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10.1245/s10434-006-9077-x
Annals of Surgical Oncology 14:340-347 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Surgical Results of Early Gastric Cancer and Proposing a Treatment Strategy

Su-Shun Lo, MD1, Chew-Wun Wu, MD1, Jen-Hao Chen, MD1, Anna Fen-Yau Li, MD2, Mao-Chie Hsieh, MD1, King-Han Shen, MD1, Hwai-Jeng Lin, MD3 and Win-Yiu Lui, MD1

1 Division of General Surgery, Department of Surgery, Taipei Veterans General Hospital and National Yang Ming University, No. 201, Section 2, Shih-pai Road, Taipei, Taiwan
2 Department of Pathology, Taipei Veterans General Hospital and National Yang Ming University, Taipei, Taiwan
3 Division of Gastroenterology, Department of Medicine, Taipei Veterans General Hospital and National Yang Ming University, Taipei, Taiwan

Correspondence: Address correspondence and reprint requests to: Su-Shun Lo, MD; E-mail: sslo{at}vghtpe.gov.tw


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Prognosis for patients with early gastric cancer after surgical resection is excellent. The 5-year or even 10-year survival is more than 90%. In the present study, we investigated the result of treating early gastric cancer surgically in our hospital, with special reference to the risk factor(s) for tumor recurrence and the relationship between age and survival.

Patients and Methods: From January 1988 to December 2002, a total of 479 patients with early gastric cancer underwent resection by our surgeons. Results of preoperative studies, operative findings, histopathology and postoperative follow-up were recorded respectively, and the postoperative disease-related survival, overall survival, tumor recurrence and recurrent patterns were analyzed. The clinicopathological factors were also analyzed to identify the risk factor(s) related to tumor recurrence.

Results: Older patients (>75 years old) had a poorer overall survival than younger patients. However, the disease-related survival was not significantly different between the two. Recurrence was observed in 21 patients, the most important factor of which was lymph node status. Lymph node metastases occurred in 54 patients (11.3%)—coming from mucosal tumors in 12 patients (4.4%) and from submucosal tumors in 42 (20.3%). When the size of the mucosal tumor was smaller than 1 cm, no lymph node metastasis was found in our patients.

Conclusions: The most important risk factor of recurrence in early gastric cancer is lymph node status. Given the low probability of lymph node metastasis and recurrence in tumors less than 1 cm in diameter limited to the mucosa, more limited surgery maybe appropriate in these carefully selected instances.

Key Words: Early gastric cancer • Survival • Recurrence • Surgical treatment


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Early gastric cancer is defined as tumor invasion limited to the gastric mucosa or submucosa, regardless of lymph node metastasis. The prognosis for patients with early gastric cancer after surgical resection is excellent. The 5-year or even 10-year survival is more than 90%, as confirmed in both Japanese and Western studies.1–5 Nevertheless, some patients experience recurrence after curative surgery. It has been shown that lymph node status is the most important risk factor for recurrence.6 Various factors—including age,7 depth of tumor invasion, differentiated type of carcinoma,6 lymphatic involvement and tumor location8—have been reported to correlate with the tumor recurrence after surgery. Those reports were from institutes in different geographical areas, and with different disease incidence, surgical volume and hospital facilities. For example, Japanese pathologists probably focus more on nuclear factors and glandular structures than Western pathologists, therefore adenoma and dysplasia may be more commonly diagnosed as early gastric cancer by Japanese pathologists.9

