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Chylothorax

Chylous Pleural Effusion

A chylothorax or chyle leak is the accumulation of chyle in the pleural cavity caused by thoracic duct blockage or disruption leading to formation of pleural effusion. It can be genetically inherited or acquired.


Presentation

Chylothorax may show no symptom in patient at the onset of the disease, except in cases where there is large accumulation of the chylous fluid in the pleural cavity. However, the symptoms may develop after several days of the disease development. On the average, the latent period between the disease development and onset of observable symptoms ranges from 7-10 days. The symptom result from  the effect of the mechanical pressure from the accumulated fluid on the lung. The general effects may include; dyspnea (difficulty breathing), tachypnea (abnormal rapid breathing) or other plleural effusion associated symptoms.

Patients with chylothoraces usually present with signs and symptoms, primarily as a result of the pressure from the large pleural fluid accumulation. The patient may observe a progressive onset of exercise intolerance, shortness of breath, general fatigue or tightening in the chest. The pleural cavity contains only sterile chyle therefore, symptoms such as fever and chest pain are rare clinical manifestation [19]. A rare condition termed Chyloptysis, where patient expulsively secrete chylous fluid following formation of a Broncho-pleural fistula has been observed in chylothorax [20]. Rarely, as a result of rapid collection of fluid in the pleural cavity, the patient may show features of tension related chylothorax. This may be a serious development following a pneumonectomy. This feature may include symptoms similar to tension pneumothorax presentations such as rapid hemodynamic or respiratory compromise that may require immediate management. The clinical findings varies depending on the size and position of the pleural effusion. Reduce breathing sounds on auscultation along with faint percussion of the affected part are commonly  seen in patients with chylothorax. Approximately, 78% of cases of patient with chylothorax showed unilateral chylous pleural effusion with high incidence of affected right hemi-thorax (67%) more common than the left side (33%) [21].

Pleural Effusion
  • In October 2008, chest x-ray showed bilateral pleural effusion.[ncbi.nlm.nih.gov]
  • CD45-gated flow cytometry of the pleural effusion showed elevated numbers of CD5- and CD23-positive lymphocytes and a high serum level of soluble interleukin-2 receptor.[ncbi.nlm.nih.gov]
  • Except for the neonatal period, chylothorax is an infrequent finding of pleural effusion in children.[ncbi.nlm.nih.gov]
  • Pleural effusion in chylothorax is typically described as a lymphocytic predominant, exudative type and it is exceedingly rare to encounter a transudative type of chylothorax.[ncbi.nlm.nih.gov]
  • After the lymphangiography, the left pleural effusion drainage immediately decreased. On POD 40, the patient was discharged.[ncbi.nlm.nih.gov]
Dyspnea
  • We treated a 39-year-old woman who presented with progressive dyspnea over 6 months. Chest computed tomography revealed a 12-cm round mass in the right anterior mediastinum.[ncbi.nlm.nih.gov]
  • We treated a young man who was a kidney transplant recipient who had a prior internal jugular vein permanent catheter for hemodialysis, who developed dyspnea and hypoxemia. Chest radiography showed bilateral pleural effusion.[ncbi.nlm.nih.gov]
  • A 28-year old man was admitted to the hospital with exertional dyspnea and dry cough. A chest X-ray showed the large opacity on the left side suggesting to the presence of pleural effusion.[ncbi.nlm.nih.gov]
  • However, the pleural effusion progressed gradually associated with exertional dyspnea and moderate edema of his lower legs. Chest computed tomography showed massive bilateral pleural effusions without evidence of malignancy in 2011.[ncbi.nlm.nih.gov]
  • He presented to our hospital with the main complaint of severe dyspnea.[ncbi.nlm.nih.gov]
Tachypnea
  • Physical examination disclosed generalized lymphadenopathy, skin lesions, abdominal distension, mild tachypnea and a left breast mass.[ncbi.nlm.nih.gov]
  • The general effects may include; dyspnea (difficulty breathing), tachypnea (abnormal rapid breathing) or other plleural effusion associated symptoms.[symptoma.com]
  • Appears dyspnea with tachypnea, tachycardia, hypotension and shock occurs rapidly.[medicaldb.blogspot.com]
Lymphedema
  • Yellow nail syndrome is diagnosed through the triad of intrathoracic findings (30% being pleural effusions), nail discoloration, and lymphedema, with any two features sufficient for diagnosis.[ncbi.nlm.nih.gov]
  • In the pediatric setting, lymphoscintigraphy is used mostly for the evaluation of lymphedema. Only a few cases of chylous anomalies and lymphatic malformations imaged with lymphoscintigraphy have been reported in the literature.[ncbi.nlm.nih.gov]
  • Four of the six patients had skin lymphedema also as a prominent feature. The chylothoraces have been treated by therapeutic pleurocentesis, intercoastal tube drainage and restriction of oral intake.[lungindia.com]
  • , including their proliferation, activation, and cytokine production, or by the inhibition of platelet-derived growth factor receptor-β (PDGFR-β) expressed in pericytes that intervene in angio-lymphangiogenesis. [22] A deficiency of PDGFR-β in human lymphedema[thoracicmedicine.org]
  • Chylothorax in adult age in association with congenital lymphedema. Eur J Respir Dis. 1986;69:285-287. 15. Smeltzer DM, Stickler GB, Fleming RE.[patientcareonline.com]
Recurrent Pleural Effusion
  • Report of a Case A 56-year-old woman was admitted to Georgetown University Hospital on July 9, 1974, for recurrent pleural effusions.[baillement.com]
  • Iodopovidone pleurodesis for recurrent pleural effusions. Chest 2002 ; 122 : 581 –3.[fn.bmj.com]
Low Fever
  • A previously healthy, 52-year-old woman presented with a nine months history of low fever and weight loss ( 30 kg).[ncbi.nlm.nih.gov]
Regurgitation
  • As we thought that the pleural effusion was caused by cardiac dysfunction due to moderate mitral regurgitation and TCAV as well as renal impairment, he was treated with diuretics and digoxin.[ncbi.nlm.nih.gov]
Failure to Thrive
  • An 18-month-old white baby girl with a complex past medical history including choanal atresia, atrioventricular septal defect, failure to thrive, developmental delay, and tracheostomy dependence developed significant hypoxemia and shock following a routine[ncbi.nlm.nih.gov]
Facial Swelling
  • Girl, 7 years old, with chronic facial swelling started after hyperemesis. During examination, she also presented with bilateral pleural effusion, with chylous fluid obtained during thoracentesis.[ncbi.nlm.nih.gov]

