Chylothorax results from the leakage of chyle from the thoracic duct or one of its lymphatic branches into the pleural space. Common causes include neoplasm and iatrogenic injury. Life-threatening metabolic derangements may occur if chylothorax is not recognized and treated promptly. Numerous maneuvers can be undertaken as part of a conservative approach to treating chylothorax, but surgical intervention is usually the most effective method of achieving definitive results.

ANATOMY AND PHYSIOLOGY

The thoracic duct was first described in humans by Veslingus in 1634. The first successful thoracic duct ligation was performed by Lampson in 1948 for a traumatic chylothorax.¹ Before this time, chylothorax was treated conservatively and associated with a mortality rate of almost 50%. An accurate understanding of the anatomic course of the thoracic duct and common sites of variant anatomy can help to minimize iatrogenic chylothorax and ensure successful surgical intervention through direct repair or mass ligation.

The thoracic duct is a continuation of the cisterna chyli as it passes from the abdomen into the thorax (Fig. 113-1). There are many variations in the course and number of divisions of the thoracic duct. In most individuals, the thoracic duct starts at the cisterna chyli and enters the chest through the aortic hiatus, coursing behind the esophagus between the aorta and azygos vein. The duct runs cephalad in the right hemithorax along the spinal column. At the level of the fifth or sixth thoracic vertebra, the duct crosses to the left hemithorax and continues cephalad along the left side of the esophagus into the superior mediastinum behind the aortic arch and posterior to the left subclavian artery. The duct terminates at the angle formed by the left internal jugular and left subclavian veins, where it drains into the venous system. Of surgical importance is the consistency in location and paucity of branching of the thoracic duct between the cisterna chyli and the level of the eighth vertebral body in the lower right hemithorax.

Chyle is a milky fluid that consists primarily of proteins, triglycerides, and lymphocytes. Under normal conditions, the thoracic duct transports up to 4 L of chyle per day. Factors that influence flow rate include diet, drug intake, intestinal function, and physical mobility. The flow of chyle is maintained by changes in intraabdominal and intrathoracic pressure along with intrinsic alterations in the muscular tone of the thoracic duct.² Valves irregularly spaced throughout the system assist in unidirectional circulation. Although valves may be present throughout the thoracic duct, there is one valve constant in location that lies within 1 cm of the lymphaticovenous junction (see Fig. 113-1, inset A). Drainage of chyle into the rapidly flowing venous system can be explained by the Bernoulli effect, the law governing the behavior of a fluid as it passes from a region of low pressure to a region of high pressure.

Most of the fluid that composes chyle comes from the gastrointestinal tract and liver. It contains high concentrations of digestive products as well as lymphocytes and immunoglobulins.² Between 60% and 70% of dietary fat is absorbed via the lymphatic system in the form of chylomicrons. Short- and medium-chain fatty acids (i.e., <10 carbon atoms in length) are taken in directly via the portal system. The absorption of dietary fat gives chyle its milky-white color. This explains the high concentration of triglycerides in chyle relative to plasma. Lymphocytes make up 95% of the cellular component of chyle (90% are T-lymphocytes), whereas the concentrations of electrolytes, antibodies, and enzymes approximate those of plasma.³ Loss of these constituents as a result of injury to the thoracic duct can be quite debilitating from both a nutritional and an immunologic standpoint.

ETIOLOGY OF CHYLOTHORAX

Congenital chylothorax is the most common cause of pleural effusion in the newborn. The condition may result from lymphovascular malformations, complete thoracic duct atresia, or trauma during birth. In the adult, the principal causes of chylothorax are trauma or iatrogenic injury, followed by obstruction or disruption secondary to a neoplastic process. Penetrating injuries to the neck, chest, or abdomen may result in direct ductal damage, whereas blunt trauma may create increased wall tension and distention injury as a result of crushing blows or spinal column hyperextension (Table 113-1).

Iatrogenic injuries occur four times more frequently than blunt or penetrating trauma.⁴ These injuries are more common after esophagectomy but also may be associated with neck dissections, lung resection, aortic surgery, and removal of mediastinal tumors.⁵ Postoperative injuries include transection, resection, tangential laceration, and tears of lateral ductal branches. Injury to the thoracic duct also may occur after interventions such as left-sided central line insertion, translumbar angiography, and sclerotherapy for esophageal varices.

