Br. J. Surg. Vol. 66 (1979) 105-109
Chylothorax following resection of the oesophagus K . H. L A M , S . T. K. LIM, JOHN W O N G AND G. B. O N G * SUMMARY
Chylothorax complicating operations on the oesophagus has been reported infrequently; it carries a mortality rate of about 50 per cent. A search of the literature has yielded only 10 cases. This paper reports 4 further cases which occurred among 685 resections of the oesophagus, giving an incidence of O.6per cent. The diagnosis should be confirmed with lyrnphangiography. Treatment should be early exploration and ligation in patients in whom the thoracic duct has been divided at operation. If the duct has been injured during blind dissection a period of conservative treatment is advisable. Parenteral nutrition is a useful adjunctive treatment.
SINCEits description by Bartolet in 1633 chylothorax has been reported as a complication of a large variety of operations. The incidence has risen in the past two decades because of the increase in the number of thoracic operations, and trauma from road accidents. Furthermore, increased awareness of the condition is also likely to contribute to the growing number of reports of this condition. Although operations on the oesophagus have now been carried out for 60 years, it is surprising to note the low incidence of chylothorax resulting from damage to the thoracic duct. A search of the literature revealed only 10 cases. It is the purpose of this paper t o review the literature, report 4 additional cases and discuss the problem of chylothorax in relation to operations on the oesophagus.
Review of the literature Bressler et al. (1953) were the first to report chylothorax complicating oesophageal surgery (Table I ) . Their patient underwent oesophagectomy for carcinoma of the middle third through a left thoracotomy. The chylothorax which complicated the operation was treated with closed chest drainage and the patient survived. Since then there have been only 5 other reports of chylothorax following oesophageal resection (Brewer, 1955; Williams and Burford, 1964; Gingell, 1965; Roy et al., 1967; Rubin et a]., 1977), and one reported series of 152 cases of carcinoma of oesophagus in which chylothorax was reported as a complication (Wu et al., 1955). Altogether 10 cases of chylothorax complicating oesophageal operations were collected from the literature. In only 8 cases was the method of treatment reported, and this included repeated aspiration in 2, chest drainage in 3, iodized talc insufflation in 1 and exploration with ligation of the duct in 2. The outcome of the patients was mentioned in 9 cases-3 succumbed and 6 survived. Case reports Since 1966 we have encountered 4 cases of chylothorax developing following oesophagectomy. Three of these cases were squamous cell carcinoma of the oesophagus, 2 at the middle third and 1 at the upper third. Oesophagectomy was performed in these patients. The fourth case was a squamous cell
carcinoma of the piriform fossa for which pharyngolaryngo-oesophagectomy was performed. Between the years 1966 and 1977 inclusive, 580 resections of the oesophagus for carcinoma were performed and 105 pharyngolaryngo-oesophagectomies for cancer of the hypopharynx or larynx. Therefore, the incidence of chylothorax complicating resection of cancer of the oesophagus was 0.5 per cent and that complicating pharyngolaryngo-oesophagectomy was 0.9 per cent. Altogether for all types of resection, the incidence was 0.6 per cent. Case 1 : B. S. M., a male aged 60, was admitted with a 3-month history of dysphagia. Investigations demonstrated a squamous cell carcinoma of the middle third of the oesophagus. As the patient could not swallow and was emaciated a feeding gastrostomy was created. Three weeks later oesophagectomy was performed through a right thoracotomy approach and, as postoperative radiotherapy was planned, no reconstruction was carried out at this stage. A segment of the thoracic duct adjacent to the tumour was resected (which was our usual practice) and the ends ligated with thread. The cervical oesophagus was brought out as an oesophagostome. The cardia of the stomach was closed with catgut and returned to the abdomen. For the first 5 days after the operation the patient was well and gastrostomy feeding with liquidized food was resumed. On day 6 a sudden gush of milky fluid issued from the right chest drain. A chylothorax was suspected and the presence of fat in the fluid was demonstrated with Sudan 111 stain. Exploration was performed through the previous right thoracotomy incision. Liquidized food was found leaking from the cardiac end of the stomach into the chest. The chest was closed and the abdomen opened. The cardia was trimmed and then closed with two layers of catgut suture. The amount of fluid draining from the right chest decreased for a few days but up to 1000 ml of milky fluid was again collected each day. The drainage fluid was again positive with Sudan 111 stain. Reexploration was carried out through the right chest and extensive adhesions were found. The defect of the thoracic duct was identified alongside the azygos vein and was transfixed. There was extensive oozing from the raw surfaces and the patient went into shock postoperatively. Resuscitation was unsuccessful and the patient died 3 days later. Case 2: L. H., a male aged 66, was admitted to our unit with carcinoma of the middle of the thoracic oesophagus. A LewisTanner operation was performed. As in Case 1, a segment of thoracic duct was resected. Postoperatively the chest drain persistently yielded a large amount of milky fluid, up to 2000ml per day. Chylothorax was confirmed when analysis of the fluid for total lipids showed that the level rose from 2.9 to 4.5 g/1 in 24 h after ingestion of 1OOg of cream. Re-exploration was performed on day 6 and the site of chyle leakage identified and ligated. Although the amount of fluid draining from the right chest decreased, it had become purulent, and Pseirdomonas aeruginosa was cultured from the fluid. The condition of the patient deteriorated and he died 8 days later. Case 3: K . Y . , a male aged 52, was admitted with hoarseness of voice and dysphagia. Endoscopy revealed a tumour arising from the right piriform fossa, extending into the larynx. Preoperative radiotherapy was given. Pharyngolaryngo-oesophagectomy was performed, during which the oesophagus was moblized blindly with thehand through an enlarged oesophageal
* Department of Surgery, University of Hong Kong, Queen Mary Hospital, Hong Kong. Correspondence to: G. B. Ong.
