the pharyngolaryngoesophageal junction area. These may be hoarseness related to vocal cord palsy and respiration and swallowing failure associated with problems of aspiration and dysphagia.[41],[43]

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Anatomy

Dimensions of Normal Esophagus

The esophagus is the musculomembranous tube that serves as a passage for food between the pharynx and the gastrointestinal tract. It is the narrowest tube of the gastrointestinal tract, spanning the interval between the cricopharyngeal constriction and the most voluminous part of the gut, the stomach. Its length, defined as the distance between the cricoid bone and the gastric orifice, ranges from 24 to 34 cm, with an average of 27.6 cm in adult human cadavers.[1] To discern the precise localization of the cricoid bone, however, is difficult, and clinicians use the incisors as a landmark; this adds up the esophageal lengths to 39 to 48 cm in clinical examinations (Figure 1).[1]

Figure 1 
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Classical division of the esophagus and projection to the related organs. The relationships to the cervical and thoracic vertebrae as radiologic landmarks are indicated on the left of the figure. The distances from the incisors and from the cricoid cartilage to the end of the esophagus are also indicated. The curves of the esophagus (arrows 1, 2, 3) are shown. UES, upper esophageal sphincter; LES, lower esophageal sphincter.

Three minor deviations are present. The first one changes from the median position at the pharyngoesophageal junction (Figures 2 and 3) toward the left at the base of the neck (see Figure 3). The second deviation is at the level of the seventh thoracic vertebra, where the esophagus shifts slightly to the right of the spine. The third and most prominent angulation occurs after traversing the diaphragmatic crura and above the esophagogastric junction, where the terminal esophagus turns to the left (see Figure 1). As a result, the esophagogastric junction takes position lateral to the xiphoid process of the sternum and to the left of the 12th vertebral body. This means the fundus and the proximal stomach lie anterolateral to the spine, with the greater curvature facing the posterior subdiaphragmatic space and the anterior gastric wall facing the left abdominal wall. This topographic relationship is inadequately shown in standard anatomic or surgical textbooks but is well seen on CT in textbooks of radiology.[2] Figures 2 and 3 demonstrate the intimate contact between the wall of the esophagus and the trachea, possessing no limiting tissue.

Figure 2 
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Diagram (caudal view) of the positional anatomy of the esophagus known from computed tomographic representations at the cervical level (top), upper chest (middle), and esophagogastric junction (bottom).
Figure 3 
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Cross section through the esophagus (1), trachea (2), and thyroid gland (3) in a human at a cervical level. Macroscopic (formaldehyde fixed) specimen (left) and histologic (hematoxylin and eosin stained) specimen (right) are viewed from cranial aspects. The positional close contact between the esophagus and trachea and the lack of a distinct structural partition are recognizable. (SPECIMENS COURTESY OF THE AUTHOR.)

At rest, the esophageal tube is collapsed. The configuration is flat in the upper and middle regions and rounded in the lower esophageal portion; mean diameters are 2.5 to 1.6 cm and 2.5 to 2.4 cm, respectively.[1],[3] The esophagus possesses two functional and anatomic narrowings, the one at the entry into the tube and the other at its end. These are called the upper and lower esophageal sphincters (UES and LES).

Surrounding Tissues, Compartments, and Anchors of the Esophagus

The esophagus is wrapped in a thin, continuous adventitial sheath, the fibroareolar lamina, that binds together the muscles, vessels, and bony constituents of the neck and chest. Unlike the digestive tube, however, the esophagus has no mesentery and no serosal coating. Its position within the loose, areolar connective tissue of the mediastinum provides transverse and longitudinal mobility to the esophagus. Respiration may induce movement over a few millimeters, and swallowing may cause movement as much as the height of one vertebral body.[4]

Cranially, the carotid sheath—a portion of the deep cervical fascia—separates to form the pretracheal (previsceral) fascia anteriorly and the prevertebral (retrovisceral) fascia posteriorly. Slit-shaped spaces between the layers of these fasciae form communicating compartments between the neck and chest (Warwick and Williams, 1978).[5] The pretracheal space surrounds the vascular structures of the anterior mediastinum but is limited distally by the fibrous tissue of the pericardium. The prevertebral space may extend from the base of the skull down to the diaphragm but is frequently obliterated below the level of the tracheal bifurcation.

