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Ann Thorac Surg 2002;73:1035-1040
© 2002 The Society of Thoracic Surgeons

Original article: general thoracic

Results of surgical treatment of adenocarcinoma of the gastric cardia

Giovanni de Manzoni, MD*a, Corrado Pedrazzani, MDa, Felice Pasini, MDb, Alberto Di Leo, MDa, Emilia Durante, MDb, Gabriele Castaldini, MDa, Claudio Cordiano, MDa

a First Division of General Surgery, University of Verona, Verona, Italy
b Division of Medical Oncology, University of Verona, Verona, Italy

Accepted for publication November 19, 2001.

* Address reprint requests to Dr de Manzoni, 1a Chirurgia Clinicizzata, Ospedale di Borgo Trento, Piazzale Stefani 1, 37126 Verona, Italia, Italy
e-mail: chirurgia.urgenza{at}univr.it


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Comparison among different studies regarding adenocarcinoma of the cardia has been difficult since the Siewert classification was introduced. This study analyzed the experience of a single institution in the treatment of gastric cardia cancer with the aim of assessing principal prognostic factors and long-term outcome.

Methods. The results of 96 patients who underwent resection with curative intent for gastric cardia cancer at the First Division of General Surgery, University of Verona, from January 1988 to February 2000, were analyzed statistically with special reference to Siewert type.

Results. Despite a high number of curative resections (85.4%), the 5-year survival rate was poor (24%) for all Siewert types (p = 0.8), and for early tumors (51%) also. Chance of cure was limited to pN0 and pN1 patients. Multivariate analysis showed that microscopic or macroscopic residual tumor and pN-positive categories had a significantly higher risk of death (risk ratio, 2.18 and 2.68, respectively) and the pN2 and pN3 category had the most negative prognostic factor (risk ratio, 7.6).

Conclusions. The long-term prognosis for gastric cardia cancer remains poor and is independent of Siewert type, with cure limited to pN0 and pN1 patients.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Recent epidemiologic studies clearly indicate that despite the decreasing overall incidence of gastric cancer in Western countries, there has been a rising prevalence of adenocarcinomas of the gastroesophageal junction [1–4]. A comparison of reports from different institutions is difficult to make as there is a great deal of controversy regarding critical issues in the management of this type of cancer, such as definition, classification, staging, surgical strategy, and the role of neoadjuvant therapy.

In this study, cancer of the cardia was defined according to the classification of Siewert and associates [5], recently approved during the 2nd International Gastric Cancer Congress in Munich in April 1997. This classification is based on the topographic characteristics of adenocarcinomas involving the gastroesophageal junction and is divided into three types. Type I is a tumor with the center lying 1 to 5 cm above the anatomic gastroesophageal junction; type II is a tumor with the center lying 1 cm above to 2 cm below the anatomic gastroesophageal junction; and type III is a tumor with the center lying 2 to 5 cm below the anatomic gastroesophageal junction.

At present, only a few reports have studied surgical strategy and prognosis according to the Siewert classification [6–8].

The aim of this study was to analyze a 12-year experience of a single institution in the management of adenocarcinoma of the cardia to assess whether lymph node involvement, T status, and Siewert classification were identifiable as prognostic factors affecting survival and long-term outcome.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Between January 1988 and February 2000, 96 consecutive patients with histologically proven primary adenocarcinoma of the cardia underwent resection with curative intent at the First Division of General Surgery, University of Verona, Italy. Median age was 67 years (range, 27 to 84 years), and 84 patients were male. All of the 96 patients underwent the same staging workup including barium swallow, endoscopy with biopsy, and computed tomography of the chest and upper abdomen. Endosonography was performed in 47 patients. Patients with unresectable or metastatic tumors and those with a poor general status precluding an extensive surgical procedure were excluded.

From 1994 patients were prospectively classified according to the classification of Siewert and colleagues [5]. Previously, patients were classified according to the classification of the Japanese Society on Esophageal Disease [9]. As the collected data included overall length of extension, and length of invasion of stomach and esophagus, it was therefore possible to accurately convert these cases into the Siewert classification.