106
K. H. Lam et al.
Table 1 : REPORTED CASES OF CHYLOTHORAX AFTER OESOPHAGEAL SURGERY No. in No. in series series of of No. of chylo- operaNature of Conservative cases thorax tion pathology Operation treatment -Author
Outcome -
Mid 1/3 carcinoma Carcinoma
Oesophagectomy, L thoracotomy Oesophagectomy
Chest drainage
None
1 repeated aspiration
-
Mid 1/3 carcinoma
Oesophagectomy
1
11
Unresectable carcinoma
? Nature
Chest drainage, 50% glucose instillation ? Nature
1 ligation 1 survived (ligation), 1 died (aspiration alone) None 1 survived, 1 died
1
3
1 2
52 14
Lower 1/3 carcinoma Carcinoma
Oesophagectomy, L thoracotomy Oesophagectomy Oesophagectom y
Iodized talc None Survived insufflation ? ? ? 1 thoracocentesis 1 ligation 2 survived
4
-
1
1
2
24
Wu et al. (1955)
2
Williams and Burford (1964) Gingell (1965) Rov et al. (1967) Rubin et al. ' { 1977) Present series (1979)
Bressler et al. (1953) Brewer (1955)
Operative treatment
?
Carcinoma of 1 oesophagectomy, oesophagus: split sternum; 1 upper 1/3, 2 oesophagectomy, 2 mid 1/3, R thoracotomy; 1 carcinoma 1 pharyngolaryngo. of piriform oesophagectomy
1 chest drainage parenteral nutrition
+
None
Survived
Died
3 ligation 1 survived, 3 died
Fig. 1. Case 3. Chest X-ray showing left chylous effusion.
Fig. 2. Case 3. Lymphangiogram showing leakage of thoracic duct.
hiatus of the diaphragm. The mediastinaI pleurae of both sides were opened during blind dissection and therefore chest drains were inserted. Postoperatively there was persistent drainage of more than 1000 ml of milky fluid from the left chest drain each day and chest X-ray showed persistent left pleural effusion (Fig. 1). Chylothorax was suspected and lymphangiography was performed (Fig. 2). Leakage from the upper segment of thoracic duct was demonstrated. As the drainage did not subside, on day 10 a right thoracotomy was
performed and the thoracic duct identified and ligated. The chylous leakage was controlled. However, the patient developed bronchopneumonia and pulmonary oedema, resulting in death 1 week later. Case 4: L. K. T., a male aged 57, was admitted with a 4-month history of dysphagia. Investigation showed a poorly differentiated squamous carcinoma of the oesophagus, at a level of 20 cm from the upper incisor teeth.
Chylothorax following resection of oesophagus
a
107
b
Fig. 3. Case 4. Serial chest X-rays showing development of chylous collection. a, Day 5 , mediastinal :..idow in the upper mediastinum. b, Day 6, mediastinal shadow decreasing in size after discharge of chyle.
well formed
A course of preoperative radiotherapy was given. Subsequently oesophagectomy was performed using the split sternum approach. The tumour-bearing part of the oesophagus was approached above the aortic arch, while the distal segment was freed by blind blunt dissection. For reconstruction the mobilized stomach was delivered to the neck through the posterior mediastinurn and anastomosed to the cervical oesophagus. Postoperatively the patient was well. Only small amounts of fluid were drained from the chest. Daily chest X-ray showed a large opacity appearing gradually at the superior mediastinum (Fig. 3). This was subsequently shown to be a collection of chyle. On the fifth postoperative day serous fluid discharged from the neck wound, and on the next day 1 litre of milky pleural fluid discharged from the left chest drain. Test with Sudan 111 stain showed the presence of lipid. A chylothorax was suspected. Lymphangiography was performed, confirming that the thoracic duct was draining into this collection of chyle at the superior mediastinum (Fig. 4). Parenterai nutrition was commenced because the excessive chest drainage amounted to 1000-2000ml per day. Seven days after the onset of chylothorax the drainage gradually decreased. A repeat lymphangiogram showed no further extravasation. Parenteral feeding was maintained for another week before oral feeding was commenced. Apart from an infected sternal wound there was no other complication. The patient was discharged well after 3 months.
Discussion The thoracic duct is in close relation with the oesophagus along most of its course, particularly in the thorax. It crosses from the right to the left side at the 5th or 6th thoracic vertebra (Van Pernis, 1949). Thus, when the lower thoracic segment is injured, chyle leaks into the right pleural cavity, whereas when the upper segment is damaged a chylothorax occurs on the left side (Ross, 1961). For carcinoma of the middle oesophagus our usual approach for oesophagectomy is through the right chest. A segment of thoracic duct near the tumour was routinely removed and the divided ends ligated with non-absorbable sutures. In Cases 1 and 2 the chylothorax probably resulted from slipping of the lower ligatures so that chyle drained
Fig. 4. Case 4. Lymphangiogram confirming leakage of thoracic duct into mediastinurn.