Which Structures Stabilize the Esophagus?

Insignificant tiny membranes of different extension attach the cranial half of the muscular esophagus to the trachea (Figure 4 and 5), the pleura, and the retroperitoneum. The membranes contain elastic and/or collagen fibers (see Figure 4) and occasional, small smooth muscle bundles or striated muscle fibers.[3],[6] The bundles run toward the posterior end in the retrovisceral fascia or blindly within the connective tissue network of the mediastinum. The membranes are all delicate, ranging from 30 to 1000 μm in thickness and 0.5 to 3 cm in craniocaudal length.[6] They are definitely much smaller than the coarse “bronchoesophageal” or “pleuroesophageal” muscle cords depicted by Netter.[7] They, however, can be viewed during mediastinoscopic dissection when the esophagus is exposed from the neck.

Figure 4 
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Histologic cross section through one of the membranes (1) that connect the human esophagus (2) and the trachea (3), viewed from cranial aspect. The finger-shaped insertion of the membrane into the esophageal muscle can be seen. (SPECIMEN COURTESY OF THE AUTHOR.)
Figure 5 
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Diagram of the anchoring structures of the esophagus viewed from the left. The inferior laryngeal constrictor muscles (1) that insert on the sphenoid bone and the longitudinal muscle of the esophagus that inserts lateral on the cricoid cartilage through the cricopharyngeal tendon (2) are shown. Bundles of elastic, collagen, and muscle fibers connect the esophageal wall with the trachea (3), pleura, and retrovisceral fascia (4). The attachment by the phrenoesophageal membrane (5) is rather mobile, whereas the posterior gastric ligaments (8) and the lesser omentum (6) yield a tight adherence. LES, lower esophageal sphincter; UES, upper esophageal sphincter.

Elastically attached by the phrenoesophageal membrane (PEM), the distal esophagus traverses the diaphragm through the esophageal hiatus (see Figure 5). At the central margin of the diaphragm, the subdiaphragmatic and the endothoracic aponeuroses blend into the PEM (Figure 6). This structure can be recognized by its well-defined lower edge and the slightly yellow color of the enclosed fat pad (see Figure 6).

Figure 6 
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The phrenoesophageal membrane (PEM) of a human autopsy specimen viewed in situ from the anterolateral aspect. This structure also became known as Laimer’s or Allison’s membrane. As shown in the photograph, the lower sheath of the membrane is inserted onto the gastric fundus (3). At the top the diaphragm is held up with a forceps. Diaphragmatic decussating fibers (1) and a submembranous pad of adipose tissue (2) are seen. The diagram shows how the PEM wraps the esophagogastric junction with a wide membranous collar (dotted lines). (FROM DURANCEAU A, LIEBERMANN-MEFFERT D: EMBRYOLOGY, ANATOMY, AND PHYSIOLOGY OF THE ESOPHAGUS. IN ORRINGER MB, ZUIDEMA GD [EDS]: SHACKELFORD’S SURGERY OF THE ALIMENTARY TRACT, VOL 1. THE ESOPHAGUS, 3RD ED. PHILADELPHIA, WB SAUNDERS, 1991, P 3.)

The PEM splits into two sheaths. One sheath extends craniad for 2 to 4 cm through the hiatus, where its fibers penetrate the esophageal musculature to insert on the submucosa. The second sheath passes down across the cardia and is separated from the muscular wall of the gastroesophageal junction by areolar connective or fat tissue.[6] At the level of the gastric fundus, the fibers of the PEM blend into the serosa and the gastric musculature (see Figure 6), the gastrohepatic ligament, and the dorsal gastric mesentery (see Figures 5 and 6). The PEM wraps the gastroesophageal junction completely like a loose collar. This guarantees sufficient plasticity for the LES to move in relation to the diaphragm. Stability is provided by the inelastic gastric ligaments that attach the cardia and the posterior fundus wall to the upper retroperitoneal fasciae.

