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Ann Thorac Surg 2001;72:306-313
© 2001 The Society of Thoracic Surgeons

Reviews

Transthoracic versus transhiatal resection for carcinoma of the esophagus: a meta-analysis

Jan B.F. Hulscher, MDa, Jan G.P. Tijssen, MDb, Hugo Obertop, MDa, J. Jan B. van Lanschot, MDa a Department of Surgery, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
b Department of Clinical Epidemiology and Biostatistics, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands

Address reprint requests to Dr Hulscher, Department of Surgery, Academic Medical Center/University of Amsterdam, Suite G-134, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
e-mail: j.b.hulscher{at}amc.uva.nl

Abstract

There is much controversy about the surgical approach to esophageal carcinoma: should an extensive resection be done to optimize long-term survival or should the extent of the operation be limited to obtain lower perioperative morbidity and mortality rates? We systematically reviewed the English-language literature published during the past decade, with emphasis on the differences between transthoracic and transhiatal resections regarding early morbidity, in-hospital mortality rates, and 3- and 5-year survival. Although transthoracic resections had significantly higher early (pulmonary) morbidity and mortality rates, 5-year survival was approximately 20% after both transthoracic and transhiatal resections.

For years the procedure of choice for esophageal resection has been the Lewis-Tanner operation, in which the tumor and periesophageal tissue with its adjacent lymph nodes are resected through a right-sided thoracotomy in combination with a laparotomy. In the past decades, two major surgical strategies to improve survival rates have emerged.

The first strategy uses radical resection to improve the cure rate, ie, an en bloc transthoracic resection (including the azygos vein, thoracic duct, overlying pleura, and pericardium) or an extended resection with two-field lymphadenectomy in which the en bloc resection is combined with a complete lymphadenectomy in the abdomen and chest [1, 2]. Some, mostly Japanese, surgeons add a lymph node dissection in the neck (three-field dissection) [3]. Alternatively, one could attempt to decrease early postoperative morbidity and mortality rates by limiting the extent of the operation. That outcome might be achieved by a transhiatal resection in which the esophagus is resected through a cervicoabdominal approach, thus avoiding a formal thoracotomy [4].

The purpose of the present study was to review the differences between transthoracic and transhiatal resections with respect to perioperative morbidity, early mortality rate, and long-term survival, limiting transthoracic resections to the standard (Lewis-Tanner), en bloc and two-field approaches. Because only a few western centers perform three-field dissections, these procedures were not included.

Patients and methods

A literature search (MEDLINE) was performed, and all human studies published in the English-language literature between 1990 and 1999 comparing transthoracic esophagectomy with transhiatal esophagectomy for carcinoma of the thoracic esophagus or the gastroesophageal junction were identified, using the medical subject headings "esophageal neoplasms" and "surgery." All titles and abstracts were scanned, and appropriate citations were reviewed. A manual search of the bibliographies of relevant papers also was done to identify publications for possible inclusion.

Included were prospective and retrospective comparative studies. Also included were single-institute observational studies regarding only transthoracic or transhiatal resections if at least 50 patients were included. When several articles reported on the same patient material, only the most recent article was included, except when one of the other articles was a randomized trial. Care was taken to avoid inclusion of (covert) double publications. Articles in which transthoracic and transhiatal approaches could not be distinguished were excluded. Also excluded were articles mixing benign and malignant diseases (which could not be distinguished) or papers in which the results of the surgical technique did not represent the main focus of the paper.

The main subject of the review was the difference between transthoracic and transhiatal resections. We ignored the differences between the transthoracic approaches. When possible, the analysis was done on the number of patients who had resection, and the patients in whom resection was attempted but not completed were excluded. When this was impossible to determine, the total number of patients was used in the calculations. For the TNM staging, the postoperative pathologic staging was used whenever available, otherwise the preoperative clinical staging outcomes were used.

