Esophageal Reconstruction

Anatomy and Physiology

The esophagus is roughly 25 centimeters in length, with upper and lower esophageal sphincters marking the entrance and exit to this elongated organ.[1] The esophagus is further subdivided into three anatomical segments: cervical, thoracic, and abdominal. The cervical segment begins at the cricopharyngeus and ends at the supracervical notch. The thoracic segment runs in the anterior mediastinum, starting at the suprasternal notch and ending at the diaphragm. The abdominal esophagus is the shortest as it extends from the diaphragm to the gastric fundus. 

The esophagus is fed by several different arterial branches. The cervical esophagus derives its blood supply from the inferior thyroid artery. The thoracic esophagus has direct, terminal branches from the esophagus. The abdominal portion is supplied by the left gastric artery and the left phrenic artery. Venous drainage is similarly segmental with drainage into the superior vena cava and the systemic system from the azygos and inferior thyroid veins. The distal esophagus drains into the left gastric, which empties into the portal vein. This connection of systemic and portal circulation can lead to distended veins in patients with cirrhosis called esophageal varices.[2]

The main function of the esophagus is the transportation of the food bolus. It accomplishes this through complex, muscular coordination of peristaltic waves. The esophagus has two different types of muscle. In the cervical esophagus, the muscular layers are striated, whereas, in the thoracic and abdominal, they are smooth muscles.[3] The interplay between these muscles is complex and beyond the scope of this article.

Indications

The main indications for esophageal reconstruction after esophagectomy includes tumor excision, corrosive injury, radiation damage, and congenital disease.[4] Patients who have adenocarcinoma or squamous cell carcinoma of the esophagus may require esophagectomy. These patients typically get radiation and chemotherapy before esophagectomy.[5]

Patients who ingest caustic substances may require esophagectomy. Substances with extremes of pH (less than 2 or greater than 12) can create severe injury and burns in the esophagus.[6] Depending on the initial injury grade, patients may require immediate esophagectomy. Patients with any caustic esophageal injury are at increased risk of squamous and adenocarcinoma esophageal cancer.[7] These patients need long term follow-up. 

Esophageal atresia is a congenital malformation of the upper gastrointestinal tract with worldwide prevalence varying from 1 in 2500 to 1 in 4500 live births.[8] Depending on the type and severity of the esophageal atresia with potential tracheoesophageal fistula, primary esophageal anastomosis can be attempted.[9] If there is a long gap esophageal atresia then an esophageal interposition graft utilizing stomach, colon, or jejunum may be utilized. The primary choice of esophageal conduit in children is colonic interposition graft.[10]

Esophagectomy can be accomplished through several different techniques including Ivor Lewis esophagectomy, transhiatal esophagectomy, or a Mckeown three incision esophagectomy.[11] All three types of esophagectomy utilize a combination of three different potential incisions. The first is an abdominal incision to prepare the esophageal reconstruction conduit whether that be stomach, colon, or jejunum. The second incision is a right thoracotomy for mediastinal esophagus exposure and anastomosis. The third incision is a left neck incision used for cervical esophagus exposure and anastomosis. The Ivor Lewis esophagectomy utilizes an abdominal and right thoracotomy. Transhiatal esophagectomy utilizes an abdominal and left neck incision with blunt mediastinal dissection without a right thoracotomy. The Mckeown three incision esophagectomy utilizes all three incisions including abdominal, right thoracotomy, and left neck incision. These operations may also be performed in a minimally invasive or open manner.[12] Depending on the tumor location, surgeon experience and patient characteristics will determine the ideal esophagectomy technique.

Contraindications

The contraindications for esophageal reconstruction include patients who are too debilitated or malnourished to tolerate an esophagectomy. Depending on the indication for esophagectomy, patients may receive gastric or jejunal tube feedings to supplement enteral feedings. 