into the right chest. During pharyngolaryngooesophagectomy for carcinoma of the piriform fossa (Case 3) and oesophagectomy via the split sternum approach (Case 4)the whole or part of the oesophagus was dissected blindly. Considering the proximity of the thoracic duct to the oesophagus and the frailness
108
K. H. Lam et al.
of this and other nearby lymphatic channels it is surprising that chylothorax did not occur more often. In both these cases the upper part of the thoracic duct was damaged, thereby resulting in left-sided chylothorax. Diagnosis of chylothorax is usually suspected when a large milky pleural effusion develops. Support for, but not confirmation of, the diagnosis may be obtained with the detection of high lipid content in the fluid, or a characteristic electrophoretic pattern (Seriff et al., 1977), or the presence of contrast medium in pleural fluid when fed orally (Klepser and Berry, 1954; Kjeldsen and Struve-Christensen, 1974). Roy et al. (1967) have emphasized that not all milky effusions are sequelae of thoracic duct fistulas. We also agree that these tests alone are not adequate for diagnosis of chylothorax, especially in patients who have undergone oesophagectomy, because of the complexity of the operative procedures involving various parts of the gastrointestinal tract. This is illustrated by Case 1, in whom fat-containing liquidized food leaked from the stomach. In another case of carcinoma of the oesophagus which we encountered, lipid-laden discharge issued via the right chest drain after oesophagectomy and stomach reconstruction. The diagnosis of chylothorax was shown to be erroneous when, at exploration, the thoracic duct was found to be intact and leakage from a perforated pyloromyotomy site was demonstrated. In both these cases, standard tests for lipid in the pleural fluid will be positive and any contrast medium given orally or by way of a nasogastric tube will also be recoverable through the chest drain. Thus confirmation of the diagnosis of chylothorax complicating oesophageal surgery should be obtained by lymphangiography, the use of which has previously been described (Heilman and Collins, 1963 ;Nusbaum et al., 1964; Chavez and Conn, 1966; Carnie1 et al., 1971; Diaconis et al., 1976). This was performed in Cases 3 and 4. Lymphangiography not only established the diagnosis, but the site and degree of extravasation were also demonstrable. In addition, repeating the investigation allowed assessment of the progress and assisted in the decision to persevere with conservative treatment (Case 4). The presence of a latent period before appearance of chylous pleural effusion (Garamella, 1958; Steiger et al., 1960; Ross, 1961; Tandon, 1968; Higgins and Mulder, 1971) is illustrated in Case 4. The delay is because of intact mediastinal pleurae holding the chyle in the mediastinum for the initial 3-5 days. On occasions when the amount of chyle is great it gives rise to a large mediastinal shadow before finally rupturing into the pleural cavity. Such an occurrence was mentioned by Bressler et al. (1953) and by Thorne (1958) and emphasized by Higgins and Mulder (1970). However, no chylous collection will develop if the mediastinal pleura has been damaged during operation, as in oesophagectomy via a thoracotomy incision (Cases 1 and 2), or if the pleura has been torn during blind dissection of the oesophagus (Case 3). Goorwitch (1955) has presented a comprehensive review of the trend of treatment of chylothorax from a variety of causes. In 1948 Lampson reported the first successful case of transthoracic ligation of the thoracic duct. Before that time the treatment of chylothorax consisted of thoracocentesis, catheter
drainage, rib resection, cervical ligation and phrenic nerve crushing, with a mortality rate of 45 per cent. Since Lampson’s review, Goorwitch had collected 31 cases, of which 15 were treated with ligation of the duct with no mortality. He concluded that when chylothorax persisted despite adequate thoracocentesis or closed drainage, the thoracic duct should be ligated before the condition of the patient began to deteriorate. Later reports, however, have advocated non-operative treatment. Schmidt (1959) advised conservative therapy because of better progcosis; Maloney and Spencer (1956) advised trial of conservative measures for at least 3-4 weeks before considering surgery; Williams and Burford (1964) concluded that surgical intervention is rarely indicated; Selle et al. (1971) reviewed the indications for surgery in chylothorax and recommended ligation of the thoracic duct when there is daily loss of more than 1500 ml and when this is likely to last more than 14days. When chylothorax results from operations on the oesophagus we agree with the principle advanced by Selle et al. (1971). However, the mechanism of injury has to be taken into account in the selection of cases for operative or conservative treatment. The success of conservative treatment depends on collateral channels opening up, as demonstrated clearly by Chavez and Conn in dogs (1966). When oesophagectomy is performed for middle or lower third tumour through a right or left thoracotomy, the whole posterior mediastinum is usually dissected clean (Cases 1 and 2), so that it is unlikely that sufficient collaterals are left behind to provide drainage of abdominal chyle. A much longer time is needed before more distant channels will open up. Therefore, early operative