Ann Thorac Surg 2005;80:2070-2075
© 2005 The Society of Thoracic Surgeons
Original article: General thoracic
Minimally Invasive Esophagectomy for Stage I and II Esophageal Cancer
Satoshi Yamamoto, MD
a
,
*
,
Katsunobu Kawahara, MD
b
,
Takafumi Maekawa, MD
a
,
Takeshi Shiraishi, MD
a
,
Takayuki Shirakusa, MD
a
a Second Department of Surgery, Fukuoka University School of Medicine, Fukuoka, Japan
b Second Department of Surgery, Oita University Faculty of Medicine, Oita, Japan
Accepted for publication June 3, 2005.
* Address correspondence to Dr Yamamoto, Second Department of Surgery, Fukuoka University School of Medicine, Jyonan-ku Nanakuma 7-45-1, 814-0180, Fukuoka, Japan (Email: y-satosi{at}fukuoka-u.ac.jp).
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Abstract
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BACKGROUND: To evaluate whether thoracoscopic and video-assisted dissections are appropriate modalities, we assessed the mortality, morbidity, and survival of patients who underwent a thoracoscopic esophagectomy for esophageal cancer.
METHODS: Between November 1995 and December 2004, thoracoscopic and video-assisted esophagectomies were performed on 112 (72.7%) patients out of 154 who underwent surgical resection for thoracic and abdominal esophageal cancer. The histologic type of cancer was squamous cell carcinoma in 109 (97.4%) patients and adenocarcinoma in 3 (2.6%).
RESULTS: Intraoperative complications occurred in 4 (3.6%) patients: tracheal injury in 3 (2.7%) and azygos vein injury in 1 (0.8%). The 30-day mortality rate was 0.8%. Early postoperative complications occurred in 29 (25.9%) patients including the following: recurrent nerve palsy in 10 (8.9%), respiratory complication in 7 (6.3%), anastomotic leakage in 9 (8.0%) with major leakage requiring reanastomosis in 4 (3.6%) of these 9, and chylothorax in 3 (2.7%). Induction chemoradiotherapy, preoperative concomitant disease, and reconstruction using the colon did not increase morbidity. Port site recurrence occurred in 3 (2.7%) patients. The overall 5-year survival rate was 52%. For stage I disease, the 5-year survival rate of patients was 87.2%. In stage II disease, it was 70.2%.
CONCLUSIONS: Thoracoscopic and video-assisted esophagectomy are considered feasible and safe options for the treatment of esophageal cancer, but further investigation is necessary. The survival of patients with stage I and II disease is satisfactory at the present time.
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Introduction
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A thoracoscopic esophagectomy is an example of minimally invasive surgery. However, the use of this procedure for esophageal malignant disease remains controversial. We performed a thoracoscopic or video-assisted esophagectomy for thoracic and abdominal esophageal cancer to accomplish a radical resection. In this study, we evaluated the use of thoracoscopic and video-assisted esophagectomy for the treatment of esophageal cancer by assessing the postoperative morbidity, mortality, and survival.
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Patients and Methods
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From November 1995 to December 2004, 154 patients underwent a surgical resection for thoracic and abdominal esophageal cancer. Thoracoscopic and video-assisted esophagectomies were performed on 112 (72.7%) patients after informed consent was obtained. The criteria for patient selection were as follows: tumors limited to the esophageal wall, no patient history of major right side thoracic surgery, and the patient's ability to tolerate left side one-lung ventilation. The ages of the patients ranged from 40 to 79 years (mean, 63 ± 9 years); 91 (81.2%) patients were male and 21 (18.8%) were female. The histologic types of tumors were squamous cell carcinoma in 109 (97.4%) patients and adenocarcinoma in 3 (2.6%). The tumor was located in the upper thoracic esophagus in 22 (19.6%) patients, the middle thoracic esophagus in 49 (43.8%), the lower thoracic esophagus in 34 (30.4%), and the abdominal esophagus in 7 (6.2%).
Concomitant double cancer was found in 22 (19.6%) patients, synchronous cancer in 10 (8.9%), and metachronous cancer in 12 (10.7%). Gastric cancer was found in 17 (15.2%) patients, laryngeal cancer in 4 (3.5%), and rectal cancer in 1 (0.8%). Preoperative concomitant disease was found in 21 (18.8%) patients; diabetes mellitus in 8 (7.1%), alcoholic liver disease in 5 (4.5%), coronary artery disease in 4 (3.6%), and emphysema in 4 (3.5%). Chronic renal failure required dialysis in 1 (0.8%).
