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From the Department of Surgery, The University of Chicago, Chicago, Illinois.
Correspondence: Address correspondence to: Mitchell C. Posner, MD, Department of Surgery, The University of Chicago, 5841 S. Maryland Ave., MC 5031, Chicago, IL 60637; Fax: 773-702-4444; E-mail: mposner{at}surgery bsd.uchicago.edu.
In this issue of Annals of Surgical Oncology, Nitti et al.1 review the prognostic significance of lymph node metastases among 277 evaluable patients treated for locoregional gastric adenocarcinoma by R0 gastrectomy and D2 lymphadenectomy at a single institution between 1980 and 2000. Lymph node metastases were evaluated by several different schemas. The location of lymph node metastases as described by the Japanese Research Society for Gastric Carcinoma (JRSGC); the number of lymph node metastases as described by the International Union Against Cancer (UICC) and American Joint Committee on Cancer (AJCC); and the ratio of lymph node metastases to total lymph nodes examined (lymph node metastasis ratio) were compared as predictors of 5-year survival. The presence of nodal metastases at higher lymph node stations, a greater number of lymph node metastases, and a greater lymph node metastasis ratio were each associated with poorer survival by univariate analysis. When multivariate analysis was performed including all three lymph node metastases classification systems as covariates, only lymph node metastasis ratio and the T classification (UICC and AJCC) of the primary tumor were independent prognostic factors.
Statistical methods suggested natural groupings of patients with lymph node metastasis ratios of 0%, 1% to 10%, 11% to 25%, and >25%. When the patients were grouped according to UICC and AJCC N classification, patients with one to six positive nodes (N1) were found to have lymph node metastasis ratios of 1% to 10%, 11% to 25%, or >25%. Similarly, patients with 7 to 15 positive nodes (N2) had lymph node metastasis ratios of 11% to 25%, or >25%. Among N1 and N2 patients, lymph node metastasis ratio predicted survival at a significance of P < .06 (N1) or P < .04 (N2).
The report by Nitti et al.1 adds to the growing body of evidence suggesting that the number of lymph node metastases currently used to stage gastric cancer by the UICC and AJCC guidelines is best interpreted in terms of the total number of lymph nodes examined from the specimen. Over the last 13 years, several groups have reported that the lymph node metastasis ratio is a powerful prognostic factor following resection of gastric cancer.2–7 This report is the first Western series to directly compare the JRSGC and lymph node metastasis ratio. The cumulative evidence suggests that when a small number of lymph node metastases are found, a greater number of normal lymph nodes in the specimen is associated with a better prognosis. At least two explanations for this phenomenon are possible. The inclusion of more lymph nodes within the specimen may be an indicator of more complete lymphadenectomy, which in turn could lead to better outcomes. Alternatively, it is possible lymph node metastases are being underdiagnosed in patients with a small number of nodes examined, and examination of more lymph nodes would lead to stage shifting of these patients to a higher N classification.
Certain limitations of the analysis are noted. This is a single institution experience where D2 lymphadenectomy is the standard and, therefore, wide applicability of its findings to the general population of gastric cancer patients is unproved. A small group of patients (<10%) was excluded from the analysis because of inadequate pathologic evaluation. Furthermore, statistical methods were used to define the most distinct groups of patients according to lymph node metastasis ratio. These cut-off values vary among similar reports, although the first prognostic classification for patients with lymph node metastases is typically 
10% to 20%. Optimizing the grouping for lymph node metastasis ratio may have resulted in a slight prognostic advantage over the standardized systems (JRSGC or UICC and AJCC) in this report. Subsequently, it is difficult to be certain that the lymph node metastasis ratio groupings used for this report would be superior to other nodal metastasis systems for all gastric cancer populations. Nevertheless, the differences in survival among N1 and N2 patients according to lymph node metastasis ratio provide suggestive evidence that this is an additional important prognostic factor.
Could or should the lymph node metastases ratio supplant the current staging system for nodal involvement by gastric cancer? This might have important implications for patients in countries such as the United States where most gastric cancer is resected with limited lymphadenectomy.8 At this time, we cannot make assumptions about the validity of the lymph node metastases ratio among patients with less extensive lymphadenectomy. It may retain its value as a prognostic factor in this population. Its value, however, may be confounded by the small number of nodes examined from each patient. To illustrate, a patient with a single nodal metastasis would fall into the 1% to 10% group if at least 15 nodes were examined from the specimen, as suggested by the UICC and AJCC guidelines. A lesser lymphadenectomy with removal of fewer than 10 nodes would place this patient in the 11% to 25% group. The range of nodes examined by Nitti et al. among their D2 lymphadenectomies was 11 to 62. A lack of correlation between the lymph node metastases ratio and survival among patients treated by limited resection would be of interest, as it would add to the argument for more extensive lymphadenectomy and more intensive pathologic examination of gastric cancer specimens. Importantly, we should keep in mind that the extent of lymph node involvement does not currently influence our treatment decisions for gastric cancer, although better prognostic indices could change that in the future.
In summary, the lymph node metastases ratio is an additional prognostic factor to consider in patients with gastric cancer resected with a D2 lymphadenectomy. It may be useful for counseling patients, and it encourages detailed pathologic lymph node examination to help determine the likelihood of tumor recurrence in patients with limited lymph node metastases. It may prove to be an important factor for stratification of patients in future trials of adjuvant treatment. Its value for patients with limited lymphadenectomy, which is far and away the standard in the United States, is yet to be determined. Therefore, it should not be used for prognostic information in patients with fewer than 15 nodes examined. Ultimately, data such as these may lead to a stricter requirement by the UICC and AJCC guidelines for the number of lymph nodes in a gastric cancer lymphadenectomy specimen or formal incorporation of the lymph node metastases ratio into the staging system.
Received for publication September 5, 2003. Accepted for publication September 23, 2003.
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