intervention with religation of the duct should be the treatment of choice. On the other hand. when the oesophagus is mobilized by transabdominal finger dissection close to its wall, adequate collateral lymphatic channels are probably still present which may open up readily. In these cases it is worth while to attempt conservative treatment for a period, if the condition of the patient permits, before resorting to operative intervention. In Cases 3 and 4, the thoracic duct was damaged in this manner. Case 3 required ligation of the duct when drainage alone failed and Case 4 recovered with intercostal drainage alone. Various other methods have been described for the treatment of chylothorax. Of interest is the method of induction of pleurodesis with iodized talc (Gingell, 1965). Among the three successfully treated cases reported by Gingell(1965), one patient had developed chylothorax following oesophagectomy for carcinoma of the lower third. This method may be employed if operation is contraindicated. Anastomosis of the thoracic duct to the azygos or hemiazygos vein (Brewer, 1955) seems unnecessarily complicated when ligation would suffice. Identification at exploration of the site of chylous leakage usually presents no difficulty. However, many methods have been described which assist localization of the site of injury of the duct. These included preoperative administration of cream (Schmidt 1959), nasogastric instillation of methylene blue at operation (Engevik, 1976), subcutaneous injection of normal saline to increase the flow of chyle (Steiger et al., 1960), subcutaneous injection of Evans blue (Merrill, 1955) and filling the thorax with saline during operation to facilitate detection of milky chyle (Elliot,
Chylothorax following resection of oesophagus 1951). These may be attempted if difficulty is encountered at exploration. A useful adjunct in the conservative management of patients with chylothorax is the use of medium chain triglycerides (Lichter et al., 1968; Tamir et al., 1968). The flow of chyle along the thoracic duct can be decreased since these triglycerides are absorbed directly into the bloodstream and do not enter the lymphatic system (Hashim et a]., 1964). It is more effective to stop oral feeding completely and commence total parenteral nutrition (Birt and Connolly, 1952). The use of this method undoubtedly contributed to the success of Case 4 reported in this paper. The mortality of chylothorax complicating oesophageal operations is high (Table I ) . Altogether 6 cases out of 13 with known outcome have died, giving a mortality rate of about 50 per cent. The high rate probably represents complications superadded to an operation which itself carries a mortality rate of 20-30 per cent. References and LEWIS R. v. (1948) Traumatic chylothorax. Ann. Surg. 128, 1056-1078. BARTOLET x. x. (1633) Cited by BOWER (1964). BIRT A B. and CONNOLLY N. Y. (1952) Traumatic chylothorax. A report of a case and a survey of the literature. Br. J. Surg. 39, 564-568. BOWER G . c. (1964) Chylothorax: observations in 20 cases. Dis. Chest 46, 464468. BRESSLER s., WIENER D. and THOMPSON s. A. (1953) Traumatic chylothorax following oesophageal resection. J. Thorac. Surg. 26, 321-324. BREWER L. A. (1955) Surgical management of lesions of the thoracic duct. The technic and indications for retroperitoneal anastomosis of the thoracic duct to the hemiazygos vein. Am. J. Surg. 90, 210-227. CARNIEL M. R., BENNINGHOFF D. L. and ALEXANDER L. L. (1971) Chylous effusions, extravasating lymphographic contrast material, hypoplasia of lymph nodes and lymphocytopenia. Chest 59, 107-110. CHAVEZ c. M. and CONN J . H . (1966) Thoracic duct laceration. Closure under conservative management based on lymphangiography evaluation. J . Thorac. Cardiovasc. Surg. 51, 724-728. DECANCQ H. G. jun. (1965) The treatment of chylothorax in children. Surg. Gynecol. Obstet. 121, 509-512. DIACONIS J . N., WEINER c. I. and WHITE D. w. (1976) Primary subclavian vein thrombosis and bilateral chylothorax documented by lymphography and venography. Radiology 11s. 557-558. ELLIOT A . w. (1954) Traumatic chylothorax. Can. Med. Assoc. J. 70, 71-72. ENGEVIK L. (1976) Traumatic chylothorax. Scand. J. Thorac. Cardiovasc. Surg. 10, 77-78. GARAMELLA J. J. (1958) Chylothorax treated by ligation of thoracic duct and studies in thoracic ductography. Arch. Surg. 76, 46-53. GINCELL J. c. (1965) Treatment of chylothorax by producing pleurodesis using iodized talc. Thorax 20, 261-269. BALDRIDGE R. R .
109
(1955) Traumatic chylothorax and thoracic duct ligation. J. Thorac. Surg. 29, 467479. HASHIM S. A., ROHOLT H. B., BABAYAN V. K. et a]. (1964) Treatment of chyluria and chylothorax with medium-chain triglyceride. N . Engl. J. Med. 270, 756-761. HEILMAN R. D. and COLLINS v. P. (1963) Identification o f laceration of the thoracic duct by lymphangiography. Radiology 81, 470-472. HIGCINS c. R . and MULDER D. G. (1970) Mediastinal chyloma, a roentgenographic sign of chylous fistula. JAMA 211, 1188. HIGGINS c. B. and MULDER D. G . (1971) Chylothorax after surgery for congenital heart disease. J . Thorac. Cardiovasc. Surg. 61, 411-418. KJELDSEN C. S . and STRUVE-CHRISTENSEN E. (1974) Chylothorax. A case report. Scund. J. Thorac. Curdiocusc. Surg. 8, 138-141. KLEPSER R. G . and BERRY I . F. (1954) The diagnosis and surgical management of chylothorax with the aid of lipophilic dyes. Dis. Chest 25, 409426. LAMPSON R. s. (1948) Traumatic