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Ann Thorac Surg 2002;73:1714-1719
© 2002 The Society of Thoracic Surgeons

Original article: general thoracic

Chylothorax complicating pulmonary resection

Françoise Le Pimpec-Barthes, MDa, Nicola D’Attellis, MDb, Antoine Dujon, MDc, Philippe Legman, MDd, Marc Riquet, MD, PhD*a

a Service de Chirurgie Thoracique, Hôpital Européen Georges Pompidou, Paris, France
b Service d’Anesthésie Réanimation, Hôpital Européen Georges Pompidou, Paris, France
c Unité de Chirurgie Thoracique, Centre Médico-Chirurgical du Cèdre, Boisguillaume, France
d Service de Radiologie, Hôpital Cochin, Paris, France

Accepted for publication February 26, 2002.

* Address reprint requests to Dr Riquet, Service de Chirurgie Thoracique, Hôpital Européen Georges Pompidou, 20 rue Leblanc, 75015 Paris, France
e-mail: marc.riquet{at}hop.egp.ap-hop-paris.fr


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Chylothorax complicating pulmonary resection (CCPR) is infrequent and surgical treatment is for the most part avoided. The purpose of this study is to analyze the clinical and therapeutic characteristics of this complication.

Methods. From March 1981 to June 2001, 26 cases of CCPR (24 men and 2 women; mean age 57 years) were treated in two departments of thoracic surgery. Twenty-five cases complicated lung resection for lung cancer (lobectomy n = 14, bilobectomy n = 3, pneumonectomy n = 8) and 1 case followed lobectomy for a benign lesion. Medical history, location, and characteristics of the chylothorax, lymphography, and clinical evolution after medical or surgical therapy were studied.

Results. Medical history was never predictive of CCPR. Chylothorax was right sided in 18 cases and left sided in 8 cases. The total amount of chyle ranged from 1.9 L to 27.9 L per patient with a mean of 7.9 L (pneumonectomy 12.3 L and lobectomy 6.3 L). In 15 patients (pneumonectomy n = 2 and lobectomy n = 13) mean quantity of daily chyle was 0.3 L. All these patients recovered with conservative therapy except for 2 patients who underwent drainage and talc slurry (n = 1) and video-assisted lysis of adhesions (n = 1). In the remaining 11 patients (pneumonectomy n = 6 and lobectomy n = 5) mean quantity of daily chyle was 1 L. The chylous leak was seen at lymphography (n = 4), during reoperation (n = 2), or at lymphography and reoperation (n = 3). The location was clearly identified at the level of thoracic duct tributaries in all cases. In 4 postlobectomy cases (4 of 7), surgery was not performed because of the therapeutic usefulness of lymphography. Reoperation was necessary in 6 cases (postpneumonectomy n = 5, postlobectomy n = 1) and consisted of duct ligation (n = 2), leak suture (n = 3), and fibrin glue (n = 1).

Conclusions. CCPR is rare and appears to respond well to medical treatment owing to the fact that the thoracic duct is generally patent as the leak is due to injury of its tributaries. When surgery is considered, lymphography may help to select cases in which conservative medical therapy should be continued. However, in a small number of cases, usually after pneumonectomy, surgery remains mandatory.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Chylothorax complicating pulmonary resection have been reported in studies dealing with chylothorax of all etiologies [1–8] or postoperative and traumatic origin [9–17]. Yet treatment of chylothorax may vary according to etiology and more importantly previous surgical procedure in postoperative cases. Accordingly, Cerfolio and colleagues [16] reported reoperation in 86.9% of patients who had undergone an esophageal operation versus 38.5% of patients who had undergone pulmonary resection. Studies dealing with postpulmonary resection chylothorax are few and are either small series with fewer than 9 cases [18, 19] or more frequently case reports [20–30].