The choice of surgical approach was based on the location of the tumor center, as described by Siewert and Stein [10], and on the length of invasion of the esophagus, with the principal aim of achieving complete surgical resection. No patients underwent neoadjuvant or adjuvant radiochemotherapy

The standard procedure for type I tumors was a right thoracotomy with a subtotal esophagectomy with proximal gastric resection. The procedure of choice for type III tumors was a total gastrectomy with transhiatal resection of the distal esophagus. A transthoracic approach was necessary in two cases to achieve a clear oral margin. Type II tumors were treated by subtotal esophagectomy, as in type I cancers, or by total gastrectomy with transhiatal or transthoracic resection of the distal esophagus, as in type III tumors; the type of resection was chosen in order to obtain clear proximal and distal margins. The mode of reconstruction after subtotal esophagectomy was a gastric tube, whereas a jejunal Roux-en-Y reconstruction was performed after total gastrectomy.

Lymph node dissection was classified according to the Japanese Gastric Cancer Association rules: D1 lymphadenectomy (resection of perigastric nodes in position 1 to 4), D2 lymphadenectomy (resection of nodes in position 1 to 11), and D3 lymphadenectomy (resection extended to the nodes in position 12 to 16) [11]. The preferred lymph nodal dissection was a standard mediastinal and D2 abdominal for type I tumors and D2 or D3 abdominal lymphadenectomy comprising nodes of the lower posterior mediastinum for type II and type III tumors. D1 dissection was chosen in the cases of palliative resection or high-risk patients. Lymph nodes around the root of the mesenteric vein (station 14) and along the middle colic artery (station 15) were not routinely dissected. Lymphadenectomy at the splenic hilum was limited to patients with enlarged nodes or tumors reaching the gastric fundus, and it was achieved by pancreas-preserving splenectomy [12]. Perigastric lymph nodes were dissected from the excised specimens by the surgeons immediately after resection, assigned to the appropriate station according to the Japanese Gastric Cancer Association classification, and sent for histologic examination. To avoid errors caused by difficulties in assigning the lymph nodes to the correct lymph node stations after en bloc resection, the N2 and N3 nodes were subdivided by the surgeon himself during lymphadenectomy as described in a previous study [13].

Tumors were staged according to the 1997 pathologic classification (pTNM) of the International Union Against Cancer [14]. The histologic classification followed the criteria of Lauren [15].

After discharge from the hospital all patients were personally followed up at 4 months and subsequently at 6-month intervals. Median follow-up was 38 months (range, 4 to 144 months), and no patients were lost to the follow-up procedure.

In 82 cases there was pathologic confirmation of curative resection (classified as R0), whereas residual tumor was present in 14 cases, either microscopic (R1) or macroscopic (R2). The 14 cases with R1 or R2 resection were excluded from the survival analysis. All survival analyses were calculated, including operative deaths. Survival curves were estimated with the Kaplan-Meier method and compared by the log-rank test; deaths from causes other than gastric cardia cancer were censored. Multivariate analysis was performed by Cox regression model. Variables were chosen according to the current literature. In particular, two demographic variables (sex and age), three well-known prognostic factors (residual tumor, depth of tumor invasion, and nodal involvement), and a novel prognostic factor, whose relevance has not been elucidated yet, were introduced in the model. Tumor stage was not entered as a variable because it is highly collinear with pT and pN classes. The {chi}2 test was used to compare the frequencies of different ordinal data.


   Results
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 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
The type of resections and reconstructions in relation to different Siewert type are reported in Table 1. In this series of 96 patients, the total number of dissected lymph nodes was 2,779, with an average (± standard deviation) of 29 ± 17.3 dissected nodes per case (median, 25.5; range, 1 to 108). The mean number of metastatic nodes was 7.5 ± 8.8 (median, 4.5; range, 0 to 39) in the overall series, and 9.3 ± 8.9 (median, 7; range, 1 to 39) in pN-positive patients. A mean of 16.4 ± 8.4 nodes was removed by D1 lymphadenectomy, 33.9 ± 17.5 by D2 or D3 lymphadenectomy.