chylothorax. J. Thorac. Surg. 17, 778-791. LICHTER I., HILL G . L. and NYE E. R. (1968) The use of mediumchain triglyceride in the treatment of chylothorax in a child. Ann. Thorac. Surg. 5 , 352-355. MALONEY J. v. jun. and SPENCER F. c. (1956) The non-operative treatment of traumatic chylothorax. Surgery 40, 121-128. MERRiLL K. (1955) The use of Evans blue to outline the course of the thoracic duct. J. Thorac. Surg. 29, 555-557. NUSBAUM M., BAUM s., HEDGES R. et al. (1964) Roentgenographic and direct visualisation of thoracic duct. Arch. Surg. 88, 105-113. ROSS I. K. (1961) A review of the surgery of the thoracic duct. Thorax 16, 12-21. ROY P. H., CAN D. T. and SPENCER PAYNE w. (1967) The problem of chylothorax. Mayo Clinic. Proc. 42, 457-467. RUBIN J. w., MOORE H. v. and ELLISON R. G. (1977) Chylothorax: therapeutic alternatives. Am. Surg. 43, 292-297. SCHMIDT A. (1959) Chylothorax. Review of 5 years’ cases in the literature and report of a case. Acta Chir. Scand. 118, 5-12. SELLE I. G., SNYDER w. H. and SCHNEIBER 1. T. (1971) Chylothorax: indications for surgery. Ann. Surg. 177, 245-249. SERIFF N. s., COHEN M. L., SAMUEL P. et a!. (1977) Chylothorax: diagnosis by lipoprotein electrophoresis of serum and pleural fluid. Thorax 32, 98-100. STEIGER Z., WElNBERG M. and FELL E. H. (1960) Postoperative chylothorax. Am. J. Surg. 100, 8-1 1. TAMIR I., HUNTER J . o., FOSBROOKE A. s et al. (1968) Serum and chyle lipids during medium drain triglycerides feeding in a child with chylothorax. Arch. Dis. Child. 43, 302-306. TANDON R. K . (1968) Chylothorax after repair of ventricular septa1 defect. J. Thorac. Cardiooasc. Surg. 56, 378-380. THORNE P. s. (1958) Traumatic chylothorax. Tubercle (Lond.) 39, 29-34, VAN PERNIS P . A. (1949) Variations of the thoracic duct. Surgery 26, 806-809. WILLIAMS K. R. and BURFORD T. H. (1964) The management of chylothorax. Ann. Surg. 160, 131-140. wu Y. K., HOWE Y. L., HUANG K. c. et al. (1955) Surgical treatment of carcinoma of the oesophagus and cardia o f the stomach. Chinese Med. J . 73, 181-195. GOORWITCH J.
Paper accepted 26 July 1978.
Chylothorax following resection of the oesophagus K . H. L A M , S . T. K. LIM, JOHN W O N G AND G. B. O N G * SUMMARY
Chylothorax complicating operations on the oesophagus has been reported infrequently; it carries a mortality rate of about 50 per cent. A search of the literature has yielded only 10 cases. This paper reports 4 further cases which occurred among 685 resections of the oesophagus, giving an incidence of O.6per cent. The diagnosis should be confirmed with lyrnphangiography. Treatment should be early exploration and ligation in patients in whom the thoracic duct has been divided at operation. If the duct has been injured during blind dissection a period of conservative treatment is advisable. Parenteral nutrition is a useful adjunctive treatment.
SINCEits description by Bartolet in 1633 chylothorax has been reported as a complication of a large variety of operations. The incidence has risen in the past two decades because of the increase in the number of thoracic operations, and trauma from road accidents. Furthermore, increased awareness of the condition is also likely to contribute to the growing number of reports of this condition. Although operations on the oesophagus have now been carried out for 60 years, it is surprising to note the low incidence of chylothorax resulting from damage to the thoracic duct. A search of the literature revealed only 10 cases. It is the purpose of this paper t o review the literature, report 4 additional cases and discuss the problem of chylothorax in relation to operations on the oesophagus.
Review of the literature Bressler et al. (1953) were the first to report chylothorax complicating oesophageal surgery (Table I ) . Their patient underwent oesophagectomy for carcinoma of the middle third through a left thoracotomy. The chylothorax which complicated the operation was treated with closed chest drainage and the patient survived. Since then there have been only 5 other reports of chylothorax following oesophageal resection (Brewer, 1955; Williams and Burford, 1964; Gingell, 1965; Roy et al., 1967; Rubin et a]., 1977), and one reported series of 152 cases of carcinoma of oesophagus in which chylothorax was reported as a complication (Wu et al., 1955). Altogether 10 cases of chylothorax complicating oesophageal operations were collected from the literature. In only 8 cases was the method of treatment reported, and this included repeated aspiration in 2, chest drainage in 3, iodized talc insufflation in 1 and exploration with ligation of the duct in 2. The outcome of the patients was mentioned in 9 cases-3 succumbed and 6 survived. Case reports Since 1966 we have encountered 4 cases of chylothorax developing following oesophagectomy. Three of these cases were squamous cell carcinoma of the oesophagus, 2 at the middle third and 1 at the upper third. Oesophagectomy was performed in these patients. The fourth case was a squamous cell