In order to understand why chylothorax after pulmonary resection appears as a specific entity and to analyze the need for reoperation in some cases, we reviewed 26 consecutives cases of chylothorax complicating pulmonary resection.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
From March 1981 to June 2001, 52 cases of chylothorax were observed in the departments of thoracic surgery of Laennec–Georges Pompidou Hospital, Paris, and Cedar Center, Boisguillaume, France. They consisted of nontraumatic chylothorax (n = 19), postoperative traumatic chylothorax of miscellaneaous etiology (n = 7), and chylothorax complicating pulmonary resections ([CCPR] n = 26). CCPR cases form the basis of this report. The patients were 2 women and 24 men aged 30 to 79 years (mean 57.5). Twenty-five patients underwent lung resection for a bronchogenic carcinoma (0.65% of 3,834 lung cancers resected over the same period): Squamous cell carcinoma (n = 14), adenocarcinoma (n = 7), large cell carcinoma (n = 2), adenosquamous carcinoma (n = 1), and neuroendocrine large cell carcinoma (n = 1). Surgery consisted of lobectomy (n = 14), bilobectomy (n = 3), and pneumonectomy (n = 8). One patient underwent a lobectomy for a benign lesion, histoplasmosis. All patients except 1 underwent complete mediastinal lymph node dissection (MLND). The lymph nodes were classified according to Mountain [31]. The diagnosis of chylothorax was based on the appearance of a milky pleural effusion with an elevated triglyceride level more than 100 mg/dL (triglycerides 1 mg/100 mL = 0.0113 mmol/L), a lymphocyte count more than 90% of total white blood cell count, and total protein concentration approaching that of plasma. Once the chylothorax confirmed conservative therapy was first attempted. In cases following lobectomy, chest tube drainage was performed in order to insure chylous evacuation and full lung expansion. At full lung expansion suction was not performed in order to avoid an increase in chylous leakage. In cases following pneumonectomy, as the pneumonectomy cavity was not routinely drained, the level of the accumulating fluid within the cavity was controlled by chest roentgenography performed twice on the day of surgery and once daily during the first week. In cases with rapid accumulation and contralateral mediastinal shift the pneumonectomy cavity was evacuated by thoracentensis thus permitting the eventual diagnosis of chylothorax and representing the first stage of treatment. Lipids were suppressed from the diet and replaced by medium chain triglycerides (MCT). Adequate nutrition correcting both electrolyte imbalance and metabolic needs was carefully maintained. Conservative therapy was judged insufficient when chylous loss was 1 L or more per day during the first week or 0.1 L to 1 L daily for the first 2 weeks. Total chylous loss was obtained either by the daily amount of drainage after lobectomy or by calculating the mean quantity of fluid obtained daily by thoracentesis after pneumonectomy. When conservative therapy proved insufficient surgery was considered. A pedal lymphography was then performed in an attempt to visualize the thoracic duct and its tributaries and the location of the chylous leak. The above guidelines remained unchanged over the entire study period.

In all patients medical history, location and side of resected lung, findings on initial pulmonary resection, clinical evolution after conservative treatment, lymphography, and reasons leading to surgical treatment and its results were reviewed. Data obtained were studied in an attempt to clarify the particularity of chylothorax after pulmonary resection, the reasons leading to its responsiveness to conservative therapy, and the causes requiring reoperation.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Medical history of patients included neoadjuvant treatment for nonsmall cell lung carcinoma (n = 4), coronary artery disease (n = 2), liver cirrhosis (n = 1), previous lung tuberculosis (n = 1), and previous laryngeal cancer (n = 1). Resected lung pathology was right sided in 18 cases (upper lobe n = 8, lower lobe n = 7, main bronchus n = 3) and left sided in 8 cases (upper lobe n = 7, lower lobe n = 1). Particular findings and events during lung resection surgery were enlarged lymph nodes, either inflammatory or calcified (n = 7), use of a pleural flap elevated along the thoracic aorta (n = 3), and chylous leak immediately repaired (n = 4). In 1 case reoperation was required for postoperative bleeding.