Malignant ductal obstruction can arise secondary to an intrinsic disease such as intraluminal involvement from neoplastic cells or from extrinsic compression. Seventy percent of malignant duct leaks occur in association with lymphoma.⁴

DIAGNOSIS OF CHYLOTHORAX

Chylothorax is a rare event, with exception of the 5-8% incidence of chylothorax associated with esophagectomy. By comparison, the incidence of chylothorax after lung resection is only about 0.5%.⁶ The diagnosis of chylothorax is rarely expected or obvious and requires a healthy index of suspicion (Table 113-2). After esophagectomy, chest tube output approaching or exceeding 1 L/day immediately should raise suspicion of a chyle leak, although high chest tube output simply may be the result of extensive operation, postoperative oozing, and volume overload in the immediate postesophagectomy period. Alternatively, a clear fluid may masquerade as chyle in an unfed patient. For the patient presenting with chylothorax in the nonpostoperative state, shortness of breath or an abnormal chest radiograph will be the presenting symptom or sign, and a number of clinical tests are helpful in making the diagnosis.

Pleural fluid analysis is an aid to diagnosis. A sampling of pleural fluid should be sent for Gram stain, protein and triglyceride determinations, and cell count with differential. Chylothorax is suspected immediately if the fluid is white but absent neutrophils and bacteria on Gram stain.

The triglyceride level may be even more helpful as a diagnostic aid. A high triglyceride concentration (>110 mg/dL) has a high specificity for chyle leak, whereas concentrations of less than 50 mg/dL are less than 5% likely to be due to a chyle leak. A cholesterol:triglyceride ratio of less than 1 is diagnostic of chyle.⁷ Many consider a lymphocyte count of greater than 90% to be equally diagnostic. The presence of chylomicrons in pleural fluid is diagnostic for chyle; however, electrophoresis is necessary to establish their presence. The diagnosis can be confounded if the patient has been fasting or is on an elemental diet. In the proper clinical setting, a fatty-food bolus (e.g., heavy cream) and subsequent increase in chest tube output also can be diagnostic of chylothorax.

Lymphangiography can confirm a chylothorax as well as identify the site of the leak. This type of localization study can prove useful in planning an operative approach for repair. Lymphangiography can demonstrate accessory ducts and the course of the main duct and has been successful in locating the leak in over 80% of patients.⁶ Lymphangiography was once performed by injecting radiographic oil into the dorsum of the foot, which sometimes resulted in lymphangitis. More recently, the study is performed with technetium-labeled sulfur colloid, although localization of the site of leak with this technique is less precise. In most cases, lymphangiography is not needed for diagnosis or planning of surgical repair.

PREOPERATIVE ASSESSMENT AND DECISION-MAKING

A large, prolonged chyle leak can have several adverse effects. Patients are often already malnourished and/or immunosuppressed as a result of prior surgery or illness. In the presence of a chyle leak, the nutritional and immunologic status of the patient is further compromised. Not only is there a significant loss of fluid and electrolytes (at times, greater than 1.5 L/day), but also a significant number of T-lymphocytes can be lost through the drainage of chyle fluid, resulting in lymphopenia and immunosuppression. Finally, there is depletion of nutritional stores through loss of fats and protein. Accumulation of chyle in the pleural cavity can quickly cause compression of underlying lung, respiratory compromise, and even tension chylothorax. The first priority in managing these patients is adequate drainage of chyle from the thorax, reexpansion of the lung, and assurance of pleural apposition. This is usually best accomplished through placement of a posteriorly directed chest tube of 24F caliber or larger. Replacement of IV fluids and electrolytes is begun. Drainage of chyle should drop significantly with cessation of oral intake; total parenteral nutrition should be instituted immediately if this route is chosen.

Noninterventional Management

We prefer the term noninterventional over conservative because this method of management for large leaks in debilitated patients carries significant risk. Observation is considered optimal management for leaks of low or moderate output (<500 mL/day) in patients who are not severely malnourished. Once the fluid is drained adequately, it is important to have accurate measurements of daily chest tube drainage. Fluids and electrolytes must be checked and replaced. The patient is given nothing by mouth, and total parenteral nutrition is instituted. Alternatively, the patient may be maintained on a very low-fat diet with oral medium-chain triglyceride supplementation. However, any oral intake at all, even without dietary fat, is a stimulus to chyle production. After 1-2 weeks, provided the drainage decreases to less than 200 mL/day, an oral low-fat diet may be instituted. If the drainage remains low, the chest tube may be removed. If the drainage persists without feedings or increases with institution of low-fat feedings, intervention is recommended.

