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Ann Thorac Surg 2000;70:418-422
© 2000 The Society of Thoracic Surgeons


Original articles: general thoracic

Thoracoscopic esophageal mobilization for pharyngolaryngoesophagectomy

Simon Y.K. Law, FACSa, Manson Fok, FRCSa, William I. Wei, FACSb, Lai Kun Lam, FRACSb, Peter H.M. Tung, FRCSa, Kent-Man Chu, FRCSa, John Wong, FACSa

a Divisions of Division of Esophageal Surgery, University of Hong Kong Medical Centre, Queen Mary Hospital, Hong Kong, China
b Division of Head and Neck Surgery, Department of Surgery, University of Hong Kong Medical Centre, Queen Mary Hospital, Hong Kong, China

Address reprint requests to Dr Wong, Department of Surgery, University of Hong Kong Medical Centre, Queen Mary Hospital, 102 Pokfulam Rd, Hong Kong
e-mail: jwong{at}hku.hk


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. Pharyngolaryngoesophagectomy (PLE) for hypopharyngeal cancers and tumors of the cervical esophagus is a procedure of significant morbidity and mortality. Conventional esophageal mobilization is performed with the transhiatal dissection technique. Thoracoscopic esophageal mobilization is tested as an alternative to determine whether surgical outcome can be improved.

Methods. From 1994 to 1998, thoracoscopic mobilization was carried out in 30 consecutive patients who underwent PLE (PLE-TS). This was compared to a historical cohort of 30 patients who had PLE with transhiatal mobilization (PLE-TH).

Results. In PLE-TS, thoracoscopic esophageal mobilization was successful in 28 patients (93%). Median blood loss was 700 mL (range, 164 to 3,000 mL) compared to 1,000 mL (range, 400 to 2,200 mL) in group PLE-TH, p = 0.21. Thoracoscopy time was 90 minutes (range, 60 to 180 minutes). Total operating time were 392 minutes (range, 180 to 570 minutes) and 300 minutes (range, 150 to 550 minutes) in PLE-TS and PLE-TH, respectively (p = 0.03). Major pulmonary complications occurred in 7 (23%) and 8 (27%) patients in PLE-TS and PLE-TH, respectively (p = 0.77). Cardiac complications occurred in 7 (23%) and 5 (17%) patients in PLE-TS and PLE-TH, respectively (p = 0.52). Thirty-day mortality rates were 3.3% and 10% (p = 0.6) and hospital mortality rates were 13% and 17%, (p = 1.0).

Conclusions. Thoracoscopy was safe and feasible. Morbidity and mortality after PLE was not significantly reduced. The theoretical advantage offered by thoracoscopy may be offset by the lengthened time of one-lung anesthesia.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Minimal access surgery has gained wider applications in recent years and these new techniques have also been applied to cancer surgery. Conventional esophageal resection as part of the operation of pharyngolaryngoesophagectomy (PLE) for hypopharyngeal or cervical esophageal cancers entails transhiatal mobilization of the esophagus. This is mostly a "blind" procedure. Complications from bleeding, tracheobronchial damage, thoracic duct injury, and cardiac compression can occur. It is hypothesized that thoracoscopic esophageal mobilization will offer theoretical advantages of allowing mediastinal dissection to be performed under direct visual control, thus preventing intraoperative problems like uncontrolled bleeding, and damage to important adjacent structures. Cardiac compression by the surgeon’s hand is also avoided. The reduction in mediastinal trauma may also enhance postoperative recovery. This study is a prospective evaluation of our experience with 30 consecutive patients, who underwent PLE with this technique.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
During the period July 1994 to May 1998, 30 consecutive patients underwent PLE with thoracoscopy (PLE-TS) at the Department of Surgery, University of Hong Kong Medical Center, at Queen Mary Hospital, Hong Kong. The patients were jointly managed under the Divisions of Esophageal Surgery and Head and Neck Surgery. Informed consent was obtained from individual patients.

Technique of thoracoscopic esophageal mobilization
The technique for esophagectomy has been described previously [1]. In brief, the patient is first placed in a left lateral decubitus position as for a posterolateral thoracotomy. Double-lumen endobronchial tube was introduced for selective single-lung ventilation. Dissection was performed through five thoracoports (US Surgical Corp, Norwalk, CT). No carbon dioxide insufflation was used during thoracoscopy.

