Layers of the Esophageal Wall

The outer layer of the esophagus is the adventitia. In the neck, the esophageal adventitia blends with the deep cervical fascia. In the thorax and abdomen, the adventitia is largely covered with pleura and peritoneum, respectively. The esophagus is loosely connected to the diaphragm by a phrenicoabdominal membrane.

The muscularis is composed of striated muscle for the entire length of the esophagus in dogs, but it changes to smooth muscle in the terminal esophagus in cats. The muscular layer arises from the cricopharyngeus muscle and the cricoesophageal tendon, which is connected to the medial dorsal crest of the cricoid cartilage and serves as the fixed cranial attachment of the esophagus. For most of the length of the esophagus, the muscular layer is composed of two poorly defined coats whose individual fibers form left- and right-handed spirals. The superficial fibers on one side become the deep fibers on the other side, with fibers crossing at right angles dorsally and ventrally to form dorsal and ventral lines of decussation. In the terminal esophagus, lines of descussation gradually diminish; fibers of the inner coat become more transverse in direction and blend into the circular and oblique fibers of the stomach, and fibers of the outer coat become more longitudinal in direction and blend into the longitudinal muscle of the stomach. At its cranial and caudal ends, the esophagus has functional sphincters that are difficult to delineate anatomically. There is no obvious thickening of the esophageal wall at the pharyngoesophageal junction to form a true cranial (or upper) esophageal sphincter. However, the thyropharyngeus and cricopharyngeus muscles and associated elastic tissue serve the function of a cranial esophageal sphincter. There is an increase in thickening of the circumferential striated muscle layer at the gastroesophageal junction in dogs, which correlates with the accepted location of the high-pressure zone at the gastroesophageal junction and may represent the caudal (or lower) esophageal sphincter. Other proposed anatomic contributors to the lower esophageal high pressure zone include the diaphragmatic crural muscles, the angle at which the esophagus and stomach meet, and the folds of the gastroesophageal mucosa.

The submucosa loosely connects the mucosa and muscularis, allowing mucosa to move independently and form mucosal folds in the undistended esophagus. The submucosa contains blood vessels, nerves, and simple mucous glands that secrete mucus, which lubricates the mucosal surface.

The esophageal mucosa is composed of a stratified squamous epithelium. In the nondistended esophagus, the mucosa forms numerous large longitudinal folds that can be seen with positive-contrast esophagography. In cats, the terminal esophagus is also folded transversely, producing a herringbone appearance on esophagrams.

Esophageal Blood Supply and Innervation

The main arterial blood supply to the cervical esophagus is from branches of the cranial and caudal thyroid arteries. The bronchoesophageal artery is the main source of blood for the cranial two thirds of the thoracic esophagus; the remaining thoracic esophagus is supplied by esophageal branches of the aorta or dorsal intercostal arteries. The terminal portion is supplied by a branch of the left gastric artery. The veins that drain the esophagus are largely satellites of the arteries that supply it. Veins leaving the cervical esophagus drain into the external jugular veins, and those from the thoracic esophagus drain mostly into the azygous vein. The vein that accompanies the left gastric vein drains into the portal venous system. The esophageal arteries and veins form a rich, intramural plexus of anastomosing vessels in the submucosal layer. Esophageal lymphatic vessels drain into the medial retropharyngeal, deep cervical, cranial mediastinal, portal, splenic, and gastric lymph nodes. The esophagus is innervated by nerve fibers arising from various branches of the vagus, beginning with the paired pharyngoesophageal nerves followed by the recurrent laryngeal and paralaryngeal nerves and concluding with the dorsal and ventral vagal trunks (Figure 90-3).

Surgical Approaches to the Esophagus

The cervical esophagus is approached by a ventral midline incision, separating the paired sternohyoid muscles and retracting the trachea to the right (Figure 90-5). Care should be taken to avoid damage to the recurrent laryngeal nerve during tracheal retraction. This approach can be extended via a cranial median sternotomy to expose the cranial thoracic esophagus to the level of the tracheal bifurcation. The cranial thoracic esophagus can also be exposed via a left third or fourth or a right third, fourth, or fifth intercostal thoracotomy.^63,115 The esophagus is exposed from a left-sided thoracotomy by ventral retraction of the brachiocephalic trunk and subclavian vessels. On the right side, the esophagus is exposed by ventral retraction of the trachea, which can be combined with retraction or ligation of the azygous vein to increase exposure of the esophagus at the base of the heart. A left-sided seventh, eighth, or ninth intercostal thoracotomy is generally preferred for approaching the caudal thoracic esophagus to avoid the caudal vena cava. The dorsal and ventral vagal nerves should be identified and preserved. The caudal esophagus and stomach can be approached by a combined ventral midline laparotomy and diaphragmatic incision or caudal median sternotomy.

