Eur J Cardiothorac Surg 2002;22:1-6
© 2002 Elsevier Science NL
Outcomes of minimally invasive esophagectomy (MIE) for high-grade dysplasia of the esophagus
H.C. Fernando*,
J.D. Luketich,
P.O. Buenaventura,
Y. Perry,
N.A. Christie
Division of Thoracic Surgery and the Minimally Invasive Surgery Center, University of Pittsburgh Medical Center Health System, Pittsburgh, PA, USA
Received 17 September 2001;
received in revised form 22 February 2002;
accepted 15 March 2002.
* Corresponding author. UPMC Presbyterian, Suite C800 200 Lothrop Street, Pittsburgh, PA 15213, USA. Tel.: +1-412-647-7555; fax: +1-412-647-7550
e-mail: fernandohc{at}msx.upmc.edu
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Abstract
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Objective: The management of high-grade dysplasia (HGD) of the esophagus is controversial with some clinicians advocating non-operative ablation or surveillance. Minimally invasive esophagectomy (MIE) allows re-section of the esophagus and may minimize morbidity. This report summarizes our experience with MIE for HGD. Methods: A retrospective review of 28 patients who underwent MIE for a pre-operative diagnosis of HGD. MIE initially involved a laparoscopic transhiatal approach (n=1), but subsequently evolved to laparoscopy with VATS mobilization (n=27) of the esophagus. Results: From August 1996 to March 2001, 28 patients underwent MIE. There were 23 males and five females; median age was 61 (40–78) years. Median hospital stay was 5 (3–20) days and ICU stay was 1 (1–20) day. One patient required conversion to laparotomy because of dense adhesions. There were ten other patients who had successful MIE despite prior laparotomy. Median operating time was 8 (5.8–13) h. One death occurred from sepsis, pneumonia and multi-system organ failure. Complications occurred in 15 patients. In addition to the patient who died, five re-operations were required for: small bowel perforation (n=1), jejunostomy leak (n=1), pyloric dilation for gastric outlet obstruction (n=1), cholecystectomy (n=1), incision and drainage of an abdominal abscess (n=1). Final pathologies were HGD (n=17), in situ cancer (n=6) and invasive cancer (n=5). At a median follow-up of 13 (2–41) months all hospital survivors are alive and free of disease. Conclusions: This report confirms the risk of occult cancer in patients with HGD (39% in this series) supporting the recommendation for esophagectomy. MIE can be performed with acceptable results and may minimize morbidity compared to previous reports of open esophagectomy for HGD.
Key Words: High grade dysplasia • Minimally invasive esophagectomy
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1. Introduction
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The incidence of esophageal adenocarcinoma is rapidly increasing in the Western world. A risk factor is the development of Barrett's esophagus in which the squamous mucosa of the esophagus is replaced by metaplastic columnar epithelium. The risk of cancer development in Barrett's esophagus increases further when high-grade dysplasia (HGD) develops. The management of HGD is controversial. Most surgeons would advocate esophagectomy because of the risk of missing an occult carcinoma [1]. However, because of concerns related to the morbidity and mortality of esophagectomy many clinicians use alternative approaches such as mucosal ablation or surveillance [2]. Since the introduction of laparoscopic fundoplication in 1991 [3], improvements in instrumentation and optics have allowed the development of minimally invasive approaches to esophageal diseases that have been traditionally managed by open operation. These include the treatment of achalasia [4], giant paraesophageal hernia [5] and the staging and treatment of esophageal cancer [6–8]. Minimally invasive esophagectomy (MIE) has the potential to minimize the morbidity of esophageal re-section and allow quicker recovery providing a good treatment option for HGD. We previously reported our initial experience of 12 patients with HGD who underwent MIE [9]. This report details our growing experience of MIE for HGD.
