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Annals of Surgical Oncology 9:625-631 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Indications of a Minimized Scope of Lymphadenectomy for Submucosal Gastric Cancer

Shouji Shimoyama, MD, Hidemitsu Yasuda, MD, Kenichi Mafune, MD and Michio Kaminishi, MD

From the Department of Gastrointestinal Surgery, University of Tokyo, Tokyo, Japan.

Correspondence: Address correspondence and reprint requests to: Shouji Shimoyama, MD, Department of Gastrointestinal Surgery, University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan; Fax: 81-3-5800-9734; E-mail: shimoyama-dis{at}h.u-tokyo.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: A recent trend for less invasive surgery has increased consideration for a minimized scope of lymphadenectomy for submucosal cancer; however, feasibility criteria have not been precisely established.

Methods: Patterns and sites of nodal involvement were retrospectively investigated in 294 patients with solitary submucosal gastric cancer in association with other clinicopathologic characteristics, including pre- and intraoperative evaluations of cancer depth (cT) and nodal involvement (cN).

Results: Among the early (cT1) and node-negative (cN0) cancer, intestinal (<=1.5 cm) and diffuse types (<=1.0 cm) of submucosal cancer showed low incidences of nodal involvement (3%) confined to the first tier. When the cancer exceeded these cutoff diameters, positive nodes of the second tier were confined to three priority stations (left gastric, common hepatic, and celiac arteries) at an incidence of 2.3%. Perigastric and preferential dissection of these three node stations (modified D2 dissection) showed survival benefits identical to those of a conventional D2 dissection.

Conclusions: When submucosal cancer is evaluated as cT1cN0, a virtually sufficient minimized scope of lymphadenectomy is a D1 dissection for that within the cutoff diameter and a modified D2 dissection for that exceeding the cutoff diameter. These two types of dissection can even cover the infrequently observed node-positive stations and can realize no residual disease at surgery.

Key Words: Submucosal gastric cancer • Less-aggressive surgery • Lymph node involvement • Lymphadenectomy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The surgical outcomes by conventional approaches for early gastric cancer have been documented as excellent, with 5-year survival rates exceeding 90% worldwide.1–3 On the basis of these observations, we and other investigators have introduced various less-aggressive approaches, such as endoscopic mucosal resection, local resection with4 or without5–7 adjacent lymphadenectomy, and gastrectomy with perigastric lymphadenectomy, 8 to optimize the amount of tissues that should be resected, to reduce potential morbidity, and to maintain a better postoperative quality of life without affecting the excellent survival rates. The proposed indication for these procedures is principally mucosal, node-negative gastric cancer, on the basis of low node-positive incidences of mucosal cancer (1.2%–4.8%).4,9–12 Therefore, especially in Japan, systematic, extended (D2) lymphadenectomy has long been considered a standard procedure for a gastric cancer that does not fulfill this criterion,12,13 although recent randomized trials in the West have failed to prove the survival benefit of a D2 dissection.14–17

With regard to submucosal cancer, the reported incidences of first- and second-tier node-positive patients range from 9% to 16% and 4% to 6%, respectively.10–12,18,19 The infrequent second-tier node-positive incidences have raised the question of whether uniformly performed D2 dissection is really necessary for all submucosal cancers and have compelled us to reconsider the Japanese style of conventional D2 dissection. However, it should be noted that minimizing the scope of lymphadenectomy apparently poses risks of residual disease for second-tier node-positive patients, even if they are observed at a low incidence.19 Therefore, only carefully selected submucosal cancer patients may undergo tailored, less-aggressive surgery. This concept will prevent the unnecessary dissection of lymph nodes as well as of the spleen and pancreas, which has been recognized as one of the reasons for increasing postoperative morbidity and in-hospital mortality.16,17

