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Ann Thorac Surg 2006;81:1083-1089
© 2006 The Society of Thoracic Surgeons

Original article: General thoracic

Risk Analysis in Resection of Thoracic Esophageal Cancer in the Era of Endoscopic Surgery

Takeshi Shiraishi, MD a , * , Katsunobu Kawahara, MD b , Takayuki Shirakusa, MD a , Satoshi Yamamoto, MD a , Takafumi Maekawa, MD a

a Department of Surgery II, Fukuoka University School of Medicine, Fukuoka
b Department of Surgery II, Oita University School of Medicine, Oita, Japan

Accepted for publication August 29, 2005.

* Address correspondence to Dr Shiraishi, Department of Surgery II, Fukuoka University School of Medicine, 7-45-1 Nanakuma, Jonan-ku, Fukuoka City, Fukuoka 814-0180, Japan (Email: tshiraishi-ths{at}umin.ac.jp).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: Surgical outcomes after thoracoscopic esophagectomy were compared with those after open esophagectomy, and the prognostic values of factors potentially related to mortality and morbidity were evaluated.

METHODS: We performed a retrospective chart review of 153 patients who underwent esophagectomy for thoracic esophageal cancer. The thoracic surgical procedures were categorized into the following three groups: esophagectomy under standard thoracotomy (n = 37), assisted thoracoscopic esophagectomy with utility minithoracotomy (n = 38), and complete thoracoscopic esophagectomy (n = 78). Mortality and morbidity were compared among the three groups. Then, in a separate multivariate analysis, data on 14 potentially prognostic variables were extracted, and the relation to postoperative outcomes was examined.

RESULTS: Respiratory complications were the most frequent complications in all three groups, and their rate of occurrence was not significantly among the three groups. The 30-day and in-hospital mortality rates were significantly higher in the open group than in the other groups. Multivariate analysis demonstrated that patient age, sex, induction chemoradiation, and forced expiratory volume were independently significant contributing factors for respiratory complications, while the serum total protein concentration and open esophagectomy were significant factors for in-hospital mortality.

CONCLUSIONS: Our results demonstrated that respiratory complications are still the main cause of operative morbidity when using the thoracoscopic esophagectomy protocol and that use of the thoracoscopic procedure does not decrease the risk of respiratory complications. The use of the thoracoscopic procedure improved postoperative in-hospital mortality. The advantages of thoracoscopic esophagectomy should be investigated further. At this point in time, however, thoracoscopic esophagectomy can be considered a feasible, safe, and advantageous surgical option.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Surgical resection of thoracic esophageal carcinoma is a challenging and high-risk procedure [1]. The mortality and morbidity rates have recently improved owing to advances in surgical technique and postoperative management, but are still high compared with other gastrointestinal or general thoracic surgeries. Both the mortality and morbidity are caused mainly by major respiratory problems that occur with or without septic complications, and that have been considered to be due, at least in part, to the invasiveness of the thoracic procedure [2–6]. Numerous analyses have been conducted to clarify the positive factors that impact mortality and morbidity after esophagectomy [1–4, 7, 8].

During the past decade, several groups, including our own, have adopted a thoracoscopic approach in esophageal resection with the hope of reducing the invasiveness and improving the postoperative outcome [9–18]. We developed and started using a protocol for thoracoscopic esophagectomy in 1995, initially restricting its use to cases of T2 or less advanced esophageal cancer without induction chemoradiation therapy. Over the next 10 years, along with the development of new endoscopic surgical techniques and new tools for thoracoscopic surgery, our procedure progressed from a so-called assisted thoracoscopic esophagectomy, in which a minithoracotomy is used to provide visual and handling support, to a more sophisticated complete thoracoscopic esophagectomy, in which the thoracic procedure is performed entirely under the thoracoscopic view with no minithoracotomy. Over the same period, the indications for thoracoscopic esophagectomy were gradually expanded. The indications currently include an advanced tumor invading the esophageal adventitia (T3 disease), irrespective of whether induction chemoradiotherapy was performed. Based on this policy, we have performed 116 assisted thoracoscopic or complete thoracoscopic esophagectomies and 37 open esophagectomies for thoracic esophageal carcinoma in the past 10 years.