The total amount of chyle ranged from 1.9 to 27.9 L per patient (mean 7.88 L). Length of drainage ranged from 4 to 19 days (mean 10.5) after lobectomy and the number of thoracenteses ranged from 2 to 9 (mean 4.25) after pneumonectomy. Chyle triglyceride levels ranged from 1.62 mmol/L to 29.7 mmol/L (mean 9.23 mmol/L) and cholesterol levels ranged from 0.77 mmol/L to 6.53 mmol/L (mean 1.86 mmol/L).

Fifteen patients responded to conservative treatment and were discharged. These cases consisted of 13 lobectomies (left n = 3, right n = 10) and 2 pneumonectomies. In 2 patients pulmonary resection followed chemotherapy. Anomaly of mediastinal lymph nodes was grossly apparent in 10 patients (N2 n = 5; enlarged LN n = 2, one due to histoplasmosis; fibrous adenopathy n = 2, asbestosis; and previous tuberculosis n = 1). Duration of chylous leak did not exceed 1 week in 5 patients and 2 weeks in 9 patients. In 1 patient, the chylous leak lasted 18 days but did not exceed 300 mL per day and decreased during the second week and conservative treatment continued until recovery. Two patients were discharged after a chylous leak lasting 10 days after right lobectomy. Both were readmitted for recurrence of pleural effusion. One patient underwent drainage; effusion was mild and talc slurry was performed through the drain leading to complete recovery in 1 week. It is of interest to note that in this patient during the pulmonary resection a chylous leak at the level of the carina had been noticed and sutured. The remaining patient underwent a videothoracocoscopy for deloculation; no chylous leak was visible and the patient recovered rapidly. In this patient, during pulmonary resection a fibrous adenopathy due to asbestosis had been noticed during mediastinal lymph node dissection.

Eleven patients did not respond to conservative therapy and were scheduled for surgery. These cases consisted of 5 lobectomies (right n = 2, left n = 3) and 6 pneumonectomies (right n = 4, left n = 2). In 2 patients surgery followed chemotherapy. Anomaly of mediastinal lymph nodes was grossly apparent in 3 patients (N2 n = 1, enlarged LN n = 1, and previous tuberculosis n = 1).

Seven patients underwent pedal lymphography (Table 1) after pneumonectomy (n = 3) and lobectomy (n = 4). The thoracic duct was opacified in all cases. It appeared patent and the chylous leak was demonstrated at the level of intrathoracic tributaries of the thoracic duct in 6 patients: right paratracheal 4R level (n = 3), peritracheobronchial subcarinal 7 level (n = 2), and lateroaortic 5 level (n = 1). In 1 patient the thoracic duct was interrupted; a chylous leak had been previously sutured at the time of the pulmonary resection (left pneumonectomy). In 4 patients surgery was not required. In 3 of these the chylous leak stopped soon after lymphography, right sided in all cases (level 7 after pneumonectomy n = 1 and level 4R after lobectomy n = 2); and in 1, the lymphatic vessel giving issue to the chylous leak was small (node level 7 after left lobectomy) and total parenteral nutrition was successfully. In 2 cases the leaking collateral (4R after right pneumonectomy and lateroaortic 5 after left lobectomy) was electively sutured with immediate success. In the remaining case (thoracic duct sutured at previous operation) the origin of the chylous leak was not apparent at reoperation, with chylous oozing at the level of the carina and fibrin glue was used. Resolution was not immediate but was obtained secondarily after an unexpected iatrogenic empyema.