Comments on Surgical Relevance and Consequences

The basis for stripping the esophagus is the mobile localization of the esophagus within the mediastinum: the mobility, which is due to the nonexistence of coarse esophagus attaching or supplying fiber structures, is the reason why we can subject the esophagus to a blunt pull-through from the mediastinum, provided that there are no contraindications such as periesophageal tumor invasion.[1],[8]

When the esophagus must be resected, stomach or bowel is used as conduit. The shortest distance between the cricoid cartilage and the celiac axis required for esophageal replacement was found to be the orthotopic route in the posterior mediastinum (= 30 cm). The retrosternal (= 32 cm) and subcutaneous routes (= 34 cm) proved to be longer.[9],[10] This should allow tension-free construction of a gastroesophageal anastomosis in the neck. Although the whole stomach can serve as conduit to replace the esophagus, it is advisable to use a nonreversed gastric tube ( tubularized gastric conduit) so that the blood circulation of the gastric substitute will not be compromised.[9],[11],[12]

Inelastic collagenous fiber elements replace the elastic fibers of the PEM with advancing age.[13] This loss of elasticity of the PEM in conjunction with a wide hiatus results in herniation, that is, displacement of the gastroesophageal junction and cardia into the thoracic cavity. Eliska suggested that abnormal anchorage of the PEM in youth and pathologic accumulation of adipose tissue in the connective tissue space between the PEM and the cardia musculature may also contribute to the development of a hiatal hernia.[13]

Mittal[14] has attributed sphincter function to the diaphragm and the PEM and its insertions. I could not confirm this claim after creating hernias in cats using long-term experiments.[15] Dissection of the diaphragmatic membranes and ligaments and positioning of the cardia within the chest by suturing the diaphragm to the middle of the stomach had no long-term effect on either the pressure values or the characteristics of the LES.[15]

A second peculiarity is the localization of the esophagus within fascial compartments. This feature allows infections to spread from anterior esophageal lesions of the esophagus through the pretracheal space to the pericardium.

The cervical region is vulnerable because of the proximity between the esophagus and the trachea (see Figure 3). Special care must be taken not to injure the trachea when developing the plane of dissection between the esophagus and the trachea. The lack of an esophagotracheal partition also paves the way for fistula formation,[3] for example, a tracheoesophageal fistula secondary to chemotherapy[16] and irradiation. This invariably leads to empyema and often death.

The retrovisceral space, however, is clinically more important. For example, oropharyngeal infections can easily descend through spaces within the different sheaths of the deep cervical fascia. Necrotizing mediastinitis resulting from peritonsillar or dental abscesses or even wisdom tooth extraction has been reported and may involve a mortality rate of nearly 40%.[17],[18] Most instrumental perforations occur in the posterior hypopharynx above the narrowing of the cricopharyngeal sphincter, below which there is no barrier to the spread of infection into the mediastinum. Noninstrumental or spontaneous perforation (Boerhaave’s syndrome) and leakage from an esophageal anastomosis behave in a similar way with rapid and disastrous dissemination of sepsis.

Vascular Structures and Nerves Supplying the Esophagus

Arterial Supply

The history of the arterial supply of the esophagus has been quoted extensively by Siewert and Liebermann-Meffert.[19] This publication gives a good review and its reading is recommended. The following description is based on new studies of my group[1],[11],[19] that we performed to answer special questions in regard to foregut surgery.

Cervical Esophagus

Branches deriving from the right and left superior and inferior thyroid arteries supply the wall of the pharynx, esophagus, and trachea (Figure 7). Compared with the thyroid arteries the vessels to the esophagus are small.[1],[19] Their equal distribution contrasts to Shapiro and Robillard’s claim in 1950 that a greater number of vessels supply predominantly the right side of the esophagus.[20]

Figure 7 
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Vascular corrosion casts of the arteries of the neck and mouth viewed from the anterior position. Top, Aorta (1), the common carotid artery (2), a network of the thyroid arteries (3), esophageal arteries (4), the left superior thyroid artery (5), and the arteries of the tongue (6). Note that there is not any vascular anastomosis between both sides of the tongue. Bottom, Vascular casts of the aortic arch (1), a bunch of bronchoesophageal arteries (2), and a network of esophageal vessels (3). The stump seen at the lateral aorta had supplied the thoracic wall. (SPECIMENS COURTESY OF THE AUTHOR.)

