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Ann Thorac Surg 2005;80:449-454
© 2005 The Society of Thoracic Surgeons


Original article: General thoracic

Incidence and Management of Chyle Leakage After Esophagectomy

Sjoerd M. Lagarde, MD * , Jikke M.T. Omloo, MD, Koen de Jong, MS, Olivier R.C. Busch, MD, Hugo Obertop, MD, J. Jan B. van Lanschot, MD

Department of Surgery, Academic Medical Center at the University of Amsterdam, Amsterdam, the Netherlands

Accepted for publication February 28, 2005.

* Address reprint requests to Dr Lagarde, Department of Surgery, Academic Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, the Netherlands (Email: s.m.lagarde{at}amc.uva.nl).


    Abstract
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Requirements for...
 References
 
BACKGROUND: Postoperative chyle leakage is a rare but well-recognized complication after esophageal surgery. The aim of this study was to identify its incidence and potentially predisposing factors and to assess the consequences and management.

METHODS: A consecutive series of 536 patients who underwent esophagectomy for malignant disease of the esophagus or gastroesophageal junction was reviewed.

RESULTS: There were 20 patients (3.7%) with chyle leakage. After transthoracic esophagectomy the risk for the development of chyle leakage was higher than after transhiatal resection (p = 0.006). Chyle leakage was associated with more positive nodes (p = 0.041). Patients with chyle leakage had significantly more pulmonary complications (p < 0.001) and longer intensive care unit (p = 0.015) and hospital stays (p = 0.001). No patient with chyle leakage died. Conservative management, consisting of no enteral feeding and total parenteral nutrition, was instituted in all patients, but was abandoned in 4 patients (20%) because of persistence of high chyle output through the chest tube. In contrast to patients who were successfully treated with conservative measures, patients who eventually needed a reoperation had a drain output of more than 2 L on the day conservative therapy was started and 1 and 2 days later.

CONCLUSIONS: Chyle leakage is seen more often in patients who undergo transthoracic esophagectomy and in patients who have more positive nodes. Patients with chyle leakage have more pulmonary complications. Conservative therapy is often successful, but operative therapy should be seriously considered in patients with a persistently high daily output of more than 2 L after 2 days of optimal conservative therapy.


    Introduction
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 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
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 References
 
Postoperative chyle leakage is a rare but well-recognized complication after thoracic surgery and is frequently seen after esophageal surgery. It results from injury to the main thoracic duct or its tributaries, which have a close anatomic relationship with the esophagus [1]. Massive drain production is easily recognized as chyle leakage. But also relative small amounts can be attributed to chyle leakage [2] and might reflect secondary damage to the lymphatic collateral system as a result of extensive lymph node dissection.

Chyle is defined as intestinal lymphatic fluid that is enriched with fat (fat-soluble vitamins, chylomicrons, and triglycerides) absorbed from the intestinal lumen giving chyle its milky appearance after enteral feeding. The lymphatic fluid consists of lymphocytes, immunoglobulins, and enzymes [3, 4]. Chyle leakage is a serious complication with a reported mortality rate varying from 0% to 50% [5–8]. Extensive loss or a long duration of chyle leakage can cause losses of calories, fluids, lymphocytes, and albumin. This may lead to immunosuppression, resulting in infection-related complications such as pneumonia and sepsis. Furthermore, chyle leakage can lead to pulmonary dysfunction and pneumonia [4, 9, 10].

Generally, adequate conservative management including total parenteral nutrition and discontinuation of enteral feeding is applied if the diagnosis of chyle leakage is suspected. It has been argued that prolonged conservative treatment should be avoided to prevent associated infectious complications. However, there is no consensus on the timing of performing a reoperation [11–16]. Only one study suggests abandoning conservative management after 5 days if high-volume drainage persists [17]. Because of the low incidence of this complication, large series of patients are not available and the management of chyle leakage complicating esophagectomy remains controversial.

The aim of this study was to identify the incidence, to detect potentially predisposing factors, to assess the consequences, and to review the management of chyle leakage.


    Patients and Methods
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 Patients and Methods
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Between January 1995 and December 2003, a consecutive series of 536 patients underwent esophagectomy for malignant disease of the esophagus or gastroesophageal junction. Operations were performed by or under direct supervision of a surgeon experienced in esophageal surgery (O.R.C.B., H.O., J.J.B.v.L.) in the Academic Medical Center of the University of Amsterdam. Clinicopathologic data from all operated-on patients are permanently collected in a prospective database.

Operations were performed using the transhiatal or transthoracic approach. During transhiatal esophagectomy, the tumor and its adjacent lymph nodes were dissected en bloc. To prevent damage to the thoracic duct, the ventral wall of the thoracic aorta was chosen as the dorsal dissection plane.