Induction Chemoradiotherapy
Before October 1999, induction chemoradiotherapy was performed in 10 (8.9%) patients for either cervical node metastasis or clinical T4 disease detected by esophagograms, computed tomographic (CT) scans, and endoscopic ultrasonography. From November 1999, induction chemoradiotherapy was performed in 16 (14.3%) patients for clinical T4 or T3N1 disease to prevent port site cancer implantation. The radiotherapy was administered in 10 Gy fractions 5 days a week for 4 weeks. The fluorouracil (5FU) was given as a continuous infusion of 250 mg · body · day for 5 days a week along with the radiotherapy. The one-hour infusion therapy of cisplatin was administered at a dose of 10 mg/body for 5 days a week along with radiotherapy.
Surgical Procedures
The technique for performing a thoracoscopic and video-assisted esophagectomy has been described by Kawahara and colleagues [1]. We usually performed a three-field (neck, thoracic, and abdominal) lymph node dissection for esophageal cancer patients. The patients were placed in the left decubitus position and left lung ventilation was started. Five or six thoracic ports for the thoracoscopic devices were inserted from the fourth to the eighth intercostal spaces in the anterior, middle, and posterior axillary lines. A 30-degree visual thoracoscope was inserted through the port placed in the seventh intercostal space at the midaxillary line. When difficulties were experienced (for example, the esophageal tumor was either too large or severe adhesion to the bronchus or left atrium was observed), a 6-cm thoracotomy was performed in the auscultation triangle. The thoracic esophagus and mediastinal nodes were dissected with a harmonic scalpel. The lymph nodes along the left recurrent laryngeal nerve were dissected with bipolar electric coagulator scissors to prevent heat injury to the nerves. After a total dissection of the thoracic esophagus, the esophagus was divided at the upper thoracic esophagus. After thoracic drainage tube insertion, the patient was placed in the supine position. A collar incision in the neck and an 8-cm upper-median abdominal incision were then made, and the surgeon used a headlamp to illuminate the peritoneal cavity. A bilateral neck and perigastric lymph node dissection was then performed. The dissection of the lower thoracic and abdominal esophagus was performed through the transhiatal route. The esophagus was then pulled into the abdominal cavity. A thin gastric tube was made and pulled up through the retrosternal route and then it was anastomosed end-to-end to the cervical esophagus using 4-0 monofilament absolvable sutures.
In 101 (90.2%) patients, a thin gastric tube was used for reconstruction. In 11 (9.8%) patients who had undergone a distal gastrectomy for a gastric cancer or peptic ulcer, the reconstruction was performed with use of the left colon in 5 (4.5%) patients and with the ileocolon in 6 (5.4%).
A statistical analysis was carried out using an SAS software package (SAS Institute, Cary, NC) on Macintosh Power PC computers (Apple Computer, Cupertino, CA). Significant differences in the survival times among the groups were calculated based on the Kaplan-Meier curves with the log-rank test. Significant differences in the incidence were calculated using the 
2test.
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Results
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The International Union Against Cancer (UICC) pathological TNM stage of esophageal cancer is shown in Table 1. Lymph node metastasis was found in 65 (58.1%) patients. In one patient with stage IVB disease, a small metastatic node was found in the left hepatic lobe at laparotomy and, as a result, a wedge resection of the hepatic lobe was performed. In the other patients, all of the stage IV disease depended on the lymph node status.
A thoracoscopic esophagectomy was performed on 65 (53.8%) patients, and a video-assisted esophagectomy was performed on 47 (46.2%). All 112 patients were extubated in the operating room after surgery. Two (1.8%) patients with emphysema were reintubated for ventilator support in the intensive care unit. The average thoracoscopic time was 111 minutes (range, 45 to 210 minutes), and average intrathoracic blood loss was 134 mL (range, 20 to 490 mL). The average number of mediastinal dissecting nodes was 28 (range, 5 to 79 nodes).