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  		Table 1. Type of Resection in Relation to Siewert Type for the 96 Patientsa

 
Postoperative general and surgical complications occurred in 27 patients (28%); in-hospital mortality was 6.7% (6 patients). Total gastrectomy with transthoracic distal esophagectomy showed the highest rate of morbidity (4 of 8 patients) and mortality (1 of 8 patients). Subtotal esophagectomy compared with total gastrectomy with transhiatal esophageal resection was associated with a similar rate of mortality (5.7% versus 4.2%) and a slightly higher number of complications (31.4% versus 20.8%, p = 0.3). No differences in morbidity (25.9% versus 29%, p = 0.8) or mortality (3.7% versus 7.2%, p = 0.5) were observed between D1 and D2 or D3 lymphadenectomy. In 27 patients (11 cases of type II and 16 of type III) abdominal lymph node dissection included paraaortic nodes (D3 lymphadenectomy).

A curative resection (R0) was achieved in 82 cases (85.4%), whereas 14 cases showed residual tumor (microscopic [R1] in 10 cases and macroscopic [R2] in 4 cases). Median survival for the R1 and R2 patients was 7 months and for R0 was 19 months. The 5-year survival rate for patients with curative resection (R0) was 24%, whereas no patients with residual tumor (R1 and R2) survived beyond 29 months (p = 0.0001).

Among the 96 patients, 21 had type I tumor, 34 type II, and 41 type III. Tumor characteristics are summarized in Table 2, and survival curves are shown in Figure 1 (p = 0.8) according to the Siewert types.


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  		Table 2. Main Demographic and Clinical Characteristics of 96 Cases With Cardia Cancer Who Underwent Resection According to the Siewert Classificationa

 


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  		Fig 1. Kaplan-Meier estimates of survival probability in 82 patients who underwent R0 resection according to the Siewert classification.

 
Early cancer (ie, tumor with invasion confined to the mucosa or submucosa regardless of the presence of regional node involvement) was found in 14 patients (14.6%), with a decrease from type I to type III tumors (Table 2). Only one tumor was limited to the mucosal layer. Nodal metastases were present in 43% of pT1 patients (Table 3), and the 5-year survival rate of this group was 51.3%.


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  		Table 3. Correlation Between Lymph Node Involvement and Depth of Invasion of the Visceral Walla

 
Lymph node metastasis rate (78% and 93%) and the 5-year survival rate were similar in both pT2 and pT3 tumors (approximately 20%; Fig 2).



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  		Fig 2. Kaplan-Meier estimates of survival probability in 82 patients who underwent R0 resection according to the depth of invasion of the visceral wall (pT).

 
Tumor-invading adjacent structures (pT4) belonged only to type III (9 cases). In 6 of these a curative resection was achieved by enlarging the exeresis to the diaphragm (4 cases) or to the left adrenal gland (2 cases). In spite of these extended resections none of these patients lived more than 14 months. At univariate analysis, median survivals were 6, 18, and 21 months for the pT4, pT3, and pT2 categories, respectively, although median survival was not reached in pT1 cases (p = 0.0016).

At univariate analysis the pN category was shown to be a significant prognostic factor. The 5-year survival rate for pN0 tumors was 50% compared with 13% for tumors with one or more metastatic nodes (p = 0.0001). Further stratification showed median survivals of 58, 26, 14, and 6 months for pN0, pN1, pN2, and pN3, respectively (p = 0.0001). A 5-year plateau of 24% was reached only by pN1 tumors (Fig 3). The remaining pN categories had a similar poor outcome.



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  		Fig 3. Kaplan-Meier estimates of survival probability in 82 patients who underwent R0 resection according to the number of metastatic lymph nodes (pN). Patients with metastasis to paraaortic lymph nodes were classified as M1a independently of the number of involved nodes.

 
The result of the multivariate analysis for R0 patients is reported in Table 4.


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  		Table 4. Multivariate Analysis of 82 Patients Who Underwent R0 Resections

 
Another model was fit including R1 and R2 patients and stratifying the pN factor as positive or negative. In this analysis R1 and R2 and pN-positive categories resulted as independent negative prognostic factors (R1 and R2: risk ratio, 2.18; 95% confidence interval, 1.13 to 4.35; p = 0.02; pN-positive: risk ratio, 2.68; 95% confidence interval, 1.16 to 6.2; p = 0.02). The other factors did not have any statistical significance.