Although located in East Asia and close to countries known to have high incidence of gastric cancer, e.g. Japan, Korea and Mainland China, the incidence of gastric cancer is not so high in Taiwan. According to the annual report of Department of Health of Taiwan, the incidence was 14.98 per 100,000 with about 3,400 newly detected patients each year and was listed as the 8th commonly occurring cancer in Taiwan. Radical gastrectomy with extended lymph node dissection was first initiated about 20 years ago in Taipei Veterans General Hospital (Taipei VGH), and over the years various new procedures have been implemented without extensive statistical analysis. In the present study, we investigated the results of surgical treatment of early gastric cancer in our hospital, with special reference to the risk factors of tumor recurrence and the relationship between age and survival.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
From January 1988 to December 2002, 1,848 consecutive patients with gastric cancer underwent surgical treatment in Taipei VGH. Results of preoperative studies, intraoperative findings, postoperative pathological staging and follow-up data were recorded. Among those patients, 479 with early gastric cancer were found in our series. All patients underwent radical subtotal or total gastrectomy, depending on their tumor locations (at least 3 cm proximal to the tumor edge as the proximal resection margin and 1–2 cm distal to the pyloric ring as the distal resection margin) with at least D1 plus No. 7, 8a, 9 and 11 (lymph nodes along left gastric artery, common hepatic artery, celiac trunk and splenic artery) or D2 lymph node dissection and reconstructed with Billroth I or II or Roux-en-Y anastomosis. Their clinical characteristics, histopathology, recurrence and survival were analyzed. The clinicopathological factors including age, sex, tumor location, tumor size, tumor cell differentiation, gross appearance, Lauren’s classification,10 depth of tumor invasion and lymph node status were defined according to the General Rules for Gastric Cancer Study.11 The gross appearance of each tumor was classified as elevated, flat or depressed. The Japanese endoscopic classification is as follows: elevated type, I (protruded) and IIa (superficial elevated); flat type, IIb; or depressed, IIc (superficial depressed) and III (excavated). Lymphovascular invasion was defined as presence of tumor emboli either in lymphatic duct or vascular lumen. Patients were examined every 3 months for the first year and then every 6 months thereafter. Follow-up procedures included gastroscopy, tumor markers, chest radiology and abdominal CT scan. The recurrence of disease was confirmed by physical findings, imaging studies, endoscopic examination with biopsy and surgery. The recurrent patterns were classified into hematogenous, lymph node recurrence, peritoneal dissemination, locoregional and combined metastases according to the first detected positive findings. All patients were followed up to date (June 2005). The median follow-up was 63 months.

Statistics
The {chi}2 test and Student’s t-test, as appropriate, were used for statistical analyses. Multivariate analysis with the logistic regression was used to assess the independent risk factors for recurrence and lymph node metastasis. A probability value of less than 0.05 was considered significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Clinicopathological features
The mean age of enrolled patients was 65.9 years old (27–90 years) with a male to female ratio of 2.7:1. Multiple lesions (synchronous lesions) were found in 14 patients (2.9%) either before or during operation. Tumor invasion was limited to the mucosal layer in 272 patients (56.8%), while in 207 patients (43.2%) tumors invaded the submucosal layer. The average number of dissected lymph nodes was 26.1 ± 13.5 per patient (12–78 nodes). There were 54 patients (11.3%) with lymph node metastases, 12 of which (4.4%) came from mucosal tumors and 42 (20.3%) from submucosal tumors. Skip metastasis was found in three submucosal tumor patients with no perigastric lymph node metastasis; however, all three patients had positive nodes in No. 7 (left gastric artery) and two patients had positive nodes in No. 8a (common hepatic artery).

Survival analysis
The 5-year and 10-year overall survivals (including all the causes of death) were 84.6% and 70.8%, respectively. Patients older than 75 years had a significantly poorer survival than those under 75 years (87.4% versus 70.6%, P < 0.001; 74.6% versus 47.5%, P < 0.01; Table 1Go). However, the disease-related survival was not significantly different between the two groups (Figs. 1Go and 2Go). The most frequent cause of death was non-cancerous death (8.9%), while the percentages of patients who died from recurrent gastric cancer (disease-related death) and other cancers were 3.9% and 3.5%, respectively. There was no correlation between cause of death and age, except for non-cancerous death. There were significantly more non-cancerous deaths in older patients (>75 years old) (14.4% versus 7.6%, P = 0.029). The 5-year and 10-year disease-specific survival values for early gastric cancer were 96.5% and 94% (Figs. 1Go and 2Go).


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  		TABLE 1. Survival and causes of death of patients with early gastric cancer after surgical treatment (1988–2002)
 

Figure 1
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  		FIG. 1. The disease-related survival values of patients with early gastric cancer after surgical treatment.