The outcome of the studies was reviewed with special attention to early postoperative morbidity and mortality rates and long-term survival. Length of hospital stay, in-hospital mortality rate, and 3-year and 5-year survival were considered primary outcomes. Cardiac complications (when defined) included cardiac arrythmia, myocardial infarction, or left ventricular failure. Pulmonary complications (when defined) included pneumonia (ie, infiltrate on the chest x-ray or pathogenic sputum culture for which antibiotics were given), atelectasis (significant collapse on roentgenogram), pulmonary embolus, significant pleural effusion, and respiratory failure, while excluding pneumothorax when possible. Anastomotic leakage included both clinical leakage and subclinical leakage (only seen radiologically). Vocal cord paralysis included both persistent hoarseness of voice and vocal cord paralysis determined by (indirect) laryngoscopy. Chylous leakage consisted of the leakage of chyle managed either conservatively or operatively. Wound infection ranged from superficial redness to fulminant infection. Complications were recorded as stated in the article under review. When possible the exact number of specific complications were identified, otherwise the article was not included in the analysis (for that specific complication). We did not review adenocarcinoma and squamous cell carcinoma separately because tumor behavior, surgical approach, and long-term prognosis are generally considered to be comparable [5–7].

Statistical analysis
Studies were divided into the following three groups: randomized trials, comparative trials (including the randomized trials), and all studies (including the randomized, nonrandomized comparative, and noncomparative studies). Overall event rates were calculated as weighted averages of the trial-specific rates, with weights proportional to the total sample sizes of the trials. After calculating values for the noncomparative studies concerning transthoracic and transhiatal resections, these results were considered together as one comparative study in the overall group.

To perform the statistical overview, standard methods for combining information from 2 x 2 tables were used [8]. For each trial, 2 x 2 tables were constructed for the numbers of patients who had transthoracic and transhiatal procedures with regard to complications, in-hospital mortality rate, and survival. When data concerning specific topics were not stated, that study was excluded for that topic only.

Relative risks (RR) were calculated with the group of patients who had transhiatal resection as the reference group, so that treatment benefit for transthoracic resection was associated with a RR less than 1. p values were calculated using the {chi}2 or Fischer exact test where appropriate. The overall point estimates for RR were calculated using the Mantel-Haenszel estimate for the common RR. The corresponding 95% confidence intervals were calculated by the test-based method using the Mantel-Haenszel {chi}2 statistic [8].

P values for comparisons of means were calculated by applying the formula for Student t test on the mean differences, the total number of patients in each treatment arm, and an estimate of the standard deviation taking a weighted average of the standard deviation in the publications in which they were mentioned. The standard deviation obtained in the overall group was also used for the randomized and comparative papers. Tests for homogeneity of the odds ratio were performed for the main endpoints mortality rate and 5-year survival.

Results

Fifty articles were identified (Table 1) [9–58]. Twenty-four studies compared transthoracic with transhiatal resections [9–32]. There were six prospective comparative studies, three of which were randomized [9–14]. The other 18 comparative studies were retrospective [15–32]. Fifteen additional studies addressed only transthoracic resections (three of which were prospective), another 11 only transhiatal operations [33–58]. Patient and tumor characteristics are depicted in Table 2.


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  		Table 1. Articles Reviewed

 

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  		Table 2. Age and Clinicopathologic Staging of Patients Who Had Transthoracic or Transhiatal Resection of the Esophagus for Malignancy

 
Reported perioperative complications are given in Table 3. There were no important differences between transthoracic and transhiatal resections, although perioperative blood loss was significantly higher after transthoracic resection. The most important postoperative complications are tabulated in Table 4. Transthoracic resections had a higher risk of pulmonary complications, chylous leakage, and wound infection. Anastomotic leakage and vocal cord paralysis were more frequent after transhiatal resections.


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  		Table 3. Peroperative Complications, Blood Loss and Operative Time in Patients Who Had Transthoracic Esophagectomy or Transhiatal Esophagectomya

 

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  		Table 4. Postoperative Complications, Hospital Stays, and Hospital Mortality in Patients Who Had Transthoracic or Transhiatal Resectiona

 
Patients stayed slightly but significantly longer in the intensive care unit after transthoracic resection, and hospital stay was also significantly prolonged. The overall in-hospital mortality rate in both groups taken together was 7.5%. The in-hospital mortality rate was significantly higher after transthoracic resections, 9.2% versus 5.7% (RR 1.60, 95% confidence interval [CI] 1.89, 1.35). This difference did not persist in the randomized trials only; in fact there were more in-hospital deaths in the transhiatal group when only the randomized trials were considered, although this difference did not reach statistical significance.

