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Originally published as Ann Surg Oncol Early Release 10.1245/ASO.2004.06.025 on April 12, 2004

Annals of Surgical Oncology 11:512-517 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Appropriate Gastric Resection with Lymph Node Dissection for Early Gastric Cancer

F. Borie, MD, N. Plaisant, MD, B. Millat, MD, J.M. Hay, MD and P.L. Fagniez, MD for the French Associations for Surgical Research;

From the Service Chirurgie Digestive A, Hôpital St Eloi (FB, NP, BM), Montpellier; Service de Chirurgie Digestive et Générale, Hôpital Louis Mourier (JMH), Colombes; and Service de Chirurgie Digestive et Générale, Hôpital Henri Mondor (PLF), Créteil, France.

Correspondence: Address correspondence and reprint requests to: Frédéric Borie, MD, Service de chirurgie Digestive A, Hopital St. Eloi, 80 avenue A. Fliche, 34295 Montpellier, France. Telephone: +33.(0)4.67.33.71.05, e-mail: fborie{at}yahoo.com


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The extent of lymphadenectomy (limited vs. extended) and that of gastric resection (partial vs. total) remain controversial issues in the management of early gastric cancer (EGC). A multicentric study was performed to elucidate the appropriate gastric resection with lymph node dissection for early gastric cancer.

Methods: From 1979 to 1988, 332 patients with EGC underwent surgery in 23 French centers. Clinicopathological data, the extent of resection, and the number of lymph nodes retrieved were reviewed retrospectively and screened for prognostic effect. The mean follow-up for the 332 EGC patients was 80 months.

Results: Postoperative mortality was correlated to age (odds ratio [OR], 1.1) and extent of gastric resection (OR,10.3). Examination of survival data (excluding postoperative deaths) with univariate analysis and the Cox proportional hazards model showed that the independent factors for excellent prognosis included no lymphatic involvement (P = .005), 10 or more lymph nodes retrieved (P = .003), site of the tumor in the lower third of the stomach (P = .01), and mucosal lesions (P = .04). The extent of resection did not influence long-term survival.

Conclusions: Our results suggest that because of the associated good prognosis, the appropriate surgical treatment for EGC is partial gastrectomy with lymphadenectomy retrieving 10 or more lymph nodes.

Key Words: Early gastric cancer • Lymph node • Surgery


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Early gastric cancer (EGC) is defined as adenocarcinoma of the stomach in which the depth of invasion is limited to the mucosa and/or submucosa, regardless of lymph node metastatic status.1 The prognosis for EGC is good, with a 5-year survival rate of over 90% after surgery.2

Several therapeutic methods, such as laparoscopic, endoscopic, and surgical gastric resections with or without lymphadenectomy, have been evaluated and described in the literature, especially in Japanese studies. Although the characteristics of early gastric cancer with lymph node metastasis have been reported in many institutions,3,4 some controversy remains as to the appropriate gastric resection and extent of lymph node dissection for early gastric cancer.

The purpose of this retrospective study was to elucidate appropriate gastric resection with lymph node dissection for early gastric cancer on the basis of data from a large number of patients in a French multicentric study.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
During a 120-month period (January 1979 through December 1988), 208 men and 124 women with EGC underwent surgery in 23 centers of the French Association for Surgical Research. These patients represented 11% of all those with gastric cancer who underwent surgery and 13.5% of those with resected gastric cancer (n = 2466) in the same centers. Demographic data on patients and follow-up and survival information (death and cause of death) were obtained from each center. The reckoning point was June 1996. Mean age was 64 years: 62 years (standard deviation [SD] = 12) for men and 66 years (SD = 13) for women.