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2. Materials and methods
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A retrospective review was performed of 28 patients with a pre-operative diagnosis of HGD who underwent MIE at the University of Pittsburgh. The diagnosis of HGD was confirmed by pre-operative review of all esophageal biopsy slides by University pathologists with expertise in esophageal cancer. Formal four-quadrant biopsies were performed in 18 (64%) of these patients. Further work-up before operation included computed tomography (CT) scan of the chest and abdomen (n=28) and endoscopic ultrasound (EUS), which was performed in 16 (57%) patients. MIE initially involved a laparoscopic transhiatal approach, which was used in one patient. All other patients (n=27) were operated on using a VATS mobilization of the esophagus in combination with laparoscopy. This technique has been described previously [10] but will be summarized subsequently.
2.1. Operative technique
Patients are intubated with a double-lumen tube and then positioned in the left lateral decubitus position. The surgeon stands on the right and the assistant on the left. Four thoracoscopic ports are used (Fig. 1
). A 10-mm camera port is placed at the seventh intercostal space in the mid-axillary line. A 5-mm port is placed at the eighth or ninth intercostal space, posterior to the posterior axillary line for the ultrasonic coagulating shears (US Surgical, Norwalk, CT, USA). A 10-mm port is placed in the anterior axillary line at the fourth intercostal space. This is used to pass a fan shaped retractor to retract the lung anteriorly allowing exposure of the esophagus. The last 5-mm port is used to place instruments for retraction and countertraction. If necessary a single retracting suture (0-Surgitek, US Surgical, Norwalk, CT, USA) will be placed near the central tendon of the diaphragm and brought out through the inferior anterior chest wall through a 1-mm skin incision. This provides downward traction on the diaphragm allowing good exposure of the distal esophagus.
The inferior pulmonary ligament is divided and the mediastinal pleura overlying the esophagus divided to expose the entire thoracic esophagus. An endoscopic stapler (Endo-GIA; US Surgical, Norwalk, CT, USA) is used to divide the azygos vein. Circumferential mobilization of the esophagus is performed, including all surrounding lymph nodes and periesophageal tissue and fat. A Penrose drain is placed around the esophagus to facilitate traction and exposure (Fig. 2
). The entire intrathoracic esophagus is mobilized from the thoracic inlet to the diaphragmatic reflection. Care is taken, however, to avoid extending the distal dissection too low into the peritoneal cavity to avoid difficulty in maintaining pneumoperitoneum during the abdominal dissection.
After placement of a single 28F-chest tube and closure of the thoracic ports the patient is turned to the supine position. The surgeon remains on the patient's right. Five abdominal ports are used (Fig. 3
). The gastrohepatic ligament is divided, exposing the right crus of the diaphragm. The stomach is mobilized by dividing the short gastric vessels using the ultrasonic coagulating shears. The gastrocolic omentum is divided with preservation of the right gastroepiploic arcade. The stomach is retracted superiorly and the left gastric vessels are identified and divided with the Endo-GIA stapler. Usually, pyloroplasty is performed. The ultrasonic shears are used to open the pylorus and the Endo-stitch (US Surgical, Norwalk, CT, USA) is used to close the pylorus transversely (Fig. 4
). A gastric tube is then constructed by dividing the stomach starting at the lessor curve and preserving the right gastric vessels with the 4.8 mm stapler (Endo-GIA II, US Surgical, Norwalk, CT, USA) (Fig. 5
). The gastric tube is attached to the esophageal and gastric specimen using sutures. An additional stitch is placed on the anterior proximal gastric tube to facilitate orientation and prevent twisting as the tube is brought up into the neck.
A feeding jejunostomy tube is placed by first attaching a limb of proximal jejunum to the anterior abdominal wall with the Endo-stitch. A needle catheter kit (Compact Biosystems, Minneapolis, MN, USA) is placed percutaneously into the peritoneal cavity and under direct laparoscopic vision, the guide wire and catheter are directed into the loop of jejunum. The jejunal puncture area is tacked completely to the anterior abdominal wall for a distance of several centimeters. The last step in the abdominal operation is the dissection of the phrenoesophageal membrane. This is performed at this stage to minimize the loss of pneumoperitoneum into the mediastinum. We also partially divide the right and left crura to prevent gastric outlet obstruction. Once the gastric tube is pulled into the mediastinum, it is tacked inferiorly to the hiatus to prevent subsequent thoracic herniation.