Intraoperative complications occurred in 4 (3.6%) patients. Azygos vein arch injury occurred in one (0.8%) patient. Hemostasis was achieved using an endoclip. The membranous portion of the trachea was injured in 3 (2.7%) patients. In 2 (1.8%) patients, the laceration was repaired with direct suture closure and wrapped with the right lobe of the thymus. In one (0.8%) patient with a large defect in the membranous portion of the trachea, we switched to an open thoracotomy and the tracheal defect was patched with a latissimus dorsi muscle flap.
The 30-day mortality was 0.8% (one patient). In this patient, the left colon, which had been used for reconstruction, developed necrosis and leakage at the colono-jejunostomy occurred postoperatively on day 5. The colon graft was removed, a cervical esophagocutaneous fistula and jejunocutaneous fistula were made, and peritoneal drainage was performed. Unfortunately, the patient died of sepsis and multiple organ failure 15 days after surgery. Hospital deaths occurred in 2 (1.8%) patients with bulky neck lymph node swelling. These patients had severe emphysema, received induction chemoradiotherapy, and required long-term mechanical ventilation support for pulmonary insufficiency after surgery. They died of respiratory failure 94 days and 217 days, respectively, after the esophagectomy. The mean duration of hospital stay was 28 19 days (range, 5 to 134 days).
Early postoperative complications occurred in 29 (25.9%) patients (Table 2). Major anastomotic leakage occurred in 4 (3.6%) patients who required reanastomosis. Chylothorax improved by fasting and intravenous hyperalimentation from 2 to 3 weeks after surgery. Induction chemoradiotherapy, preoperative concomitant disease, and reconstruction with use of the colon did not increase morbidity (Table 3).
Port site recurrence occurred in 3 (2.7%) patients from 4 to 6 months after surgery, and pleural dissemination was simultaneously observed in 2 patients (1.8%). All patients underwent a thoracoscopic esophagectomy between November 1995 and November 1999, and none received induction chemoradiotherapy. Two (1.8%) patients had pathological T3N1M1B stage IVB disease, while another patient had pT3N1M0 stage III disease. These 3 (2.7%) patients underwent either a chest wall resection or tumor extraction and chemotherapy for recurrent disease. They died of pleuritis carcinomatosa and lung metastasis 211, 353, and 798 days, respectively, after the esophagectomy. Since December 1999, we have performed preoperative chemoradiotherapy for patients with clinical T4 or T3N1 disease and port site recurrence has not occurred in patients for whom we performed such trimodality therapy. The tumor response rate to preoperative chemoradiotherapy was 78.9%. There were no patients with progressive disease in the term of preoperative therapy.
The survival curves are shown in Figures 1 through 3.
The overall 5-year survival rate was 52% (Fig 1). All patients with stage 0 disease were alive after 4 years. The 5-year survival rate was 87% in stage I disease, 70% in stage IIA disease, 68% in stage IIB disease, and 27% in stage III disease (Fig 2). There were no patients with stage IV disease who survived 4 years or longer (Fig 2). The 5-year survival rate of the patients with node-negative disease was 75%, and for these with node-positive disease it was 31%. There was a significant difference in the survival times between the patients with node-positive and node-negative diseases (p < 0.01) (Fig 3).
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Fig 3. The survival curves for a T-video-assisted thoracic esophagectomy based on the degree of lymph node metastasis.
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Comment
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Thoracoscopic esophageal mobilization and laparoscopic dissection are minimally invasive approaches that have been tried for the treatment of esophageal cancer. The majority of surgeons have shown that a thoracoscopic esophagectomy is feasible and can be safely performed for select patients [2, 3]; however, no clear advantages over a traditional open thoracotomy have been shown [3, 4]. Table 4
shows our experience, and the investigation experience of others, using a thoracoscopic approach.
For a thoracoscopic resection of the esophagus, the reported mean thoracoscopic procedure time was 104 to 198 minutes [3–7]; the mean blood loss was 165 to 450 mL [3, 5–7], and the mean number of dissecting thoracic lymph nodes was 7 to 12 [3, 5, 7]. The mean thoracoscopic procedure time and the blood loss amount in our series were similar to the findings in these reports, whereas the mean number of dissecting thoracic lymph nodes in our series was greater. Paratracheal node dissection may have contributed to the increased number of dissecting nodes.