The overall 3-year and 5-year survival rates for all studies combined were 25.6% and 20.6%. When all data were combined for all tumor stages, there was no difference in 3-year survival rates between transthoracic and transhiatal resections (25.0% versus 26.7%, RR 0.94, 95% CI 0.83, 1.07). When only the comparative trials were considered there was a statistically significant difference in 5-year survival favoring transthoracic resection, but when all studies were included, the 5-year survival ratewas not significantly higher after transthoracic resection (23.0% versus 21.7%, RR 1.06, 95% CI 1.18, 0.96) (Table 5). Tests for homogeneity of the odds ratio did not show statistically significant heterogeneity of the odds ratios concerning mortality and 5-year survival. (p = 0.30 and 0.06, respectively)


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  		Table 5. Long-Term Survival After Transthoracic or Transhiatal Esophagectomy for All Tumor Stages Combineda

 
Comment

There has been much debate about the optimal type of resection for esophageal cancer. Only three randomized trials have been published, including a total of only 138 patients (of a total of 7,527 patients in the articles reviewed, Table 1). The other studies are mostly retrospective, consecutive case studies that described the authors’ experience with one or several procedures, thereby reflecting the personal preference of the surgeon. The paucity of prospective comparative studies (six of 50, three of which were randomized) might be due to the relatively low number of procedures performed. There was one large noncomparative study of transhiatal resections in 1,085 patients, which amounts to approximately one third of all patients to have had this procedure. This study, therefore, weighs heavily on the data, improving the figures of the transhiatal procedures because of its excellent results. Many complications were not defined properly, which makes comparison difficult and might be the cause of the large variation in incidence of some postoperative problems such as pulmonary complications.

Because of the low number of patients, most studies encompassed many years. Therefore neoadjuvant therapies, anesthesiologic techniques, and administration of perioperative antibiotics often varied between the studies and between different subgroups within a study. This variation probably influenced several outcomes, including early deaths and long-term survival.

The lack of proper controlled studies is a major limitation in the field of esophageal surgery. Randomized trials with sufficient numbers of patients should be done to compare the different types of resection. Recently, enrollment was completed for a randomized multicenter trial in The Netherlands comparing transthoracic resection with two-field lymphadenectomy and transhiatal resection, results of which will be available early 2001.

When all data were combined, perioperative complications did not differ significantly between transthoracic and transhiatal procedures (Table 3). Although these complications are generally feared, there is a low risk of injury to the major airways or major hemorrhage during transhiatal resections. Blood loss was significantly greater after transthoracic resections, which might influence immunologic factors. Although operative time was significantly longer for transthoracic resections in the randomized trials, this difference disappeared when all studies were combined, which might result from more operator experience.

Postoperative complication rates varied between 40% and 80%, partly depending on the applied criteria, and tended to decrease with increasing experience [48, 59, 60]. Overall, transthoracic resections resulted in worse postoperative complications than transhiatal resections, with the exception of vocal cord paralysis and anastomotic leakage (Table 5). However, those differences did not persist when only the randomized trials were analyzed. This finding might be due to the low number of patients in the randomized studies or to the lack of specific definitions for the different complications. Moreover, many surgeons consider transhiatal resections especially suited for older patients who have more comorbidity, which might also negatively influence the incidence of postoperative complications [11, 12, 22, 27, 61].

Theoretically, transthoracic resections have the disadvantages of a formal thoracotomy, which might result in a higher number of pulmonary complications. This was confirmed by the present data. Transthoracic resections can be associated with transient deterioration of pulmonary function during one-lung ventilation in the left-lateral position, although this might be partly compensated for during the intervention when two-lung ventilation is resumed [11]. With modern anesthesiologic techniques and perioperative respiratory care the incidence of cardiopulmonary complications might decrease.