Suture Materials and Techniques

Monofilament, minimally reactive, slowly absorbable suture materials, such as polydioxanone or polyglyconate, are often recommended for closure of esophageal incisions.⁴¹ Sutures should be placed approximately 2 mm from the cut edge and 2 to 3 mm apart.¹³⁹

A multitude of esophageal suturing techniques have been advocated in dogs and cats,⁴¹ including double-layer appositional and single-layer inverting, everting, and appositional.^{114,139,144,157} Traditionally, a two-layer closure technique is used, consisting of a first layer incorporating the mucosa or submucosa with placement of the knots in the esophageal lumen and a second layer consisting of an inverting pattern in the muscularis.¹³⁹ The rationale for this suture technique was based on the assumptions that the thick stratified squamous mucosal layer was the holding layer of the esophagus and that suture knots in the submucosa would provoke inflammation and fibrosis.⁴¹ In a study of the functional suture-holding layer of the canine esophagus, there was no significant difference between the tensile strength of the submucosa alone and the mucosa and submucosa combined, with the full esophageal wall having the greatest tensile strength and the muscularis alone the least.²⁸ The author concluded that the submucosa was the functional suture-holding layer of the esophagus and therefore should be incorporated in at least one layer of sutures.²⁸ In another study, esophagotomy incisions in healthy dogs healed adequately with double-layer simple interrupted, single-layer simple continuous, or single-layer simple interrupted patterns.¹¹⁴ Because incisions closed with a simple continuous single-layer pattern had the least wound strength and poorest tissue apposition, a single-layer simple interrupted or double-layer suture pattern was recommended.¹¹⁴ An interrupted pattern is generally preferred for esophageal anastomoses to permit esophageal dilatation and to avoid potential interference with the intramural blood supply, although a simple continuous pattern is acceptable for esophagotomy closure.⁴¹ Single-layer interrupted closure of esophagotomy and esophageal anastomoses using an absorbable suture material has been used successfully clinically in dogs and cats.¹⁴⁴

Esophagotomy

Indications for esophagotomy include foreign body removal and closure of esophageal perforations and diverticula. Esophagotomy can be performed on any portion of the esophagus. The surgical site is isolated with moistened laparotomy sponges, and the esophagus is suctioned transorally to reduce contamination. If fluid or ingesta is present in the esophagus, the esophageal lumen can be occluded cranial and caudal to the proposed incision site with fingers, umbilical tape, or noncrushing clamps. Alternatively, stay sutures and suction can be used to minimize spillage (Figure 90-6). A stab incision is made into the esophageal lumen, and the incision is extended longitudinally as necessary. The esophagotomy incision can be closed with a one- or two-layer interrupted or continuous suture pattern. With a two-layer pattern, the first layer incorporates mucosa and submucosa, and knots are placed in the esophageal lumen. The second layer apposes the muscularis and adventitia, with knots placed extralumenally. With a one-layer closure, the suture passes through all layers of the esophageal wall, with limited penetration of the mucosa, and knots are placed extralumenally. Sutures should be placed approximately 2 mm from the cut edge and 2 to 3 mm apart.¹³⁹ Integrity of the closure can be tested by distending the esophagus with saline and placing additional sutures to seal any areas of leakage. The patient should not receive food or water by mouth for at least 24 to 48 hours after surgery.⁶⁷ Healing of a cervical esophagotomy incision can be delayed by contact with pharyngostomy tubes.

Esophageal Resection and Anastomosis

Indications for esophageal resection and anastomosis include treatment of congenital obstructions, acquired discrete strictures, severe localized esophageal injury, esophageal diverticula that cannot be excised by simple esophagotomy, and esophageal neoplasia.¹¹⁵ The extent of the proposed resection should be estimated before surgery by esophagoscopy, contrast esophagography, magnetic resonance imaging, or computed tomography (CT). The length of esophagus that can be resected without undue risk of dehiscence is limited by anastomotic tension.¹¹⁵ Resection and primary anastomoses of up to 20% of the cervical esophagus and 50% of the thoracic esophagus have been reported in experimental dogs;^99,141 in clinical patients, however, resection of more than 3 to 5 cm of esophagus has been associated with an increased risk of dehiscence.⁶³ Esophageal substitution techniques should be considered when extensive esophageal resection is unavoidable, although clinical experience of these techniques in dogs and cats is limited.