Intraoperative complications, such as intercostal artery [8, 9], azygous vein [7] or aortic arch laceration [6, 10], and bronchial injury [4] have been reported to be associated with this approach. In our series, injury to the azygous vein arch and the membranous portion of the trachea occurred. In one patient, the thoracoscopic approach was converted to open surgery, and the lacerated trachea was repaired. A dissection should be performed with care, and the prompt recognition of the necessity to convert to open surgery in difficult cases is important.
The postoperative mortality and morbidity rates are reported to range from 0 to 11% and 0 to 38.9% [4, 5, 7, 9–12], respectively. The incidence of postoperative respiratory complications is reported to range from 0 to 36%, recurrent laryngeal nerve palsy ranges from 0 to 29.4% [3, 4, 6, 12, 13], and anastomotic leakage ranges from 0 to 17.6% [3, 4, 6, 7, 12]. In our series, the rate of major postoperative complications was similar to the rate noted in these reports.
Port site recurrence is a potential risk of thoracoscopic surgery for malignant disease, and four such cases have been reported [3, 7, 14, 15]. In our series, port site recurrence occurred in 3 (2.7%) patients with stage III or IVB disease from 4 to 6 months after surgery. In these patients, the metastatic nodes or an esophageal tumor could have been crushed by endoscopic instruments during thoracoscopic procedures. Direct parietal seeding by the repeated passage of dissecting instruments through the ports appears to be the mechanism of such disease because no gas insufflation was used [3]. Protective thoracoports and sterile vinyl bags for surgical specimens should be used, and direct tumor or lymph node manipulation by thoracoscopic instruments should be minimized to avoid implantation. We believe that induction chemoradiotherapy for large tumors may help prevent port site recurrence. None of our patients have developed parietal seeding since induction chemoradiotherapy for stage III or IV disease was introduced.
There have been few reports of the long-term survival of patients with a thoracoscopic esophagectomy for esophageal cancer. Smithers and colleagues [5] reported an overall 5-year survival rate of patients who underwent a thoracoscopic esophagectomy for esophageal cancer of 40%.
We reviewed our experience with conventional approaches for an esophagectomy (Table 5). In conventional approaches, the 30-day mortality rate was reported to range from 2% to 4% [16–19], and the hospital mortality rate was reported to range from 4% to 22% [17–21]. The morbidity rate was high, from 45% to 71% [19, 20]. Van Lanschot and colleagues [24] reported a significant relationship between the hospital volume and hospital mortality, decreasing from 12.1% in low volume centers (1 to 10 esophagectomies a year) to 7.5% in medium volume centers (11 to 20 esophagectomies a year) and 4.9% in high volume centers (> 20 esophagectomies a year) in the Netherlands. The incidence of respiratory complications was reported to range from 17% to 30%. In our series, the respiratory complication rate was significantly lower than that in recent reports. Early enteral nutrition to prevent fluid overload, which increases bronchial secretion, and therapeutic bronchofiberscopy or minitracheostomy to suction off excess sputum contribute to decreased rates of respiratory complications after an esophagectomy.
Locoregional recurrence occurred in from 1% to 27% [20, 22] of patients, and distant metastasis occurred in 18% to 31% in other reported studies. In our study, the thoracoscopic mobilization of the esophagus for esophageal cancer may be an acceptable approach because of the low incidence of respiratory complications, the low locorecurrence rate, and the low mortality rate. The overall 5-year survival rate of patients with a conventional right thoracotomy was reported to range from 22% to 52% [20, 22, 23]. According to the comprehensive registry of cases of esophageal cancer in Japan [23], the overall 5-year survival rate of patients with an esophagectomy for esophageal cancer was 36.1%. The 5-year survival rate was 70.2% in stage 0 disease, 64.5% in stage I, 51.5% in stage IIA, 34.0% in stage IIB, 19.8% in stage III, 13.7% in stage IVA, and 5.5% in stage IVB with regard to the UICC-pathological stage. In our series, the survival of patients with stage 0, I, II, and III disease compared satisfactorily with this annual report of the Japanese Society for Esophageal Diseases.
However, this series is a retrospective study in an institute. Further examination is needed to show the reliable effects of thoracoscopic esophagectomy for esophageal cancer. Both thoracoscopic and video-assisted esophagectomies are thus considered feasible and safe options for the treatment of esophageal cancer, and the survival time of patients with stage I and II disease has been found to be satisfactory.
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References
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Abstract
Introduction