In 1 patient, the prone-posterior jack-knife position was used as described by Cuschieri [2]. The patient had supports beneath the epigastric and upper sternal regions to enable respiratory excursion of the chest walls. The upper arms were placed hanging on either side of the operating table with the forearms and hands supported in a sling with the elbow flexed 90 degrees or more to result in lateral displacement of the scapula. Four ports were placed through the right chest wall. The camera port was placed just below the apex of the scapula. One port was placed posterior to the scapula for a retractor used by the assistant. Two other ports in line to the camera port were used for dissecting instruments.

Mobilization of the esophagus was commenced by first incising the mediastinal pleura overlying the esophagus below the level of the azygous vein. A short segment of esophagus about 10 cm in length was exposed first anteriorly and then posteriorly. A window was created below the esophagus so that a sling could be put around it allowing the esophagus to be lifted up and away from other mediastinal structures. The esophagus could then be gradually dissected away from its mediastinal bed. The segment of the azygous vein crossing the esophagus was ligated with extracorporeal ties with a knot pusher, absorbable self-locking clips, or endovascular stapler (Endo-GIA; Ethicon, Somerville, NJ). The dissection was continued up to the apex of the thoracic cavity. Hemostasis was achieved and a size 24F Argyle chest tube (Division of Sherwood Medical, St. Louis, MO), and in more recent patients, a 18F vacuum drain (Drevac drain, Astra-Meditec, AB, Limburg, Germany) was inserted through one of the ports before the lung was reinflated [3].

With the entire esophagus mobilized, the patient was turned to the supine position. The stomach was mobilized in the conventional manner through a laparotomy, the stomach being brought up to the neck through the posterior mediastinum for anastomosis to the oropharynx. Feeding jejunostomy tubes were not routinely placed. Patients were managed in a high-dependency unit immediate after operation until stable.

Intraoperative events, postoperative morbidity and mortality were prospectively documented. Long-term follow-up data was also studied. Comparisons were made with a historical cohort of 30 consecutive patients who underwent PLE with conventional transhiatal approach (PLE-TH) during 1988 to 1994, immediately before the introduction of thoracoscopy. There had been no major change in perioperative management during the study period. The same group of surgeons managed all patients.

Statistical analysis
Statistical difference between groups were determined by Mann-Whitney U test, the {chi}2, or Fisher’s exact test where appropriate. Survival was calculated with the Kaplan-Meier method and comparisons made with the log-rank test. Survival calculations included operative deaths. A p value of less than 0.05 was regarded as significant. All calculations were performed with the program Statistical Package for the Social Sciences (SPSS-X version 7.5, SPSS Inc, Chicago, IL).


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The demographics of the two patient groups are shown in Table 1. The baseline characteristics did not differ significantly in the age, gender distribution, and prior treatment with radiotherapy or chemotherapy. The indications for operation and the stage of the cancers are shown. A variety of tumors were operated on, which included cancer of the larynx, hypopharynx, cervical esophagus, and intrathoracic esophagus associated with those of the head and neck.


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Table 1. Comparisons of Characteristics of Patients in Pharyngolaryngoesophagectomy With Transhiatal and Pharyngolaryngoesophagectomy With Thoracoscopic Mobilization

 
Of the four patients in PLE-TS group with double tumors, they were cancers of the (1) hypopharynx (stage III) + lower esophagus (stage III), (2) cervical esophagus (stage III) + lower esophagus (stage III), (3) recurrent cancer of the hypopharynx after radiotherapy (stage IVa) + middle esophagus (stage IIa), and recurrent cancer of larynx after laryngectomy (staging not appropriate) and midesophagus (stage I).

Of the 2 patients in PLE-TH group with double tumors, they were cancer of the hypopharynx (stage III) + lower esophagus (stage III), and cancer of the tongue base (stage III) and cervical esophagus (stage III).

All patients had squamous cell cancers except 1 patient had recurrent papillary cancer of the thyroid after previous thyroidectomy.

In the PLE-TS group, additional surgical procedures carried out were as follows: 2 patients underwent left hemicolectomy because of incidental findings of cancer of the splenic flexure. In 4 patients, manubrial resections were required for tumor resection and construction of mediastinal tracheostomy. Two of these 4 patients also required the use of a deltopectoral flap for reconstruction of the neck defect. Seven patients underwent radical or selective lymph node neck dissection together with PLE. The gastric tube was the favored conduit to restore intestinal continuity. The right ileocolon was used in 2 patients because of previous gastrectomy for benign disease. Postoperative radiotherapy was given to 19 patients.

