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10.1245/ASO.2004.06.012
Annals of Surgical Oncology 11:203-206 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Comparative Evaluation of Gastric Carcinoma Staging: Japanese Classification Versus New American Joint Committee on Cancer/International Union Against Cancer Classification

Chikara Kunisaki, MD, Hiroshi Shimada, MD, Masato Nomura, MD, Goro Matsuda, MD, Yuichi Otsuka, MD, Hidetaka Ono, MD and Hirotoshi Akiyama, MD

From the Second Department of Surgery, Yokohama City University School of Medicine, Yokohama, Japan.

Correspondence: Address correspondence and reprint requests to: Chikara Kunisaki, MD, Second Department of Surgery, Yokohama City University School of Medicine, 3–9, Fukuura, Kanazawaku, Yokohama 236–0004, Japan; Fax: 081-45-782-9161; E-mail: s0714{at}med.yokohama-cu.ac.jp


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The TNM and Japanese classifications of regional lymph node spread (N categories) for gastric cancer differ, whereas the classifications of local extent (T categories) are identical. This study was designed to compare these staging systems and devise a more rational system for gastric carcinoma.

Methods: A series of 1244 patients with gastric cancer were enrolled in the study. Survival rates were evaluated to clarify which aspects of each staging system (feasibility, reproducibility, and accuracy of prognostic stratification) were superior.

Results: The TNM and Japanese classification systems differ in their categorizations of lymph node spread. A significant difference in survival rate was observed in lymph node metastasis classified as N1 and N2 by the Japanese classification and then subclassified by the TNM classification, although there was no significant difference in the survival in cases of lymph node metastasis classified by TNM into pN1 and pN2 and then subclassified by the Japanese classification. Among patients with M1 metastasis (number 16 a2 and b1 in Japanese classification) in the TNM classification, there was a significant difference in survival. A new classification that included the para-aortic lymph nodes (number 16 a2 and b1) as regional lymph nodes within the TNM classification provided homogeneity and an improvement in staging.

Conclusions: TNM classification was more rational and homogenous than Japanese classification. New classification could lead to worldwide uniformity in the description of patients and make possible uniform interinstitutional comparisons of surgical results.

Key Words: Gastric cancer • Japanese classification • Lymph node metastasis • Staging system • TNM classification


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The Japanese Classification of Gastric Carcinoma1 (JC) provides lymph node station numbers for anatomically separate sites of regional lymph nodes. This classification is based on the study of lymphatic flow and surgical results. In contrast, the American Joint Committee on Cancer (AJCC) Manual for Staging of Cancer and the International Union Against Cancer TNM Classification of Malignant Tumors2 (TNM) adopted a classification system based on the number of metastatic lymph nodes. This variable has proved to be an independent prognostic factor in gastric cancer.3,4 Furthermore, there have been reports discussing the importance of the anatomic distribution of lymph nodes in gastric cancer.5,6 This study sought to identify the classification system that more rationally reflected outcome.


    PATIENTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A series of 1244 patients (855 men and 389 women; average age, 58.6 ± 12.3 years) who underwent potentially curative gastrectomy with lymph node dissection at the Second Department of Surgery of Yokohama City University School of Medicine during the period 1975 to 1998 were enrolled in the study. All patients recruited for the study had 15 or more lymph nodes dissected. Lymph nodes were mapped according to the JC, and metastases were examined histologically. The degree of lymph node metastasis and histological depth of invasion were determined according to both the JC and the TNM (sixth edition) systems. Distal gastrectomy was performed on 852 patients (68.5%). The degree of lymph node dissection was determined according to JC. D2 dissection was performed in 841 patients, D1 in 235, and D3 in 168. Mean tumor diameter was 44.3 ± 29.3 mm. The number of dissected lymph nodes was 38.0 ± 20.0 and the number of metastatic lymph nodes, 7.1 ± 9.0. Involvement of the retropancreatic, mesenteric, and para-aortic lymph nodes is classified as distant metastasis in TNM. Para-aortic lymph nodes located between the upper margin of the celiac trunk and the upper margin of the inferior mesenteric artery, which are defined as numbers 16a2 and 16b1, are regional lymph nodes (N3) in JC.