Workup

The first line of investigation in diagnosing chylothorax involves analysis of the pleural fluid, coupled with a lymphangiography technique to further aid clinical diagnosis.

The standard in establishing chlothorax diagnosis is by pleural fluid analysis after thoracocentensis. Also, post surgical patient with an invasive tube could be evaluated using thoracostomy output technique. High level of triglyceride in a pleural fluid is indicative of chyle. Therefore, estimation of the level of triglyceride in pleural fluid analysis is very important to establish diagnosis in patient suspected with chylothorax. Triglyceride value following pleural fluid analysis that is highier than 110mg/dl is an absolute indication that the fluid is rich in chyle but a triglyceride value, which is lower than 50 mg/dl is not conclusive (5% probability) of chyle rich fluid. However, if the triglyceride value is between 50-110 mg/dl, lipoprotein analysis is required as a differential test  to determine the content of the pleural fluid (either chylomicron lipoprotein or cholesterol crystals). Also, pleural fluid cholesterol with a ratio value lower than 1 when compared with triglyceride is indicative of chylothorax. Analysis of pleural fluid helps to differentiate the normal chylothorax from the pseudo-chylothorax. For example, the pleural fluid appears milky white in pseudo-chlothorax when compared with the normal chylothorax and the fluid also contains high level cholesterol (value higher than 200 mg/dl) with cholesterol crystals. In pseudo-chylothorax, the triglyceride amount is characteristically and no chylomicrons.