The purpose of this study was to compare surgical outcomes after thoracoscopic esophagectomy with those after conventional open esophagectomy and, in a separate multivariate analysis, to evaluate the ability of numerous clinical, laboratory, and surgical factors to predict mortality and morbidity after esophagectomy.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
We performed a retrospective chart review of 153 consecutive patients who underwent three-field esophagectomy for thoracic esophageal cancer at the Department of Surgery II at Fukuoka University Hospital from 1995 to 2004.

Patient Groups
We first began performing thoracoscopic esophagectomies using a so-called assisted thoracoscopic protocol, in which a utility minithoracotomy (6 to 8 cm width) is made for visual and handling access. Owing to the progress in endoscopic surgical devices and surgical skill over the last decade, the procedure has progressed from a so-called assisted thoracoscopic esophagectomy to a complete thoracoscopic esophagectomy without a minithoracotomy. In the present analysis, therefore, the thoracic surgical procedures were classified as one of three types: conventional esophagectomy under a standard posterolateral thoracotomy (open group, n = 37); assisted thoracoscopic esophagectomy (assisted thoracoscopic group, n = 38); and complete thoracoscopic esophagectomy (complete thoracoscopic group, n = 78).

A thoracoscopic approach—either assisted or complete—was basically indicated if patients had (1) absence of contiguous tumor spread to an adjacent structure, (2) no prior thoracic surgery, (3) no extensive pleural adhesion, and (4) adequate pulmonary function capable of sustaining single-lung ventilation. Patients who had received induction chemoradiation therapy were considered as contraindicated for thoracoscopic esophagectomy during the first 5 years of this series (1995 to 1999), as there was the possibility of severe adhesion around the radiation area that could have interfered with the thoracoscopic approach. Over the second 5 years of the series (2000 to 2004), however, such patients were considered eligible owing to technical advances in thoracoscopic technique. Patients who did not meet the above criteria received conventional esophagectomy under standard posterolateral thoracotomy. Induction chemoradiation therapy was indicated if the patient had T2 or more-advanced disease and showed satisfactory renal and bone marrow function. The protocol for induction chemoradiation during this period was basically low-dose cisplatinum (10 mg/day, days 1 to 5 for 4 weeks) and 5-fluorourasil (250 mg/day, days 1 to 5 for 4 weeks) with 40.5 Gy concurrent radiation.

Surgical Technique
The techniques we used for the thoracoscopic esophagectomy and reconstruction have been described elsewhere [9]. Reconstruction using a gastric tube or left or right colon graft was performed followed by resection of the thoracic esophagus. Briefly, the patient was first placed in a supine position. Circumferential mobilization of the cervical and upper mediastinal esophagus was performed through a neck collar incision. Bilateral cervical lymph node dissection, including the nodes around the bilateral recurrent nerve and upper mediastinal esophagus, was performed if necessary. The cervical esophagus was transected 3 cm distal from the cricopharyngeal sphincter. The abdominal esophagus was divided through an upper median laparotomy 10 cm in length and transected at 1 to 2 cm above the esophagogastric junction. After dissection of the perigastric and celiac axis lymph nodes, a gastric tube was prepared and elevated through the substernal route. If the stomach was not available for reconstruction, other conduits such as a right or left colon graft were used through a subcutaneous route. The procedure was completed with an anastomosis between the cervical esophagus and the reconstruction conduit.

The patient was then placed in the decubitus position under general anesthesia with one-lung ventilation. Generally, six access ports (Fig 1)with respective internal diameters of 5 mm or 11.5 mm were introduced at the sixth and eighth intercostal spaces on the posterior axillary line (1, 2), the fifth and seventh intercostal spaces on the middle axillary line (3, 4), and the fourth and sixth intercostal spaces on the anterior axillary line (5, 6).