With regards to cancer, patients who present with metastatic or locally advanced, inoperable esophageal cancer are best treated with palliative measures. Instead of esophageal reconstruction, these patients should be treated with chemoradiation, esophageal stents, and possible esophageal dilations.[13]

Equipment

The equipment for esophageal reconstruction depends on the type of esophagectomy, operative technique, and the choice of the conduit. Operating room equipment should be capable of manipulating abdominal and thoracic organs if the operation is done in an open fashion. These include retractors, staplers, and absorbable and nonabsorbable suture. If the esophagectomy is done laparoscopically or robotically, then the appropriate laparoscopic equipment, including ports, needle drivers, staplers, graspers, and drains, should be available. Finally, if free flaps are used for esophageal reconstruction, microscopes should be available in the operating room.[14]

Personnel

Personnel required for esophageal reconstruction include surgeons, specifically thoracic, plastic, or abdominal; operating room team members including nurses, scrub techs, and anesthesia; radiologists, gastroenterologists, oncologists, and radiation oncologists.

Preparation

Before any esophageal operation, patients need preoperative cardiac, pulmonary, and anesthesia clearance. Patients should also be evaluated for optimal nutrition including serum albumin, prealbumin, and weight loss preoperatively. High prealbumin levels have correlated with improved long term survival in esophageal cancer patients.[15] To achieve optimal nutrition, many patients require jejunostomy tubes, although there is some controversy.[16] Patients should also be counseled on the potential complications of esophagectomy and esophageal reconstruction.

Technique or Treatment

There are various methods of esophageal reconstruction that have been previously described in the literature. Advances in microsurgery have made it possible to accomplish both the resection of large pharyngoesophageal tumors and subsequent reconstruction of circumferential esophageal defects in a single operation.[17] The main conduits used for esophageal reconstruction after esophagectomy include interposition grafts such as gastric, colon, and jejunum. There are also a number of free flaps that can be utilized, including pedicled, local flaps such as the pectoralis major and supraclavicular island flaps, or free flaps such as the radial forearm free flap, anterolateral thigh (ALT) free flap, and jejunal free flap.[18][19][20][21][22]

The posterior mediastinum is the most commonly used conduit after esophagectomy, although other routes such as substernal and subcutaneous have been described. Besides the posterior mediastinum, the alternative routes are rarely used only in special situations in which patients required esophageal diversion or when multiple operations preclude the posterior mediastinal space.[23]

Gastric Pull-up

Despite the number of options, the main conduit is the stomach, which is advanced cephalad into the posterior mediastinum in the "gastric pull-up" isoperistaltic technique.[24] The relative ease of utilizing the stomach based on its location, blood supply, and single anastomosis makes it the most common and reliable option. During the esophagectomy,  the proximal stomach and lymph nodes are typically resected along with the segment of the esophagus. The gastric conduit is then fashioned by tubularization of the stomach and preserving the right gastroepiploic artery along the greater curvature. The rich supply of submucosal vascular networks can preserve the stomach on this single vessel. It is of utmost importance the right gastroepiploic artery is preserved as ischemia to the stomach will result in anastomotic leakage, stricture, and even dehiscence. The other gastric arteries are typically ligated to make ample length and mobility for the conduit. Once the stomach conduit is made, it is pulled into the chest or neck for the anastomosis, depending on the initial indication. The esophagogastric anastomosis is the area on the gastric conduit with the highest incidence of ischemia since the right gastroepiploic artery is supplied from the gastroduodenal artery and begins near the pylorus. There are many ways to evaluate anastomosis, but recently, indocyanine green (ICG) has been a promising fluorescence imaging tool to access the anastomosis and may lead to reduced anastomotic leaks and graft necrosis.[25] 

The single anastomosis of the gastric esophageal conduit makes it less technically demanding than any of the other conduit choices. Anastomotic leaks can be managed conservatively if the leak is small and contained. If there is a large leak or any undrained fluid collections, then the patient may need a thoracotomy to repair the leak. If there is complete graft necrosis, then the stomach conduit should be resected, and a cervical esophagostomy should be constructed along with exploratory laparotomy for jejunal tube placement.[26]