Of the 30 patients with PLE-TS, full mobilization could not be completed in two. In the first patient, there was technical difficulty in placement of a double-lumen endotracheal tube. Poor exposure during attempted dissection resulted in conversion to conventional transhiatal mobilization. In the second patient, lung adhesions precluded satisfactory approach to the esophagus. The patient also had an advanced tumor of the lower esophagus. In neither patient was an open thoracotomy required for control of bleeding or damage to mediastinal structures. The time spent on thoracoscopy before conversion to transhiatal approach were 50 and 30 minutes, respectively.

The median blood loss was 700 mL (range, 164 to 3,000 mL) and 1,000 mL (range, 400 to 2,000 mL) for the PLE-TS and PLE-TH groups, respectively (p = 0.21). Blood loss during the thoracoscopy phase was minimal in all patients. Only in 1 patient, excessive blood loss of 3 L was encountered because of injury to the brachiocephalic vein during tumor dissection in the neck. In the 28 patients whose esophagus was fully mobilized by thoracoscopy, the median thoracoscopy time was 90 minutes (range, 60 to 180 minutes). The median total operating time was 392 minutes (range, 180 to 570 minutes) for PLE-TS and was 300 minutes (range, 150 to 550 minutes) for PLE-TH (p = 0.02).

Postoperative complications are shown in Table 2. Overall pulmonary complications occurred in 12 (40%) and 11 (37%) patients in PLE-TS and PLE-TH groups, respectively (p = 0.79). Of these, major pulmonary complications (included bronchopneumonia, respiratory failure, aspiration) occurred in 7 (23%) and 8 (27%) respectively (p = 0.77). Cardiac complications, which were mostly arrhythmia, affected 7 (23%) and 5 (17%) patients in the respective groups, p = 0.52.


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Table 2. Complications After Pharyngolaryngoesophagectomy With Thorascopic and Transhiatal Mobilization

 
None of the surgical complications in the PLE-TS group were related to the thoracoscopic esophageal mobilization. In the PLE-TH group, 1 patient developed postoperative hemothorax due to inadequate hemostasis from the blind mediastinal dissection. The median duration of postoperative hospital stay was 22 days (range, 12 to 105 days) and 24 days (range, 9 to 107 days) for PLE-TS and PLE-TH groups, respectively (p = 0.96).

There were four hospital deaths (13%). One patient developed tracheal ischemia after resection of an extensive cervical esophageal tumor, for which further resection of the ischemic portion of the tracheal was required with a pectoralis myocutaneous flap for repair. Although the repair was successful, the patient stayed in hospital for 3.2 months and died of widespread systemic metastases. Two patients died of pneumonia and respiratory failure. Both also had advanced residual malignancy. Another patient who had bronchiectesis and chronic obstructive airway disease developed pleural effusion after operation. A chest drainage tube inserted produced lung parenchyma injury and hemorrhage, which led to her demise 3 months after operation. In group PLE-TH during 1988 to 1994, there were five hospital deaths (17%). This was not significantly different from group PLE-TS (p = 1.0).

Because the tumors encountered were not homogeneous, overall comparisons of survival between the PLE-TS and PLE-TH groups were considered not meaningful. For patients with only cervical esophageal cancers, the median survival figures were 34 months and 16 months for PLE-TS and PLE-TH, respectively (p = 0.1). For patients with hypopharyngeal cancers only, the respective figures were 34 months and 19 months (p = 0.17). Although it appears that PLE-TS group had a longer survival duration, these figures did not reach statistical significance.


    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Turner [4] in 1933 carried out the first successful transhiatal esophagectomy for carcinoma and reestablished intestinal continuity using an antethoracic skin tube as a staged operation. In 1960, Ong and Lee [5] first described the procedure of PLE as a one-stage, three-phase operation that involved cervical, abdominal incisions, and a thoracotomy. Tumors involving the hypopharyngeal and upper cervical esophageal region were resected together with the entire esophagus, and the stomach was delivered through the posterior mediastinum to the neck for pharyngogastric anastomosis. For many years, this operation was the procedure of choice for all tumors that involved the hypopharynx in which hypopharyngeal resection was necessary for tumor extirpation. In recent years, the availability of myocutaneous flaps and free visceral grafts have widened the choice of reconstruction of partial or circumferential hypopharyngeal defects. For tumors involving the cervical esophagus, however, a total esophagectomy is still required to gain adequate distal resection margin.