Intervention

Chyle leaks of greater than 500 mL/day are less likely to heal without intervention. (Some surgeons may use a cutoff value of 1 L.) While observation is an option, if the output is not decreased significantly in 7 days, operative intervention should be considered. In the postesophagectomy patient, however, intervention is mandated as soon as a leak is diagnosed because it is usually high output, the patient is already malnourished and debilitated, and the leak can be fixed readily through intervention.⁸

The operative approach involves either direct repair of the leak or right-sided mass ligation of the thoracic duct just above the aortic hiatus. We favor mass ligation of the duct for patients who have had a prior thoracotomy, when the leak is difficult to localize, and to avoid potential injury of adjacent structures. More explicitly, this approach avoids the necessity of reopening a preexisting thoracotomy or dissecting around the site of previous aortic surgery, and for neck dissections, potential injury to nearby vital structures such as the phrenic nerve or subclavian vessels is obviated. Right-sided mass ligation of the thoracic duct above the diaphragmatic hiatus can be used to treat a leak in any location.

Alternatively, a direct repair can be attempted, with incision made in the right or left chest or neck (if secondary to prior neck surgery or dissection). Usually this repair is performed by using a limited, muscle-sparing thoracotomy because localization of the leak and ligation of the tiny structure with fine sutures are difficult with a purely thoracoscopic approach. Intraoperative enteral administration of cream can be very helpful in locating the leak.

More recently, thoracic duct embolization for leak or rupture in the cisterna chyli has been described by means of percutaneous cannulation.⁹ This therapy is currently investigational but seems to be effective in the majority of patients with favorable thoracic duct anatomy. A single, large duct in the upper abdomen is necessary to perform the procedure, and the anatomy is predetermined by MRI. The duct is cannulated percutaneously, and the catheter is threaded up the thoracic duct under fluoroscopic guidance. The leak is located, and coils are injected into the duct. Postembolization injections are performed to verify cessation of the leak. For a detailed description of this technique, see Chap. 111.

Chyle leaks associated with mediastinal lymphoma or neoplasia metastatic to the mediastinum can be difficult to manage. Effective treatment of the underlying malignancy, if possible, with radiation or chemotherapy, often will cause the leak to stop. In instances where the malignancy responds poorly to chemoradiation, numerous interventions have been attempted, including percutaneous embolization of the duct. Ligation or direct repair of the duct may be difficult or impossible owing to the burden of disease. Insertion of a tunneled subcutaneous valved pleuroperitoneal shunt may allow for evacuation of the pleural space and reabsorption in the peritoneum. However, the patient must pump the catheter manually throughout the day. Pleurodesis, either chemical or by complete pleurectomy, is usually the last and least favored option but may stop the leak through obliteration of the pleural space.

TECHNIQUE

Thoracic Duct Leak Repair

A direct repair can be considered when the leak has been clearly identified. The site of the leak may be determined preoperatively by placement of right- or left-sided thoracostomy tubes or by the appearance of a milky-white drainage from a neck incision. The traditional approach for a leak in the pleural cavity is a muscle-sparing posterolateral thoracotomy. If the patient has had a recent thoracotomy, the prior incision is reopened. On the right side, the course of the duct is inspected between the aorta and azygos vein along the spine (Fig. 113-2). The duct crosses into the left chest at the level of the fifth or sixth vertebral body.

Before incision, up to 1 L or more of heavy cream is administered enterally. A limited posterolateral thoracotomy is performed, sparing the serratus muscle. The chest is entered through the fifth interspace, although for leaks localized to the upper chest a fourth interspace incision can be used. Alternatively, a sixth or seventh interspace incision can be used for leaks localized to the lower chest. Magnifying loops may be helpful in identifying the thoracic duct and the site of leak. A search is conducted along the predicted course of the duct. If the leak is not found, further inspection of all midline operative sites is performed (i.e., sites of mediastinal nodal dissection, aortic surgery, etc.) The easiest, most secure method of repair is to use a pledgeted fine suture (i.e., 4-0 polypropylene). If a large duct has been interrupted, clips to either side of the duct may be applied, although this method may be less secure than direct suture ligation. The site of repair should be observed before and after repair for several minutes to ensure cessation of the chyle leak. A tissue sealant also can be used in conjunction with repair or ligation but should not be relied on as the sole treatment.