Colon Interposition

If the stomach cannot be used for an esophageal reconstructive conduit, then the colon may be used. The right or left colon can be utilized. The main conduit is typically the right colon due to its rich blood supply, and part of the transverse colon is also typically used.[27] To prepare the colonic conduit, the colon should receive a bowel preparation to ensure all stool has been removed. If known preoperatively that the colon will be used, it is advisable to do a colonoscopy to rule out occult malignancy. Once the decision to use colon has been decided upon, the operation to fashion the colonic conduit begins with the identification of the ascending right colon. The lateral attachments are taken down up to the hepatic flexure. Then the right colic and middle colic arterial branches are ligated as proximal as possible. The colonic conduit is then taken cephalad and placed in the posterior mediastinum in the same location as the esophagus after esophagectomy. The colonic conduit is completely supplied from the inferior mesenteric artery and the left colic artery with its multiple collaterals. After ensuring adequate blood supply to the entire ascending colon, the colon-esophageal anastomosis is created. Next, the colon is divided, and the colon-stomach anastomosis is created. After this, the cecum is anastomosed to the left colon. Using the colon for an esophageal reconstruction conduit is a technically challenging operation that requires three separate anastomoses. Occasionally, the esophagogastrectomy may be required. In these instances, a Roux-en-Y colon conduit-jejunal anastomosis may be required. This adds another separate jejuno-jejunal anastomosis.

Jejunum Free Flap

The jejunal free flap is one of the best reconstructive options for circumferential defects of the cervical esophagus.[18][28]. The free flap can be based on any one of the jejunal arteries and their concomitant arcades. This flap may be harvested to measure up to 20 cm on a single vessel. As a result of its limit in length, the jejunal free flap is not suitable for subtotal and total esophageal reconstruction, which may require a larger amount of tissue to achieve a functional reconstruction. The jejunal free flap is particularly appropriate for cervical esophageal reconstruction because other methods of reconstruction, such as the gastric pull-up, may reach cephalad regions of the esophagus without significant tension. Relative contraindications to the jejunal free flap include past abdominal surgeries, severely limited cardiovascular and pulmonary function, history of thrombotic events, uncontrolled diabetes, and severe atherosclerosis as identified by a mesenteric angiogram. Careful planning and communication with the oncological surgeon are crucial since the maximum ischemia time for free jejunal flaps is a mere 2-2.5 hours. Fistula rates range from 5% to 18% and are most common in patients who underwent radiation therapy.[29][30][31] On the other hand, the overall flap success rate ranges between 91% and 100%.[30]

Pedicled, Local Flaps: Deltopectoral and Supraclavicular Island Flaps

The deltopectoral and supraclavicular island flaps were the mainstay for the reconstruction of partial pharyngoesophageal defects prior to the widespread use of microsurgical techniques. These flaps are still excellent options for patients who may have definite contraindications to free flap reconstruction, such as occluded donor vessels secondary to atherosclerotic disease, lack of recipient's vessels, and severely impaired cardiopulmonary reserve. The main advantages of these flaps are the fact that they are relatively easy to harvest compared to free flaps, their large arc of rotation, and their robust blood supply.[20][32] The main limitation with these flaps is their reduced reach and decreased surface areas since they are still attached to their blood supply, which makes them less adequate for large, circumferential defects.[33]

Radial Forearm Free Flap

The radial forearm free flap can be used for both partial and circumferential esophageal defects. In partial defects, the radial forearm flap acts can be used as a tissue patch to cover the defect. In circumferential defects, the radial forearm flap can be tubularized to restore the continuity of the esophagus and ultimately achieve adequate deglutition.[21] The radial forearm flap leads to less overall donor site morbidity when compared to the free jejunal flap since it does not require a laparotomy to be harvested. As a result of the decreased morbidity and invasiveness associated with the radial forearm flap, this approach may be best suitable for patients who are elderly, have a history of chronic intestinal disease such as Crohn’s disease, or may have undergone multiple abdominal operations.[34]