The conventional method of esophageal mobilization in PLE was the transhiatal technique [6]. Potential pitfalls of the operation stem from the "blind" element of the procedure, especially for the upper and mid-esophagus that lies behind the tracheobronchial tree, and where important structures like the azygous vein and thoracic duct cross. Extensive experience exists in the literature for transhiatal resection for intrathoracic esophageal cancers. A review of transhiatal resection in the literature in the 1980s of 1,353 patients showed an overall mortality rate of 7.2% [7]. Specific complications included bleeding, tumor rupture and contamination, chylothorax, tracheobronchial injury, pneumothorax, Horner’s syndrome, and a consistently high incidence of recurrent laryngeal nerve damage. Even when no specific complication ensures, episodes of intraoperative hypotension can result from cardiac compression with the surgeon’s hand and forearm inserted into the posterior mediastinum for dissection [8, 9]. All the complications mentioned above have been reported for PLE.

In the present study it was hypothesized that with the thoracoscopic technique, dissection can be carried out under vision and with less traumatic mediastinal manipulation. Intraoperative mishaps can be avoided and postoperative recovery enhanced. Another advantage of thoracoscopy is that when a synchronous tumor of the intrathoracic esophagus exists, thoracoscopic dissection with more controlled and more radical lymphadenectomy than the transhiatal approach can be performed [1, 10, 11]. Intrathoracic tumor was present in 4 of our 30 patients.

Blood loss during the thoracoscopic phase was minimal, although overall blood loss was not significantly less, because much of the loss occurred from tumor extirpation in the neck. No tracheobronchial injury was encountered. Hypotension from cardiac compression was eliminated. No surgical complication in the present series was attributed to thoracoscopy. One disadvantage of thoracoscopy is that one-lung ventilation is required for adequate exposure. Indeed, technical difficulty in placing a double-lumen endotracheal tube led to failure in full esophageal mobilization in 1 patient. Pleural adhesion may prevent access to the mediastinum. The total operating time was prolonged. Most of our patients had advanced cancer in the neck and most of the operating time was spent on tumor resection. Overall, approximately 23% of the total operating time was needed for thoracoscopy. In patients whose cervical phase was straightforward and completed quickly, a more significant proportion of the total time may be taken up by the thoracoscopy phase. During conventional transhiatal esophageal mobilization, if a two-team synchronous approach is used for the neck and abdomen, preparation of the gastric conduit is usually more rapid than the cervical tumor resection. Esophageal mobilization can then proceed while dissection in the neck is still being performed. This is not possible when thoracoscopic mobilization was carried out. As we have gained experience, thoracoscopy time has become shorter. The shortest time so far attained was 60 minutes for complete esophageal mobilization. With practice, further reduction of thoracoscopic mobilization time is to be expected.

We have not been able to demonstrate a clear advantage of thoracoscopy in terms of postoperative cardiopulmonary morbidity. The genesis of cardiopulmonary complications is multifactorial and may not be solely related to the method of access. Many patients are elderly with poor operative risk, and have advanced cancer. Surgical resection is often done after failure of other therapies like radiotherapy and chemotherapy. Sometimes PLE are performed as a salvage operation for extensive primary or recurrent disease, as other options for palliation are inadequate. This is the situation in the majority of our patients. Previous operation or radiotherapy was present in one-third of patients. The lengthened time of single-lung anesthesia was a disadvantage. The extrathoracic trauma in these patients was substantial. Given the factors detailed above significant morbidity and mortality rates are not unexpected.

Other methods of esophageal mobilization have been described, including eversion stripping [12, 13], laparoscopic-assisted method [14], total laparoscopic esophagectomy [15], and combined laparoscopic and thoracoscopic esophagectomy [16]. These techniques remain investigational. For most patients, PLE is carried out with the transhiatal method, and if performed by an experienced surgeon, this approach is no doubt safe. In the largest series of transhiatal esophagectomy, Orringer and colleagues [17] reported in their series of 1,085 patients, a mortality rate of 4%, and a mean blood loss of 689 mL.

A recent review of 978 patients with PLE reported in the literature revealed a hospital mortality rate of 16% and morbidity of 37%, although a trend of improvement over time was observed [18]. Recent series still report a mortality rate of about 10% [1921]. Our results are in keeping with what is reported in the literature.

Survival of patient with only cervical esophageal cancer or hypopharyngeal cancers appears longer in the PLE-TS group, although not statistically significant. However, it is difficult to draw firm conclusions due to the small number of patients and the use of historical controls. Prospective randomized trials would be required to test this hypothesis. The use of historical controls for comparison and the small number of patients are the main drawbacks of this study. Interpretation requires caution. Over the study period, however, all patients were managed by the same group of surgeons and there has not been in our view major changes in perioperative management. The baseline characteristics of patients, tumor status, and indications for operation were not substantially different between the two groups. We believe that comparisons between the two groups, in particular in terms of operative and perioperative events, were justified.