Lymphangiography is another method of establishing diagnosis. The gold standard to establish diagnosis of chylothorax is by demonstrating the leakage of chyle either through direct examination or lymphangiography. However, it is usually a difficult procedure to examine the leakage, when the thoracic movement is not rapid or diffuses even when the fluid characteristically is indicative of chylothorax.
Normal chest X-ray can show the part of the chest with pleural effusion although, it is less important in analyzing the type of effusion and the possible etiology. Specialized imaging technique such as computed tomography (CT) of the chest for including the thorax and abdomen is useful in identifying abnormal lymphadenopathy or the presence of occult mediastinal masses and the location of thoracic duct damage or rupture. Lymphangiography (which is also called lymphoscintigraphy) are usually helpful to determine the leakage site is not imaged by the CT scan. Laboratory investigations such as full blood count, serum electrolytes analysis and serum albumin estimations are required though not for different diagnosis but to determine the patients general health status. In chylothoraces resulting from surgical trauma, both the etiology and the leakage site are usually known depending on the surgical technique. Post-surgical CT scan coupled with lymphangiography or lymphoscintigraphy are sometimes useful to examine and visualize the thoracic duct leakage site. However, it is important to handle this technique with care because the outcome of the diagnosis may influence the condition's prognosis or otherwise therapeutic approach remains controversial [21].

Paracoccidioides Brasiliensis
  • Biopsies of the breast mass, skin and lymph nodes were performed and all of them showed large round yeast cells with multiple narrow-based budding daughter cells, characteristic of Paracoccidioides brasiliensis.[ncbi.nlm.nih.gov]
Pleural Effusion
  • In October 2008, chest x-ray showed bilateral pleural effusion.[ncbi.nlm.nih.gov]
  • CD45-gated flow cytometry of the pleural effusion showed elevated numbers of CD5- and CD23-positive lymphocytes and a high serum level of soluble interleukin-2 receptor.[ncbi.nlm.nih.gov]
  • Except for the neonatal period, chylothorax is an infrequent finding of pleural effusion in children.[ncbi.nlm.nih.gov]
  • Pleural effusion in chylothorax is typically described as a lymphocytic predominant, exudative type and it is exceedingly rare to encounter a transudative type of chylothorax.[ncbi.nlm.nih.gov]
  • After the lymphangiography, the left pleural effusion drainage immediately decreased. On POD 40, the patient was discharged.[ncbi.nlm.nih.gov]

Treatment

There are two major approach in treating chylothorax. They are categorized into: clinical conservative care and surgical methods.

In about 50% cases of affected patients, leakage in thoracic duct resolves spontaneously. As a result, a conservative method is first employed in managing the patient. Gradual recovery from symptoms followed by the decrease in the level of chyle expelled through thoracostomy tube are the main features of this type. By employing the conservative method, the decompression of the pleural cavity using tube thoracostomy or continuous thoracentesis can assist in keeping the lung expanded against the chest wall or mediastinum. These methods are usually used in the early management of effusions of non-traumatic or non-surgical etiology. They are effectively employed in managing outpatients with history of spontaneous reaccumulation of pleural fluid or with mild, acute respiratory symptoms while simultaneously resolving the chyle leak by conservative management. Reduction in intake of fat-rich diet or fasting decreases the rate of chyle flow in the thoracic duct and thereby assist in gradual blockage of the thoracic duct leakages. The pathophysiological mechanism result from the decrease in production of monoglycerides or free fatty acids from the long-chain triglycerides (LCT), which are transported in chylomicrons form into lymph duct of the intestines. Therefore, patient management with total parenteral nutrition (TPN) or oral dietary fat-restriction foods, with supplement of medium-chain triglycerides may help to reduce the level of chyle production thereby preventing its leakage in the thoracic duct. Somatostatin, or its derivative analogue called octreotide, has been succesfully used for treating many pediatric cases with postoperative or iatrogenic chylothorax [14] [16] [17].
Chemoradiation is limitedly used in managing patients with malignant chylothorax but not admitted for invasive surgical procedure.

Surgical intervention is also effectively used in chylothorax treatment. Patients with chylothorax may require surgical intervention if the following indications are observed:

  • Large amount of chyle leakage that is greater than 1 L/d for 5 days or continuous leak of more than 2 weeks following conservative management
  • Observed nutritional and metabolic complications such as electrolyte imbalance with immunosuppression.
  • Presence of abnormal features like loculated chylothorax, polymerized fibrin clots or trapped (unexpandable) lung.
  • Post-esophagectomy chylothorax. Conservative management of this type is indicated wit high mortality rate [22].