Definitions
EGCs were grossly classified, according to the Japanese Society for Gastroenterology Endoscopic criteria,5 as type I (protruded), type IIa (elevated; these two types were grouped together in our study as "elevated"), type IIb (flat), type IIc (depressed), and type III (excavated). EGCs were classified as intramucosal or submucosal tumors according to the depth of invasion1 and were further classified histologically according to the World Health Organization (WHO) classification.6 In our series, well or moderately differentiated EGCs were said to be differentiated and undifferentiated, while independent cell EGCs were considered to be undifferentiated.7 Although neither the method of lymph node (LN) sampling nor the exact group of LN dissection was known for all patients, the location of LN metastasis was systematically recorded. Gastric resection was defined as total gastrectomy or partial gastrectomy (limited resection, antrectomy, subtotal gastrectomy). Postoperative morbidity was classified as total morbidity, intra-abdominal sepsis (abscess, fistula, peritonitis), extra-abdominal sepsis, or no septic complication.

Statistical Analysis
Data related to the following clinicomorphological features, postoperative morbidity and mortality, and the number of LN retrievals were compared for patients with partial gastrectomy and total gastrectomy ({chi}2 for discrete parameters and t-test and Mann Whitney test for continuous parameters). Sex, age, tumor site, multiple locations (EMGC), size (largest diameter <15 mm or >=15 mm of the lesion when single or of the largest lesion when multiple), macroscopic aspect, histological type, depth of infiltration, and lymphatic involvement were recorded for each patient. Nonconditional logistic regression was used to identify the factors associated with postoperative mortality. The number of LNs retrieved and analyzed was noted, and the prognostic value of LN retrieval on survival was calculated according to whether the number of LN retrieved amounted to less than 10 or 10 or more. Survival curves were calculated according to the Kaplan-Meier method. For the purposes of survival analysis, overall mortality (including postoperative deaths) and specific mortality (excluding postoperative deaths) were calculated. Stepwise regression analysis was performed on all variables. Significance level for entry and retainment in the Cox proportional hazards model was 0.1 (10%). The SAS statistical package version 6 (SAS Institute, Cary, NC) was used for statistical evaluation on a Digital MicroVAX computer (Compac, Houston, TX). The accepted level of significance was P < .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient Variables
Of the 243 patients undergoing partial gastrectomy for EGC, 145 were males. Of the 89 patients with total gastrectomy, 63 were males. The mean age was 64 (SD, ±12) years: 64 (±12) years for patients with partial gastrectomy and 62 (±12) years for patients with total gastrectomy. There was no statistical difference between the two groups for any of these patient variables (Table 1).


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  		TABLE 1. Clinicopathological features of patients with EGC according to extent of gastric resection
 
Tumor-Related Variables
Of the 34 cases of patients with early multiple gastric cancer, 13 had a total gastrectomy and 21 had a partial gastrectomy. The extent of resection of the stomach was correlated to tumor location. One hundred eighty-six patients with EGC (87.3%) located in the lower third had a partial gastric resection, whereas 27 (12.7%) had a total gastric resection. Of patients with EGC located in the upper two-thirds, 57 had a partial gastric resection and 57 had a total gastric resection. Nineteen of 21 positive nodes (90.5%) were found in the N1 LN chains, but in two patients (9.5%), positive nodes were detected around the N2 LN chains. Macroscopic type, histology, depth of infiltration, size of tumor, and lymphatic involvement were equivalent by design between the patients with partial gastrectomy and those with total gastrectomy.

Treatment-Related Variables
The number of LNs harvested was significantly higher after total gastrectomy than after subtotal gastrectomy (median, 10 (0–47) versus 7 (0–51), respectively; P = .015). Forty-eight percent of patients with total gastrectomy had 10 or more LNs retrieved. Among patients with partial gastrectomy, 32% had <10 LNs retrieved. Postoperative morbidity and mortality rates were not correlated to the number of LNs retrieved: 21.4% (45 of 210) and 5.7% (12 of 210), respectively, for patients with <10 LNs retrieved, versus 23.7% (45/122) and 1.6% (2/122), respectively, for patients with 10 or more LNs retrieved (P = .7 and P = .09). The rate of lymph vessel and/or node metastasis was higher for patients with 10 or more LNs retrieved than for those with <10 LNs retrieved (14% [17/122] versus 8% [17/210]; P = .09).