Thoracoscopy is sometimes used to identify the site of leak and to guide the location of a minithoracotomy utility port (Fig. 113-3). A 5-mm camera can be inserted in the midaxillary line at approximately the seventh interspace. An additional 10-mm port is placed in the anterior axillary line at approximately the fifth or sixth interspace, and a grasping instrument is used to draw the lung forward. Alternatively, a fan retractor can be used. If the leak is not found, an additional posterior port can be placed behind and inferior to the tip of the scapula and the camera moved to this location. A figure-of-eight heavy silk stitch can be placed in the central tendon near the esophageal hiatus and passed out through the 5-mm port to retract the diaphragm inferiorly and expose the course of the thoracic duct near the diaphragm. Again, direct repair (other than clipping) of a fine thoracic duct can be difficult when following a purely thoracoscopic approach, and a minithoracotomy [i.e., video-assisted thoracic surgery (VATS)] incision placed directly over the leak can simplify the repair.

Mass Ligation of Duct

Mass ligation of the duct can be performed by thoracotomy, VATS, or even entirely by a thoracoscopic approach. In this region, between the diaphragmatic hiatus and the point where the thoracic duct passes over the spine to the left chest, the path of the duct is consistent in nearly all patients, even though the duct itself may have a plexiform configuration (see Fig. 113-1, inset C). A serratus-sparing sixth interspace thoracotomy incision is made, and the lung is retracted forward. The diaphragm is retracted inferiorly. The esophagus, or neoesophagus, is retracted anteriorly. Just above the aortic hiatus, the course of the thoracic duct can be visualized between the aorta and azygos vein overlying the spine. The pleura is incised over the edge of the aorta and over the edge of the spine. Several techniques may be used. A large, blunt right-angle clamp is passed under the duct alongside the aorta, onto the surface of the spine, and out again medial to the azygos vein, and a large suture (e.g., 0 silk) is tied around the tissues (Fig. 113-4). Alternatively, a size 0 stitch or a smaller pledgeted stitch could be used to encompass all the tissues between the aorta and azygos vein along the spine. Rarely, the suture or ligature may tear through the duct, creating a new leak. Hence the ligation should be inspected carefully for several minutes to verify the integrity of the repair. In addition, the area of original leak should be inspected to ensure that it has fully sealed (especially if it was repaired by means of mass ligation as opposed to the direct suture technique).

VATS mass ligation can be performed as described for repair, with the utility incision placed at approximately the eighth interspace, centered over the posterior axillary line. Suture ligation or passage of a large tie around the ductal area can be performed as described earlier. All fibrinous debris should be removed from the chest, and if there is any fibrin peel on the lung, it must be removed before closure to ensure complete lung reexpansion. Posteriorly directed drainage tube(s) should be placed.

Postoperative Care

Properly placed thoracostomy drainage tubes are important for continued control of chest drainage and pleural apposition. In theory, fatty foods should not interfere with the patient's recovery once the ductal injury has been controlled, and the diet can be advanced as tolerated. If there is concern regarding the effectiveness of the repair, it may be prudent to keep the patient on a low-fat oral diet and/or with elemental tube feedings. Total parenteral nutrition should be discontinued when the patient is able to achieve full oral intake. The chest tube drainage amount and character should be recorded and monitored closely. The chest tubes can be removed when the drainage is clear and less than 200 mL/day after resumption of a full-fat diet. Chest radiography should be followed to rule out residual effusion not controlled by thoracostomy drainage.

PROCEDURE-SPECIFIC COMPLICATIONS

Failure to Identify or Inadequate Repair of Chyle Leak

Intraoperative administration of enteral cream is an invaluable method of increasing the rate of chyle production, visualizing the leak intraoperatively, and verifying cessation of the leak. Direct closure of the frail injured duct probably is accomplished most reliably with fine suture (e.g., 4-0 polypropylene) with pledgets. Adjacent tissue is incorporated into the pledgets to compress and seal the duct. Alternatively, if a single, large duct is seen, clips can be used above and below the site of tear. The risk of failure may be somewhat increased with simple clipping because collaterals with other lymph ducts or with the azygos vein may be present.

