Annals of Surgical Oncology 9:27-34 (2002)
© 2002 Society of Surgical Oncology
The Superiority of Ratio-Based Lymph Node Staging in Gastric Carcinoma
Kentaro Inoue, MD,
Yasushi Nakane, MD,
Hitoshi Iiyama, MD,
Mutsuya Sato, MD,
Tatsuya Kanbara, MD,
Koji Nakai, MD,
Syunichiro Okumura, MD,
Keigo Yamamichi, MD and
Koshiro Hioki, MD
From the Second Department of Surgery, Kansai Medical University, Osaka, Japan.
Correspondence: Address correspondence and reprint requests to: Kentaro Inoue, MD, Second Department of Surgery, Kansai Medical University, 10-15 Fumizonocho, Moriguchi, Osaka 570-8507, Japan; E-mail: inoueke{at}takii.kmu.ac.jp
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ABSTRACT
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Background: The need for a precise lymph node staging without stage migration is of paramount importance when comparing and evaluating international treatment results.
Methods: We reviewed 1019 patients who underwent R0 resection at Kansai Medical University between 1980 and 1997. The patients were classified according to the 1997 International Union Against Cancer (UICC)/American Joint Committee on Cancer (AJCC) pN classification or the N staging depending on the ratio between the number of excised and the number of involved lymph nodes (pN1, 
25%; pN2, 50%; pN3, >50%).
Results: Among the 1997 UICC/AJCC pN subgroups, prognosis worsened with an increase in lymph node ratio. In contrast, the ratio-based classification showed more homogenous survival according to the number of involved lymph nodes. Multiple stepwise regression analysis showed that the ratio-based classification was the most significant prognostic factor, whereas the 1997 UICC/AJCC classification was not found to be an independent predictor of survival. In addition, the ratio-based classification showed a superiority to the 1997 UICC/AJCC classification with respect to stage migration.
Conclusions: Ratio-based lymph node staging is simple and gives more precise information for prognosis with fewer problems related to stage migration than the 1997 UICC/AJCC staging system.
Key Words: Gastric carcinoma • Lymph node classification • Lymph node metastasis • Prognostic factor • TNM classification • Lymph node ratio
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INTRODUCTION
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It is now well recognized that local and lymphatic spread are the most important prognostic factors for patients with gastric carcinoma undergoing R0 resection, which is defined by the International Union Against Cancer (UICC) and American Joint Committee on Cancer (AJCC) as no macroscopic or microscopic residual tumor. The classification of the local spread (T classification) is well established and is also identical in the three main staging systems proposed by the UICC, the AJCC, and the Japanese Gastric Cancer Association (JGCA).1–4 In contrast, considerable controversy exists in regard to the classification of lymphatic spread (N classification). Until recently, all staging systems used for this disease defined N classification by the location of lymph node metastases relative to the primary tumor.3–7 At many institutions in the Western world, the anatomical localization of lymph nodes is determined by pathologists on the basis of formalin-fixed en-bloc resected specimens, and compliance of these staging systems has been low.8–10 In 1997, the UICC and AJCC redefined the pathologic nodal status on the basis of the number of involved nodes rather than their location.1,2 The UICC and AJCC reached complete agreement that the cutoff points for the N classification should be as follows: pN1, 1–6 involved regional lymph nodes; pN2, 7–15 involved regional lymph nodes; and pN3, more than 15 involved regional lymph nodes.
To date, many investigators have discussed the evaluation of the 1997 UICC/AJCC staging system,8–20 and the findings in these reports strongly suggest that the 1997 UICC/AJCC N classification is associated with higher reproducibility and increased strength of prognostic stratification than N classification by the location of lymph node metastases, and as a result this classification increases the possibilities for meaningful international comparisons of treatment results. However, in our previous publication we reported that the ratio between the number of excised and the number of involved lymph nodes was a parameter of prognostic significance, and some other investigators have shown similar results.21–24 Furthermore, some reports have suggested the superiority of the N classification according to the lymph node ratio with respect to the stage migration.22–24 A precise lymph node staging without stage migration is of paramount importance when comparing and evaluating international treatment results. However, previous researchers have shown no definitive superiority of the ratio-based N classification regarding the prognostic significance, compared with the number-based N classification. These investigators analyzed data by univariate analysis alone. In most malignant tumors, there are several interactions of risk for death among the different factors. Therefore, to investigate the prognostic factors, univariate analysis alone is not sufficient; multivariate techniques are mandatory. The aim of this study was to investigate, by using multivariate analysis, whether the ratio-based N classification or the 1997 UICC/AJCC N classification is superior regarding the prognostic significance.