Surgical procedure depends on the trauma site and the known etiology resulting in the chylothorax. Thoracic duct ligation is one of the surgical technique used in the condition management. It is a main surgical technique standard in which the thoracic duct is  ligated at the 8th and 12th thoracic vertebrae, at the superior end of the aortic hiatus. This approach is often performed at the right chest, either through an opening in the right thoracotomy or by thoracoscope [23] [24]. Another method is pleuroperitoneal shunt. This can be applied to treat refractory chylothorax but may be complicated due to infection or obstruction. Also, pleurodesis, is usually used in managing malignant chylothorax. It may not be applicable in managing cases of loculated chylothorax or unexpanded (trapped) lung. Pleurectomy is another surgical alternative. Chemical pleurodesis is usually done for patients when there is increase accumulation of chyle after repeated thoracentesis and nutritional control measures. Available alternatives include, bedside procedure involving talc slurry instillation in the pleural cavity, talc insufflation using a video-assisted thoracoscopy, and other types of chemical and mechanical pleurodesis during thoracoscopy or thoracotomy [25] [26] [27]. Other procedures such as pleurovenous, pleuroperitoneal shunting and embolization involving thoracic ducts have been tested in clinical trials for small studies in patients and particularly in failed treatment, with previously described therapeutic techniques.

Prognosis

Chylothorax often occur as a symptom or complication  of an underlying condition or disease. Therefore, the prognosis varies depending on the underlying cause or etiology that result in the disease formation. Improved clinical condition or positive prognosis is anticipated if the underlying or/and associated clinical condition is treatable or can be reversed [18].

Etiology

There are different etiological factor of chylothorax. These can be differentiated into either traumatic or non-traumatic chylothorax.

Nontraumatic Chylothorax 

Malignancy is a major cause of this type. The most common of the malignancy is lymphoma, although there are contradicting report on the effect [11]. Metastatic cancer in the body including chronic lymphocytic leukemia have been associated with chylothorax [11]. Also, diiseases such as tuberculosis, nephrotic syndrome, sclerosis and amyloidosis Other diseases include, sarcoidosis, fibrosis, mediastinitis (acute or chronic), lymphangiectasia and rare Gorham disease may also cause chylothorax [12] [13]. Moreover, the etiology may result from unknown or Idiopathic cause. This is commonly observed among the neonates and sometimes in adult. However, in  5-10 percent cases of idiopathic etiology, there are reported cases of underlying occult neoplasm, which are detected following proper clinical investigations [11] [14].

Traumatic Chylothorax
An injury to the thoracic duct or the tributary may lead to the development of chylothorax [15]. Surgical procedures involving any organ or tissue closely related anatomically to the thoracic duct or the tributaries may  damage them leading to accumulation of chyle in pleural space [16] [17]. Apart from lymphoma, a surgical procedure involving block dissection of the neck accounts for the main cause of chylothorax. Other non-surgical trauma conditions such as thoracic vertebrae fractures resulting into thoracic duct laceration may cause chylothorax

Epidemiology

There is no specific age or gender difference in chylothorax.The global prevalence rate of the condition that develop following surgical therapy for different cardiothoracic conditions ranges from 0.2-1%. Also, there is high mortality and morbidity rates of chylothorax, with an approximate value of 10% are commonly seen reported in major health facilities. Most often, complications occur due to malnutrition and immunosuppression in patients with chylothorax.

Sex distribution
Age distribution

Pathophysiology

Accumulation of the chylous fluid in the pleural cavity due to a damaged or leaking thoracic duct results in the formation of chylothorax. This may lead to acute or chronic distruption in the pulmonary system. In an adult, the volume of the chyle transported in the thoracic duct is estimated to 4L/day.

Prevention

The current preventive approach to control chylothorax formation is designed mainly for postoperative cases because the disease constitutes one of the major devastating complications following esophagectomy in some patients. However, a special intraoperative procedure which involves mass ligation of the thoracic duct in patients that previously undertook transthoracic esophagectomy for malignancy, was shown to be safe, effective, and appropriate preventive measures in managing any risk of postoperative chylothorax formation [28].

Summary

A chylothorax or chyle leak is a condition caused by accumulation of chyle in the pleural cavity due to blockage or disruption of thoracic duct or the tributary thereby causing formation of pleural effusion. This clinical condition due to similarity may be misdiagnosed as cholesterol pleural (chliform) effusion in which there is accumulation of cholesterol in the pleural cavity as a result of pleural inflammation or microbial infection. The color (milky white) of the pleural fluid in both chylotorax and chyliform effusion  appears similar, which account for the misdiagnosis. However, biochemical analysis of chylothorax showed that it contains high level of triglyceride compared to cholesterol pleural effusion which significantly contains high cholesterol level or lecithin-globulin complex.