Feasibility criteria of less-aggressive surgery for submucosal cancer have not been precisely established, and such criteria are, if present, based on histological findings.9 As we have argued in a previous article, 4 preoperative and intraoperative evaluations in combination with postoperative histological findings are apparently required and practical for surgeons planning less-aggressive surgery, because decision-making regarding the scope of lymphadenectomy should be done before and during surgery. Our current combined analyses of pre-, intra-, and postoperative diagnoses have revealed that only perigastric and some regional node dissections represent a sufficient scope of lymphadenectomy for submucosal cancer, if it is diagnosed as an early gastric cancer and as node negative before and during surgery.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Definition of Lymph Node Tiers and Scope of Lymphadenectomy
There are three defined lymph node tiers, which are made up of several lymph node stations according to the Japanese Classification of Gastric Carcinoma.20 This classification shows the lymph node number assigned to each station and which lymph node station belongs to which lymph node tier. Under these classifications of the lymph node tiers, the scope of lymphadenectomy (D number) was classified as D1 if dissection included only the first-tier node, as D2 if it included both the first- and second-tier nodes, and as D3 if it included the first-, second-, and third-tier nodes, as described previously.21 In this study, modifications of the extent of lymphadenectomy were defined as a modified D18 if node dissection included first-tier nodes and station 7 and as a modified D2 if it included first-tier nodes and stations 7, 8, and 9. The most noticeable merit of a modified D2 dissection is leaving intact node stations 10 and 11, which allows preservation of the spleen and pancreas. The extent of lymphatic spread was expressed as N0, N1, N2, and N3, which corresponds to no nodal involvement, involvement confined to first-tier nodes, up to second-tier nodes, and up to third-tier nodes, respectively.

Patient and Tumor Characteristics
This study comprises 294 patients with histologically confirmed solitary submucosal gastric cancer who underwent a curative resection between 1976 and 1999 in the Department of Gastrointestinal Surgery, University of Tokyo. The clinicopathologic characteristics of the gastric cancer included age, sex, location of cancer, depth of invasion, maximum cancer diameter, gross form, Lauren’s histological type,22 lymphatic and vascular invasion, and N number, all of which, except the histological type, followed the Japanese Classification of Gastric Carcinoma.20 The location of the cancer was expressed by any combination of the three subdivided areas, such as the upper, middle, and lower third of the stomach, as well as a whole area. Early (mucosal and submucosal) and advanced cancer was defined as T1 and >=T2 cancer, respectively. Submucosal invasion was further subdivided into three degrees: invasion up to superficial one third (sm1), middle one third (sm2), and deep one third (sm3) submucosal layers.18 Maximum cancer diameter was evaluated histologically. Gross form was divided into four types: elevated, superficial depressed without ulceration, superficial depressed with ulceration, and mixed. The lymphatic and vascular involvement of the stomach wall was classified as present and absent. The definition of N number was mentioned previously. Curative resection signifies no residual disease macroscopically and microscopically, irrespective of the extent of lymphadenectomy actually performed.

Pre-, Intra-, and Postoperative Evaluations for T and N Classification
Pre- and intraoperative diagnoses of T and N classifications were based on a barium roentgenogram, upper gastrointestinal endoscopy, abdominal ultrasonography, computed tomography whenever possible, and findings of the surgical exploration. Endoscopic ultrasonography has been applied for the evaluation of T classification since 1987. These pre- and intraoperative evaluations were noted by the prefix c (clinical), such as cT and cN. Postoperative T and N classifications were based on the histological examinations in the resected specimens and were noted by the prefix p (pathologic) to distinguish the histological T and N findings (pT and pN) from the cT and cN findings. According to these evaluatory systems, 227 patients (77.2%) were believed to have cT1 cancer at the time of resection.

