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Eur J Cardiothorac Surg 1998;14:460-466
© 1998 Elsevier Science NL


Chylothorax following oesophagogastrectomy for malignant disease1

C. Alexiou, M. Watson, D. Beggs, F.D. Salama, W.E. Morgan

Thoracic Surgery Unit, City Hospital, Hucknall Road, Nottingham, NG5 1PB, UK

Received 23 February 1998; received in revised form 10 August 1998; accepted 1 September 1998.

Corresponding author. Tel.: +44 115 9691169; fax: +44 115 8402605; e-mail: dbeggs@ncht.org.uk


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Conclusions
 References
 
Objective: To define the incidence, causes, management and impact of Chylothorax after oesophagogastrectomy for malignant disease in Nottingham Thoracic Surgery unit. Patients and methods: Retrospective analysis of 523 patients with cancer of the oesophagus or the gastro-oesophageal junction who underwent oesophageal resection between January 1987 and November 1997 in a single unit using similar techniques and uniform routine perioperative management. Results: Chylothorax occurred in 21 patients (4.0%). There were 12 males and 9 females with a mean age of 64.7 years (SD 7.5). Age, sex, tumour site, length, histological type, depth of wall penetration, nodal status and type of operative approach were not significant predisposing factors on univariate and multivariate analysis. Seventeen patients were treated conservatively (four deaths, 23.5%) and four surgically (one death, 25.0%), effective control of the chylous leak being achieved in all four cases. Eleven patients with a chylous drainage of up to 2.2 l/day, diminishing within 1 week of conservative treatment had an uneventful recovery. However, a chylous drainage of more than 2.5 l/day in the remaining ten patients was associated with increased morbidity, hospital stay, operative mortality and the need for surgical intervention. In comparison with the remaining patients (n=502), those who developed chylothorax (n=21) had more respiratory complications (42.8%, P=0.008), longer mean hospital stay (23.8 days, P=0.004), higher operative mortality (23.1%, P=0.004) and, unexpectedly, reduced 5 year survival rate (P<0.0001). Conclusions: There appeared to be no clear predisposing factor in the development of a chylous leak other than the routine extensive dissection. Although definitive conclusions can not be drawn, where there is early reduction of the initial amount (in this series up to 2.2 l/day) of drainage, there may be a place for successful non-surgical management; in cases of high output chylothorax, persisting after a few days of conservative treatment, however, early re-operation and ligation of the thoracic duct, seems to be advisable.

Key Words: Oesophagectomy • Chylothorax


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Conclusions
 References
 
Traumatic chylothorax is mainly the result of unrecognised injury to the main thoracic duct or its tributaries during operations within the chest particularly oesophageal resections [1].

Chylothorax following oesphagectomy for malignant diseases is still unusual and there are few relevant studies available. These involve small numbers of patients and report variable results following differing treatment approaches and do not allow conclusions to be drawn as to the best management strategy.

The aim of this analysis was to define the incidence, detect potential predisposing factors, assess the short- and long-term consequences and discuss the management of chylothorax complicating oesophagogastrectomy for carcinoma.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Conclusions
 References
 
A retrospective analysis of 523 patients who underwent oesophagectomy between January 1987 and November 1997 for malignant disease was undertaken. Information was obtained from medical records, the Thoracic Surgery Unit Audit Database and from family doctors where appropriate.

Detailed analysis of these patients, e.g. patient selection, operability, resectability, morbidity, operative mortality and their causes, survival rates etc. has been reported elsewhere [2]. Patient demographic details are shown in Table 1.


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Table 1. Evaluation of potential predisposing factors for development of post-oesophagectomy chylothorax

 
The operations were performed by the same team of three consultant thoracic surgeons using similar operative techniques and uniform routine perioperative management.

Operative technique
Extensive mediastinal dissection was routinely carried out during oesophagectomy and included all perioesophageal tissues with the sub-carinal, paratracheal and parahiatal lymph nodes, both parietal pleurae overlying the oesophagus and the aortic adventitia. In the abdomen the lymph nodes from the left gastric artery pedicle were routinely excised, flush ligation of the left gastric pedicle being achieved by application of a vascular stapler (TLV-30 AutoSuture UK).

Management of chylothorax
The initial management was uniformly conservative directed towards optimising patients' general condition. After the diagnosis of chylothorax was established, patients were kept nil by mouth and total parenteral nutrition was commenced. Intercostal tube drainage was maintained until the leak had ceased and care was taken to ensure good lung expansion. If the initial amount of chylous drainage was not diminishing and the general condition of the patient allowed the conservative management was abandoned and the patient was subjected to repeat thoracotomy through the previous incision and the main thoracic duct ligated.

There was no strict unit policy, however, regarding the time of discontinuation of the conservative and institution of the surgical treatment.