carcinoma of the piriform fossa for which pharyngolaryngo-oesophagectomy was performed. Between the years 1966 and 1977 inclusive, 580 resections of the oesophagus for carcinoma were performed and 105 pharyngolaryngo-oesophagectomies for cancer of the hypopharynx or larynx. Therefore, the incidence of chylothorax complicating resection of cancer of the oesophagus was 0.5 per cent and that complicating pharyngolaryngo-oesophagectomy was 0.9 per cent. Altogether for all types of resection, the incidence was 0.6 per cent. Case 1 : B. S. M., a male aged 60, was admitted with a 3-month history of dysphagia. Investigations demonstrated a squamous cell carcinoma of the middle third of the oesophagus. As the patient could not swallow and was emaciated a feeding gastrostomy was created. Three weeks later oesophagectomy was performed through a right thoracotomy approach and, as postoperative radiotherapy was planned, no reconstruction was carried out at this stage. A segment of the thoracic duct adjacent to the tumour was resected (which was our usual practice) and the ends ligated with thread. The cervical oesophagus was brought out as an oesophagostome. The cardia of the stomach was closed with catgut and returned to the abdomen. For the first 5 days after the operation the patient was well and gastrostomy feeding with liquidized food was resumed. On day 6 a sudden gush of milky fluid issued from the right chest drain. A chylothorax was suspected and the presence of fat in the fluid was demonstrated with Sudan 111 stain. Exploration was performed through the previous right thoracotomy incision. Liquidized food was found leaking from the cardiac end of the stomach into the chest. The chest was closed and the abdomen opened. The cardia was trimmed and then closed with two layers of catgut suture. The amount of fluid draining from the right chest decreased for a few days but up to 1000 ml of milky fluid was again collected each day. The drainage fluid was again positive with Sudan 111 stain. Reexploration was carried out through the right chest and extensive adhesions were found. The defect of the thoracic duct was identified alongside the azygos vein and was transfixed. There was extensive oozing from the raw surfaces and the patient went into shock postoperatively. Resuscitation was unsuccessful and the patient died 3 days later. Case 2: L. H., a male aged 66, was admitted to our unit with carcinoma of the middle of the thoracic oesophagus. A LewisTanner operation was performed. As in Case 1, a segment of thoracic duct was resected. Postoperatively the chest drain persistently yielded a large amount of milky fluid, up to 2000ml per day. Chylothorax was confirmed when analysis of the fluid for total lipids showed that the level rose from 2.9 to 4.5 g/1 in 24 h after ingestion of 1OOg of cream. Re-exploration was performed on day 6 and the site of chyle leakage identified and ligated. Although the amount of fluid draining from the right chest decreased, it had become purulent, and Pseirdomonas aeruginosa was cultured from the fluid. The condition of the patient deteriorated and he died 8 days later. Case 3: K . Y . , a male aged 52, was admitted with hoarseness of voice and dysphagia. Endoscopy revealed a tumour arising from the right piriform fossa, extending into the larynx. Preoperative radiotherapy was given. Pharyngolaryngo-oesophagectomy was performed, during which the oesophagus was moblized blindly with thehand through an enlarged oesophageal
* Department of Surgery, University of Hong Kong, Queen Mary Hospital, Hong Kong. Correspondence to: G. B. Ong.
106
K. H. Lam et al.
Table 1 : REPORTED CASES OF CHYLOTHORAX AFTER OESOPHAGEAL SURGERY No. in No. in series series of of No. of chylo- operaNature of Conservative cases thorax tion pathology Operation treatment -Author
Outcome -
Mid 1/3 carcinoma Carcinoma
Oesophagectomy, L thoracotomy Oesophagectomy
Chest drainage
None
1 repeated aspiration
-
Mid 1/3 carcinoma
Oesophagectomy
1
11
Unresectable carcinoma
? Nature
Chest drainage, 50% glucose instillation ? Nature
1 ligation 1 survived (ligation), 1 died (aspiration alone) None 1 survived, 1 died
1
3
1 2
52 14
Lower 1/3 carcinoma Carcinoma
Oesophagectomy, L thoracotomy Oesophagectomy Oesophagectom y
Iodized talc None Survived insufflation ? ? ? 1 thoracocentesis 1 ligation 2 survived
4
-
1
1
2
24
Wu et al. (1955)
2
Williams and Burford (1964) Gingell (1965) Rov et al. (1967) Rubin et al. ' { 1977) Present series (1979)
Bressler et al. (1953) Brewer (1955)
Operative treatment
?
Carcinoma of 1 oesophagectomy, oesophagus: split sternum; 1 upper 1/3, 2 oesophagectomy, 2 mid 1/3, R thoracotomy; 1 carcinoma 1 pharyngolaryngo. of piriform oesophagectomy
1 chest drainage parenteral nutrition
+
None
Survived
Died
3 ligation 1 survived, 3 died
Fig. 1. Case 3. Chest X-ray showing left chylous effusion.
Fig. 2. Case 3. Lymphangiogram showing leakage of thoracic duct.
hiatus of the diaphragm. The mediastinaI pleurae of both sides were opened during blind dissection and therefore chest drains were inserted. Postoperatively there was persistent drainage of more than 1000 ml of milky fluid from the left chest drain each day and chest X-ray showed persistent left pleural effusion (Fig. 1). Chylothorax was suspected and lymphangiography was performed (Fig. 2). Leakage from the upper segment of thoracic duct was demonstrated. As the drainage did not subside, on day 10 a right thoracotomy was
performed and the thoracic duct identified and ligated. The chylous leakage was controlled. However, the patient developed bronchopneumonia and pulmonary oedema, resulting in death 1 week later. Case 4: L. K. T., a male aged 57, was admitted with a 4-month history of dysphagia. Investigation showed a poorly differentiated squamous carcinoma of the oesophagus, at a level of 20 cm from the upper incisor teeth.