Surgery
Distal, total, or proximal gastrectomy was performed in all patients. The scope of lymphadenectomy was a modified D1 dissection in 78 patients,8 a modified D2 dissection in 99 patients, and a >=D2 dissection in 117 patients. When the cancer was pre- and intraoperatively diagnosed as mucosal or node negative or when patients had poor general conditions, a modified D1 dissection could be applied with curative intent.8 In brief, modified D1 dissection is a clearance of lymph nodes in the first tier and those around the left gastric artery (station 7). Our modified D1 dissection is based on the findings that metastasis to station 7 occurs most frequently among the second-tier nodes in mucosal gastric cancer, and it is further supported by the observation of aberrant lymphatic drainage toward the left gastric artery in the recent sentinel node navigation studies.23–25 Those who fulfilled the criteria were, therefore, rationally allocated for a modified D1 dissection. For those patients who did not fulfill the criteria, a modified D2 or >=D2 dissection was a standard choice of dissection. Although the allocation was not randomized, the choice was based on the extent of gastrectomy or was the surgeon’s decision to achieve a curative resection. Among the patients undergoing a >=D2 dissection, clearance of station 10 was principally achieved by splenectomy or, in 14 patients, by skeletonizing the short gastric artery and splenic hilum. Clearance of station 11 was achieved by a combined resection of the distal pancreas or skeletonizing of the splenic artery, as proposed by Maruyama et al.26

Statistics
An unpaired Student’s t-test was used to test the equality between the two means of variables. Fisher’s exact test or a {chi}2 test was used to test the independence between the two groups. The cutoff for follow-up was December 2000. Cumulative postoperative survival curves were calculated by Kaplan-Meier methods, and the differences between the two curves were tested by a generalized Wilcoxon test. A probability of <.05 was considered significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The overall incidence of nodal involvement was 18.4% (n = 54). The pN1, pN2, and pN3 classifications were seen in 12.2%, 5.1%, and 1.0% of patients, respectively. Univariate analyses revealed that node-positive patients had significantly larger cancers (P = .004), higher incidences of lymphatic vessel involvement (P < .0001), and higher incidences of more invasive cancers (P = .0006) than node-negative patients (Table 1). The distributions of other clinicopathologic factors and the mean numbers of dissected nodes were not significantly different between node-positive and node-negative patients.


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  		TABLE 1. Clinicopathologic comparisons between patients with and without lymph node metastases
 
Distributions of node-positive patients were investigated in relation to the cTcN classification, maximum cancer diameter, and histological type (Fig. 1). Among cT1cN0 cancers, when they were the intestinal type, pN1 and >=pN2 patients came to be observed if the maximum cancer diameter was >1.0 cm and >1.5 cm, respectively, whereas when they were the diffuse type, both pN1 and >=pN2 patients became to be observed if the maximum cancer diameter was >1.0 cm. No nodal involvement was observed if the maximum cancer diameter was <=1.0 cm, irrespective of histological type (n = 9).



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  		FIG. 1. Distributions of pN0, pN1, and >=pN2 patients in relation to cTcN classification, histological type, and maximum cancer diameter. ({circ} pN0; ({image}) pN1; (•) >=pN2. Each circle represents one patient. Numbers in parentheses are numbers of patients.

 
The site-specific analyses of pN2 were performed among those patients undergoing modified D2 or >=D2 dissection (Table 2). Patients undergoing a modified D1 dissection were excluded from these analyses to eliminate the possibility of underscoring the actual pN number. Among the patients undergoing >=D2 dissection, five (11.4%) of the >=cT2 and/or >=cN2 patients (n = 44) had pN2 diseases at stations 7 through 9 as well as at stations 10, 11, and 14 or had pN3 disease. By contrast, six (9.8%) and three (4.9%) of the cT1cN0 patients (n = 61) had pN1 and pN2 disease, respectively; however, all pN2 stations were confined to stations 7 through 9. These three pN2 disease patients had histologically sm3 cancer. Similarly, among the patients undergoing a modified D2 dissection, all positive nodes of cT1cN0 patients were confined to the first tier. On the other hand, only pN0 or pN1 diseases were observed in cT1cN1 patients; however, they comprised only 8.3% (n = 18) of those undergoing a modified D2 or >=D2 dissection.