The patients who developed chylothorax were identified and the incidence of this complication defined.

Eight parameters were evaluated as potential predisposing factors: patient age, sex, tumour length, site and histology, pathological T and N stage and type of the operative approach. To assess the impact of chylothorax on the outcome following oesophagectomy, the patients who developed chylothorax (n=21) were compared with those who did not develop this complication (n=502) regarding incidence of additional complications, length of hospital stay, operative mortality and long term survival.

Operative mortality includes all in-hospital deaths plus any death occurring after the patient was discharged from the hospital within 30 days from the operation.

Statistics
The actuarial survival, adjusted for hospital mortality, was calculated using the Kaplan–Meier method. Survival curves were compared with the log-rank test, means with Student's t-test and proportions with the {chi}2-test or Fisher's exact test as appropriate. Multivariate analysis (logistic regression–Cox model) was done to identify significant factors predisposing to the development of chylothorax. A P-value of less than 0.05 was considered significant.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Conclusions
 References
 
Incidence
Chylothorax occurred in 21 patients, giving an incidence of 4.0%. There were 12 male and nine female patients with a mean age of 64.7 years (SD 7.5, range 36–81 years). Their clinico-pathological features are shown in Table 2; their management and early and late outcome are shown in Table 3.


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Table 2. Clinico-pathological features of the patients with post-oesophagectomy chylothorax

 

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Table 3. Management and outcome of the patients with post-oesophagectomy chylothorax

 
Predisposing factors
Although the upper (7.1%) and middle third (7.4%) tumour sites, the positive lymph nodal status (4.9%) and trans-hiatal approach (7.1%) appeared to be associated with a somewhat higher incidence of chylothorax, the differences, owing perhaps to the small number of the patients with this complication, were not statistically significant on univariate and multivariate analysis (Table 1).

Presentation and diagnosis
Chylothorax became clinically apparent between the 2nd and 6th postoperative day in 20 cases (mean 3.2 days, SD 0.9). In one patient however, this occurred on the 23rd day. The diagnosis was suspected by excessive drainage (>1 l/day) of straw coloured fluid through the intercostal drain and confirmed by the change in its character to milky after commencement of enteral feeding and the presence of chylomicrons on biochemical analysis of the pleural fluid.

In four cases the diagnosis of chylothorax coincided with or complicated a severe chest infection. In all other cases this was the first or the only postoperative complication to be diagnosed.

The mean duration of chylous drainage was 16.5 days (SD 5.5, range 6–36) with a mean volume of 2.3 l/day (SD 0.6, range 1–3.3 l/day).

Conservative management
Seventeen patients (81%) were treated conservatively. There were four deaths (mortality 23.5%). Three patients had a stormy postoperative course characterised by the early onset of acute respiratory tract infection and high output chylous fistula and they succumbed to their complications. In one patient chylothorax complicated on the 23rd postoperative day the already existing severe bronchopneumonia from which he eventually died 21 days later.

Two patients had prolonged (28 and 36 days) high output (up to 2.8 and 2.9 l/day) chylous fistula and their condition was complicated by a chest infection resulting in prolonged hospital stay even after the chylous leak had stopped.

The remaining 11 patients made an uneventful recovery following 7–20 days (mean 14.7 days, SD 3.8) of chylous drainage of an initial amount of 1–2.2 l/day (mean 1.7 l/day, SD 0.4) and they were discharged 2–4 days after the chylous leak had stopped (mean 2.4, SD 0.5) (Table 3).

Surgical management
Four patients were treated surgically (19.0%) after they had a failed initial conservative treatment and were considered fit for a re-operation. In all four cases a repeat thoracotomy was performed and the chylothorax was controlled by ligation of the main thoracic duct following 17–22 days (mean 20, SD 1.5) of 2.9 to 3.3 l/day (mean 3.1 l/day, SD 0.1) of chylous drainage. Three patients were discharged from the hospital 6–9 days after re-operation making an uneventful recovery but one patient developed ARDS and died 4 days later (mortality 25.0%) (Table 3).

Impact of chylothorax
The patients with chylothorax (n=21) had significantly more respiratory complications (42.8%, P=0.008), a longer hospital stay (mean 23.4 days, P=0.004) and higher mortality (23.1%, P=0.004) than those (n=502) who did not develop this complication (Table 4).


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Table 4. Impact of chylothorax

 
Unexpectedly, the patients with chylothorax had also a shorter median survival time (13 months) and none of this group survived longer than 26 months (Table 3) after the operation while the remaining patients had an overall 5-year survival (adjusted for postoperative mortality) of 25.8%, P<0.0001 (Table 4).


    Discussion
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Conclusions
 References
 
Chylothorax can occur after any type of operation within the chest, however the close anatomical relationship of the thoracic duct with the oesophagus makes its inadvertent injury more likely during oesophageal resections.