Figure 1
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  		Fig 1. Access ports for complete thoracoscopic esophagectomy. Six access ports were introduced at the sixth and eighth intercostal spaces on the posterior axillary line (1, 2), the fifth and seventh intercostal spaces on the middle axillary line (3, 4), and the fourth and sixth intercostal spaces on the anterior axillary line (5, 6). The operator and main assistant mainly used access ports 1, 2, 3, and 5 through the small trocar (internal diameter, 5 mm). Another assistant used ports 4 and 6 for access of the thoracoscope and lung retraction device.

 
In the complete thoracoscopic group, all procedures were performed through the access ports with the endosurgical instruments completely under a thoracoscopic view; however, in the assisted thoracoscopic group, a minithoracotomy lengthened 6 to 8 cm was made at the position of port 1 for direct visual and handling access. The azygous vein was divided and transected using an endoscopic stapler for vascular use. The mediastinal pleura was opened using an ultrasonic coagulator from the top to the bottom of the mediastinum to expose the entire esophagus. After the thoracic esophagus was completely divided from the mediastinal structure with the surrounding lymph nodes, the esophageal specimen was put in an vinyl bag and pulled out from the minithoracotomy. The mediastinal lymph nodes, including the nodes around the right and left laryngeal nerve, were then dissected.

In the open group, the thoracic procedures were performed under a standard posterolateral thoracotomy at the fourth or fifth intercostal space.

Intergroup Comparison of Mortality and Morbidity
Variables related to mortality and morbidity, including respiratory, cardiac, and other surgical complications such as anastomotic leak or recurrent nerve palsy, were recorded in order to assess differences in their prevalence among the three treatment groups. Patients who had already been weaned from anesthesia, but for whom pneumonia, atelectasis, or respiratory distress syndrome necessitated airway reintubation or tracheostomy for ventilation support, or airway suctioning for increased production of sputum, were considered to have major respiratory complications. Patients requiring reintubation for unilateral or bilateral vocal cord palsy were not included within this group. In-hospital mortality was defined as death occurring during hospitalization after surgery regardless of the length of stay, but excluded death due to tumor relapse.

Risk Analysis for Mortality and Morbidity
The following 14 clinical, laboratory and surgical variables were extracted to estimate the mortality and morbidity (see Appendix): age, sex, body mass index (body weight [kg] / height [m]2), %FVC (percent forced vital capacity), %FEV1 (percent forced expiratory volume in 1 second), serum total protein concentration (g/dL), current cigarette consumption, preoperative (induction) chemoradiotherapy, period of surgery (1995 to 1999 versus 2000 to 2004), thoracic surgical procedure (open versus assisted thoracoscopic versus complete thoracoscopic), reconstruction conduit (gastric tube versus colon), depth of tumor penetration (invasion to the adventitia versus no invasion to the adventitia), operation time (minutes), and blood loss during surgery (mL).

Statistical Analysis
Continuous data are expressed as the mean ± SD. Discrete data are presented as absolute numbers or percentages. Differences among groups were examined by two-way analysis of variance for continuous variables and {chi}2 analysis for categorical variables. The relations among the 14 variables and the outcome variables were examined by univariate logistic regression analysis. Based on these results, multivariate stepwise logistic regression analysis was performed on the variables deemed significant (p < 0.1). Differences were considered to be statistically significant when the p value was less than 0.05.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
The characteristics of the 153 patients who received three-field subtotal esophagectomy and reconstruction of the thoracic esophagus are described in Table 1. There were 125 men and 28 women, with a mean age of 63.1 ± 8.9 years. The pathologic types of tumor were squamous cell carcinoma (n = 144 cases; 94%), adenocarcinoma (n = 4), small-cell carcinoma (n = 2), carcinosarcoma (n = 2), and undifferentiated carcinoma (n = 1). The data are categorized according to the type of thoracic surgical procedure. There were significant differences among the groups in age, the period of surgery, the depth of tumor penetration, operation time, and blood loss during surgery; thus, we should consider that there were some biases in patient selection among the procedure groups.