Postoperative morbidity and mortality rates were higher after total gastrectomy than after subtotal gastrectomy. The postoperative morbidity rate was 35% after total gastrectomy and 18% after subtotal gastrectomy (P = .001). Postoperative intra-abdominal sepsis and no septic complications were correlated to extent of gastric resection. The postoperative mortality rate was 10% after total gastrectomy and 2% after subtotal gastrectomy (P = .001). Among patients with EGC located in the upper two-thirds, the postoperative mortality rate was 13% after total gastrectomy and 1.7% after subtotal gastrectomy (P = .06). Among patients with EGC located in the lower third, the postoperative mortality rate was 3.7% after total gastrectomy and 2% after subtotal gastrectomy (P = .9). The predictive factors of postoperative mortality were age and the extent of resection (Table 2).


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  		TABLE 2. Factors associated with postoperative mortality
 
Follow-Up
The mean follow-up for the 332 EGC patients was 80 months, ranging from 0 to 197 months. At the reckoning date, 104 patients (30.6%) had died: 14 deaths (4%) were due to postoperative complications, 31 (9.3%) to EGC, 55 (17%) to unrelated diseases, and 4 to unknown causes. The anastomotic recurrence rate for the 21 patients with EMGC was not statistically different from that for the 222 patients with EGC after partial gastrectomy: 5% (n = 1) versus 3% (n = 7), respectively (all P = .6).

Survival Analysis
The cumulative 5-year and 7-year survival rates for the 332 EGC were 82% and 72%, respectively, for the entire group and 92% and 87.5%, respectively, when both operative and unrelated mortality were excluded.

The cumulative 5-year and 7-year survival rates of the patients with subtotal gastrectomy were not statistically different from those of the patients with total gastrectomy (94% and 90.5% versus 95% and 91%, respectively [all P = .42]). The cumulative 5-year survival rate of the 21 patients with EMGC was not statistically different from that of the 222 patients with EGC after partial gastrectomy (90% versus 92%, respectively [all P = .79]).

The results of univariate analysis of the potential prognosis factors are presented in Table 3. Prognosis was significantly worse for patients with EGC N+V+ than for those with EGC N–V–, as 5-year survival was 94% for the 298 N–V– patients versus 78% for the 34 N+V+ patients (P = .006)). The cumulative 5-year and 7-year survival rates of the patients from whom <10 LNs were retrieved were significantly worse than those for patients from whom 10 or more LNs were retrieved (90.5% and 84.5% versus 95.5% and 94%, respectively [P = .001]). Tumors located in the lower third of the stomach had a better outcome than those in all other locations (P = .016). The 5-year disease-free survival rates of 159 patients with intramucosal EGC and 167 patients with submucosal EGC were 95% and 82%, respectively (P = .02).


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  		TABLE 3. Univariate analysis of factors related to the prognosis of early gastric cancer (Kaplan-Meier method)
 
The results of multivariate analysis are presented in Table 4. The number of LNs retrieved (<10, P = .003) was the most important independent prognostic factor, followed by lymphatic involvement (P = .005), tumor site in the upper two-thirds of the stomach (P = .01), and submucosal invasion (P = .04).


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  		TABLE 4. Cox multiple regression analysis of early gastric cancer
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The purpose of this retrospective study was to elucidate the appropriate gastric resection with LN dissection for EGC with use of data from a large number of patients in a French multicentric study. The extent of resection did not influence long-term survival but did influence postoperative morbidity and mortality. Conversely, the number of LNs retrieved modified the prognosis but not postoperative morbidity and mortality.

To improve the treatment of EGC, recent developments have resulted in less invasive procedures, requiring the identification of patients who will benefit from such an approach. Endoscopic mucosal resection (EMR) for selected EGCs has been widely accepted as a curative therapeutic strategy in Japan. The criteria for curative EMR are very strict: (1) tumor confined to the mucosal layer; (2) tumor of elevated type (I or IIa) or depressed type (IIc) without ulcer or ulcer scar (endoscopically, no fold convergence); (3) well or moderately differentiated adenocarcinoma; and (4) tumor smaller than 2.0 cm.8 Endoscopy and biopsy were used to diagnose the second and fourth items. Therefore, the histological examination only confirms the four items for the specimen and the curative procedure.