Chylothorax following resection of oesophagus
a
107
b
Fig. 3. Case 4. Serial chest X-rays showing development of chylous collection. a, Day 5 , mediastinal :..idow in the upper mediastinum. b, Day 6, mediastinal shadow decreasing in size after discharge of chyle.
well formed
A course of preoperative radiotherapy was given. Subsequently oesophagectomy was performed using the split sternum approach. The tumour-bearing part of the oesophagus was approached above the aortic arch, while the distal segment was freed by blind blunt dissection. For reconstruction the mobilized stomach was delivered to the neck through the posterior mediastinurn and anastomosed to the cervical oesophagus. Postoperatively the patient was well. Only small amounts of fluid were drained from the chest. Daily chest X-ray showed a large opacity appearing gradually at the superior mediastinum (Fig. 3). This was subsequently shown to be a collection of chyle. On the fifth postoperative day serous fluid discharged from the neck wound, and on the next day 1 litre of milky pleural fluid discharged from the left chest drain. Test with Sudan 111 stain showed the presence of lipid. A chylothorax was suspected. Lymphangiography was performed, confirming that the thoracic duct was draining into this collection of chyle at the superior mediastinum (Fig. 4). Parenterai nutrition was commenced because the excessive chest drainage amounted to 1000-2000ml per day. Seven days after the onset of chylothorax the drainage gradually decreased. A repeat lymphangiogram showed no further extravasation. Parenteral feeding was maintained for another week before oral feeding was commenced. Apart from an infected sternal wound there was no other complication. The patient was discharged well after 3 months.
Discussion The thoracic duct is in close relation with the oesophagus along most of its course, particularly in the thorax. It crosses from the right to the left side at the 5th or 6th thoracic vertebra (Van Pernis, 1949). Thus, when the lower thoracic segment is injured, chyle leaks into the right pleural cavity, whereas when the upper segment is damaged a chylothorax occurs on the left side (Ross, 1961). For carcinoma of the middle oesophagus our usual approach for oesophagectomy is through the right chest. A segment of thoracic duct near the tumour was routinely removed and the divided ends ligated with non-absorbable sutures. In Cases 1 and 2 the chylothorax probably resulted from slipping of the lower ligatures so that chyle drained
Fig. 4. Case 4. Lymphangiogram confirming leakage of thoracic duct into mediastinurn.
into the right chest. During pharyngolaryngooesophagectomy for carcinoma of the piriform fossa (Case 3) and oesophagectomy via the split sternum approach (Case 4)the whole or part of the oesophagus was dissected blindly. Considering the proximity of the thoracic duct to the oesophagus and the frailness
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of this and other nearby lymphatic channels it is surprising that chylothorax did not occur more often. In both these cases the upper part of the thoracic duct was damaged, thereby resulting in left-sided chylothorax. Diagnosis of chylothorax is usually suspected when a large milky pleural effusion develops. Support for, but not confirmation of, the diagnosis may be obtained with the detection of high lipid content in the fluid, or a characteristic electrophoretic pattern (Seriff et al., 1977), or the presence of contrast medium in pleural fluid when fed orally (Klepser and Berry, 1954; Kjeldsen and Struve-Christensen, 1974). Roy et al. (1967) have emphasized that not all milky effusions are sequelae of thoracic duct fistulas. We also agree that these tests alone are not adequate for diagnosis of chylothorax, especially in patients who have undergone oesophagectomy, because of the complexity of the operative procedures involving various parts of the gastrointestinal tract. This is illustrated by Case 1, in whom fat-containing liquidized food leaked from the stomach. In another case of carcinoma of the oesophagus which we encountered, lipid-laden discharge issued via the right chest drain after oesophagectomy and stomach reconstruction. The diagnosis of chylothorax was shown to be erroneous when, at exploration, the thoracic duct was found to be intact and leakage from a perforated pyloromyotomy site was demonstrated. In both these cases, standard tests for lipid in the pleural fluid will be positive and any contrast medium given orally or by way of a nasogastric tube will also be recoverable through the chest drain. Thus confirmation of the diagnosis of chylothorax complicating oesophageal surgery should be obtained by lymphangiography, the use of which has previously been described (Heilman and Collins, 1963 ;Nusbaum et al., 1964; Chavez and Conn, 1966; Carnie1 et al., 1971; Diaconis et al., 1976). This was performed in Cases 3 and 4. Lymphangiography not only established the diagnosis, but the site and degree of extravasation were also demonstrable. In addition, repeating the investigation allowed assessment of the progress and assisted in the decision to persevere with conservative treatment (Case 4). The presence of a latent period before appearance of chylous pleural effusion (Garamella, 1958; Steiger et al., 1960; Ross, 1961; Tandon, 1968; Higgins and Mulder, 1971) is illustrated in Case 4. The delay is because of intact mediastinal pleurae holding the chyle in the mediastinum for the initial 3-5 days. On occasions when the amount of chyle is great it gives rise to a large mediastinal shadow before finally rupturing into the pleural cavity. Such an occurrence was mentioned by Bressler et al. (1953) and by Thorne (1958) and emphasized by Higgins and Mulder (1970). However, no chylous collection will develop if the mediastinal pleura has been damaged during operation, as in oesophagectomy via a thoracotomy incision (Cases 1 and 2), or if the pleura has been torn during blind dissection of the oesophagus (Case 3). Goorwitch (1955) has presented a comprehensive review of the trend of treatment of chylothorax from a variety of causes. In 1948 Lampson reported the first successful case of transthoracic ligation of the thoracic duct. Before that time the treatment of chylothorax consisted of thoracocentesis, catheter