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  		Table 1. Lymphographies Performed Before Surgery

 
Three patients underwent surgery without lymphography. In all cases pulmonary resection consisted of a pneumonectomy. The first patient was operated on after neoadjuvant chemotherapy and presented at surgery with a lung cancer invading the esophageal muscle. Injury of the thoracic duct was discovered during surgery and the thoracic duct was sutured. A tension chylothorax rapidly developed and a right thoracotomy was performed. Chyle was seen at the level of the previous thoracic duct ligation and the area was resutured successfully; the patient died of adult respiratory distress syndrome 10 days after pneumonectomy. This was the only reported death in our series. A second patient operated on after neoadjuvant chemotherapy had a chylothorax of 2 weeks’ duration (700 mL per day). A lymphography was not performed owing to the occurrence of simultaneous empyema (Staphylococcus aureus). At reoperation a chylous leak located at the level of the left mediastinal lymph node chain (level 5) was sutured. The pneumonectomy cavity was cleaned and drained and the patient recovered from both affections. The third patient had a chylothorax after a right pneumonectomy. This patient presented with lymph node sequelae from previous pulmonary tuberculosis. The chylous effusion was abundant (14.6 L over a week) leaving little time for lymphangiography. At reoperation the chylous leak was observed at the contralateral 4L level. The thoracic duct was ligated, resulting in immediate cure.

One patient presented with an abundant chylous leak despite its discovery during pulmonary resection (left upper lobectomy) and its immediate suturing. This patient was 73 years old with liver cirrhosis and arteritis. During lobectomy an extrapleural dissection was performed owing to lung cancer invading the posterior portion of the aorta. A postoperative chylous effusion (1.8 L per day) would have prompted reoperation but the poor general status of this patient contraindicated surgery. Strict parenteral nutrition was started on the sixth postoperative day. Somatostatine (6 mg daily) was administrated. Medical treatment was continued over a 9-day period and proved successful. The total loss of chyle was 27.9 L over a 15-day period.

In summary 6 patients underwent reoperation, which consisted of duct ligation (n = 2), suture of leaking collateral (n = 3), and fibrin glue (n = 1). All surgical cases treated by ligation or suture resulted in immediate cure. Surgery was significantly more frequent when pulmonary resection consisted of a pneumonectomy (5 of 8 versus 1 of 18, corrected {chi}2 = 7.162). Grouped information by pulmonary resection is reported in Table 2. The higher frequency of right-sided CCPR was not related to the pulmonary resection performed (right pneumonectomy 6 of 8, right lobectomy 12 of 18; not significant). The need for reoperation was not due to surgical site (left reoperation 3 of 8, right reoperation 3 of 18; not significant).


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  		Table 2. Grouped Information by Pulmonary Resection

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
Medical history of our patients was not predictive of either chylous leak or the influence of its occurrence. In the patient suffering from liver cirrhosis, however, portal hypertension may have played a major role both in the occurrence and severity of the lymphatic leak. In fact spontaneous occurring chylothorax associated with portal hypertension and liver cirrhosis has been reported [32]. It is well known that in patients with liver cirrhosis an increased rate of flow in the lymphatics of the liver and in the thoracic duct is observed [32, 33]. In such cases the thoracic duct distends up to two to three times its normal diameter [33] and if collateral lymphvessel injury occurs backflow of chylous fluid may result in chylothorax. Although this 1 case in our series does not permit definitive conclusions, we believe cirrhotic patients may be at risk of developing chylothorax.

During pulmonary resection all patients except 1 underwent radical MLND for lung cancer surgery. MLND is certainly the main cause for the occurrence of CCPR [9, 19] with the majority of published cases occurring after pulmonary resection for lung cancer. Surgeons must be aware of the possibility of creating a chylous leak by elevation of a pleural flap along the thoracic aorta, however, as described in 1 of our patients. Other surgical lung pathologies complicated by CCPR have been reported but remain anecdotal: aspergilloma [10], tuberculosis [9, 21], granuloma due to Blasmocyces dermatitides [22], and histoplasmosis (1 case of our series). At surgery mediastinal lymph nodes appeared grossly pathologic in half our patients (13 of 26), 6 of these proving to be N2. Altough of interest this cannot be considered as a predictive fator of CCPR after surgery for both the number of patients and the incidence of CCPR complicating lung cancer surgery procedures (0.65%) are small. A greater number of patients presented with gross pathologic LN aspect without the ensuing complication. However, it is likely that the incidence of chylothorax is greater but missed owing to their small size and quick resolution. In order to further decrease the incidence of CCPR we advise clipping the lymphatic vessels to assure lymphostasis when performing MLND. In any case, because of its low incidence, the occurrence of CCPR does not proscribe MLND.