Cerfolio et al. [1] described 47 cases of chylothorax amongst 11 315 patients who underwent various general thoracic operations (0.4%) with an incidence about 0.3% following lung resection and 2.9% following oesophagectomy.

Various incidences of chylothorax following oesophageal resections ranging from 0 to about 4.0% have been reported from other institutions (Table 5). The 4.0% rate in our series is attributed to the radical mediastinal dissection carried out routinely. Similar rates of chylothorax have been reported from other centres employing similar techniques during oesophagectomy for malignant disease [3].


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Table 5. Reported incidence of chylothorax following oesophageal resection, type of management and mortality (in chronological order in which they have been reported)

 
Bolger et al. [4] found a significantly increased rate of chylothorax following the trans-hiatal approach and Dougenis et al. [3] reported a significant decrease in the incidence of post-oesophagectomy chylous fistula in patients who had prophylactic ligation of the thoracic duct intraoperatively.

None of the eight factors assessed in these series, including the type of operation, (Table 1) emerged as a significant predisposing factor.

Chylothorax in the fasting post-oesophagectomy patient presents typically with increased intercostal drainage, straw coloured or blood stained and needs to be differentiated from other causes of pleural effusions. A cholesterol/triglyceride ratio of less than 1, triglyceride concentration of more than 100 mg/dl and the presence of chylomicrons are all characteristic of a chylous pleural effusion. Fat globules in chyle stain with Sudan III and administration of cream with a lipophylic dye (green No. 6, Evans Blue) through the nasogastric tube should result in staining of a chylous effusion [5]. Lymphangiography may demonstrate the site and size of the leak [6] and may be of value in differentiating between thoracic duct damage and anastomotic leaks. However this may not be a simple investigation to perform in a postoperative patient and its use for diagnostic purposes is infrequent. Clinical confirmation after resuming oral feeding is obtained by the change of the pleural effusion to the milky, forming layers on standing. The diagnosis in our patients was based on the presence of chylomicrons in the pleural fluid and on clinical grounds.

The thoracic duct transports up to 4 litres of chyle daily in a healthy adult [7] which is rich in lipids and proteins and contains lymphocytes (particularly the T-subclass), immunoglobulins, vitamins and electrolytes. Prolonged loss of chyle and its accumulation within the pleural cavity may have therefore serious local, metabolic and immunological effects [8].

Chylothorax may compress the lung, cause mediastinal shift and provoke hypovolaemia, hypoprotenaemia, hypocalcaemia, acidosis or other metabolic abnormalities [7]. Immunological changes include a reduction in plasma antibody levels and T cells and an altered state of immune response [9] which renders the often malnourished and debilitated patient with oesophageal cancer vulnerable to viral and bacterial infections [10] [11].

The chest infection rate observed in our patients (42.8%) was indeed significantly higher than in those without chylothorax and the consequences serious (Table 3Table 4).

The avoidance of a chylous leak in patients undergoing oesophageal resection for malignant disease is highly desirable but the optimal management is not certain.

Some authors recommend early surgical intervention in all cases of post-oesophagectomy chylothorax [1] [12] while others suggest discontinuation of conservative management if daily chylous drainage exceeds 1.5 l of chyle per day for more than 4 days, if drainage persists for more than 2 weeks or if there is daily loss of more than 1.5 l/day likely to last more than 2 weeks [13] [14].

Different institutions have reported variable results following differing types of management of post-oesophagectomy chylothorax (Table 5).

Bolger et al. [4] reported a mortality of 46.0% in their series of 11 patients with no significant difference between conservative and surgical management. Lam et al. [15] quoted a mortality of 75.0% in their series of four patients, all three deaths having occurred in the patients who received surgical treatment. Dougenis et al. [3] reported an overall mortality of 20.0% in 10 patients in whom chylous fistula was treated mainly surgically. Cerfolio et al. [1] reported a low 3.7% mortality in their series of 27 chylothoraces, 23 of whom have been treated surgically while Orringer et al. [12] had no mortality in a series of 11 patients following trans-hiatal oesophagectomies who were treated aggressively with early surgical intervention and ligation of the thoracic duct through a transthoracic approach (Table 5).

The 23.8% mortality in our series compares favourably with that reported from Lam et al. [15] and Bolger et al. [4], is similar to that reported by Dougenis et al. [3] but is considerably higher from the figures quoted by Cerfolio et al. [1] and Orringer et al. [12].

Although an early re-operation with control of the chylous leak is likely to shorten hospital stay and reduce morbidity and operative mortality rates, surgery can be difficult and some patients are not fit for an early re-operation. If the diminution of the chylous drainage can be anticipated it seems logical to try to avoid a repeat thoracotomy with its associated morbidity.

In our series a diminishing amount of chylous drainage of up to 2.2 l/day ceased after 7–20 days of conservative management in 11 patients who went on to make a completely uneventful recovery.

