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10.1245/ASO.2005.03.008
Annals of Surgical Oncology 12:981-987 (2005)
© 2005 Society of Surgical Oncology
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Original Article

Inadequacy of Lymph Node Staging in Gastric Cancer Patients: A Population-Based Study

Nancy N. Baxter, MD, PhD1 and Todd M. Tuttle, MD, MS1,2

1 Department of Surgery, Division of Surgical Oncology, University of Minnesota, 420 Delaware Street S.E., Minneapolis, Minnesota 55455
2 University of Minnesota Comprehensive Cancer Center, University of Minnesota, 420 Delaware Street S.E., Minneapolis, Minnesota 55455

Correspondence: Address correspondence and reprint requests to: Todd M. Tuttle, MD, MS; E-mail: tuttl006{at}umn.edu.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: In 1997, examination of at least 15 lymph nodes was recommended for adequate gastric cancer staging. However, the proportion of patients undergoing an adequate lymph node examination (LNE) has not been studied in a population-based manner.

Methods: We used Surveillance, Epidemiology, and End Results cancer registry data to assess LNE adequacy in adults with nonmetastatic gastric adenocarcinoma. We selected patients aged 18 through 80 years whose disease was diagnosed from 1998 through 2001 and who underwent at least partial gastrectomy. We evaluated the overall number of nodes, estimated the likelihood of adequate LNE (i.e., ≥15 nodes examined), and determined the influence of selected tumor and patient characteristics on LNE.

Results: In this 4-year period, 3593 patients met our study’s selection criteria. The median number of nodes examined was 10: 32% of patients underwent adequate LNE, and 9% of patients had no nodes examined. Node-positive patients were more likely to have undergone an adequate LNE than node-negative patients (42% vs. 23%; P < .0001). Younger age, female sex, and more radical surgery were associated with adequate LNE in both univariate and multivariate analysis (P < .0001). Geographical site was an important predictor; patients from one registry (Hawaii) were significantly more likely to have undergone adequate LNE than patients from all other registries (56% vs. 30%; P < .0001).

Conclusions: Our 4-year review of the Surveillance, Epidemiology, and End Results database revealed that only a third of patients with gastric cancer underwent adequate LNE, i.e., had the recommended minimum of 15 nodes examined for gastric cancer staging. Better results at one registry (Hawaii) indicate that substantial improvements could be made.

Key Words: Staging • Patterns ofcare • Standard of care • Gastric cancer • Surgery • Pathology


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In 2005, almost 22,000 Americans are expected to develop gastric cancer.1 The current 5-year survival rate for patients with gastric cancer is only 23%, so most will die of their disease.1 Although the incidence of gastric adenocarcinoma is declining in the United States, this disease remains a significant cause of cancer death worldwide. The survival of patients with potentially curable gastric cancer is primarily determined by pathologic tumor (T) and lymph node (N) staging. The extent of lymph node dissection (D1 vs. D2) for curable gastric cancer has been debated for several decades. In 1997, the American Joint Committee on Cancer (AJCC)/International Union Against Cancer (UICC) staging systems were revised to recommend that a regional lymph node specimen for gastric cancer contain at least 15 nodes.2,3 The staging systems were also revised to incorporate the number of involved lymph nodes in the staging of gastric cancer.3 In this revised staging system, N0 represents no involved lymph nodes; N1, 1 to 6 involved nodes; N2, 7 to 15 involved nodes; and N3, >15 involved lymph nodes. Previously, nodal staging was based on the location of metastatic lymph nodes.4

Before the 1997 staging system recommendation and revision, there was evidence that lymph node examination (LNE) was not adequate in the United States. In a mid-1990s patient care survey of cancer programs approved by the American College of Surgeons,5,6 information regarding LNE techniques was obtained through questionnaires completed by tumor registrars from the programs. Standard elements of LNE were often not performed at the surveyed programs: dissection of perigastric lymph node stations was documented in less than half of all gastric resections; sampling of common hepatic lymph nodes was documented in only 6% of cases; celiac lymph nodes, in only 14%; and splenic lymph nodes, in only 8%. Again, of course, that survey was conducted before the AJCC/UICC staging system recommendation and revision.

The purpose of this study was to determine the adequacy of LNE for patients with gastric cancer in the United States since the 1997 AJCC/UICC staging system recommendation and revision. Using a population-based registry, we sought to determine whether certain patient, treatment, and pathologic factors were associated with adequate LNE in a large, unselected group of patients.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Data
We used data from the Surveillance, Epidemiology, and End Results (SEER) cancer registry to conduct our study. SEER, a population-based registry sponsored by the National Cancer Institute, collects information on cancer incidence and survival from 11 population-based cancer registries, including approximately 14% of the US population.7 Because SEER reports data by registry, our study period includes data from those corresponding 11 distinct geographical sites. The information collected by SEER includes patient characteristics, primary tumor site, tumor grade, stage at diagnosis, first course of treatment (through completion of the initial treatment plan, including treatment within the first year after diagnosis or until there is evidence either of disease progression or of treatment failure within the first year), timing of radiation, number of lymph nodes examined, number of positive lymph nodes, geographical registry of residence, and follow-up for vital status.7 SEER does not report the extent of LNE in detail.