drainage, rib resection, cervical ligation and phrenic nerve crushing, with a mortality rate of 45 per cent. Since Lampson’s review, Goorwitch had collected 31 cases, of which 15 were treated with ligation of the duct with no mortality. He concluded that when chylothorax persisted despite adequate thoracocentesis or closed drainage, the thoracic duct should be ligated before the condition of the patient began to deteriorate. Later reports, however, have advocated non-operative treatment. Schmidt (1959) advised conservative therapy because of better progcosis; Maloney and Spencer (1956) advised trial of conservative measures for at least 3-4 weeks before considering surgery; Williams and Burford (1964) concluded that surgical intervention is rarely indicated; Selle et al. (1971) reviewed the indications for surgery in chylothorax and recommended ligation of the thoracic duct when there is daily loss of more than 1500 ml and when this is likely to last more than 14days. When chylothorax results from operations on the oesophagus we agree with the principle advanced by Selle et al. (1971). However, the mechanism of injury has to be taken into account in the selection of cases for operative or conservative treatment. The success of conservative treatment depends on collateral channels opening up, as demonstrated clearly by Chavez and Conn in dogs (1966). When oesophagectomy is performed for middle or lower third tumour through a right or left thoracotomy, the whole posterior mediastinum is usually dissected clean (Cases 1 and 2), so that it is unlikely that sufficient collaterals are left behind to provide drainage of abdominal chyle. A much longer time is needed before more distant channels will open up. Therefore, early operative intervention with religation of the duct should be the treatment of choice. On the other hand. when the oesophagus is mobilized by transabdominal finger dissection close to its wall, adequate collateral lymphatic channels are probably still present which may open up readily. In these cases it is worth while to attempt conservative treatment for a period, if the condition of the patient permits, before resorting to operative intervention. In Cases 3 and 4, the thoracic duct was damaged in this manner. Case 3 required ligation of the duct when drainage alone failed and Case 4 recovered with intercostal drainage alone. Various other methods have been described for the treatment of chylothorax. Of interest is the method of induction of pleurodesis with iodized talc (Gingell, 1965). Among the three successfully treated cases reported by Gingell(1965), one patient had developed chylothorax following oesophagectomy for carcinoma of the lower third. This method may be employed if operation is contraindicated. Anastomosis of the thoracic duct to the azygos or hemiazygos vein (Brewer, 1955) seems unnecessarily complicated when ligation would suffice. Identification at exploration of the site of chylous leakage usually presents no difficulty. However, many methods have been described which assist localization of the site of injury of the duct. These included preoperative administration of cream (Schmidt 1959), nasogastric instillation of methylene blue at operation (Engevik, 1976), subcutaneous injection of normal saline to increase the flow of chyle (Steiger et al., 1960), subcutaneous injection of Evans blue (Merrill, 1955) and filling the thorax with saline during operation to facilitate detection of milky chyle (Elliot,
Chylothorax following resection of oesophagus 1951). These may be attempted if difficulty is encountered at exploration. A useful adjunct in the conservative management of patients with chylothorax is the use of medium chain triglycerides (Lichter et al., 1968; Tamir et al., 1968). The flow of chyle along the thoracic duct can be decreased since these triglycerides are absorbed directly into the bloodstream and do not enter the lymphatic system (Hashim et a]., 1964). It is more effective to stop oral feeding completely and commence total parenteral nutrition (Birt and Connolly, 1952). The use of this method undoubtedly contributed to the success of Case 4 reported in this paper. The mortality of chylothorax complicating oesophageal operations is high (Table I ) . Altogether 6 cases out of 13 with known outcome have died, giving a mortality rate of about 50 per cent. The high rate probably represents complications superadded to an operation which itself carries a mortality rate of 20-30 per cent. References and LEWIS R. v. (1948) Traumatic chylothorax. Ann. Surg. 128, 1056-1078. BARTOLET x. x. (1633) Cited by BOWER (1964). BIRT A B. and CONNOLLY N. Y. (1952) Traumatic chylothorax. A report of a case and a survey of the literature. Br. J. Surg. 39, 564-568. BOWER G . c. (1964) Chylothorax: observations in 20 cases. Dis. Chest 46, 464468. BRESSLER s., WIENER D. and THOMPSON s. A. (1953) Traumatic chylothorax following oesophageal resection. J. Thorac. Surg. 26, 321-324. BREWER L. A. (1955) Surgical management of lesions of the thoracic duct. The technic and indications for retroperitoneal anastomosis of the thoracic duct to the hemiazygos vein. Am. J. Surg. 90, 210-227. CARNIEL M. R., BENNINGHOFF D. L. and ALEXANDER L. L. (1971) Chylous effusions, extravasating lymphographic contrast material, hypoplasia of lymph nodes and lymphocytopenia. Chest 59, 107-110. CHAVEZ c. M. and CONN J . H . (1966) Thoracic duct laceration. Closure under conservative management based on lymphangiography evaluation. J . Thorac. Cardiovasc. Surg. 51, 724-728. DECANCQ H. G. jun. (1965) The treatment of chylothorax in children. Surg. Gynecol. Obstet. 121, 509-512. DIACONIS J . N., WEINER c. I. and WHITE D. w. (1976) Primary subclavian vein thrombosis and bilateral chylothorax documented by lymphography and venography. Radiology 11s. 557-558. ELLIOT A . w. (1954) Traumatic chylothorax. Can. Med. Assoc. J. 70, 71-72. ENGEVIK L. (1976) Traumatic chylothorax. Scand. J. Thorac. Cardiovasc. Surg. 10, 77-78. GARAMELLA J. J. (1958) Chylothorax treated by ligation of thoracic duct and studies in thoracic ductography. Arch. Surg. 76, 46-53. GINCELL J. c. (1965) Treatment of chylothorax by producing pleurodesis using iodized talc. Thorax 20, 261-269. BALDRIDGE R. R .
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Paper accepted 26 July 1978.