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PATIENTS AND METHODS
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Between 1980 and 1997, 1826 patients were admitted to the Department of Surgery in Kansai Medical University with a diagnosis of primary gastric cancer. In 1772 cases operation was performed, and 1310 (73.9%) underwent an R0 resection. In 87 patients, there were insufficient data for this study; 8 patients had peritoneal or liver metastases, and in 204, fewer than 15 lymph nodes were histologically examined. Thus, these 299 patients were excluded from this study. Finally, 1019 patients were included in this study. Of the 1019 patients, 474 were found to have lymph node metastases, and the evaluation of this group provides the basis for this report.
N Classification
Nodal status was classified according to the 1997 UICC/AJCC staging system. Of the 474 patients with involved lymph nodes, 32 were found to have nonregional lymph nodes, such as retropancreatic, mesenteric, and paraaortic. These patients were also classified into the pN groups on the basis of the number of regional nodes. The median number of examined regional lymph nodes was 32 (mean, 35.1; range, 15 to 118) for all 1019 patients and 36 (mean, 39.3; range, 15 to 118) for the 474 patients with involved lymph nodes. The median number of involved regional nodes was 5.0 (mean, 7.1; range, 1 to 42). For comparative purposes, we also categorized N stage by the lymph node ratio according to our previous report, as follows: pN1, ratio between the number of excised regional nodes and the number of involved regional nodes was 25%; pN2, ratio was 50%; and pN3, ratio was >50%. The median of the lymph node ratio was 12.8% (mean, 18.8%; range, 1.1% to 93.3%).
Clinical and Histopathological Records
To further elucidate the prognostic significance of these N classifications, the clinical and histopathological records of these 474 patients were analyzed. The relationships between 5-year survival rates and time period of the operation, sex, age, tumor location, histopathological grading, macroscopic type, lymph node dissection, and depth of tumor invasion were determined. Tumor location, macroscopic type, and lymph node dissection were graded according to the Japanese Classification of Gastric Carcinoma proposed by the JGCA.4 Histopathological grading was defined according to the fifth edition of the TNM classification.1
Statistical Analysis
The final date for follow-up was December 31, 1999. The median follow-up from the date of surgery was 52.0 months (range, 0–179) for all patients and 65.0 months (range, 1–179) for survivors. Five-year survival rates and 95% confidence intervals (CI) were calculated according to the Kaplan-Meier method and included deaths from any other causes and postoperative mortality. The lost cases were treated as censored data for the analysis of survival rates. The log-rank test was used to assess the statistical differences between groups. Prognostic factors were assessed by multiple stepwise regression analysis by using the Cox proportional hazards model. The 
2 test was used in statistical comparison between the pN categories and clinical or histopathological factors. StatView J for Macintosh Version 5.0 (SAS, Inc., Cary, NC) was used to generate these analyses.
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RESULTS
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The 5-year survival rate was 71.9% (95% CI, 68.9%–74.9%) for all 1019 patients. The 5-year survival rates were 90.1% (95% CI, 87.4%–92.8%) for the node-negative patients and 51.0% (95% CI, 46.2%–55.9%) for the node-positive patients.
Clinical and Histopathological Features
Clinical and histopathological records for the 474 patients with involved lymph nodes and their observed 5-year survival rates are shown in Table 1. The 271 patients who underwent operation between 1990 and 1997 had a slightly better prognosis than the 203 patients who underwent operation between 1980 and 1989. This difference was significant (P = .0344) among the patients who had T2 tumor (1990s, 58.0% [95% confidence interval, 49.7%–66.3%]; 1980s, 47.2% (38.2%–56.2%]). The sex ratio was 2:1 for men. There was no survival difference between women and men. However, age at diagnosis was a significant prognostic factor. Patients younger than 50 years had the best prognosis, and the prognosis of patients younger than 70 years was also better than that of those more than 70 years old. Prognosis was also related to the location of the tumor; cancers located in the upper third had the worst survival rates among the three portions of the stomach. The macroscopic features of the tumor had an important bearing on survival; the highest survival rates were found for type 0 and the lowest for type 4. In contrast, histopathological grading was not a significant prognostic factor. There was no significant difference in survival among D1 dissection, D2 dissection, and D3 and D4 dissection. The extent of tumor spread was a major prognostic factor. The T1 patients had a good prognosis. Among the 474 patients, 421 (88.8%) had T2 or higher tumors. Significant differences (P < .05) were seen in following factors: age, macroscopic type, and tumor spread.