Thoracic Esophagus

Down to the level of the tracheal bifurcation, the upper thoracic esophagus receives branches from the thyroid arteries, but the majority of the supplying vessels to the esophagus and tracheal bifurcation are derived from the bunch of arteries arising at the inflection of the aorta.[1],[20] More caudally, most often only one singular artery arises from the anterior aspect of the aorta. Although this vessel clearly supplies the distal part of the trachea and the stem bronchi, small branches also form the esophageal vascularization, as seen in Figures 7-8. In general, these vessels are straight and short, connecting tightly the aorta, the trachea, and the esophagus.[1] At variable localization, one other unpaired artery may arise from the anterior aortic aspect. This vessel, however, courses obliquely down from its origin (Figure 9) to divide—still within the mediastinum—into an ascending and a descending branch.[1],[19]

Figure 8 
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Arterial corrosion cast of thoracoabdominal organs—aorta, esophagus, and stomach—viewed from the anterior aspect. The bronchial artery is shown deriving from the aorta and giving off several smaller branches that form the minute esophageal network. The stump left of the aorta is the residual of the rami intercostalis. (BERACRYL INJECTION INTO THE AORTA BY THE AUTHOR.)

Abdominal Esophagus

The distal esophagus and the gastric cardia are nourished by up to 11 small arteries that originate at intervals from the left gastric artery.[1],[19] These vessels travel straight upward alongside the anterior aspect of the cardia (see Figure 9) and follow the wall through the diaphragm in the longitudinal esophageal axis to subdivide into periesophageal tributaries before they dip into the muscular layers. The posterior wall of the terminal esophagus receives several large vessels derived from the splenic artery and/or from vessels of the dorsal fundus, but previous claims that nutritional vessels arise from phrenic arteries have not been substantiated.[1]

Figure 9 
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Diagram of the most common vascular pattern of blood supply to the esophagus and cardia in the human adult. 1, aorta; 2, esophagus.

Concerning the vascularization as a whole, the esophagus is an organ of shared vasculature with poor “proper” extrinsic support. In fact, apart from the few “vasa propria” that derive from the aorta directly, the esophagus receives its blood via vessels feeding mainly other organs, such as the thyroid gland, trachea, and stomach. Even though the vessels are minute within the periesophageal tissue, previous claims of a poor or missing vascularization in the wall of the midesophagus could not be substantiated because connections within and throughout the submucosa and mucosa form a complete and vast intramural network of fine vessels (Figure 10).[1],[19] And nowhere is the wall of the esophagus avascular.

Figure 10 
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Sample of the submucosal microvascular esophageal blood supply displayed in a scanning electron micrograph. The arteries and veins are small and form a minute polygonal network. (RESIN-INJECTED SPECIMEN BY THE AUTHOR.)

Comments on Surgical Relevance and Consequences

The correctly mobilized esophagus retains an excellent blood supply over a long distance. The vascularization is seldom responsible for a failed anastomosis.[21] This circulation is evidently due to the rich and complete network of vessels within the wall.

Blunt pull-through esophagectomy without thoracotomy for esophageal cancer is relatively safe and causes a minimum of blood loss.[1],[22],[23] When hemorrhage has occurred after stripping of the esophagus, it was from the site of tumor adhesions rather than from the periesophageal vessels.[24] A usually limited bleeding may occur because the major supporting arteries divide into minute branches at some distance from the esophageal wall, and, when torn, benefit from contractile hemostasis.[1]

Venous Drainage

Intraesophageal (Intrinsic) Veins

The intraesophageal veins include the subepithelial plexus, which is located in the lamina propria of the tunica mucosa.[25] The veins are arranged mainly in the longitudinal axis of the esophagus and extend through the whole length of the esophageal submucosa.[26]

The subepithelial plexus receives blood from the adjacent capillaries and drains into the submucous plexus. At the lower end of the esophagus, the systemic and the portal system obviously anastomose; in case of portal venous obstruction the thin-walled superficial veins presumably enlarge to form varices. Vianna and colleagues[26] described a specialized longitudinal venous arrangement prevalent in the lower third of the esophagus and in the cardia. This structure consists of perforating veins deriving from the small communicating veins of the submucous plexus that pierce the muscular wall of the esophagus. The intramural veins receive tributaries from the muscle coats and form the veins on the surface of the esophagus.