The incidence of anastomotic leakage varied widely (3% to 50%), which is probably a definitional problem: some authors mentioned only clinically significant leaks, whereas others included both subclinical and clinical leaks. Overall there was a significant difference favoring transthoracic approaches (Table 4), which is probably partly due to the location of the anastomosis. In transthoracic resections, the anastomosis can be made cervically, but often it is made in the chest. During transhiatal procedures, the anastomosis is always made in the neck. A cervical anastomosis carries a higher risk of leakage than an intrathoracic anastomosis, but the risk of (highly lethal) mediastinitis diminishes when leakage occurs [13, 15, 18, 23, 24, 39, 61]. However, most cervical leakages are subclinical, ie, only seen radiologically, and do not require surgical exploration because they resolve spontaneously 10 to 35 days postoperatively [14, 21, 23, 24, 39]. When surgical drainage is required, opening the cervical incision almost always provides sufficient drainage. Although the risk of mediastinitis might be diminished after a cervical anastomosis, severe complications have been described [24, 61]. Unfortunately, approximately one third of the patients who have anastomotic leakage in the neck will develop subsequent stricture that jeopardizes the long-term functional result [48].

Vocal cord paralysis from injury of the recurrent laryngeal nerve is another frequent complication of esophagectomy, but frequently the paralysis resolves within a few months [13, 62]. A high incidence of vocal cord paralysis was mentioned after cervical anastomoses, after both transthoracic and transhiatal procedures, indicating that the recurrent nerve is mainly at risk during the cervical dissection and the construction of the anastomosis [8, 52, 63–65].

Twenty years ago the average hospital mortality rate after resection of esophageal carcinoma was 29% [62]. Ten years later the resection mortality rate was more than halved to 13% [1]. Today, the average hospital mortality rate is almost halved again: when all data were combined the hospital mortality rate was 7.5%. Mortality rates varied widely (0% to 27.8%) and decreased with increasing experience and a higher hospital volume [66, 67]. In experienced centers, hospital mortality rates should be below 5%.

Although most individual reports did not find significant differences in in-hospital mortality rates between transthoracic and transhiatal approaches, the overall in-hospital mortality rate was significantly higher after transthoracic resections (Table 4), despite that many surgeons performed transhiatal resections on older patients with more comorbidity [11, 12, 22, 27, 61]. This finding was confirmed recently by Rindani and coworkers [68], who reviewed the literature from 1986 to 1996 and found almost the same mortality rates, 9.5% for Lewis-Tanner resections compared with 6.3% for transhiatal resections. However, in their series pulmonary complications occurred more often after both transthoracic resections and transhiatal resections (25% and 24%, respectively), which might be a reflection of the improvement in pulmonary care or better definitions [68]. The main cause of death was probably respiratory insufficiency. Transthoracic resections lead to more pulmonary complications, which might also be reflected in the prolonged stay in the intensive care unit. Transthoracic resections had a higher risk of chylous leakage or wound infection, but those complications rarely were lethal.

The overall 5-year survival rate in the 1990s of 20.7% is not substantially better than the 5-year survival rate described by Müller and associates [1] (20% during the period 1980 to 1988) or Earlam and Cunha-Melo [69] (18% during the period 1953 to 1978), whether transthoracic or transhiatal approaches were used. There was no difference in survival at 3 or 5 years postoperatively between transthoracic and transhiatal resections (Table 5) although the groups were generally comparable with regard to age and TNM stage. (However, there were slightly more early and advanced tumors in the transthoracic group [Table 2].) When only the comparative studies were considered, there was a difference favoring transthoracic resection. Rindani and coworkers [68] found approximately the same 5-year survival rates in their review (26% and 24% for transthoracic and transhiatal procedures, respectively). After both transthoracic and transhiatal resections, the 5-year survival rate was not much lower than the 3-year survival rate, reflecting the fact that aggressive behavior of the tumor might be more important than surgical approach. In the reviewed studies, most authors did not report different survival rates between transthoracic and transhiatal resections when tumor stage was taken into account, although in selected subgroups a difference was suggested [14, 16, 27]. However, selection bias and stage migration might also influence these results. Stage migration is the phenomenon that a more extended lymph node dissection increases the number of resected nodes and thereby the chance of nodes being positive. This might lead to an upgrade of the tumor stage after more extended resections, which might have a favorable effect on the outcome statistics.

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