The high frequency of right-sided CCPR in our series (18 versus 8 left sided) although not significant because of the small number is in contradiction with data from the literature. In the literature, of 58 patients with CCPR, 25 cases were located on the right side and 34 on the left side [2–12, 14–15, 17, 19–30]. The majority of these cases were reported because of their clinical severity leading to reoperation (63.8%, n = 37). Although the number of left-sided CCPR was equivalent in the non-reoperated subset (59.46% versus 52.63%) it paradoxically compared well with our own results (50%, n = 3 of 6). Such results raise the question of whether right-sided CCPR are more frequent and better tolerated than left-sided CCPR. The higher frequency of right-sided CCPR may be simply explained by the patients underlying pathology: bronchial carcinomas occur more frequently in the right than in the left lung (ratio of approximately 6 to 4) [34], thus leading to more frequent right-sided MLND. In addition the higher frequency of right-sided lymphatic and chylous leaks may also be explained by anatomy. Lymphatic drainage from the lungs is predominatly along the right side mediastinal lymph node chains for two reasons: first, the right lung is larger than the left; and second, lymph flow to the right paratracheal nodes from the left lung is greater than lymph flow from the right lung to the left paratracheal nodes. This was demonstrated both on cadavers [34, 35] and patients by lymphoscintigraphy [37]. Furthermore MLND is more complete on the right than on the left side. Collaterals of the the thoracic duct lymphatic tributaries are thus more often injuried on the right side and with increased amounts of lymph flow on this side, they are at greater risk of developing valve insufficiency. In fact CCPR is mainly due to injury to the collaterals of the thoracic duct tributaries and is rarely due to injury of the thoracic duct itself, the exception being when decortication on the right side is performed [19] or when extrapleural dissection of the left side is associated. In only 1 case in our series did tumor invade the posterior esophagus, at the level of the thoracic duct, and the CCPR was due to direct injury of the thoracic duct. In all other cases CCPR was due to back flow of chyle into tributaries draining the lymph form the lung directly into the thoracic duct as was observed at lymphography or at reoperation.

The thoracic duct tributaries involved have been well described in an anatomical study [38]. They proved to be responsible for the leak when visualized either during pulmonary resection or by lymphography (Table 1) or at reoperation: mediastinal LN 7 (n = 3), 4R (n = 4), 4L (n = 1), aortic 5 (n = 2); in this latter group 1 was due to pleural flap elevation and upper part of the left mediastinal lymph node chain (also level 5) [38]. In the literature the location of the chylous leak is not always mentioned either because conservative treatment was successful and lymphangiography was not performed [3–5, 9, 11, 12, 14, 20, 21, 24, 28, 30] or because the leak was not identified or not described during reoperation [1, 2, 6, 7, 10, 11, 15, 19] or at lymphography [8, 13, 27] or both [16]. In some instances the location of the leak may be approximated: LN 10 or 4R [21, 24], 7 or 9 [9], 4L or 7 [3, 15]. In other cases the identified locations are in accord with our observations and the anatomical patterns [38], LN 7 (n = 3) [9, 15], 4R (n = 3) [15, 25, 29], 4L (n = 2) [18, 20], aortic arch LN 5 (n = 3) [9, 23], LAMC 5 (n = 1) [26], and also LN 9 (n = 3) [9, 18]. In only 1 case was the leak due to another cause and located at the level of fixation of an intrathoracic parietal drain [15].