During a right-sided transthoracic esophagectomy, selective proximal and distal ligation was performed, and the thoracic duct was resected en bloc with the tumor and adjacent lymph nodes.

In all patients a right-sided chest tube (28F Argyle; Sherwood Medical, St. Louis, MO) was placed and in most patients, also a left-sided drain. Negative pressure was only applied in case of air leakage. In all patients a percutaneous jejunostomy catheter (9F; Fresenius Medical Care, Bad Homburg, Germany) was inserted, and enteral feeding (Impact; Novartis AG, Fremont, MI) was started at a rate of 25 mL/h on postoperative day one, which was gradually increased to 85 mL/h on postoperative day four.

The fluid output from the chest drain(s) was measured on a daily basis. If more than one drain was inserted after the operation, the total amount of pleural effusion was calculated. In general, a drain was removed when the drainage volume fell to less than 100 mL/d.

Chyle leakage was diagnosed if the drain output changed from yellow to milky after start of enteral feeding (or administration of cream) and changed back again to yellow after discontinuation of enteral feeding. The diagnosis was confirmed when the triglyceride concentration in the drain output was greater than 1.2 mmol/L [18]. After the diagnosis of chyle leakage was established, all patients were initially treated conservatively (no enteral intake and total parenteral nutrition). In patients with a low-volume drain output (<500 mL/d) a medium-chain triglyceride diet was started. Volumes of chyle and duration of chest drainage were calculated from the day conservative treatment was started.

There was no strict indication for surgical intervention other than a high-volume drain output for several days, insufficiently responding to conservative therapy.

Patients’ age, sex, operative approach, histology, tumor diameter, TNM stage, lymph node ratio, radicality, and tumor differentiation were evaluated as potential predisposing factors. To assess the impact of chyle leakage on outcome, the incidence of additional complications (atelectasis, pneumonia, pleural empyema, sepsis, wound infections, and atrial fibrillation) and the length of intensive care unit and hospital stay were evaluated.

Statistical analysis was performed using the SPSS package version 12.0 (SPSS Inc, Chicago, IL). To compare categorical data the chi-square or Fisher’s exact test was used. The Mann-Whitney U test was used to compare continuous variables. Two-tailed probabilities were calculated with values of less than 0.05 considered statistically significant.


    Results
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 Abstract
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 Patients and Methods
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Incidence of Chyle Leakage
Chyle leakage occurred in 20 of 536 patients (3.7%) after esophagectomy for malignant disease. Chyle leakage was clinically recognized between the 1st and the 13th postoperative days (mean, 4.7 days). All patients presented with drainage of yellow fluid through the chest tube changing to milky after commencement of enteral feeding or after cream administration through the percutaneous jejunostomy. The median triglyceride concentration was 8.0 mmol/L after a fat challenge (range, 1.3 to 15.9 mmol/L)

Predisposing Factors
Of the 20 patients with chyle leakage, 15 patients were male and 5, female, with a mean age of 62 years (range, 44 to 79 years). After a transthoracic esophagectomy with extended en bloc lymph node dissection, the incidence of chyle leakage was 7% and after transhiatal resection 2% (p = 0.006). Patients with chyle leakage had significantly more positive nodes (resected and identified) and consequently a higher lymph node ratio, defined as the number of positive nodes divided by the total number of lymph nodes resected and identified (p = 0.041 and p = 0.033, respectively). Moreover, a trend was seen toward a more advanced T stage (Table 1).


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Table 1. Clinicopathologic Characteristics of Patients Who Underwent Esophagectomy for Malignant Disease With and Without Chyle Leakage
 
Consequences of Chyle Leakage
Patients with chyle leakage had more pulmonary complications (85%) compared with patients without chyle leakage (42%; p < 0.001), more frequently experienced atelectasis (p < 0.001), and exhibited a trend toward a higher incidence of pneumonia. There were no significant differences in pleural empyema, sepsis, wound infection, and atrial fibrillation (Table 2). Patients with chyle leakage had a significantly longer intensive care unit and hospital stay. No patient with chyle leakage died postoperatively. Hospital mortality was not different (Table 2).


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Table 2. Association Between Chyle Leakage and Additional Complications and Impact on Intensive Care Unit and Hospital Stays and In-Hospital Mortality
 
Management of Chyle Leakage
All patients with chyle leakage were initially managed conservatively with total parenteral nutrition and no enteral intake, resulting in successful resolution of the chyle leak in 16 patients (80%). Conservative management was unsuccessful in 4 patients (20%) after a median of 4 days (range, 3 to 14 days), when high output through the chest tube persisted. Before reoperation, cream was given through the feeding jejunostomy to facilitate perioperative localization of the leak. Three patients underwent a rethoracotomy, and 1 patient had a thoracoscopy. In all 4 patients a clear leak from the thoracic duct was identified, which was subsequently ligated or clipped just above the diaphragm.