A 4–6 cm horizontal neck incision is made. The cervical esophagus is exposed and finger dissection performed down into the mediastinum until the thoracic dissection plane encountered. The esophagogastric specimen is pulled out of the neck incision and the cervical esophagus divided. The specimen is removed from the field and an anastomosis performed between the cervical esophagus and gastric tube using standard techniques. The completed reconstruction is shown in Fig. 6
.
All data was entered into an SPSS file (version 10 for Windows) for analysis. Dysphagia severity using a scale from 1 (no dysphagia) to 5 (severe dysphagia) was measured pre-operatively and at follow-up. Pre- and post-operative scores were compared using a paired t-test analysis.
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3. Results
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From August 1996 to March 2001, 28 patients with HGD underwent MIE. There were 23 males and five females. Median age was 61 (40–78) years. Operative procedures included a laparoscopic transhiatal approach in one patient and a right VATS mobilization of the esophagus with laparoscopy and a neck incision as described above in the remaining 27 patients. Conversion to laparotomy was required in one patient who had extensive adhesions from previous operations including placement of an Angelchik prosthesis. Prior laparotomy, however, did not preclude a minimally invasive approach. In total, 12 (43%) patients had undergone laparotomy before MIE. Pyloroplasty was performed in 20 patients and pyloromyotomy in seven patients. Feeding jejunostomy was performed in 25 patients. The mean operative time was 8 (5.8–13) h. Intensive care unit admission was required in 24 patients at a median of 1 (1–20) day. Median hospital stay was 5 (3–20) days. Median duration of chest tube drainage was 2 (1–6) days. There was one post-operative death. This occurred in a 66-year patient who developed pneumonia with septic hemodynamic parameters on the third post-operative day. Endoscopy at that time showed no evidence of anastomotic leak and a viable gastric tube. However, he deteriorated further developing multi-system organ failure, ischemia of the gastric tube and leakage from his pyloroplasty site by the 11th post-operative day requiring re-operation for takedown of his gastric tube. He continued to deteriorate with support withdrawn on the 20th post-operative day. Including this patient, complications occurred in a total of 15 patients. Major and minor complications are summarized in Table 1. There was one anastomotic leak. Re-operation was required in six patients. This included the one patient who died. The other five re-operations were for small bowel perforation (n=1), leakage at the jejunostomy site (n=1), pyloric dilation for gastric outlet obstruction following pyloromyotomy (n=1), incision and drainage of a superficial abdominal abscess (n=1) and one patient who required cholecystectomy for gallstone pancreatitis. This same patient also required pyloric dilation for delayed gastric emptying.
The mean number of lymph nodes removed was 16. Final pathologies were HGD in 17 (61%), carcinoma in situ in six (21%) and invasive cancer in five (18%) patients. Four of the patients with invasive cancer had T1N0 tumors and one patient had a T1N1 tumor. In the five patients with invasive cancer pre-operative work-up had included four-quadrant biopsies in three (60%) and EUS in five (100%). At a median follow-up of 13 months (2–41), there have been no deaths. None of the 27 hospital survivors have evidence of cancer. Mean pre-operative and follow-up dysphagia scores were 1.6 and 1.4, respectively (P=0.285). At follow-up, five patients complained of occasional difficulty with hard solids (dysphagia score 2) and three patients complained of difficulty with soft solids (score 3).
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4. Discussion
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The optimal management of Barrett's with HGD remains controversial. One option is continued endoscopic surveillance with frequent four-quadrant biopsies along the length of the esophagus. However, biopsy sampling errors and failure of patients to follow-up for endoscopy may lead to a missed diagnosis of cancer. The argument favoring endoscopic surveillance is that some patients will not progress to cancer. In a Veterans Administration study of 75 patients with HGD undergoing endoscopic surveillance, 12 (16%) progressed to cancer, while the remaining 84% of patients did not develop cancer at a mean follow-up of 7.3 years [11].