Statistics
All the statistical analyses were performed with the statistical software SPSS version 9.0 for Windows (SPSS, Chicago, IL). Univariate analysis of each staging group in each system was performed by the Kaplan-Meier method and comparisons were made with the log-rank test. P < .05 was considered significant.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Correlation Between Classifications of Lymph Node Metastasis in Different Systems
The number of patients classified by each classification and the correlation between the N numbers in JC and the pN numbers in TNM are listed in Table 1. The largest group was recognized to be the N0 group, which is equivalent to the pN0 group, and the most obvious discrepancies were observed in N2. All tumors classified under N3 in JC belonged to the distant metastasis category (M1) when reclassified in TNM.


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TABLE 1. Correlation between the two current different classifications of lymph node metastasis
 
Survival Rates by Lymph Node Metastasis Reclassified According to Each System
Cumulative survival rates according to TNM in patients with N1 or N2 by JC differed significantly. In patients with N1 lymph node metastasis in JC, there was a significant difference in survival between pN1 and pN2. Moreover, in patients with N2 lymph node metastasis, there were significant differences between pN1, pN2, and pN3 (Fig. 1). In contrast, there were no significant differences in survival according to JC of patients with pN1, pN2, and pN3 by TNM (Fig. 2).



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FIG. 1. Survival rates according to lymph node metastasis by JC (Japanese classification) after subclassification according to TNM. There were significant differences among pN1, pN2, and pN3 in both N1 and N2.

 


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FIG. 2. Survival rates according to lymph node metastasis by TNM after subclassification by JC. There was no significant difference between N1 and N2 in either pN1 or pN2.

 
Survival of Patients With Para-Aortic Lymph Node Metastasis
In TNM, there were significant differences in survival according to the number of metastatic lymph nodes in patients with para-aortic lymph node metastasis (numbers 16a2 and b1) classified as regional by JC. The cumulative 5-year survival rates were 50% of patients with 1–6 metastatic lymph nodes (pN1), 30% of those with 7–15 (pN2), and 7.3% of those with 16 or more (pN3) (Fig. 3).



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FIG. 3. Survival of patients with M1 according to number of metastatic lymph nodes in TNM. In TNM, the surgical results for patients with fewer metastatic lymph nodes were fairly good, and there were significant intergroup differences.

 
Survival Rates Classified by Each Staging System
In TNM, para-aortic lymph nodes are classified as distant metastases. However, on the basis of our results mentioned above, we advocate our new classification in which para-aortic lymph nodes (numbers 16a2 and b1) are included among the regional lymph nodes. The classification of lymph node metastasis should be exactly the same as in TNM. In short, lymph node metastases should be classified according to the number of metastatic lymph nodes. When the survival rates were calculated with the new classification, rationality and homogeneity of survival curve by lymph node classification were more clearly confirmed, whereas the survival rate of N2 and that of N3 overlapped each other in JC and the survival rate of pN3 and that of M1 were upside down in TNM (Fig. 4). In the new classification, there was a significant difference in survival between each N category.



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FIG. 4. Survival rates by lymph node classification according to the new system. Survival rates were clearly and homogenously differentiated by lymph node metastasis.

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The current study revealed that the TNM system, which classifies lymph node metastasis on the basis of the number of metastatic lymph nodes, proved to be a more rational prognostic determinant than the JC system, which classifies lymph node metastasis according to the anatomic sites of metastatic lymph nodes. Moreover, a new classification structured by integrating both classifications would be more homogenous in lymph node staging.