Circumferential partial myotomy may reduce anastomotic tension. The outer muscle layer is incised 2 to 3 cm proximal or distal to the anastomosis, or both, leaving the inner muscle layer intact.40,67,108 Separation of the muscle layers may be improved by injecting saline into the muscularis.¹⁰⁸ Use of a partial myotomy prevents disruption of the submucosal vascular plexus and subsequent esophageal ischemia, which are observed with full-thickness myotomy, while providing a similar reduction in anastomotic tension.¹⁰⁸ The myotomy heals by secondary intention without stricture or diverticulum formation.

Esophageal resection and anastomosis can be performed on any portion of the esophagus. A small amount of esophageal mobilization during surgery is necessary to control spillage and reduce anastomotic tension, but excessive mobilization may compromise segmental esophageal blood supply. The esophagus should be isolated with moistened laparotomy sponges, and the lumen can be occluded with fingers, umbilical tape, or noncrushing clamps (Figure 90-7). The diseased portion of the esophagus is resected. Stay sutures facilitate gentle tissue handling and maintain alignment. The remaining segments are reapposed with a one- or two-layer suture pattern as described for esophagotomy, with the far esophageal wall sutured first.

Esophageal anastomoses can also be performed with surgical stapling instruments or using a biofragmentable anastomosis ring.88,89,122,154 The stapling device can be inserted through the mouth or through a pharyngotomy, esophagotomy, or gastrotomy incision.¹²² In one study comparing biofragmentable anastomosis ring with an end-to-end anastomotic stapler, there was no significant difference in the complication rate or healing with either method. The mortality rate was 13.3% (four of 30 biofragmentable anastomosis ring dogs), and leaks were noted only in the biofragmentable anastomosis ring group (14.3%). Two of 18 dogs in the stapler group developed strictures within 28 days after anastomosis.⁸⁹

After esophageal resection and anastomosis, fluid and nutritional requirements are provided for at least 1 week through a gastrostomy or enterostomy tube.⁶⁷ Contrast esophagograms may be performed at 1 and 3 months after surgery to evaluate esophageal structure and function.¹¹⁵

Esophageal Patching

Patches can be used to reinforce existing esophagus (“on-lay” patch) or for partial circumferential replacement of the esophageal wall (“in-lay” patch). On-lay patches are applied on esophagotomy incisions or esophageal anastomoses that are at risk for dehiscence because of reduced vascularity or anastomotic tension.41,115 The most common application for in-lay patches is for esophagoplasty after longitudinal division of an esophageal stricture.¹¹⁵

Materials that can be used for esophageal patching include host tissues, such as omentum, pericardium, local muscle flaps, stomach, or intestine, and xenogeneic or artificial substances, such as porcine small intestinal submucosa, lyophilized dura mater, collagen-coated Vicryl mesh, and expanded polytetrafluoroethylene patches.* Omentum is exceptional for supporting caudal thoracic esophageal wounds and closing small defects because of its vascularity and availability; esophageal stricture formation may also be minimized with omental patching.^41,62,70,106 A paracostal or midline abdominal incision is necessary to create an omental pedicle flap. The right gastroepiploic artery and its branches to the omentum are ligated. The flap is brought through a small incision in the diaphragm, taking care to preserve the blood supply. The omentum is then tacked at multiple sites around the esophageal wound with absorbable suture.

Pedicle grafts can be created from local muscle to support the esophagus. Cervical esophagus has been successfully patched with sternothyroideus and longus colli muscles.16,73 Experimentally, longus colli muscle patch graft in dogs reduced stricture formation when compared with primary closure of a partial circumferential cervical esophageal defect. The addition of a free buccal mucosal graft further reduced the extent of stricture formation.¹⁶ In the thoracic esophagus, a vascularized pedicle graft of external and internal intercostal muscle can be created by incision and elevation of the periosteum of two adjacent ribs, with division of either the dorsal or ventral attachment.²² Diaphragmatic pedicle grafts can be used to patch the caudal thoracic esophagus.⁹²

Pericardial grafts significantly increase the strength of esophageal anastomoses without increasing the risk of stricture formation.⁶⁹ Esophageal patches can also be created from the gastric wall^74,75 or jejunum after mucosal stripping.¹¹¹ The adjacent lung has been used experimentally in dogs to repair esophageal defects;¹⁰⁴ this technique should be used with caution because of the risk of esophagopulmonary fistula formation.