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  		Table 1. Characteristics of Patients Who Received Three-Field Subtotal Esophagectomy and Reconstruction for Thoracic Esophageal Cancer
 
Table 2 show the rates of postoperative complications and operative (within 30 days) or in-hospital mortality that occurred as a consequence of each of the three procedures in the 153 patients. Respiratory complications occurred in 24.2% of all patients and were five times more frequent than cardiac complications. However, there was no significant difference in the prevalence of either respiratory or cardiac complications among the three surgical subgroups. Anastomotic leak was more frequent in the open group than in the assisted thoracoscopic or complete thoracoscopic groups. Recurrent nerve palsy, including temporary palsy, occurred in 40% of cases, and its rate of occurrence was not significantly different among the three treatment groups. The 30-day and in-hospital mortality rates were significantly higher in the open group than in the other two treatment groups.


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  		Table 2. Postoperative Complications and Death Among 153 Patients Who Received Three-Field Subtotal Esophagectomy
 
Prognostic Factors
Table 3 shows the predictors considered in the univariate analysis and their relation to morbidity and mortality. Regarding the respiratory complications, univariate analysis of variance identified seven covariates that were significantly (p < 0.05) or nearly significantly (p < 0.1) related to the risk of respiratory complications, including the patient's age, sex, %FVC, %FEV1, induction chemoradiation therapy, depth of tumor penetration, and blood loss during surgery. Stepwise logistic regression analysis was performed on these seven variables and identified age, male sex, and induction chemoradiotherapy as the significant contributory factors. Because %VC, depth of tumor penetration, and blood loss were not identified as important covariates in this model, we eliminated them and performed a second stepwise logistic regression analysis. Finally, the risk of respiratory complication was significantly associated with age, male sex, and induction chemoradiotherapy (Table 4). The results of multivariate logistic regression analysis for other complications or mortality are presented in Table 4. Multivariate analysis demonstrated that two covariates, the serum total protein concentration and the thoracic procedure performed, were significant factors for in-hospital mortality.


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  		Table 3. Variables and Univariate Analysis of Their Relation to Morbidity and Mortality
 

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  		Table 4. Results of Multivariate Logistic Regression Analysis for Complications or Mortality
 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
Although endoscopic surgeries are less invasive, in the field of thoracic surgery their use has generally been restricted to cases of benign and malignant lung diseases. There have been numerous reports, including our own, on thoracoscopic major pulmonary resection for early stage lung cancer over the last decade, and most have emphasized that the procedure is less invasive than a standard resection, but has a comparable long long-term survival rate [19–24]. The thoracoscopic pulmonary lobectomy is now accepted, if not universally, then at least as an alternative surgical option for early stage lung cancer.

Cushchieri and associates [11] published the first report on thoracoscopic esophagectomy in 1992. During the early era of thoracoscopic surgery after this publication, several groups made alterations to the procedures, or developed new ones [9, 10, 12, 13, 18, 25]. The esophagectomy itself is associated with high mortality and morbidity rates, especially in terms of pulmonary complications, and thus the thoracoscopic esophagectomy captured the interest of surgeons as a minimally invasive technique that might lower this surgical risk. Regarding the advantages over standard open esophagectomy, however, very few reports have proven the less invasiveness of thoracoscopic esophagectomy such as preserving postoperative lung function or decreasing the incidence of postoperative complications [17, 25, 26]. The other matter of concern regarding the feasibility of thoracoscopic esophagectomy is its oncologic propriety, which is still under discussion and has been over a period of years. Several reports have asserted that the procedure is associated with acceptable long-term survival rates comparable to those in the conventional procedure under standard thoracotomy [25–27]. Based on this limited information about the advantages of thoracoscopic esophagectomy, the most accurate current statement that can be made is that it is a "procedure with unknown less invasiveness and probably with an acceptable prognosis." We suspect that the reason why endoscopic esophagectomy has not yet been widely accepted by surgeons may be because its advantages are still not clear.