Patients successfully treated with conservative therapy lost a total amount of 4.6 L of chyle (range; 0.15 to 25 L) during 9 days of chest drainage compared with 16.1 L (range, 10 to 38 L) in 13 days in patients who underwent reoperation (p = 0.021, p = 0.219, respectively, Table 3, Fig 1). Patients who were treated conservatively or operatively lost a median amount of 480 mL and 1,467 mL per day, respectively (p = 0.007; Fig 2). After reoperation the chest drain(s) could be removed on median day 8 (range, 4 to 11 days), and the median daily volume dropped from 3,123 mL to 272 mL (p = 0.029; Fig 2). Four conservatively treated patients needed chest drainage for more than 14 days. However, the amount of chyle loss per day was not different (p = 0.203). The 4 patients who needed a reoperation had a significantly higher drain output on the day (day 0) conservative therapy was started (p = 0.021) and 1 (p = 0.016) and 2 days (p = 0.003) later, compared with patients treated conservatively (Fig 3, Table 3). All 4 patients had more than 2 L of drain production on the day conservative therapy was started, and conservative treatment did not change median drain output (from 2,753 mL on day 0 to 2,688 mL 2 days later; p = 0.886). Three patients in the conservative group did also have a drain output of more than 2 L on day 0. However, on the second day after commencing conservative treatment the drain output of these patients had dropped to less than 2 L per day.


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Table 3. Daily Amount of Drain Production (in mL) on Day of Commencing Conservative Treatment (day 0), and 1 and 2 Days Later a
 


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Fig 1. Duration of chest drainage calculated from start of conservative therapy until removal of the chest drain. The patients are divided in those successfully treated (boxes) and those who underwent reoperation (reop., stars). Values are given for the total drainage duration, before reoperation, and after reoperation. The filled boxes represent conservatively treated patients who needed chest drainage for more than 14 days. Horizontal lines represent medians.

 


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Fig 2. Volume of chyle loss per day calculated from start of conservative therapy until removal of the chest drain(s). The patients are divided into those successfully treated conservatively (boxes) and those who underwent reoperation (reop., stars). Values are given for the total drainage duration, before reoperation, and after reoperation. The filled boxes represent conservatively treated patients who needed chest drainage for more than 14 days. Horizontal lines represent medians.

 


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Fig 3. Daily drain production after starting (day 0) conservative therapy (total parenteral nutrition and no enteral intake). The patients are divided into those successfully treated conservatively (boxes) and those who underwent reoperation (stars). The filled boxes represent conservatively treated patients who needed chest drainage for more than 14 days. Horizontal lines represent medians.

 

    Comment
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 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Requirements for...
 References
 
The thoracic duct and its lymphatic collateral network can be damaged during esophageal surgery, leading to chyle leakage. This is a rare but well-known complication after esophageal surgery. In this retrospective analysis of prospectively collected data of 536 patients we encountered 20 patients (3.7%) with chyle leakage. This is in line with earlier published series [7–9]. Chyle leakage was associated with more pulmonary complications and longer intensive care unit and hospital stays, but not postoperative mortality.

Chyle leakage was recognized on a mean of 4.7 days after the operation. The diagnosis was probably missed in the early postoperative period because of limited enteral feeding during the first postoperative days prohibiting milky colorization. If chyle leakage was suspected, confirmation was obtained by a triglyceride concentration in the drain output of 1.2 mmol/L or more during enteral fat challenge [18]. Other biochemical tests, such as protein content and the presence of chylomicrons in the drain output, were not performed [19–21].

Massive drain production as done by others was readily recognized as chyle leakage, but in this study 7 patients had milky drain output of less than 1 L of chyle on the day conservative therapy was started. Probably this leakage was not because of damage of the thoracic duct itself, which transports up to 4 L to the venous system daily, but owing to extensive damage of the lymphatic collateral system.

Patients who underwent a transthoracic esophagectomy with extended lymphadenectomy had a higher risk of chyle leakage. Despite intended careful ligation of the thoracic duct in these patients, extended mediastinal lymphadenectomy is most likely associated with more damage to collateral lymphatic vessels as has been reported in pulmonal surgery with lymphadenectomy [22, 23]. Patients with more positive lymph nodes resected had a higher risk of developing chyle leakage. This suggests that the collateral network of lymphatic vessels is more extensive in these patients as a result of obstruction caused by metastatic lymph nodes.

The daily amount of chyle produced contains up to half of the total body protein. The ongoing loss of fluids and proteins further compromises the already malnourished patient with esophageal cancer [24, 25]. Therefore, conservative management of chyle leakage requires nil by mouth and adequate total parenteral nutrition. A medium-chain triglyceride diet is thought to have only a limited role in cases of massive chyle leakage [12, 26]. Octreotide may be valuable as part of the conservative program to treat chyle leakage, but evidence is limited to an animal study and case series [27–31].