In this study, the heterogeneity of lymph node categories was observed in N1 and N2 of JC, especially in N2. With regard to surgical results, there were significant differences, according to TNM, in each JC category. However, there was no significant difference in surgical results, according to JC, in each TNM category. These results mean that the subgroup defined by JC is composed of heterogenous patients, whereas the TNM category consists of homogenous patients. TNM is therefore more rational than JC. In light of the fact that the numerical staging system is simpler, a numerical staging system would be more practical than the distributive staging system. Moreover, these results denied the advantages of the sophisticated and meticulous Japanese mapping system for dissected lymph nodes. Other reports have discussed the same results.7–9 Whereas the TNM staging system has an advantage in classifying only the number of metastatic lymph nodes and not the specific location, our study disclosed that this system has a disadvantage: para-aortic lymph nodes are defined as distant metastases (M1), not as regional lymph nodes. The surgical results in M1 were heterogeneous and the treatment outcomes for patients with 1–6 metastatic lymph nodes were fairly good, which suggested that categorization as distant metastasis by TNM was unreasonable.

We therefore devised a new classification by fusing the JC and TNM systems. The new classification consists of a staging system that is based on the total number of metastatic lymph nodes and includes the para-aortic lymph nodes as regional lymph nodes. When the surgical results were examined according to lymph node metastasis grouping, the categories were found to be homogeneous and had a better differentiation in survival analysis. These results serve to recommend our new classification system from the viewpoints of excellent clinical applicability and convenience. However, there is a disadvantage in this new system: we have to take the anatomic site of para-aortic lymph nodes into consideration again.

In conclusion, TNM is superior to JC. The new classification system has an advantage over the present two classifications, which are in common use in Japan and across the world. We believe that by combining the merits of each of the current classification systems, the new classification may serve as an appropriate and comprehensive system for surgeons the world over.


    ACKNOWLEDGMENTS
 
The authors are grateful to Dr. Kenji Ohshige (Department of Public Health, Yokohama City University, Graduate School of Medicine) for support in the statistical analysis for the manuscript.


    FOOTNOTES
 
With respect to classification of lymph node metastasis, the TNM system is a more rational prognostic tool than the Japanese system. A new staging system adopting the good points in the two systems would be more useful.

Received for publication June 16, 2003. Accepted for publication October 7, 2003.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma. In: Gastric Cancer. 2nd English ed. 1998: 10–24.
  2. Sobin LH, Wittenkind CH, eds. International Union Against Cancer. TNM Classification of Malignant Tumors. 6th ed. New York: John Wiley-Liss, 2002.
  3. de Manzoni G, Verlato G, Guglielmi A, Laterza E, Genna M, Cordiano C. Prognostic significance of lymph node dissection in gastric cancer. Br J Surg 1996; 83: 1604–7.[Medline]
  4. Adachi Y, Kamakura T, Mori M, Baba H, Maehara Y, Sugimachi K. Prognostic significance of positive lymph nodes in gastric carcinoma. Br J Surg 1994; 81: 414–6.[Medline]
  5. Boku T, Nakane Y, Okumura S, et al. A clinical study of adequate lymphadenectomy for gastric cancer from the aspect of the location of cancer. Jpn J Gastroenterol Surg 1992; 25: 7–13.
  6. Kunisaki C, Yamaoka H, Wakasugi J, et al. Lymphatic flow using activated carbon particles in lymph node metastasis and skip metastasis in gastric cancer. Jpn J Gastroenterol Surg 1997; 30: 2127–33.
  7. Ichikura T, Tomimatsu S, Uefuji K, et al. Evaluation of the New American Joint Committee on Cancer/International Union Against Cancer Classification of lymph node metastasis from gastric carcinoma in comparison with the Japanese classification. Cancer 1999; 86: 553–8.[CrossRef][Medline]
  8. Katai H, Yoshimura K, Maruyama K, Sasako M, Sano T. Evaluation of the New International Union Against Cancer TNM staging for gastric carcinoma. Cancer 2000; 88: 1796–80.[CrossRef][Medline]
  9. Fujii K, Isozaki K, Okajima K, et al. Clinical evaluation of lymph node metastasis in gastric cancer defined by the fifth edition of the TNM classification in comparison with the Japanese system. Br J Surgery 1999; 86: 685–9.[CrossRef][Medline]



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