   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
Numerous studies indicate an increase in the incidence of the adenocarcinoma of the gastroesophageal junction in Western countries [1–4]. The optimal treatment strategy is still a matter of debate given the peculiarities of this tumor, such as the spread to both the mediastinal and abdominal lymph nodes. In fact, the main lymphatic pathways originating from the lower esophagus advance both up into the mediastinum and down along the celiac axis [10], whereas those from the gastric cardia and subcardial region preferentially proceed to the celiac and paraaortic lymph nodes [16, 17]. This is reflected in the pattern of the lymphatic spread, in that type I tumors differ from those of type II and III tumors, which in turn have a similar pattern. Based on these considerations, Siewert and Stein [10] proposed a classification that provides a useful tool for the selection of surgical approach, although without having a definite prognostic significance, as emerges also from our experience.

In the literature long-term survival rates in curatively resected patients ranged between 22% and 38% [6, 18–20]. Consistent with these figures, the 5-year survival rate of the R0 patients in this series was 24%. Moreover, this subset represented 85% of patients who were operated on, a percentage among the highest reported [6, 8, 18–20]. On the other hand, with univariate and multivariate analysis, R1 and R2 patients showed both a very poor median survival and a significantly higher risk of death.

Prognosis of the adenocarcinoma of the cardia is severe, because lymph node involvement and advanced depth of invasion of the visceral wall are mostly present at onset [7, 21–23].

Consistent with this, 81% of our patients had nodal involvement; half of them had seven or more positive lymph nodes (pN2 and pN3). Overall, the subgroup with positive lymph nodes had a 5-year survival rate of only 13% compared with 50% of the pN0 subset. Multivariate analysis confirmed that pN-positive patients, considered as a whole, had a risk of death nearly three times higher than pN0 patients.

Stratification among pN-positive patients showed no long-term survivors in the pN2 and pN3 subset, whereas a 5-year plateau of 24% was reached only by the pN1 subset. This long-term survival percentage appears similar, if not somewhat better, when compared with the 16% to 18% reported by other authors [7, 19]. Multivariate analysis confirmed that pN2 or pN3 status was the most negative prognostic factor (Table 4).

If the 34% reported by Kodera and coworkers [24] is excluded, the percentage of early cardia tumor has been reported in the range between 10% and 18% [7–10, 25]; accordingly, in this study the percentage of early tumors was 14.6%. It is of note that even in the pT1 subset, 43% of our patients had lymph node involvement, compared with the 17% to 25% reported by other authors [17, 26, 27]. Data regarding survival in the pT1 subgroup is scarce and somewhat inconsistent; 5-year survival rates of 36% [28], 51% [19], and 85% [7] have been reported in the major series. These results are therefore comparable with our experience (51%).

The pT2 and pT3 subsets had similar outcome, both in terms of median survival and long-term survival rate. This result confirms previous observations [29] suggesting that given the lack of the serosa in the cardia region, tumors with transmural growth and invasion of perigastric fat (pT2) should be grouped with pT3.

Moreover, although radical resection was possible in 6 of the 9 pT4 patients, median survival was very poor, suggesting that the actual role of resection alone in this group, if any, remains controversial.

On the whole, with multivariate analysis, the pT category appears to be less important than pN category; also with univariate analysis, a survival longer than 3 years was restricted only to pN0 and pN1 subgroups, irrespective of the pT status.

Interestingly, at approximately 5 years, we observed some late relapses; this finding stresses that a follow-up longer than 5 years is needed before a firm assessment can be made about the long-term cure rate.

In summary, the Siewert classification proved to be a useful guideline in planning surgical treatment, a high curative resection rate was achieved, and the overall prognosis remains poor and chances of cure are limited to pN0 and pN1 patients. To assess whether results can be improved, a phase II study based on preoperative concomitant chemoradiation has been started at our institution.


   References
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 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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