Vallieres and colleagues [27] believe that lymphography should be performed as soon as possible after the diagnosis of CCPR. We believe it is sufficient to perform a lymphangiography only when reoperation is planned. In addition to identifying the actual location of the tributaries involved, lymphangiography demonstrates the anatomy of the thoracic duct and its integrity and patency. Furthermore, in 3 of the 7 lymphographies we performed the chylous leak stopped soon thereafter, thus avoiding reoperation (Table 1). If such a result is considered as not necessarily coincidental the explanation may be due to a beneficial effect of the iodine contrast on the laceration itself, provided the laceration is not too large. Lymphangiography may also help determine which patients are likely to respond to conservative measures as was the case in one of our observations (Table 1). In fact thoracic duct patency associated with chylous leaks from small tributaries may justify the continuation of conservative treatment as already suggested [3, 13].

In our series reoperation was performed in only 23% of cases: 5 postpneumonectomy and 1 postlobectomy, that is 62.5% (5 of 8) and 5.6% (1 of 18), respectively. Postpneumonectomy chylothorax is usually poorly tolerated and may lead to tension chylothorax as was observed in 1 of our cases. More frequently rapid reaccumulation of chyle with no tendency toward decreasing output render these patients candidates for surgery. Similar results were reported by Sarsam and coworkers [18] in 4 of 9 postpneumonectomy chylothorax and in several other case reports [23, 24]. On the contrary, chylous effusions after lobectomy appear better tolerated. In these cases the chylous leak is less important and many patients are not reoperated on and therefore probably not submitted for publication. After lobectomy we believe that the remaining lung comes to adhere to the chest wall and mediastinum thus plugging the leak, diminishing its flow, and facilitating closure of the injuried thoracic duct tributary. This of course differs from the postpneumonectomy cavity.

Both in our series and in the literature the majority of surgical procedures performed for CCPR consisted of thoracic duct ligation or, when visible, direct suturing. The thoracic duct being the most important lymph vessel in humans it would appear essential to favor suturing over duct ligation. Recently such procedures have been replaced by less invasive techniques such as clipping under videothoracoscopy [7, 17] or plugging with fibrin glue through a drain [25] or thoracoscope [26]. Fibrin glue was used in 1 of our cases but was not immediately successful, probably owing to underlying sepsis. Otherwise surgical procedures prove generally successfully. In the literature failure of surgery in controlling the chylothorax was reported in 4 cases. Of these, 2 were reoperated on [9] and 2 were successfully treated by conservative management [2, 15]. Complications after surgical treatment of chylothorax are rare. Death after reoperation has been reported by Witz and colleagues [2] and by Chauvin and associates [3] and also occurred in 1 of our patients. The mortality rate including our data and that of the literature observed after CCPR is 4.5% (5 of 110 CCPR).

Other techniques in the management of CCPR have been described such as pleuroperitoneal shunting [6] and percutaneous catherization with thoracic duct embolization [8]. In addition somatostatin has proved useful for the conservative management of chylothorax of other origin [39]. Recently we used somatostatin successfully as an adjuvant in reinforcing the conservative management of our patient presenting with liver cirrhosis. Somatostatin inhibits a wide variety of physiologic regulatory functions in the gastrointestinal tract as well as in the exocrine and endocrine pancreas. It has been used with success in the control of bleeding esophageal varices [40] by reducing hepatic, splanchnic, and portal blood flow. Somatostatin in a randomized animal study proved its effectiveness in the treatment of chylothorax due to thoracic duct injury [41]. It is our opinion that somatostatin could be of benefit in such cases, further decreasing the indications for reoperation.

In conclusion CCPR is rare and for the most part appears well tolerated with appropriate medical treatment. Conservative management should be attempted first and will often prove successful. When leakage is important and prolonged surgery becomes mandatory and it is advisable to perform a lymphangiography. Lymphangiography demonstrating a patent thoracic duct with chylous leaks due to small collateral lacerations after lobectomies permit the continuation of conservative medical treatment. In one fourth of cases, however, mostly occurring after pneumonectomy, surgery is required. The occurrence of new procedures could probably decrease the number of these cases. Finally it appears preferable to suture the injuried collateral tributaries when feasible rather than systematically ligating the thoracic duct itself.[36]


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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