Despite the strict criteria, three problems persist. The first is the distinction between mucosal and submucosal. Endoscopic ultrasonography (EUS) correctly distinguished between mucosal and submucosal in approximately 77% to 84% of tumors.9,10 Twenty percent of patients undergoing EMR were thus incorrectly diagnosed. The second problem with EMR is the diagnosis of LN involvement. Diagnosis of node involvement depends on the performance of preoperative investigations. EUS of gastric cancer has been shown to be superior to computed tomography or ultrasonography in predicting the T stage and the N stage.11 However, false-positive and false-negative results due to invisible microscopic invasion,12 technical failures, artifacts, and peritumoral inflammatory or fibrous changes13 may be responsible for diagnostic failures. Despite its limited use in our series and notwithstanding the retrospective character of our study, EUS does not appear to be able to influence the choice of therapeutic procedures. The final problem is that after successful EMR, close follow-up of the patient by endoscopy is nevertheless mandatory, because multifocal lesions, either synchronous or metachronous, are not uncommon in the stomach.14 For these reasons, we think that EMR should be restricted to elderly and inoperable patients.

Therefore, patients with EGC should have the appropriate surgical treatment. The theoretical advantages of total gastrectomy are the guarantee of no infiltration of the margin of proximal transection owing to multicentric cancers or the microscopic intramural spreading of tumoral cells beyond the macroscopically detectable boundaries of the lesion. However, these expectations are not substantiated, because multicentric tumors are rare and a safe margin of resection can be achieved, maintaining proximal clearance of 6 cm from the cranial edge of the tumor. In our study, 10% of patients had multiple cancers and the prognosis was no different than that for patients with a single cancer location. Moreover, recurrences confined to the gastric stump, after subtotal gastrectomy (and originally preventable with total gastrectomy) are extremely rare, according to the literature.15

In our study, only 3.3% of patients had an anastomotic recurrence after partial gastrectomy, and no statistical difference was found in long-term survival between patients with EGC and patients with EMGC after partial gastrectomy. Analysis of the published series of patients undergoing an en principle total gastrectomy fails to demonstrate any advantage for long-term survival in comparison with patients treated by subtotal gastrectomy.15 The findings of two randomized trials comparing these two procedures (total gastrectomy versus partial gastrectomy) for patients with gastric cancer are in keeping with the above-mentioned conclusions.15,16 However, no randomized trial has compared these two procedures for patients with EGC.

In our series, total gastrectomy did not improve long-term survival over that with partial gastrectomy. Nevertheless, it is true that the gap in surgical mortality for total and subtotal gastrectomy tends to disappear when total gastrectomy is electively performed in patients with tumors of the distal stomach. Nonfatal complications and death occurred in 9% to 34% and 1% to 3.2% of cases of subtotal gastrectomy, respectively, and in 13% to 32% and 1.3% to 2% of cases of total gastrectomy, respectively, in both randomized trials.15,16 Our results were identical for patients with EGC located in the lower third. However, the postoperative mortality rate for patients with EGC located in the upper two-thirds was higher after total gastrectomy than it was after partial gastrectomy.

Furthermore, current experience suggests that the extent of LN dissection is not affected by the extent of resection of the stomach. The incidence of nodal metastasis in EGC is 10% to 20%. However, the optimal nodal dissection for early gastric carcinoma has not been established. In our study, 37% of patients with EGC had 10 or more LNs retrieved after gastric surgery. This number was correlated to the extent of resection of the stomach. Moreover, patients with 10 or more LNs retrieved had a better prognosis than those who had <10 retrieved.