The thoracoscopic technique described has eliminated intraoperative complications like massive mediastinal bleeding and tracheobronchial injury, although postoperative outcome remained unchanged. Further refinement in thoracoscopy and head and neck procedures will be necessary to enhance surgical result of these technically challenging operations.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Law S., Fok M., Chu K.M., Wong J. Thoracoscopic esophagectomy for esophageal cancer. Surgery 1997;122:8-14.[Medline]
  2. Cuschieri A. Thoracoscopic subtotal oesophagectomy. Endosc Surg Allied Technol 1994;2:21-25.[Medline]
  3. Lau H., Law S., Wong J. Prospective evaluation of vacuum pleural drainage after thoracotomy in patients with esophageal carcinoma. Arch Surg 1997;132:749-752.[Abstract]
  4. Turner G. Excision of the thoracic oesophagus for carcinoma, with construction of an extra-thoracic gullet. Lancet 1933;2:1315-1316.
  5. Ong G.B., Lee Y. Pharyngogastric anastomosis after oesophago-pharyngectomy for carcinoma of the hypopharynx and cervical oesophagus. Br J Surg 1960;48:193-200.[Medline]
  6. Orringer M.B. Anterior mediastinal tracheostomy with and without cervical exenteration. Ann Thorac Surg 1992;54:628-636.[Abstract]
  7. Katariya K., Harvey J.C., Pina E., Beattie E.J. Complications of transhiatal esophagectomy. J Surg Oncol 1994;57:157-163.[Medline]
  8. Fok M., Law S., Stipa F., Cheng S., Wong J. A comparison of transhiatal and transthoracic resection for oesophageal carcinoma. Endoscopy 1993;25:660-663.[Medline]
  9. Chu K.M., Law S.Y., Fok M., Wong J. A prospective randomized comparison of transhiatal and transthoracic resection for lower-third esophageal carcinoma. Am J Surg 1997;174:320-324.[Medline]
  10. Akaishi T., Kaneda I., Higuchi N., et al. Thoracoscopic en bloc total esophagectomy with radical mediastinal lymphadenectomy. J Thorac Cardiovasc Surg 1996;112:1533-1540.[Abstract/Free Full Text]
  11. Collard J.M., Lengele B., Otte J.B., Kestens P.J. En bloc and standard esophagectomies by thoracoscopy. Ann Thorac Surg 1993;56:675-679.[Abstract]
  12. Akiyama H., Hiyama M., Miyazono H. Total esophageal reconstruction after extraction of the esophagus. Ann Surg 1975;182:547-552.[Medline]
  13. Rajan R., Rajan N., Pai U.S. Gastric pull-up by eversion stripping of oesophagus. J Laryngol Otol 1993;107:1021-1024.[Medline]
  14. Montgomery P., Willson P.D., Mochloulis G., Tolley N.S., Rosin R.D. Laparoscopically assisted total laryngopharyngoesophagectomy with gastric transposition. J Laryngol Otol 1996;110:1072-1074.[Medline]
  15. Swanstrom L.L., Hansen P. Laparoscopic total esophagectomy. Arch Surg 1997;132:943-947.[Abstract]
  16. Watson D.I., Davies N., Jamieson G.G. Totally endoscopic Ivor Lewis esophagectomy. Surg Endosc 1999;13:293-297.[Medline]
  17. Orringer M.B., Marshall B., Iannettoni M.D. Transhiatal esophagectomy. Ann Surg 1999;230:392-400.[Medline]
  18. Wei W.I., Lam L.K., Yuen P.W., Wong J. Current status of pharyngolaryngo-esophagectomy and pharyngogastric anastomosis. Head Neck 1998;20:240-244.[Medline]
  19. Bardini R., Ruol A., Peracchia A. Therapeutic options for cancer of the hypopharynx and cervical oesophagus. Ann Chir Gynaecol 1995;84:202-207.[Medline]
  20. Azurin D.J., Go L.S., Kirkland M.L. Palliative gastric transposition following pharyngolaryngoesophagectomy. Am Surg 1997;63:410-413.[Medline]
  21. Wight R.G., Birchall M.A., Stafford N.D., Stanbridge R.L. Management of hypopharyngeal carcinoma. J R Soc Med 1992;85:545-547.[Abstract]
  22. In: Sobin L.H., Wittekind C., eds. TNM classification of malignant tumours, Fifth ed. New York: Wiley-Liss, 1997.
Accepted for publication February 21, 2000.




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