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TABLE 1. Observed 5-year survival rates of the 474 patients with involved lymph nodes, depending on clinical and histopathological features
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Observed 5-Year Survival Rates According to the pN Classification
Figure 1 shows the observed 5-year survival rates of the 474 patients with involved lymph nodes in relation to the 1997 UICC/AJCC pN classification and ratio-based pN classification. The 5-year survival rates of the patients staged by the UICC/AJCC pN classification were 62.2% (56.1%–68.2%) for pN1, 39.6% (30.8%–48.3%) for pN2, and 19.7% (7.5%–31.9%) for pN3. When the patients were classified by the involved lymph node ratio, the 5-year survival rates were 59.4% (53.9%–65.0%) for pN1, 36.1% (25.3%–47.0%) for pN2, and 6.2% (0%–16.7%) for pN3. Both lymph node classifications defined groups with widely differing prognoses and showed a marked significant difference (P < .0001).
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FIG. 1. Comparison of observed 5-year survival rates of the 474 patients with involved lymph nodes for the pN1, pN2, and pN3 categories according to the 1997 International Union Against Cancer (UICC)/American Joint Committee on Cancer (AJCC) and to the lymph node ratio (the ratio between the number of excised regional nodes and the number of involved regional nodes). The error bars show 95% confidence intervals. P values refer to log-rank tests for differences between categories within each pN classification.
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Figure 2 compares the 5-year survival rates of the UICC/AJCC pN subgroups separated according to the ratio-based classification. Among these pN subgroups, different survival was noted according to their lymph node ratio; prognosis worsened with an increase in lymph node ratio. In contrast, the ratio-based classification showed more homogenous survival according to the number of involved lymph nodes, with the exception of the patients in the UICC/AJCC pN1/Ratio-based pN1 subgroup, who had the best prognosis.
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FIG. 2. Observed 5-year survival rates of the 474 patients with involved lymph nodes are shown in relation to the number of involved regional lymph nodes and the lymph node ratio. The error bars show 95% confidence intervals. UICC, International Union Against Cancer; AJCC, American Joint Committee on Cancer.
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Multivariate Analysis
Stepwise regression analysis was performed for 474 patients with involved lymph nodes to determine the independent prognostic factors (among age, macroscopic finding, depth of tumor invasion, the 1997 UICC/AJCC pN classification, and the ratio-based pN classification) that were found by univariate analysis to be significantly associated (P < .05) with survival. Patients’ distribution between pN categories and other prognostic factors are shown in Table 2. In both pN classifications, patients were classified into a more advanced stage with advancement of tumor spread and macroscopic features. There was no difference between the UICC/AJCC classification and ratio-based classification. The UICC/AJCC classification was significantly associated with survival (pN1, set at 1; pN2, 1.719 [1.267–2.333]; pN3, 2.196 [1.471–3.276]; P < .0001) when the multivariate analysis was performed without the ratio-based pN classification. When a model including only the ratio-based pN classification was applied, the ratio-based classification was also significantly associated with survival (pN1, set at 1; pN2, 1.623 [1.159–2.273]; pN3, 2.875 [1.919–4.309]; P < .0001). When a model including both pN classifications was applied, the ratio-based pN classification was the most significant prognostic factor, followed by age, depth of tumor invasion, and macroscopic type; however, the 1997 UICC/AJCC pN classification was not found to be an independent predictor of survival (Table 3).
Stage Migration
To evaluate the influence on the number of examined lymph nodes, the patients were also classified into two groups: patients in which 36 or fewer nodes were examined and those with more than 36 examined lymph nodes. The prognostic differences between the two groups in the 1997 UICC/AJCC pN categories were higher than in the ratio-based classification (Table 4). Thus, the pN classification according to the lymph node ratio shows superiority in comparison to the 1997 UICC/AJCC classification with respect to the stage migration.