Extraesophageal (Extrinsic) Veins

The extraesophageal veins drain into locally corresponding large vessels. These are the inferior thyroid veins, which empty into the brachiocephalic veins, the azygos and hemiazygos veins, the left gastric vein, and the splenic vein.

Comments on Surgical Relevance and Consequences

The azygos vein, because of its vicinity to the root of the lung and its lymph nodes, is one of the initial structures affected by the extramural spread of tumors of the midesophagus. In this situation, the azygos vein can be easily damaged during esophageal resection. In particular during blunt pull-through dissection, this vein represents a high risk factor causing fatal bleeding if the tumor is adherent to the venous wall. Collateral circulation may exist between the azygos vein and the hemiazygos vein. The hemiazygos vein, if not ligated, can be a source of severe hemorrhage when resecting the esophagus through a right thoracotomy.[27]

Lymphatic Pathways

Lymphatic drainage comprises two systems: lymph channels and lymph nodes. The details of these systems, in particular the initial pathways, have recently received special attention because of the lymphatic spread of malignant tumors. Lymph capillaries commence in tissue spaces (Figure 11) as a network of endothelial channels or as blind endothelial sacculations (Partsch, 1988).[28]

Figure 11 
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Diagram showing the initial lymphatic network, which is reconstructed from mesentery preparations. The color red indicates the lymphatic channel. Most probably, this pattern equals that of the esophagus. (MODIFIED FROM ZWEIFACH BW, PRATHER JW: MANIPULATION OF PRESSURE IN TERMINAL LYMPHATICS IN THE MESENTERY. AM J PHYSIOL 228:1326, 1975.)

Intraesophageal (Intrinsic) Lymphatics

Because of the considerable technical difficulties to identify by injection or anatomic preparation these slender, normally collapsed structures,[29],[30] the anatomic knowledge of the esophageal initial lymphatics in healthy individuals is still sparse. Some investigators such as Idanov, in 1959,[31] or Rouvière, in 1932,[32]emphasized the existence of a rich lymphatic network in the lamina mucosa and tela submucosa of the esophagus. Their claims have never been substantiated by convincing or reproducible documentation. According to recent studies one may assume that tiny precapillary spaces also exist in all the levels of the esophageal lamina mucosa, similar to descriptions of interstitial tissues; other authors have stressed the almost complete absence of true anatomic lymph capillaries in the upper and middle levels of the lamina mucosa of the human stomach[29] and esophagus.[30] Transmission electron microscopic studies have shown anastomosing lymph capillaries only in the lower mucosal levels and small valve-containing vessels in the tela submucosa of the esophagus. These appeared to form long channels that parallel the organ axis.

Extraesophageal (Extrinsic) Lymphatics

The submucosal lymph channels give off occasional branches to the collecting subadventitial and surface trunks.

Thoracic Duct

The principal lymphatic vessel of the body is the thoracic duct (Figure 12). It begins with the cisterna chyli at level L1-2, emerges through the aortic hiatus of the diaphragm, and travels in more than half of cases as a single trunk craniad with the aorta on its left and the azygos vein on its right. Then the duct turns at the level of T5-6 behind the left mainstem bronchus toward the left and ascends lateroposteriorly to the trachea and esophagus to end at the angle between the left subclavian and jugular veins by draining the lymph into the bloodstream. Anatomic variations are manifold.[31] The close local relationship of the flimsy duct to the esophagus explains its occasional damage during esophageal resection and chylothorax.