However, chylous drainage of more than 2.5 l daily, in the remaining ten patients, was associated with the need for re-operation, chest infection with prolonged hospitalization or death (Table 3).

The anatomy of the thoracic duct varies considerably and lymphangiography before attempting its ligation at re-operation has been suggested [1], [16]. This useful, but somewhat complex investigation, was not performed in any of our four patients who had prolonged, high output chylous leak and the site of the source of the leak was readily seen.

Intra-operative identification of the thoracic duct may be facilitated by various methods including the administration of cream shortly before the operation [17], nasogastric instillation of methylene blue at operation, [18] and subcutaneous injection of normal saline to increase flow of chyle [19].

Recently the use of an upper abdominal incision to ligate the main thoracic duct just above the cisterna chyli has been described [16]. In this report there were five patients with various causes of chylous fistula, one of them following oesophagectomy. This approach was successful in controlling the chylous leak in four out of five cases and it was suggested that it would be particularly but not solely applicable to cases of post-operative chylothorax [16].

Other treatments for chylothorax including induction of pleurodesis with iodized talc, tetracycline or fibrin glue, pleurectomy and use of pleuroperitoneal shunts have been reported with variable success rates [20] [21] [22] [23] [24] and they seem to have a place in the setting of intractable recurrent chylothorax or when surgery is contraindicated.


    Conclusions
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Conclusions
 References
 
This study did not show any significant predisposing factor for the development of chylothorax following oesophageal resection for malignant disease, the 4.0% incidence of which is attributed to the surgical technique employed involving extensive mediastinal resection.

We feel the initial management of a patient shown to have a chylous leak includes early institution of total parenteral nutrition and optimisation of the patients' general condition before considering a surgical or conservative management, paying particular care to ensure adequate intercostal drainage and lung expansion.

The question of the optimal timing for a surgical inervention in cases of a persisting chylothorax complicating oesophagectomy for malignant disease cannot be answered with certainty and it may well have to be tailored to the individual patient.

Nevertheless, we suggest that where the initial amount of chylous drainage (up to 2.2 l/day in our series) diminishes within a few days of conservative treatment, these patients may be well managed without resorting to an early re-operation.

High output chylothoraces, however, with no signs of reduction of the daily amount of drainage within a week of conservative treatment should be managed, where possible, with surgical intervention if protracted hospital stay and increased morbidity and operative mortality rates are to be avoided.


    Acknowledgments
 
The authors wish to thank Mrs Lynda Beggs, Thoracic Surgery Audit Officer, for without her continuous help the completion of this work would have been impossible.


    Footnotes
 
Presented at the 6th International Thoracic Surgery Congress, 14–17 May 1998, Prague, Czech Republic. Back


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Conclusions
 References
 

  1. Cerfolio R.J., Allen S.A., Deschamps C., Trastek V.F., Pairolero P.C. Postoperative chylothorax. J Thorac Cardiovasc Surg 1996;112:1361-1366.[Abstract/Free Full Text]
  2. Alexiou, C., Beggs, D., Salama, F.D., Brackenbury, E.T., Morgan, W.E. Surgery for oesophageal cancer in the elderly: the view from Nottingham. J Thorac Cardiovasc Surg 1998; in press.
  3. Dougenis D., Walker W.S., Cameron E.W.J., Walbaum P.R. Management of chylothorax complicating extensive esophageal resection. Surg Gynaecol Obstet 1992;174:501-506.
  4. Bolger C., Walsh T.N., Tanner W.A., Keeling P., Hennessy T.P.J. Chylothorax after oesophagectomy. Br J Surg 1991;78:587-588.[Medline]
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  6. Sachs P.B., Zelch M.B., Rice T.W., Geisinger M.A., Risius B., Lammert G.K. Diagnosis and localization of laceration of the thoracic duct: usefulness of lymphangiography and CT. Am J Roentgenol 1991;157:703-705.[Abstract/Free Full Text]
  7. Paes M.L., Powell H. Chylothorax: an update. Br J Hosp Med 1994;51:482-490.[Medline]
  8. Merrigan B.A., Winter D.C., O'Sullivan G.C. Chylothorax. Br J Surg 1997;84:15-20.[Medline]
  9. Machleder H.I., Paulus H. Clinical and immunological alterations observed in patients undergoing long term thoracic duct drainage. Surgery 1978;84:157-165.[Medline]
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  12. Orringer M.B., Bluett M., Deeb G.M. Aggressive management of chylothorax complicating transhiatal esophagectomy without thoracotomy. Surgery 1988;104:720-726.[Medline]
  13. Taba L., Dedhia H.V., Bowen R., Alexander J.C. Chylothorax review. Crit Care Med 1985;13:49-52.[Medline]
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