Esophageal Substitution

Patients with extensive disease from injury or neoplasia may require massive esophageal resection.⁴¹ If primary anastomosis is not feasible because of expected tension, esophageal substitution may be considered. Reports of esophageal substitution in humans and experimental animals are fairly common; however, clinical experience with esophageal replacement in small animals is minimal.

The cervical esophagus can be replaced in a multistage procedure with an inverse tubed skin graft.121,161 A cranially based single pedicle skin flap is formed into an inverse tube and sutured distally to the cut end of the esophagus.¹²¹ Two weeks later, the cranial skin pedicle is cut and anastomosed cranially to the remaining end of the esophagus. Alternatively, the proximal and distal ends of the cervical esophagus can be sutured to the skin after esophageal resection to form two esophagocutaneous fistulae (Figure 90-8).¹⁶¹ Several weeks later, the skin is incised and inverted to form a tube connecting the two ends of the esophagus. The remaining cervical skin is closed over the top of the tube. An omocervical cutaneous island axial pattern flap, based on the omocervical vessels, has been advocated as an alternative one-stage inverse tubed skin graft for substitution of the cervical esophagus.¹²⁰ Potential complications of esophageal skin graft include luminal obstruction with hair, lack of peristalsis, and indistensibility of the graft.

Muscle grafts have been used experimentally in dogs for complete segmental reconstruction of the esophagus.107,156,183 The cranial thoracic esophagus was successfully replaced with a tubed intercostal musculopleural pedicle graft,¹⁰⁷ and the caudal thoracic esophagus was replaced with a diaphragmatic pedicle graft.¹¹⁹ A longer segment of the esophagus was successfully reconstructed with an epithelial-lined esophageal conduit using a tubed latissimus dorsi musculocutaneous flap based on the thoracodorsal vessels.^182,183

The caudal-most portion of the thoracic esophagus can be replaced by gastric advancement and esophagogastric anastomosis.23,25,122,154 Potential complications include leakage, stricture, chronic vomiting, reflux esophagitis, gastric dilatation within the thoracic cavity, and herniation of other abdominal viscera through an inadequately reconstructed diaphragm.⁴¹ Isoperistaltic and antiperistaltic gastric tubes created from the greater curvature of the stomach and based on the gastroepiploic vessels may be better alternatives for caudal esophageal replacement.⁶⁵ Splenectomy and ligation of the omental branches of the gastroepiploic vessels are required with these techniques; surgery is greatly facilitated by the use of stapling instruments.^65,154 An antiperistaltic, or reverse, gastric tube is created from the greater curvature of the stomach, maintaining the luminal connection at the fundus. The tube is advanced into the thoracic cavity and anastomosed to the cut end of the esophagus. An isoperistaltic gastric tube is created in a similar fashion, but the tube is separated at both ends to create a pedicle graft. The isoperistaltic tube technique maintains gastric tube peristalsis in an aboral direction but requires two anastomoses. With both techniques, a portion of the gastric tube should be maintained within the abdomen to reduce the risk of gastroesophageal reflux, and a pyloromyoplasty procedure should be performed to enhance gastric emptying because disruption of vagal innervation is likely.^23,65 Animals are fed by jejunostomy tubes for at least 1 week after surgery.⁴¹

In dogs, segmental esophageal replacement with a small intestinal or colonic pedicle graft is hampered by the limited mobility of the vascular pedicle; free microvascular grafts of the intestine are therefore considered more feasible.⁴¹ Colonic autografts are more tolerant of ischemia than jejunum and thus provide a longer length of intestine for single-pedicle anastomosis. Additionally, the middle colic vessels are larger than the jejunal vessels, making the procedure less technically demanding.⁹⁰ Experimentally, replacement of the canine thoracic esophagus with free intestinal grafts has been unsuccessful because of vascular thrombosis and anastomotic leakage.^17,90 In the cervical region, the graft vessels can be successfully anastomosed to the carotid or cranial thyroid artery and the jugular, omobrachial, or lingofacial vein.^17,55,90 In one dog with an esophageal stricture, the cervical esophagus was replaced with a free jejunal autograft.⁵⁶ Complications included leakage and aspiration pneumonia. After surgery, decompression of the stomach and esophagus should be maintained with a nasogastric tube to reduce intraluminal pressure and prevent disruption of the anastomosis.⁵⁶