Figure 12 
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Diagram of the lymphatic pathways and lymph node distribution. During human organogenesis, the lymphatic pathways develop from two different sources, the branchiogenic mesenchyme and the body mesenchyme. As a result, lymph drains toward two different directions (arrows) with a zone of bidirectional flow at the tracheal bifurcation. This feature is consistent with clinical observations. The knowledge of lymph flow and the corresponding lymph node distribution is essential in understanding potential spread of malignancy.

Normally the thoracic duct is collapsed and then appears, like a string of beads, at preparation, because of numerous strong valves. The thoracic duct is 0.5 to 2.0 mm wide (mean, 1.3 mm) at the distal third, 1.0 to 3.0 mm (mean, 1.7 mm) at the middle, and 1.0 to 4.0 mm (mean, 2.3 mm) at the proximal third (threshold, 4.0 mm) as has been shown in 500 lymphograms of healthy individuals by Wirth and Frommhold.[33]

Lymph Nodes of the Esophagus

In noncancer autopsy specimens, we found most of the lymph nodes of the thoracic mediastinum piled up around the tracheal bifurcation (see Figure 12). These were rather large, dark nodes. Anatomically, it was impossible to determine whether they drain the esophagus or the lungs or whether they transport proximally or distally. There is an accumulation of small nodes in the neck and cardia region, but few lymph nodes are normally present in the lateral and ventral mediastinum of the upper third and in the dorsal mediastinum in the lower third of the thorax in healthy individuals. We could not identify the classic chain of lymph nodes along and around the esophagus, as described in textbooks and seen in Netter’s[7] illustration at routine autopsy. This statement is in accordance with that of Wirth and Frommhold,[33] who identified mediastinal lymph nodes in only 5% of 500 normal lymphograms. We found, instead, a greater number of lymph nodes of macroscopic dimensions cranial to the tracheal bifurcation within the tracheoesophageal groove. Considering tumor involvement, the classic lymph node arrangement was elegantly illustrated by Matsubara in 1988.[34]

Comments on Surgical Relevance and Consequences

The initial (terminal) lymphatics (see Figure 12) take up fluid, colloid material from the tissue, cell debris, microorganisms, and eventually tumor cells.[35] The contents are emptied into collecting lymph channels. Paired semilunar valves within the channels determine the direction of flow. They join to form small trunks that convey the fluid and the other absorbed material through the interpositioned lymph nodes. In its passage through the node, noxious material may be filtered off. It is evident that this system of channels provides easy pathways for tumor spread.

Lehnert’s concept that the lymphatics form long channels within the submucosa in which the lymph flows more easily cranially or caudally than through the few channels that pierce the muscular coat supports the clinical observation that the initial submucosal cancer spread follows the longitudinal axis of the organ.[29] Consequently, primary esophageal tumors may extend over a long distance within the esophageal wall before obstructing the lumen.

The absence of lymphatics from the superficial part of the mucosa and the widely anastomosing plexus within the deep layer of the mucosa and the submucosa may explain why the intramural spread of cancer occurs predominantly in the submucosa. Free tumor cells may follow the lymphatic channels over a considerably long distance before passing through the muscular coat into regional lymph nodes.

From the anatomic studies, and the clinical observations, it may be deduced[3],[22],[24],[29],[34],[35] that lymph from areas above the tracheal bifurcation drains mostly craniad toward the thoracic duct whereas lymph from below the carina flows mainly toward the lower mediastinal, left gastric, and celiac lymph nodes. Flow in the area of the tracheal bifurcation normally seems to be bidirectional (see Figure 12), owing to the embryologic development of the two mesenchymal sources.[3],[36],[37] Flow may change under pathologic conditions (tumor invasion). When the lymph vessels become blocked and markedly dilated, either the valves may become incompetent and the flow reversed or a collateral lymphatic circulation may develop; retrograde spread in some malignant tumors may thus be explained. Unfortunately, this possibility also limits the value of establishing normal flow pathways.