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  		TABLE 2. Distributions of node-positive patients in relation to pre- and intraoperative diagnoses of tumor depth (cT) and lymph node involvement (cN)
 
Survivals were compared between cT1cN0 patients undergoing a D2 dissection and those undergoing a modified D2 dissection to evaluate the difference in quality between the two types of lymphadenectomy. The mean and median follow-up of the survivors were 100 and 99 months, respectively, in the patients undergoing a D2 dissection and 90 and 85 months, respectively, in those undergoing a modified D2 dissection. The respective 5- and 10-year survival rates were 97% and 91% in patients undergoing a D2 dissection, and they were 98% and 91% in those undergoing a modified D2 dissection (Fig. 2). No patient in either group died as a result of cancer, and therefore the disease-specific survivals of the two groups were 100%.



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  		FIG. 2. Overall survivals of cT1cN0 patients undergoing a modified D2 dissection and those undergoing a >=D2 dissection. There was no statistical difference between the two survival curves.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
With the background of the negative effect on patient quality of life by D2 dissection in randomized trials,16,17 the infrequent >=pN2 positivity ratio (6.1%) in this study promotes a refinement of traditional D2 dissection for many submucosal cancer patients. In this respect, pre- and intraoperative evaluations, including cancer depth and nodal involvement, as well as postoperative diagnoses, are indispensable in the attempt to establish indications for minimally invasive surgery, because the rationale for this surgical approach in each individual patient should be determined before surgery. Considering the recent proposal of a D1 dissection for submucosal cancer with a maximum diameter of 1 to 4 cm on the basis of histological results,9 we believe that our approach holds great importance from a practical point of view.

There was no difference in the mean number of dissected nodes between node-positive and node-negative patients. In addition, the incidences of overall lymph node metastasis, as well as of pN1, pN2, and pN3 diseases in this study, are consistent with previously reported incidences, which range from 11% to 20%, 9% to 16%, 4% to 6%, and .3% to 1%, respectively.9–12,18,19 These observations confirm the balanced surgical qualities and nonbiased patient population of our series. We have found that maximum cancer diameter, lymphatic invasion, and degree of submucosal invasion correlate significantly with nodal involvement. These observations are in agreement with previous univariate and multivariate results, in which tumor size, 9,10,18 histological type,10 lymphatic invasion,18 and degree of submucosal invasion18 were the significant factors correlating with nodal involvement. Because lymphatic invasion and degrees of submucosal invasion are currently difficult to evaluate accurately before surgery,18 we have focused on the preoperatively assessable determinants in combination with cT and cN classifications.

Gastric cancer patients, even if they are pN0, may have a potential risk of residual diseases if lymphadenectomy is omitted, because recent immunohistochemical results have revealed a high frequency of nodal microinvolvement that cannot be otherwise detected by routine histology.27 Considering the stepwise progression of gastric cancer, cN0 patients may have a potential risk of microinvolvement in the first-tier node, and cN1 patients may have this in the second-tier nodes. Therefore, minimizing the scope of lymphadenectomy, i.e., less than D2 dissection, is essentially justified for cN0 cancers to cover the possible microinvolved pN1 nodes.

Our results demonstrate that submucosal cancers with a maximum cancer diameter of <=1.5 cm in the intestinal type (n = 29) and <=1.0 cm (n = 1) in the diffuse type, if they are cT1cN0, actually exhibited pN0 or pN1 diseases, even if nodal involvement was proved to be present after surgery. These observations suggest that these 30 patients could be treated by a modified D1 dissection. This possibility is realistic not only because these 30 patients, predominantly had the intestinal type (n = 29), constituted 15% of all cT1cN0 patients (n = 202) and 22% of the intestinal type cT1cN0 patients (n = 134), but also because the infrequent pN1 disease, at an incidence of 3% (1 of 30 patients), even if present, could be covered by the modified D1 dissection. Furthermore, more limited surgery, such as local resection, may be possible for intestinal type cT1cN0 cancer if the maximum cancer diameter is <=1.0 cm, because none of these patients was node positive. This possibility of local resection, however, awaits further prospective study.