Vascular Ring Anomalies

Vascular rings are developmental anomalies of the great vessels that result in the encircling of esophagus and trachea by a complete or incomplete ring of vessels. In embryos, the great vessels are derived from the paired dorsal and ventral aortas and the six interconnecting pairs of aortic arches that correspond to the six brachial arches (Figure 90-9). The vascular system forms around the embryonic foregut and pulmonary bud, and as the embryo develops, selective involution and reconnection of the vessels result in the formation of the definitive cardiovascular system and release of the esophagus and trachea.^{35,41,165,181}

During normal embryologic development, the ventral aortas fuse caudally to form the heart. The first and second aortic arches involute early in development. The ventral aortas that served as origins of the first two aortic arches develop into the external carotid arteries, and corresponding sections of the dorsal aortas form the internal carotids. The ventral aortas between the third and fourth arches form the common carotid arteries, and the dorsal aortas between the third and fourth arches involute bilaterally. The left ventral aortic root of the fourth arch and the fourth left aortic arch develop into the adult aortic arch; the caudal dorsal aortas fuse to form the descending aorta. The right ventral aortic root of the fourth arch becomes the brachiocephalic trunk. The right fourth aortic arch forms the right subclavian artery, with the left subclavian arising from the left seventh intersegmental artery. The fifth aortic arches involute bilaterally. The sixth aortic arches form the pulmonary arteries; the left pulmonary artery retains a connection to the aorta—the (left) ductus arteriosus—that becomes the ligamentum arteriosum after birth. The right ductus arteriosus and the right dorsal aorta between the right sixth arch and the point of fusion of the dorsal aortas involute to release the esophagus and trachea.

Several types of vascular ring anomalies are described in dogs and cats (see Figure 90-9). The most common vascular ring anomaly is persistent right aortic arch with a left ligamentum arteriosum, in which the aortic arch develops from the right fourth aortic arch. Persistent right aortic arch and right ductus arteriosum would be the mirror image of the normal anatomy and would not result in a vascular ring. Persistent right aortic arch with an aberrant left subclavian artery occurs when the left subclavian artery passes dorsal to the esophagus from the right-sided aorta, resulting in an incomplete vascular ring. Persistent right aortic arch with an aberrant left subclavian artery has been described in conjunction with either a left ligamentum arteriosum, resulting in the formation of two strictures, or with a right ligamentum arteriosum, resulting in a single stricture associated with the aberrant subclavian artery.^20,72,163 Double aortic arch results from persistence of both left and right fourth aortic arches and can produce significant tracheal stenosis.^41,166, Persistent right ligamentum arteriosum with normal (left) aortic arch is the mirror image of a persistent right aortic arch and, although uncommon, is significant in that it cannot be corrected via a left lateral thoracotomy.^68,76 Aberrant right subclavian artery with normal (left) aortic arch occurs when the right subclavian artery passes dorsal to the esophagus, resulting in an incomplete vascular ring.^13,162 To the author’s knowledge, an aberrant right subclavian artery combined with a right ligamentum arteriosum has not been reported in dogs. Persistent left cranial vena cava with a non-elastic band around the esophagus has been reported.⁹⁴ Vascular ring anomalies are reported less frequently in cats and include persistent right aortic arch with left ligamentum arteriosum, persistent right ligamentum arteriosum with a left aortic arch, persistent right aortic arch with a right ligamentum arteriosum and aberrant left subclavian artery, and double aortic arch.*

Congenital anomalies of the great vessels have been reported in 20% of dogs and cats, but most variants are not clinically significant.¹⁴⁹ The most common vascular ring anomaly described in humans and dogs (6%; 8 of 136 dogs) is an aberrant right subclavian artery; this anomaly frequently does not result in clinical signs.^18,149 Persistent right aortic arch with left ligamentum arteriosum accounts for 95% of clinical cases of vascular ring anomalies reported in dogs.^41,165 The ductus arteriosus may remain patent in up to 10% of dogs with persistent right aortic arch.¹⁶⁵ Persistent left cranial vena cava (Figure 90-10) has been reported in up to 45% of dogs with vascular ring anomalies;¹⁶⁵ this anomaly can complicate surgical approach.

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