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DISCUSSION
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There are several purposes for a staging system: (1) to give some indication of prognosis for cancer patients, (2) to aid the clinician in planning treatment, and (3) to compare the interinstitutional and international treatment results. To accomplish these purposes, the staging system must be feasible, reproducible, and accurate for prognostic stratification without stage migration. In Japan, during the immediate postoperative process, lymph nodes are retrieved from the resected specimen by experienced surgeons, who obtain a three-dimensional view of the anatomical relationships during the operation. On the basis of this, a precise but complex localization-based N classification has been developed.3,4 The JGCA system considers the lymphatic pathway, and from the viewpoint of surgical application, the JGCA system is useful. In our institution, the 271 patients who underwent operation between 1990 and 1997 had a slightly better prognosis than the 203 patients who underwent operation between 1980 and 1989. This difference was significant (P = .0344) between patients who had T2 tumors at the two different time periods (1990s, 58.0% [49.7%–66.3%]; and 1980s, 47.2% [38.2%–56.2%]). Thus, we speculate that the JGCA pN classification and the systematic lymphadenectomy based on it are important for improving the prognosis for patients with gastric carcinoma. Furthermore, when the 1997 UICC/AJCC, ratio-based, and JGCA classifications were combined and assessed by multiple stepwise regression analysis with the Cox proportional hazards model, the JGCA classification was selected as the most significant prognostic determinant (data not shown). However, considering the feasibility and reproducibility of pN classification, number-based or ratio-based classifications are the classification of choice. In several studies, the prognostic significance of the number of involved lymph nodes has been investigated, but because the positive-node number is a continuous variable, the definition of significant prognostic cutoff points varies.25–36 In our previous report, we suggested one to three as a cutoff for N1, four to six for N2, and more than six for N3.21 In this analysis, there was no survival difference between one to three positive nodes (62.8%, 55.2%–70.4%) and four to six (61.6%, 51.8%–71.3%). Furthermore, the 1997 UICC/AJCC pN classification was significantly associated with survival, when stepwise regression analysis was performed without the ratio-based pN classification. Our updated findings support the strong prognostic value of using 1 to 6 involved nodes as N1, 7 to 15 as N2, and >15 as N3. However, the lymph node ratio is also an important prognostic factor. In our previous publication we reported that the lymph node ratio, together with the number of involved lymph nodes, was a parameter of prognostic significance, and the prognostic significance of assessing the lymph node ratio has been appreciated for some time.22–24 Siewert et al.22 evaluated the 10-year results of 1654 patients in the German Gastric Cancer Study (prospective multicenter observation trial) and identified the lymph node ratio (<<20% vs. >20%) and the residual tumor status (R classification) as the major independent prognostic factors in patients with resected gastric cancer. They also reported that the ratio between positive and removed nodes is a simple measure of the efficacy of lymphadenectomy and constitutes the most important independent prognostic factor in patients with an R0 resection. Yu et al.23 analyzed 886 patients who underwent gastrectomy with D2 or more extended lymphadenectomy with curative intent and reported significant prognostic differences among N0, N1 (metastasis in 1%–25% of dissected nodes), and N2 (metastasis in more than 25% of dissected nodes). Kodera et al.24 analyzed 656 patients with advanced gastric cancer who underwent D2 lymphadenectomy and reported significant prognostic differences among 0%, 1%–19%, 20%–60%, and >60% of lymph node ratio.
In this study, we compared the prognostic determinant of the 1997 UICC/AJCC classification with the classification based on the lymph node ratio (0%, <<25%, <<50%, and >50%) in patients who underwent an R0 resection. From the analysis by multiple stepwise regression analysis with the Cox proportional hazards model, the ratio-based classification was selected as the most significant prognostic determinant when both N classifications were included in the analysis. Thus, the lymph node classification according to lymph node ratio was considered a better prognostic determinant than the 1997 UICC/AJCC staging system. We also found that the 1997 UICC/AJCC N staging system had different survival between the two groups (36 or fewer examined lymph nodes vs. more than 36 examined lymph nodes). These findings are suggestive of the effect of lymph node dissection on prognosis, but the role of the lymph node dissection in the survival of gastric cancer is still highly speculative. To date, two large randomized trials comparing D1 with D2 dissection in patients undergoing potentially curative resection have been completed: one by the Medical Research Council in the United Kingdom and the other by the Dutch Gastric Cancer Group in the Netherlands.37,38 These trials could not confirm the hypothesis that the extended (D2) lymph node dissection leads to better survival. In the light of present evidence with reference to the rule of lymph node dissection in gastric cancer, we should primarily interpret that the 1997 UICC/AJCC N staging system had different survival according to the number of examined lymph nodes as the result of the stage migration of the number-based N classification. The number of involved lymph nodes is influenced by the number of examined nodes. In the 1997 UICC/AJCC N classification, it is routine practice for more than 15 regional lymph nodes to be examined, but errors still occur in staging, as shown in Table 4. Kodera et al.24 analyzed the patients with retrieval of more than 20 lymph nodes and reported that the number of metastatic nodes was still found to be affected by the nodal yield. An extended lymph node dissection with careful examination for metastases allows more accurate number-based N staging, and this should be performed whenever feasible. However, at institutions where the extended lymph node dissection is not a standard procedure, the procedure is more complicated, and the number-based staging is of no value in such a situation. The ratio-based N classification minimized this potential source of clinicians’ error or bias, and we could single out this classification as the most important prognostic factor by multivariate analysis. Our findings strongly suggest that the ratio-based N classification is more appropriate as an international staging system.
Received for publication January 23, 2001.
Accepted for publication September 10, 2001.
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TOP
ABSTRACT
INTRODUCTION