Alternative treatment options involve ablation of the Barrett's mucosa. Methods of ablation have included laser ablation, photodynamic therapy and argon plasma coagulation (APC). A Belgian study described the use of APC in 31 patients with Barrett's esophagus [12]. Endoscopic examination suggested complete squamous re-epithelialization in 25 patients after a mean of 2.4 treatments. However, histological examination confirmed true squamous epithelium in only 19 patients with six demonstrating residual Barrett's under the squamous epithelium. Additionally, eight patients with histological and endoscopic eradication of Barrett's demonstrated islands of metaplasia after 1 year. Other mucosal ablative modalities are also associated with recurrences. A German study described the use of the potassium-titanyl-phosphate (KTP) laser in ten patients with Barrett's or early carcinoma [13]. Although complete response was initially seen in all ten patients, two patients had recurrent Barrett's, at a mean of 10.6 months post-treatment despite acid suppression with 80 mg of omeprazole daily. We have previously described the use of photodynamic therapy (PDT) for palliation of advanced esophageal cancer [14]. PDT is used in some centers as ablate HGD and superficial cancers [15]. However, HGD may persist, and cancers may occur despite an initial response to PDT. Our preference is to reserve the use of PDT in HGD for patients who refuse or are not candidates for esophagectomy [16].
The main advantage of esophagectomy is that the high-risk esophageal mucosa is removed. Additionally, since the majority of occult cancers will be early stage tumors re-section will likely be curative. The main disadvantage of operation, are the risks of morbidity or mortality after operation. This is particularly pertinent with HGD as these patients are relatively asymptomatic compared to the typical patient who has dysphagia from an obstructing esophageal carcinoma. Our results demonstrate no significant difference in dysphagia scores before and after operation. Additionally, the 39% incidence of occult cancer demonstrated in our series support a role for esophageal re-section.
Surgical results are dependent to some degree on the case volume and experience of the centers and the surgeons involved. This was demonstrated in a report from Texas where mortality rates ranged from 12.2% in low volume centers to 3% in high volume centers after esophagectomy [17]. Total morbidity rates are often not documented, although appear to be around 50–60% [17,18]. Most authors tend to report specific complications such as anastomotic leak rate. The series by Orringer of 1085 patients is one of the largest reported and serves as a standard to compare to Ref. [19]. The leak rate in Orringer's series was 13%. Fifty-three percent of patients were discharged by the tenth post-operative day, although the average length of stay had decreased to 7 days in patients operated towards the last 2 years of this experience. Our mortality of one (3.6%), anastomotic leak rate of one (3.5%) and length of stay of 5 days compare well to these open esophagectomy series.
MIE was first described by DePaula from Brazil [20]. His initial series included many patients with end-stage achalasia from Chagas' disease. Swanstrom was the first to report the use of MIE in North America [8]. Both authors described a laparoscopic transhiatal approach to MIE. The advantages of the transhiatal approach are that no re-positioning of the patient or single lung ventilation is required. We initially adopted this approach [21]. Because of the limitations of working through the small esophageal hiatus, impairing dissection of the middle and upper esophagus and thoracic lymph nodes, our preferred approach includes VATS mobilization as described above.
Although not proven by randomized studies MIE may decrease morbidity, allow quicker recovery and return to home than open esophagectomy (OE). Additionally, the inclusion of thoracoscopy allows a much better lymph node dissection to be performed in the chest than with transhiatal esophagectomy which is the standard operation performed in many centers in the US. Disadvantages of MIE include high equipment costs, and the requirement that the surgeon be comfortable with advanced minimally invasive techniques.
Only one study has compared MIE to open esphagectomy [22]. This was a single institution retrospective review of operations performed by four different surgeons over different periods. Although observed differences may have been due to bias in pre-operative management and experience of the different surgeons, MIE patients had shorter operative times, less blood loss, fewer transfusions, shortened intensive care unit stays and hospital stays compared to OE.
In summary, esophagectomy should be the preferred approach for the patient with HGD because of the risk of missing an occult cancer or a new cancer during follow-up. MIE is a technically feasible and safe option in a center such as ours, which has extensive experience with minimally invasive and open esophageal operations. Controlled trials will be necessary to confirm any perceived advantages over open operation.
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Footnotes
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Presented at the joint 15th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 9th Annual Meeting of the European Society of Thoracic Surgeons, Lisbon, Portugal, September 16–19, 2001.
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Abstract
1. Introduction