In 1995, we started the thoracoscopic esophagectomy program that was firstly indicated for selected patients with relatively early stage esophageal cancer whose tumors had not invaded the adventitia and who had not undergone prior chemoradiation therapy. Because of the technical progress that has been made since and the progress in the instruments used, the indications for endoscopic surgery have been expanded. In addition, our endoscopic surgical procedure has advanced from so-called assisted thoracoscopic esophagectomy with utility minithoracotomy to 100% thoracoscopic esophagectomy in the past 10 years. Our current policy is to perform endoscopic esophagectomy on patients whose tumor is not invading neighboring organs or other mediastinal structures (T4 disease), who do not have an anatomical problem, such as massive pleural adhesion, that would prevent the completion of the endoscopic surgery, and who can tolerate unilateral ventilation irrespective of induction chemoradiation therapy. As a result, either an assisted or complete thoracoscopic esophagectomy was successfully performed in almost 82% of our cases during the latter half of the 10-year study period (2000 to 2004), whereas only 69.3% were given this procedure during the first half of this period (1995 to 1999; p < 0.01).

Our results demonstrated that the rates of both respiratory and cardiac complications were similar between the open and thoracoscopic esophagectomy groups. The hospital mortality rate was 7.1% overall, 13.5% in the open thoracoscopic group, and 2.6% in the complete thoracoscopic group (p = 0.003). The incidence of anastomotic leak was significantly lower in the endoscopic surgery group. These findings suggest that either form of thoracoscopic esophagectomy is a feasible surgical option. However, we should consider that there were some biases in patient selection among the procedure groups, including those for age, depth of tumor penetration, and operation time. Thus, a comparison of the outcome variables, including complications or mortality rates, among the three groups would be rather meaningless. A prospective randomized study would be ideal, but is nearly impossible to conduct within a reasonable time frame. Thus, we used multivariate risk analysis to investigate the effects of the thoracoscopic surgical procedure on postoperative course.

Respiratory complications, which have been recognized as the most common complication after esophagectomy, are reported to be strongly associated with postoperative mortality [1, 4, 28–30]. Since the main advantage of the thoracoscopic procedure is its reduced invasiveness due to minimization of the chest trauma, we suspected that there would be less morbidity from pulmonary complications. The results of the multivariate analysis, however, showed that the factors associated with pulmonary complication were age, male sex, and induction chemoradiation. There was no significant relation between the thoracic surgical procedure and incidence of major pulmonary complications. Theoretically, the thoracoscopic procedure minimizes surgical trauma to the chest wall, including postoperative pain, which helps preserve lung and chest wall compliance and may be linked to improved tolerance against respiratory complications. A possible explanation for this regrettable result is that the degree of surgical insult caused by the surgical stresses involved in thoracic surgery far outweighed any possible advantages of the thoracoscopic procedure. Regarding one of the positive factors related to respiratory complications, induction chemoradiation, several investigations have reported that there was no important detrimental effect on surgical morality or morbidity, but our results indicated that this was one of the most significant covariates on postoperative pulmonary complications [31–36]. Since induction chemoradiation has been reported to decrease the lung diffusion capacity, it may increase the incidence of respiratory complications [37].

There were two significant risk factors for in-hospital mortality: the serum total protein concentration and the thoracic surgical procedure. We found the thoracoscopic procedure to have a beneficial effect on in-hospital mortality. The in-hospital mortality is a complex outcome variable based on several factors, including the patients' surgical tolerance, and, therefore, explaining this significant relation is somewhat difficult. However, we thought it likely that the endoscopic procedure minimized tissue damage, thus reducing the systemic inflammatory response or the postsurgical immunosuppressive status, which may be linked to improved mortality.

In summary, our current results demonstrated that thoracoscopic esophagectomy does not improve operative morbidity from the point of view of pulmonary complications. However, the use of the thoracoscopic procedure improved postoperative in-hospital mortality. The advantages of thoracoscopic esophagectomy over the standard procedure need to be investigated further, possibly by using a randomized prospective trial. At this time, however, we can state that there are no survival disadvantages when using thoracoscopic esophagectomy over the conventional method for thoracic esophageal cancer, but there is an advantage in terms of reduced invasiveness. We therefore believe that thoracoscopic esophagectomy is a feasible, safe, and advantageous surgical option for selected cases of thoracic esophageal carcinoma.


   Appendix
 
Variables Collected and Used in Analysis


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   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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