Generally, both cholesterol and chylothorax effusions are pleural fluids, and are similar in appearance (i.e milky or opalescent in color). However, the pathophysiological development and treatment of these conditions are different. Chylothorax results from the accumulation of lymph fluid in the pleural cavity due to the disruption or blockage of the thoracic duct. Aspirated pleural fluid of Chylothoraces contains high level of chylomicron-triglyceride type except in patient with no dietary fat intake [1] [2] [3] [4]. Cholesterol (pseudochylothorax or chyliform) effusions are pleural effusions, which contains high level of cholesterol. The rate of incidence of chyliform effusion development is lower compared to chylothoraces. It usually occur in patients with  pleural fibrosis or calcification in the pathological process of chronic pleural inflammation [5] [6].

Anatomically, the thoracic duct originates from a sac called cisterna chyli located at the inferior end of the thoracic duct. The intestinal lymphatic trunk along with the two lumbar ones drain into the cisterna chyli . The thoracic duct is positioned the anteriorly to the first and second lumbar vertebra, extending  through the aortic hiatus of the diaphragm into the thorax and the posterior mediastinum. There are wide anatomical variation in the positioning of the duct [7]. The diameter of thoracic duct in this location is 2 -3 mm extending posteriorly to the aortic arch bending over the paired subclavian artery, descends and draining into the venous circulation at the left internal jugular and left subclavian veins.There are anatomical differences in the number and projection of the thoracic duct, therefore it is more susceptible to injury during surgical procedures. Some patient may have two thoracic ducts in the thoracic cavity. However, single thoracic duct may occasionally drain into the venous system especially the right side of the circulation compared to the left. The location of effusion development after an injury depends on the position and extension of the thoracic duct in the mediastinum. An injury that occur at any site lower than the fifth thoracic vertebra usually results into formation chylothorax at the right side of the cavity while an injury above vertebrae will cause effusion development on the left side as a result of the duct extension from right to left [8].

The thoracic duct is filled with a lymphatic fluid called chyle, which originated from the intestine and conducted into the blood.

  • The chyle comprises of triglycerides which exist in the chylomicron form and are produced in the intestine causing the lymphatic fluid to appear milky and opalescent in color. Fasting condition often cause the disappearance of the milky color which rapidly reoccur following an ingestion of fat-rich diet.
  • Chyle is also consisted of lymphocytes (mostly T-lymphocytes) as part of its main cellular compositions, the concentration of which ranges from 400-6,800 cells/μl and are bacteriostatic in nature[8].
  • Also, the electrolytes commonly seen in chyle are identical to the plasma constituents, with a protein concentration that is greater than 3g/dL.
  • Immunoglobulins are found in chyle and contains important fat soluble vitamins that are absorbed in the intestine.

Non-chylous lymphatic fluids from the thoracic tributaries, which drain the site of the pulmonary parenchyma or parietal pleura also finally emptied into the thoracic duct when passing through the mediastinum [9]. This account for the high concentration of total lymphatic flow of about 1,500-2,400ml/day in the thoracic duct [10], the rate of which increases with dietary intake of fat-rich foods, especially those containing long-chain triglycerides.

Patient Information

Chylothorax is a condition caused by the accumulation of chyle (a type of fluid in the lymphatic system that develops from the intestine) in the pleural cavity as a result of damage, disruption or blockage in the thoracic duct. This fluid which are characteristically turbid or milky white in color consists mainly of high triglyceride concentration. It is different from cholesterol pleural effusion, which has similar appearance, but contain high  cholesterol content and accumulated lecithin-globulin complexes that result from either inflammation of pleural cavity or infection. Most often, patients with chylothoraces manifest signs and symptoms that are cloely related to the pleural effusion. In patients with cases of nontraumatic chylothoraces, an acute, mild symptoms such as reduced exercise tolerance, difficult breathing, fatigue and heavy feeling or discomfort in the chest may be observed. Also, rare symptoms like fever and chest pain may be a presentation due to the sterile nature of the chyle in the pleural space and usually does not elicit inflammatory response.