Conservative therapy is often successful because the thoracic duct and its tributaries have the ability to be sealed off with time [32]. In the present study, eventually 16 patients (80%) did not need a reexploration, 12 of whom were healed within 11 days. Probably, these patients have had damage to the collateral lymphatic vessels rather than injury to the main thoracic duct.

Chyle leakage leads to a higher rate of (pulmonary) complications with more atelectases and a trend toward more frequent pneumonia. This reflects the seriousness of this complication which until recently was accompanied by substantial in-hospital mortality [5–8]. Therefore, reoperation should not be undertaken too late. Moreover, early reoperation facilitates access to the mediastinum, in the absence of postoperative adhesions. A reoperation for chyle leakage is generally performed through a transthoracic approach. Especially after a transhiatal resection, it is attractive to perform a minimally invasive thoracoscopic reoperation, thus avoiding a formal thoracotomy [33]. Successful supradiaphragmatic duct ligation through a transabdominal approach has also been described [34]. Fatal outcome can be prevented by promptly instituting proper conservative therapy and considering timely reoperation if nonsurgical therapy fails.

In the literature, indications for abandoning conservative treatment are only scarcely described. It is generally advised that persistently high output or continuation of leakage for more than 2 weeks should be avoided and surgical repair should be considered [16]. A specific guideline to abandon conservative therapy after 5 days has been described. A chyle output of less than 10 mL/kg on the fifth day after the onset of leakage reliably predicted the success of continuing nonoperative treatment [17]. On the basis of the data from this study, a treatment strategy for chyle leakage can be proposed, as is depicted in Figure 4.



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Fig 4. Treatment strategy for chyle leakage after esophagectomy. (THE = transhiatal esophagectomy; TPN = total parenteral nutrition; TTE = transthoracic esophagectomy.)

 
In conclusion, chyle leakage is seen more often in patients who undergo a transthoracic esophagectomy and in patients who have more positive nodes resected. Patients with chyle leakage have more pulmonary complications. Conservative therapy is often successful, but operative therapy should be seriously considered in patients with a persistent daily output of more than 2 L after 2 days of optimal conservative therapy.


    Requirements for Recertification/Maintenance of Certification in 2006
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 Requirements for...
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Diplomates of the American Board of Thoracic Surgery who plan to participate in the Recertification/Maintenance of Certification process in 2006 must hold an active medical license and must hold clinical privileges in thoracic surgery. In addition, a valid certificate is an absolute requirement for entrance into the recertification/maintenance of certification process. if your certificate has expired, the only pathway for renewal of a certificate is to take and pass the Part I (written) and the Part II (oral) certifying examinations.

The American Board of Thoracic Surgery will no longer publish the names of individuals who have not recertified in the American Board of Medical Specialties directories. The Diplomate’s name will be published upon successful completion of the recertification/maintenance of certification process.

The CME requirements are 70 Category I credits in either cardiothoracic surgery or general surgery earned during the 2 years prior to application. SESATS and SESAPS are the only self-instructional materials allowed for credit. Category II credits are not allowed. The Physicians Recognition Award for recertifying in general surgery is not allowed in fulfillment of the CME requirements. Interested individuals should refer to the Booklet of Information for a complete description of acceptable CME credits.

Diplomates should maintain a documented list of their major cases performed during the year prior to application for recertification. This practice review should consist of 1 year’s consecutive major operative experiences. If more than 100 cases occur in 1 year, only 100 should be listed.

Candidates for recertification/maintenance of certification will be required to complete all sections of the SESATS self-assessment examination. It is not necessary for candidates to purchase SESATS individually because it will be sent to candidates after their application has been approved.

Diplomates may recertify the year their certificate expires, or if they wish to do so, they may recertify up to two years before it expires. However, the new certificate will be dated 10 years from the date of expiration of their original certificate or most recent recertification certificate. In other words, recertifying early does not alter the 10-year validation.

Recertification/maintenance of certification is also open to Diplomates with an unlimited certificate and will in no way affect the validity of their original certificate.

The deadline for submission of applications for the recertification/maintenance of certification process is May 10 each year. A brochure outlining the rules and requirements for recertification/maintenance of certification in thoracic surgery is available upon request from the American Board of Thoracic Surgery, 633 N St. Clair St, Suite 2320, Chicago, IL 60611; telephone: (312) 202-5900; fax: (312) 202-5960; e-mail: mailto:info{at}abts.org. This booklet is also published on the website: www.abts.org.


    References
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 Abstract
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 Patients and Methods
 Results
 Comment
 Requirements for...
 References
 

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