 

Figure 2
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  		FIG. 2. The overall survival for patients with early gastric cancer after gastrectomy.

 
Recurrence
Recurrent patterns are summarized in Table 2Go; the hematogenous metastasis is demonstrated to be the main recurrent pattern. Since it was difficult to distinguish second primary tumors from synchronous tumors overlooked at the first operation in the gastric stump, four patients with gastric cancers detected in the remnant stomach during the follow-up were excluded from the recurrence analyses. Recurrence was observed in 18 patients within 5 years and in 3 patients beyond 5 years. Of these patients, 17 are dead of recurrence and 4 are still alive. After univariate analysis, it was found that only depth of tumor invasion, lymph node status and lymphovascular invasion were significantly correlated with tumor recurrence. Multivariate analysis of the three factors revealed that the most important factor for tumor recurrence was lymph node metastasis (Table 3Go), and the independent risk factors for lymph node metastasis were lymphovascular invasion, depth of tumor invasion and tumor size (Table 4Go). Since lymphovascular invasion cannot be evaluated preoperatively, the relationship among the lymph node status, tumor size and depth of tumor invasion was analyzed and is shown in Table 5Go. Results show that when the size of the mucosal tumor was less than 1 cm, no lymph node metastasis could be found. All 12 mucosal tumors with lymph node metastases were limited to the nearest perigastric lymph nodes. All 9 patients with anatomic N2 lymph node metastases (four with No. 8a and five with No. 7) were from submucosal tumor patients.


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  		TABLE 2. Recurrent patterns (21 patients)
 

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  		TABLE 3. Uni- and multivariate analyses of precipitating factors of recurrence
 

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  		TABLE 4. Uni- and multivariate analyses of risk factors of lymph node metastasis
 

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  		TABLE 5. Relationship between tumor size and lymph node status in mucosal and submucosal tumors.
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
It has been widely accepted that with surgical treatment there is a good prognosis for patients with early gastric cancer. Although the proportion of cases of early gastric cancer in our gastric cancer patients was 26%, which is lower than in both Japan (50%)12 and Korea (33%),13 low recurrence rate (5.0%) and excellent survival after surgical treatment (96.5% of 5 years survival and 94.0% of 10 years) of early gastric cancer were as expected in this study. The results are comparable to a recurrence rate of 0.25–4.18% reported in many Japanese series.6 The reported risk factors associated with recurrence of early gastric cancer, including age, depth of tumor invasion, lymph node status, differentiated carcinoma and lymphatic involvement, have been discussed in several reports.6,7,8,14 The significant risk factors for recurrence in this series after univariate analyses were depth of tumor invasion (P = 0.027), lymphovascular invasion (P = 0.012) and lymph node metastasis (P = 0.001). There were 7 recurrences (2.6%) from mucosal tumors and 14 (6.5%) from submucosal tumors found in our patients. Recurrence was experienced in 13 of 400 patients (3.3%) with no lymphovascular invasion and in 8 of 75 (10.7%) with lymphovascular invasion. In comparison, only 3.1% of early gastric cancer patients with no lymph node involvement saw recurrence, while 14.8% of those with positive lymph nodes experienced it. However, as in other series,14–16 after multivariate analysis, the lymph node metastasis was the most important factor of recurrence.

Although the precipitating factor of recurrence was lymph node metastases, hematogenous recurrence (liver, lung, bone, adrenal gland or brain) was the major recurrent pattern (52.4%), followed by lymph node metastasis (24%) in our series. This distribution of recurrent patterns was similar to that reported by Sano et al.,6 Ichiyoshi et al.17 and Basili et al.,7 which suggests that lymph node metastasis might implicate a more aggressive tumor behavior and not just a tendency for lymphatic metastasis. Although lymph node metastasis was the most important factor for tumor recurrence, 62% (13/21) of recurrent tumors had no lymph node metastases at the time of operation. Micrometastasis was proposed to answer the question, and some authors have reported that D2 lymphadenectomy improved survival even in pN0 patients.18,19 However, the role of micrometastasis of lymph node in prognosis is still controversial.20–23 The reported incidence of a synchronous tumor in the stomach was 2–15%;24–27 3–9% for metachronous.25–28 There have been reports indicating that synchronous lesions, advanced age and microsatellite instability also increased the incidence of metachronous lesion.28,29 Even with the fact that three of four of our patients with recurrent cancer in the gastric stump were detected within 1 year and one patient was detected 3 years after primary operation, it was not clear whether the tumors were second primary or overlooked in the initial operation.