Patients
We included patients aged 18 through 80 years who had nonmetastatic invasive adenocarcinoma of the stomach from January 1998 through December 2001. We excluded patients presenting with in situ or metastatic disease, patients with malignancies other than adenocarcinoma, patients who did not undergo at least partial gastrectomy, and patients who underwent preoperative radiation. Because our study used preexisting data with no personal identifiers, it was exempt from review by the University of Minnesota Institutional Review Board.

Statistical Analysis
We calculated the mean and median number of nodes examined. We then determined the proportion of patients who had no nodes examined and the proportion of patients who had at least 15 nodes examined (defined as adequate LNE). We compared the number of lymph nodes examined between groups by using Student’s t-test. We compared the proportion of patients who underwent an adequate LNE between groups by using the {chi}2 test. We tested, by logistic regression, for any association between adequate LNE and patient age, race, sex, and geographical site; nodal status (positive or negative); tumor grade and depth of wall penetration (T stage); anatomical site; and extent of surgical resection. We tested for interactions between nodal status (positive or negative) and all other covariates, planning to repeat a stratified analysis if interactions were detected. We used SAS version 9.1 (SAS Institute, Cary NC) for our analysis. All statistical tests were two sided. In the past, we have successfully used similar methodology to evaluate nodal examination in patients with colorectal cancer.8


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In this 4-year period, 3593 patients (37% female and 63% male) met our study’s selection criteria. Most patients were white (62.5%) and had poorly differentiated tumors (68%) with advanced T stages (67%) (Table 1Go). The number of lymph nodes examined could be determined for 3445 (96%) patients. The median number of lymph nodes examined for all patients was 10 (Fig. 1Go). No lymph nodes were examined in 9% of the patients. With a cutoff of 15 nodes, only 32% of patients underwent adequate LNE. Most patients (60%) were node positive. Node-positive patients were more likely to have advanced T stages and advanced tumor grades compared with node-negative patients (advanced T stage: 85% vs. 41%, P < .0001; advanced tumor grade: 77% vs. 56%, P < .0001) (Table 1Go). Node-positive patients were also more likely to undergo a near-total or total gastrectomy than were node-negative patients (28% vs. 20%; P < .0001).


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  		TABLE 1. Patient and tumor characteristics
 

Figure 1
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  		FIG. 1. Number of lymph nodes evaluated per patient in patients with gastric cancer identified by using the Surveillance, Epidemiology, and End Results database.

 
We next evaluated whether selected patient and tumor characteristics were associated with a higher rate of adequate LNE (Table 2Go). Other than the anatomical site of the tumor, all characteristics evaluated (age, sex, race, T stage, tumor grade, gastrectomy type, and nodal status) were associated with the number of nodes examined (P ≤ .004, all variables) and with LNE adequacy (P < .0001, all variables). For example, younger (vs. older) patients were statistically significantly more likely to have undergone adequate LNE: 37% of those ≤64 years underwent adequate LNE versus 27% of those ≥75 years (P < .0001). Node-positive (vs. node-negative) patients had a higher median number of lymph nodes examined and were more likely to have undergone adequate LNE (median number of nodes examined, 12 vs. 8; P < .0001; adequate LNE: 42% vs. 23%, P < .0001).


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  		TABLE 2. Effect of patient and tumor characteristics on LNE adequacya
 
The results of our multivariate analysis are presented in Table 3Go. After adjusting for potential confounders, we found that younger patients, women, patients of nonwhite race, and patients undergoing more radical surgery (i.e., near-total or total gastrectomy or en-bloc resection of other organs) were significantly more likely to have undergone adequate LNE than their corresponding comparison groups (P < .03, all variables). Node-positive (vs. node-negative) patients were more than twice as likely to have undergone adequate LNE (odds ratio, 2.2; 95% confidence interval, 1.8–2.6). We found no significant statistical interactions between nodal status and the other variables in our analysis, thus indicating that nodal status did not affect the relationship between other variables and the likelihood of adequate LNE; therefore, we did not stratify by nodal status.


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  		TABLE 3. Effect of patient and tumor characteristics on LNE adequacy—multivariate analysisa
 
In all our analyses, geographical site was an important predictor of adequate LNE. Patients from one registry (Hawaii) were significantly more likely to have undergone adequate LNE compared with those from all other registries (56% vs. 30%; P < .0001), in both univariate and multivariate analyses. In our multivariate analysis (adjusting for race), patients in Hawaii were between 2 and 4 times more likely to have undergone adequate LNE compared with patients from other registries (range, 2.4–4.2 times; P < .0001) (Fig. 2Go).