The retrieval of at least 10 LNs is an important prognostic factor, for two reasons. The first is to be able to provide optimal staging for patients who undergo surgery for an ECG with at least 10 LNs retrieved. The second reason is that the number of LNs retrieved is an independent prognostic factor and in the future may enable a decision about whether to use additive treatment as a complement to surgery. This result would justify surgical treatment with lymphadenectomy for all operable patients with EGC. Most LN metastasis in EGC is confined to the N1 and/or N2 LNs. According to previous studies13,17,18 and in our experience, the incidence of LN 1 involvement ranges from 80% to 90% in EGC N+ cases. The incidence of group 2 and 3 involvement is lower, ranging from 10% to 19% and from 0% to 1%, respectively.13,17,18 On the whole, for all EGC, the incidence of LN metastasis confined to N2 LNs is very low, ranging from 1% to 4%. These observations and the results of our study did not seem to favor D2 lymphadenectomy.19 Another argument against D2 lymphadenectomy is that no randomized, controlled study has proven the superiority of D2 lymphadenectomy versus D1 lymphadenectomy in patients undergoing total or partial gastrectomy for EGC.19–22

In conclusion, our results suggest that the surgical treatment of choice for EGC is partial gastrectomy with lymphadenectomy involving the retrieval of 10 or more LNs, because of the good prognosis.


   ACKNOWLEDGMENTS
 
The following centers participated in this study: Adloff Michel (Strasbourg), Baumel Hugues (Montpellier), Chipponi Jacques (Clermont-Ferrand), De calan Loïc (Tours), Delaitre Bernard (Cochin), Dubois Francois (Paris), Escat Jean (Toulouse), Fagniez Pierre-Louis (Créteil), Fékété Francois (Clichy), Gayet Pierre (Clichy), Gignoux Marc (Caen), Gouzi Jean-Luc (Toulouse), Hay Jean-Marie (Colombes), Huguier Michel (Paris), Huten Noël (Tours), Julien Michel (Créteil), Laborde Guy (Pau), Langlois Odile (Maubeuge), Lenriot Jean-Pierre (Lonjumeau), Levard Hugues (Paris), Marescaux Jacques (Strasbourg), Millat Bertrand (Montpellier), Samama Guy (Caen), Tenières Paul (Rouen), Testard Jacques (Rouen), Triboulet Jean-Pierre (Lille), and Veyrières Michel (Pontoise).


   FOOTNOTES
 
A multicentric study was performed to elucidate the appropriate gastric resection with lymph node dissection for early gastric cancer. The results suggest that the appropriate treatment for early gastric cancer is partial gastrectomy with lymphadenectomy involving retrieval of 10 or more lymph nodes.

Received for publication June 23, 2003. Accepted for publication January 5, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  7. Maehara Y, Okuyama T, Morigushi S, et al. Predictor of lymph node metastasis in early gastric cancer. Br J Surg 1992; 79: 245–7.[Medline]
  8. Yoshida. S. Endoscopic treatment. In: Sugimura T, Sasako M, eds. Gastric Cancer. Oxford: Oxford University Press, 1997: 252–62.
  9. Sano T, Okuyama Y, Kobori O, Shimizu T, Morioka Y. Early gastric cancer: endoscopic diagnosis of depth of invasion. Dig Dis Sci 1990; 11: 1340–4.
  10. Ohashi S, Segawa K, Okamura S, et al. The utility of endoscopic ultrasonography and endoscopy in the endoscopic mucosal resection of early gastric cancer. Gut 1999; 4: 599–604.
  11. Rösch T, Classen M. Gastric Carcinoma in Gastroenterologic Endosonography: Textbook and Atlas. New York: Thieme Stuttgart, 1992: 71–80.
  12. Siewert JR, Kestelmeier R, Bush R, et al. Benefit of lymph node dissection for patients with gastric cancer and pN0 and pN1 lymph node metastases. Br J Surg 1996; 83: 1144–7.[Medline]
  13. Sowa M, Kato Y, Nishimura M, et al. Surgical approach to early gastric cancer with lymph node metastasis. World J Surg 1989; 13: 630–6.[CrossRef][Medline]
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