In our study it was found that depth of tumor invasion, tumor size and lymphovascular invasion were correlated with lymph node metastasis. Of 479 patients, 54 (11.2%) were found to have positive lymph nodes. Among them, the incidence of lymph node metastasis in mucosal and submucosal tumors was 4.4% and 20.3%, respectively, which is comparable to that reported by Sano et al.6 and Fukutomi et al.30 Tumor size is also an independent factor for lymph node metastasis. When tumor size was less than 1 cm, only 2.6% had positive nodes; however, when tumor size was larger than 3 cm, 16.7% had lymph node metastases. Similar to the findings of Maehara et al.1 and Borie et al.,8 lymphovascular invasion was also correlated with lymph node metastasis.

Since long-term survival of early gastric cancer patients after operation can be expected, life quality after surgical treatment is getting more important. Considering the lower incidence of lymph node metastasis, limited surgery for selected patients was suggested to improve the life quality. The incidence of lymph node metastasis was 11% in our study, while 85% (46 of 54) of patients with early gastric cancers with lymph node involvement were cured by gastrectomy with lymph node dissection. Therefore, adequate lymph node dissection appears to be necessary for those patients. However, it is very difficult to evaluate lymph node status preoperatively, even with endoscopic ultrasonography examination.31 Only a retrospective analysis of clinicopathological data obtained from the patients with early gastric cancer who underwent extensive enough lymph node dissection can accurately portray the true rate of lymph node positivity. Therefore, the extent of dissection could only rely on the results of our patients and hospital facilities. Although the lymphatic invasion, gross appearance of tumor, depth of tumor invasion, tumor size and cellular differentiation were reported to be the risk factors for lymph node metastasis,1,8 only lymphovascular invasion, depth of tumor invasion and tumor size were found as factors in our patients; the latter two could be assessed by means of endoscopic examination preoperatively. In our series, no lymph node metastasis was found in mucosal tumor smaller than 1 cm, and anatomic N1 (perigastric lymph node) lymph node was involved only when tumor size was larger than 1 cm. Anatomic N1 plus N2 but limited in No. 7 and 8a (left gastric artery and common hepatic artery) lymph node metastases were found in submucosal tumors. Therefore, it was proposed that the surgical strategy for mucosal tumors less than 1 cm was local excision with endoscopic mucosal resection or wedge resection; for mucosal tumors larger than 1 cm, a limited surgery with radical gastectomy plus D1 (perigastric lymph node) lymph node dissection could be recommended. For submucosal tumor, however, a radical gastrectomy with D1 (perigastric lymph node) plus No. 7, 8a, 9 and 11 (splenic artery) lymph node dissection would be necessary. Our surgical strategy was similar to that proposed by Nakamura et al.32 However, whether this strategy can really result in equivalent outcomes and a better quality of life requires further studies. Although gross appearance of tumor and the degree of tumor cell differentiation are included in the current Japanese guideline, our strategy is proposed according to the results of our own patients and studies. Overall survival after gastrectomy, especially the non-cancerous death in patients older than 75 years of age, was significantly poorer than in younger patients, although the surgical complications, cancer recurrence and second cancer death were similar in both groups (≤75 years and >75 years). Since the disease-related survival after gastrectomy is excellent, minimally invasive treatments—including endoscopic mucosal resection and laparoscopic gastrectomy—were reported to obtain surgical results no worse than those of conventional surgery.33–35 However, results of these procedures are dependent on the individual surgeon’s experience and accurate preoperative diagnoses of early lesions; therefore, use of the procedures is still controversial.

Received for publication April 11, 2006. Accepted for publication May 19, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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