Theoretically, cT1cN0 cancers exceeding the above-mentioned cutoff diameter require a wider scope of lymphadenectomy because of the existence of pN2 patients. Among the second-tier nodes, stations 7 through 9 should be considered separately from other stations of the second-tier, such as stations 10, 11, and 12, because dissection of the former stations can be performed relatively more easily than dissections of the latter stations, which should sometimes accompany a combined resection of the spleen and pancreas. From this point of view, the selection of patients with positive nodes confined to stations 7 through 9, but with negative nodes in the other second-tier nodes, is of great importance. For this purpose, 117 patients undergoing a D2 dissection were selectively investigated, because cancer-positive or -negative conditions in the second-tier nodes cannot be strictly evaluated if these lymph nodes are not dissected. It is interesting to note that our results demonstrate that the submucosal cancers, if they were cT1cN0 (n = 61), exhibited a low incidence of pN2 (n = 3; 5%) and that all involved second-tier nodes were confined to stations 7 through 9. By contrast, pN2 patients with positive nodes beyond these three stations were preoperatively evaluated as having >=cT2 and/or >=cN2 cancer. These cancers should be essentially outside the concept of minimally invasive surgery despite the submucosal cancer histologically, and therefore >=D2 dissection should be considered before surgery in such instances. Furthermore, no survival difference between cT1cN0 patients undergoing modified D2 and those undergoing D2 dissection suggests that the modified D2 dissection does not affect patient survival even if it leaves other second-tier nodes. Taken together, these results show that a modified D2 dissection could be applied for cT1cN0 cancers outside the aforementioned criteria for a modified D1 dissection. For these patients, we believe that a modified D2 dissection, rather than D1 dissection, is appropriate to avoid the lymph node recurrence that could occur by leaving positive nodes (stations 7 through 9) and to maintain excellent patient survival, although the overall estimated risk of pN2 (stations 7 through 9) was 2.3% (n = 3) among cT1cN0 patients. Finally, it should be noted that those who could enjoy the benefits of a modified D2 dissection (n = 61) comprised 52% of patients among those who actually received a >=D2 dissection (n = 117).

In the same sense, a modified D2 dissection may be possible for the cT1cN1 patients, because no patient had pN2 diseases. However, this possibility is not conclusive from our study, because only 18 patients with cT1cN1 cancers underwent a modified D2 or >=D2 dissection. This possibility should be investigated by further studies that include a large number of cT1cN1 patients.

If the degrees of submucosal invasion can be accurately evaluated before surgery, they will give more valuable and additional information on decision making for minimally invasive surgery. However, perfect discriminations of sm1, sm2, and sm3 are currently impossible even with the introduction of endoscopic ultrasonography.18 Our proposals are practical in this regard because pathologic or relatively complicated factors, such as degrees of submucosal invasion, are not included as determinants. Results from this study suggest that submucosal cancers, when they are cT1cN0, could be rationally treated by a modified D1 dissection if they are <=1.5 cm (of the intestinal type) and <=1.0 cm (of the diffuse type) or by a modified D2 dissection if they exceed these cutoff diameters. A modified D1 or modified D2 dissection can achieve complete clearance of even infrequently occurring positive nodes, which results in the absence of residual disease at surgery.


   Footnotes
 
Submucosal gastric cancers, when they are cT1cN0, could be rationally treated by a modified D1 dissection if they are <=1.5 cm (of the intestinal type) and <=1.0 cm (of the diffuse type) or by modified D2 dissection if they exceed these cutoff diameters. A modified D1 or D2 dissection can achieve complete clearance of even infrequently occurring positive nodes and result in the absence of residual disease at surgery.

Received for publication February 15, 2002. Accepted for publication May 14, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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