Innervation

The vegetative (autonomous) nervous system regulates the function of the esophagus. It is subdivided into two parts, the sympathetic and the parasympathetic nervous system. The nerve fascicles may carry parasympathetic and sympathetic components that exert antagonistic influences on the esophagus and control the striated and smooth muscle, glands, and blood vessels.[38],[39]

Sympathetic Nervous System

The sympathetic innervation comes from the cervical and the thoracic sympathetic chain (see Figure 13). The sympathetic pathways are concerned with the movement of the esophageal tract, contraction of the sphincters, relaxation of the muscular wall, increase in glandular and peristaltic activity, and vasoconstriction.

Figure 13
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Diagram of the topographic relationships between the esophagus and its innervation. This shows the situation from the anterior aspect. The dimensions are out of scale.

The sympathetic trunks are two ganglionated nerve cords that extend from the base of the skull down to the sacrum. They are located lateral to the spine (see Figure 13) and possess 11 to 12 thoracic paravertebral ganglia on each side. The sympathetic innervation of the proximal esophagus is derived from the cervical and upper thoracic ganglia.[38] Besides the direct approach to the organ, the fibers form a profuse, delicate network between and around the esophagus.[38]

Parasympathetic Nervous System

The parasympathetic innervation comes from the vagus nerve (see Figure 13). The esophageal branches of the vagus nerve provide motor innervation to the muscular coats and secretomotor innervation to the glands. The vagus nerve is the paired 10th cranial nerve. Its motor fibers arise in the dorsal vagal nucleus, and its sensory fibers derive from the superior and inferior ganglion of the vagus nerve in the neck. The nerve fibers that innervate the upper part of the esophagus and pharyngoesophageal “striped” musculature arise in the nucleus ambiguus.[38] Unlike those of the “smooth” muscles, which receive motor input via preganglionic autonomic fibers and synapse on neurons of the myenteric ganglia, the nerve endings of the striped muscle make direct synaptic contacts through motor end plates.[40]From their origin in the medulla, the vagus nerves descend as a paired trunk and pass through the corresponding jugular foramen. The branches are shown on Figure 13.

CERVICAL ESOPHAGUS. By giving off branches to the pharynx, larynx, and trachea (Figures 14 and 15; see also Figure 13), these fibers form the cervical plexus that also innervates the proximal esophagus.[40] The bilateral superior laryngeal nerves (SLNs) originate from the vagal trunks of the respective side, that is, from the ganglion nodosum (see Figure 13). Both nerves descend alongside the carotid arteries before dividing into branches that enter the pharynx to innervate the muscles of the pharynx, hypopharynx, and larynx.[41],[42]

Figure 14
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Vagal innervation of the upper esophagus by the inferior (recurrent) laryngeal nerve. Posterior aspect of the muscular wall of the esophagus (1) and pharynx (2) is shown. The left (7) and the right recurrent laryngeal nerves are exposed. Laterally on both sides the turning points around the arch of the aorta (6) and the subclavian artery (5) are displayed. The ramifications of the recurrent laryngeal nerves alternatively enter the lateral wall of the esophagus (1) and trachea. The thyroid gland (3) and the common carotid artery (4) are shown. (FROM LIEBERMANN-MEFFERT D, ET AL: RECURRENT AND SUPERIOR LARYNGEAL NERVES: A NEW LOOK WITH IMPLICATIONS FOR THE ESOPHAGEAL SURGEON. ANN THORAC SURG 67:212, 1999. COPYRIGHT 1999, WITH PERMISSION FROM THE SOCIETY OF THORACIC SURGEONS.)
Figure 15
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Vagal innervation of the upper half of the esophagus. The specimen obtained from autopsy shows the neck area from the posterior aspect. The meandering left inferior (recurrent) laryngeal nerve (1) wriggles, being loosely adherent to the periesophageal connective tissue from the aorta (2), cranially to dip under the lower lobe of the thyroid gland (4). It will endure some stretching. Common carotid artery (3). (FROM LIEBERMANN-MEFFERT D, ET AL: RECURRENT AND SUPERIOR LARYNGEAL NERVES: A NEW LOOK WITH IMPLICATIONS FOR THE ESOPHAGEAL SURGEON. ANN THORAC SURG 67:212, 1999. COPYRIGHT 1999, WITH PERMISSION FROM THE SOCIETY OF THORACIC SURGEONS.)