The approach in managing symptomatic chylothorax initiated by nonsurgical episode is often by conservative methods. These include chest tube insertions, maintenance of body fluid and serum electrolyte balance and monitored dietary intake e.g parenteral nutrition. These help in reducing chylomicrons formation and subsequent rate flow of chyle in the thoracic duct. Surgical methods are employed in failed conservative approach and usually depends on the expertise or choice of the surgeon. However, there are varying limited data on the relative outcome of these different surgical interventions in the management of patient.

References

Article

  1. Roy, PH, Carr, DT, Payne, WS. The problem of chylothorax. Mayo Clin Proc 1967; 42:457.
  2. Hillerdal G. Chylothorax and pseudochylothorax. Eur Respir J 1997; 10:1157.
  3. Garcia-Zamalloa A, Ruiz-Irastorza G, Aguayo FJ, Gurrutxaga N. Pseudochylothorax. Report of 2 cases and review of the literature. Medicine (Baltimore) 1999; 78:200.
  4. Agrawal V, Sahn SA. Lipid pleural effusions. Am J Med Sci 2008; 335:16.
  5. COE JE, AIKAWA JK. Cholesterol pleural effusion. Report of 2 cases studied with isotopic techniques and review of the world literature. Arch Intern Med 1961; 108:763.
  6. Hillerdal G. Chyliform (cholesterol) pleural effusion. Chest 1985; 88:426.
  7. Valentine VG, Raffin TA. The management of chylothorax. Chest 1992; 102:586.
  8. Doerr CH, Miller DL, Ryu JH. Chylothorax. Semin Respir Crit Care Med 2001; 22:617.
  9. Weidner WA, Steiner RM. Roentgenographic demonstration of intrapulmonary and pleural lymphatics during lymphangiography. Radiology 1971; 100:533.
  10. Macfarlane JR, Holman CW. Chylothorax. Am Rev Respir Dis 1972; 105:287.
  11. Doerr CH, Allen MS, Nichols FC et-al. Etiology of chylothorax in 203 patients. Mayo Clin. Proc. 2005; 80 (7): 867-70. doi:10.4065/80.7.867.
  12. Jarman PR, Whyte MK, Sabroe I et-al. Sarcoidosis presenting with chylothorax. Thorax. 1995; 50 (12): 1324-5.
  13. Collins J. Case 92: Gorham syndrome. Radiology. 2006; 238 (3): 1066-9.doi:10.1148/radiol.2383032126.
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  16. Ferguson MK, Little AG, Skinner DB. Current concepts in the management of postoperative chylothorax. Ann Thorac Surg 1985; 40:542. 
  17. Terzi A, Furlan G, Magnanelli G, et al. Chylothorax after pleuro-pulmonary surgery: a rare but unavoidable complication. Thorac Cardiovasc Surg 1994; 42:81. 
  18. Ergaz Z, Bar-Oz B, Yatsiv I, Arad I. Congenital chylothorax: clinical course and prognostic significance. Pediatr Pulmonol. 2009 Aug; 44(8):806-11. doi: 10.1002/ppul.21070. 
  19. Prakash, UBS. Chylothorax and pseudochylothorax. Eur Respir Mon 2002; 7:249. 
  20. Lim KG, Rosenow EC 3rd, Staats B, et al. Chyloptysis in adults: presentation, recognition, and differential diagnosis. Chest 2004; 125:336.
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  22. Callari C, Perretta S, Diana M, Dagostino J, Dallemagne B, Marescaux J. Thoracoscopic management of chylothorax after esophagectomy. Surg Endosc. 2011 Nov 15.
  23. Nath DS, Savla J, Khemani RG, Nussbaum DP, Greene CL, Wells WJ. Thoracic duct ligation for persistent chylothorax after pediatric cardiothoracic surgery. Ann Thorac Surg. 2009 Jul. 88(1):246-51; discussion 251-2.
  24. Guo W, Zhao YP, Jiang YG, Niu HJ, Liu XH, Ma Z, et al. Prevention of postoperative chylothorax with thoracic duct ligation during video-assisted thoracoscopic esophagectomy for cancer. Surg Endosc. 2011 Nov 2.
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  28. Lai FC, Chen L, Tu YR, Lin M, Li X. Prevention of chylothorax complicating extensive esophageal resection by mass ligation of thoracic duct: a random control study. Ann Thorac Surg. 2011 Jun; 91(6):1770-4. doi: 10.1016/j.athoracsur.2011.02.070. Epub 2011 May 4.

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Last updated: 2017-08-09 17:41