Anterolateral Thigh (ALT) Free Flap

The ALT flap can also be used for both partial and circumferential defects of the esophagus. It is based on the lateral descending branch of the circumflex femoral artery and its venous output on a pair of venae comitantes that drain into the profunda femoral vein.[35] The ALT flap may be harvested as a myocutaneous flap including the vastus lateralis muscle, or as a perforator-based fasciocutaneous flap. This flap does entail a split-thickness skin graft to cover the donor site, which leads to higher donor site morbidity. Just like the radial forearm flap, the ALT flap can be tabularized to reconstruct circumferential defects of the esophagus. It is important to acknowledge that tubularization of the radial forearm and ALT flaps requires an additional suture line throughout the entire longitudinal length of the reconstructed esophageal tube. This extra suture line may lead to an increased risk of leakage and increased operative time. Although there is an additional suture line in tabularized ALT flaps, rates of fistula and stricture formation are not significantly higher than jejunal flap reconstructions.[34]

Complications

Esophagectomy with esophageal reconstruction is a large, complex operation. Complications after esophageal reconstruction are common. In a large systematic review with over 17,000 patients after esophagectomy, the overall morbidity was 50.8%, and mortality was 8.7%.[36] The most common complications were pulmonary at 29.9%, followed by gastrointestinal (14.9%), cardiovascular (10.4%), procedure-specific (7.8%), and infection (7.0%). The overall mortality was 8.7%. There was a significant decrease in overall mortality when comparing high volume to low volume centers (5.8% vs. 10.6% (p<0.001)).

Procedure specific complications include anastomotic leak, conduit ischemia, or anastomotic stricture. The incidence of anastomotic leak after esophagectomy varies but is reported around 10%.[37] Cervical anastomosis has a higher percentage of leakage compared to mediastinal anastomoses.[38] In the large STS trial, the leak rate was higher in patients with cervical anastomosis compared with those with intrathoracic anastomosis, 12.3% versus 9.3%, respectively (p = 0.006). This is likely due to the length of the esophageal conduit required for the anastomosis tends to lead to higher rates of ischemia. Once an anastomotic leak is identified, it is critical to make sure the fluid collection is properly drained. If the leak is well-drained, the patient can be observed on broad-spectrum antibiotics, nil per os (NPO), and enteral feeding through a jejunostomy tube. If the patient is properly drained, most leaks will resolve over the course of weeks to months. If the leak does not spontaneously resolve, the standard of care is to place an endoscopic stent.[39]

Patients with large undrained leaks or patients who become septic will likely need reoperation with thoracotomy for repair and drainage of the esophageal leak. If the esophageal conduit has large dehiscence, then the patient will need esophageal resection and diversion with a cervical esophagostomy and jejunostomy.

Conduit ischemia after esophagectomy is reported to be around 10%. Ischemia can be avoided by limiting hypotension and tension on the anastomosis. Ischemia can lead to anastomotic leakage and stricture. Anastomotic strictures occur in roughly 20-25% of patients. These strictures can be safely managed with serial dilation. Most strictures present within the first several months.[40] Late strictures could be concerning for cancer recurrence, and biopsies should be taken. 

When using colonic interpositions for esophageal reconstruction, the most common late complication is colonic redundancy. This leads to mechanical dysfunction of the neo-conduit, causing disabling symptoms that may develop decades after the original surgery. When symptoms caused by food retention in the colonic loop occur, surgical correction may be necessary.[41]

Clinical Significance

Esophageal cancer is increasing worldwide and is currently the 8th most common cancer.[42] In 2018, there were an estimated 17,290 new cases of esophageal cancer with 15,850 dying from the disease in the USA.[43] Due to the severity of esophageal cancer, and the esophageal reconstruction that is required after esophagectomy, all clinicians should be familiar with its management. From primary care doctors to thoracic surgeons, all clinicians should be versed on the intricacies of the esophageal reconstruction as these patients require knowledgeable, prompt care.

Enhancing Healthcare Team Outcomes

Esophageal reconstruction requires a multidisciplinary approach to treatment. Patients will likely be evaluated by several types of doctors, including hospitalists, cardiologists, oncologists, radiation oncologists, thoracic surgeons, general surgeons, and plastic surgeons. Besides physicians, these patients may need to meet with physical therapists, occupational therapists, dietitians, and even psychologists. They will also be cared for by numerous nurses, care managers, and ancillary staff. Every member of the team is required to care for these patients after esophageal reconstruction.