Of the inferior (recurrent) laryngeal nerves (RLNs), the right one arises from the vagus nerve in front of the subclavian artery and turns posteriorly around the artery (see Figures 13 and 14) before ascending obliquely to the right lateral aspect of the trachea behind the common carotid artery. The left RLN originates from the vagus nerve in front of the aortic arch, surrounds the aorta posteriorly, and ascends, maintaining a meandering course (see Figure 16). Both the RLNs approach the esophagus during their lateral ascent and give off an equal number of nerve branches (6 to 12) to the esophagus as well as to the trachea (see Figure 14). When approaching the pharyngoesophageal junction (see Figure 14), both the right and the left RLNs have obtained an intimate proximity with the wall of the esophagus and trachea.[41],[42] This proximity is particularly pronounced when the proximal RLNs become positioned underneath the medial plane of the thyroid glands. There they entangle the thyroid vessels before they enter the larynx from lateral and caudal to the cricopharyngeal muscle band.[41]

Figure 16
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Vagal innervation of the midesophagus (1) shown from an anterior aspect. The specimen obtained from autopsy displays elegantly the loosely adherent vagal network of the midesophagus, when pulled up by the forceps (3). Caudad to the tracheal bifurcation (2) large dark lymph nodes are a frequent finding. (SPECIMEN COURTESY OF THE AUTHOR.)

The terminal branches of the RLNs are most often 1.0 to 1.5 mm thick and divide into several branches to innervate all the laryngeal muscles, including the vocal and epiglottic muscles.[41],[42],[43] The observation of a nonrecurrent laryngeal nerve is an unfrequent event.[44] The situation is almost never found on the right side (31 [0.1%] of 6000 cases of thyroid surgery done by Toniato and associates[44] and none on the left). This corresponds to the data presented by Hiebert and colleagues.[43]

THORACIC ESOPHAGUS. At the level of the tracheal bifurcation, the ongoing main vagal trunks pass posterior to the roots of the lung and divide into multiple small branches to form pulmonary and esophageal plexuses. Caudal to the tracheal bifurcation, the esophageal vagal trunks break up into a network of fascicles (Figure 15). The left vagus builds up mainly the anterior plexus, and the right vagus, the posterior plexus. At a variable distance from the cardia, the fibers of both the anterior plexus and the posterior plexus reorganize into two thick trunks that travel down on the anterior and posterior esophageal wall (Figure 16). Both vagal trunks may now contain fibers from the upper contralateral side.

ABDOMINAL ESOPHAGUS AND STOMACH. Together with the esophagus, the vagus nerves pass through the diaphragmatic hiatus, where they are barely distinguishable under the phrenoesophageal membrane. The posterior vagus nerve often divides into smaller branches that lie 2 to 4 cm distant from the end of the esophagus and to its right. The anterior vagus nerve runs at the left side to the anterosuperior surface of the stomach.

Intramural Innervation

Branches from the periesophageal, parasympathetic, and sympathetic plexus enter the wall of the esophagus together with the blood vessels. They form the intrinsic innervation, which is composed of fine nerve fibers and numerous groups of ganglia. The ganglia lie either between the longitudinal and the circular layers of the tunica muscularis, in which case they are called myenteric or Auerbach’s plexus, or in the tela submucosa, in which case they are called the submucous or Meissner plexus. The one regulates the contraction of the muscle coats; the other regulates the peristalsis of the muscularis mucosae and the secretion. Both are interconnected by a meshwork of fibers.[45] The number of ganglia is fairly uniform within the esophageal wall.[46] Near the junctional zone, however, the nerve fascicles become thicker and ganglia accumulate.[45]

Comments on Surgical Relevance and Consequences

During esophageal resection and goiter operations, the RLNs are at high risk. Injuries involving the SLNs and RLNs cause clinical pictures of a variety of transient or even lasting motor and sensory disorders of the pharyngolaryngoesophageal junction area. These may be hoarseness related to vocal cord palsy and respiration and swallowing failure associated with problems of aspiration and dysphagia.[41],[43]

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Last updated: December 4, 2019