Injury to Adjacent Structures

Approaching a duct repair via mass ligation may be useful when one wishes to avoid a duct leak that lies adjacent to a phrenic nerve injury or to a prior surgical site (e.g., aortic repair or replacement).

SUMMARY

A thoracic duct leak can be a life-threatening condition because it often occurs in a malnourished patient recovering from a major illness or surgery. Drainage of the pleural space, reexpansion of the underlying lung, and quantification of the leak are important first steps. Small leaks (typically <500 mL/day) may be given a trial of observation with diet modification or cessation of oral intake and parenteral hyperalimentation. Postesophagectomy leaks and large-volume leaks (>1000 mL/day) almost always require surgical correction. Observation of these leaks for greater than 7 days can have adverse effects on patient outcome.

CASE HISTORIES

Case 1

A 61-year-old man with stage III (T₃N₁M₀) adenocarcinoma of the esophagus underwent esophagectomy after neoadjuvant chemoradiation. A three-incision technique was used for the esophageal resection, including a radical lymphadenectomy and prophylactic thoracic duct ligation. The chest tube drainage persisted after a normal postoperative swallow evaluation and with advancement to a full-liquid diet plus supplemental tube feeds. Despite a dietary restriction of clear liquids and elemental tube feedings, the drainage from the chest tube remained elevated at 800-1200 mL/day during the second week of postoperative care. Since the patient was not responding to conservative measures, there was concern that he was in jeopardy of nutritional compromise. Therefore, the patient was evaluated and treated by the interventional radiology team with a percutaneous thoracic duct embolization. A preprocedure MRI revealed suitable anatomy for the percutaneous approach. After a lymphangiogram via a lower extremity cutdown, the cisternal chyli was identified and cannulated. The duct was embolized successfully with coils and embolic agent glue. The chest tube was removed several days later, after the patient was back on a full-liquid oral diet plus standard supplemental tube feeds and producing minimal output from the chest tube.

Case 2

A 46-year-old man with tonsillar squamous cell carcinoma underwent resection and left modified radical neck dissection after induction chemotherapy coupled with combined chemoradiation. During dissection in the deep cervical fibrofatty plane, a prominent lymphatic structure representing the thoracic duct was identified and doubly ligated. No active drainage was noted before closure despite provocative Valsalva maneuvers. In the subsequent postoperative period, the neck drainage became milky in color, yielding 900 mL/day. The patient underwent duct ligation by a thoracoscopic approach on the right side. The duct was clearly visible as it coursed through the tissues between the azygos vein and the aorta and crossed over the mediastinum into the left chest at the level of the subcarinal lymph nodes. Clips were used to ligate the duct, which resulted in evidence for proximal dilatation and distal decompression consistent with successful ligation. The chest drain was removed 2 days later with the patient on a full diet.

Case 3

A 59-year-old man with adenocarcinoma of the esophagus underwent esophagectomy after neoadjuvant chemoradiation. The resection was done using a three-incision technique and prophylactic thoracic duct ligation. However, after the operation, chylous drainage was noted with an output of up to 2 L/day. The patient was taken back to the OR for exploration. Two areas were in question for the source of chyle leak, one around the lymph node dissection at the level of the azygocaval junction and the other over the hiatus. The tissue around both areas was ligated with polypropylene sutures and covered with a fibrin sealant (Tisseel, Baxter International, Inc., Biosurgery Division, Deerfield, IL). Additionally, a pleurectomy was done to ensure good apposition of the lung to the chest wall for obliteration of the pleural space. The chest tube was removed 3 days later with the patient on a full diet with minimal drainage.

EDITOR'S COMMENT

There is an important practical distinction between surgically induced and tumor-related chylothoraces. Both etiologies can produce identical clinical presentation, fluid chemistries, and cell composition; however, surgical injury to the thoracic duct usually occurs in the setting of an unobstructed lymphatic system. In contrast, tumor-related chylothoraces—typically, a consequence of lymphoma—occur as a result of an obstructed lymphatic system and pose a far more difficult management problem.

–SJM

REFERENCES