Figure 2
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  		FIG. 2. Proportion of patients with an adequate number of lymph nodes evaluated (at least 15) by the Surveillance, Epidemiology, and End Results (SEER) registry. 1, Hawaii; 2–11, other SEER registries; LNE, lymph node examination.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Survival rates of patients with gastric cancer are consistently higher in Japan than in the United States or Europe5,9,10: one of the proposed reasons for this difference is the more extended lymph node dissection typically performed by Japanese surgeons. Because observational studies found an improved survival rate for patients who underwent extended dissection, the Japanese Research Society for the Study of Gastric Cancer recommends routine performance of a D2 lymph node dissection11 (a D1 dissection is defined as the removal of all N1 [perigastric] lymph node stations; a D2 dissection, removal of N1 and N2 [common hepatic, left gastric, celiac, and splenic] lymph node stations). However, two large European randomized clinical trials found no convincing evidence that a D2 dissection improves overall survival.12–14 In fact, in those two European trials, the morbidity and mortality rates were higher after a D2 resection. Those two studies were limited by a lack of surgical and pathologic quality control, by documented contamination and noncompliance, and by the adverse effect of pancreatic and splenic resections required after a D2 dissection.12–16

Nevertheless, other studies in US populations have found that survival after curative gastric resection is associated with the number of lymph nodes examined. In a recent analysis of the SEER database, Schwarz and Smith17 reported that for every subgroup analyzed, survival for patients with gastric cancer was highly dependent on the number of lymph nodes examined. Karpeh et al.18 reported that for stage II, IIIA, or IIIB gastric cancer, survival improved when 15 or more lymph nodes were examined. Using the Maruyama Index of Unresected Disease, Hundahl et al.19 reported that improved survival was not simply a result of stage migration, but may be related to improved regional control when lymph node dissection was adequate.

In the United States, the minimum curative surgery that is considered adequate for patients with gastric cancer is gastrectomy (partial or total) and a D1 lymph node dissection. However, many patients undergo less than an adequate dissection (D0). Hundahl et al.19 reviewed the surgical data from the Intergroup 0116 (Southwest Oncology Group 9008) trial. In that randomized trial evaluating postoperative chemoradiation, 54% of patients underwent less than a D1 lymph node dissection, despite the protocol recommendation of a D2 lymph node dissection. D0 resections were performed less frequently after total gastrectomy because the perigastric lymph node stations were better dissected. The current edition of the AJCC staging manual recommends examining at least 15 lymph nodes for adequate gastric cancer staging. Several single-institution studies have demonstrated that this recommendation is achievable.18,20,21 For instance, Karpeh et al.18 reported that the mean number of lymph nodes examined was 23.9 at Memorial Sloan-Kettering Cancer Center after curative gastric resection; only 27% of their patients did not have at least 15 lymph nodes examined.

However, the overall proportion of patients nationwide who undergo adequate LNE is substantially less than the proportion reported by single-institution studies. An analysis of the National Cancer Data Base of 50,169 patients with gastric cancer, diagnosed from 1985 through 1996, found that only 18% had more than 15 lymph nodes examined.22 Likewise, the American College of Surgeons patient care survey indicated that most patients did not undergo adequate perigastric lymph node dissection.5,6

In contrast to previous studies, the time period chosen for our study began after the current AJCC recommendation and revision. Nonetheless, we found that only 32% of patients had undergone adequate LNE. Our findings for gastric cancer are similar to those for colorectal cancer: in 2001, only 44% of patients with colorectal cancer underwent adequate LNE.8

The number of lymph nodes present in any given individual is variable and can be influenced by patient, tumor, and treatment characteristics. In our study, younger patient age, female sex, and more radical surgery were associated with higher rates of adequate LNE. African American and Asian patients had more lymph nodes examined than white patients. Node-positive patients were also more likely to have undergone adequate LNE. Some of these differences may reflect true differences in the number of lymph nodes present; for example, the number of lymph nodes present may decrease with age. Alternatively, in some cases, differences between groups may be due to the ease of lymph node detection: for example, obesity is known to influence the ease of lymph node detection,23 and obesity varies by race.24 However, some differences cannot be explained by tumor or patient characteristics. For example, we identified differences in LNE by geographical site; patients from the Hawaii registry (after adjustment for race) had significantly higher rates of adequate LNE compared with patients from other registries, thus indicating that local practice patterns may affect LNE. Similar geographical variation has been identified for LNE in patients with colorectal cancer.8

Our study used population-based data; we did not have detailed patient and tumor information and had no information regarding surgical and pathologic techniques. Certainly surgical factors (such as procedure volume) and pathologic factors (such as the use of specialized fat-clearing techniques) would affect LNE. Additionally, the quality of surgical care and the quality of pathologic assessment likely vary, but neither factor is measured by SEER. However, given that SEER is a population-based registry that includes 14% of the US population, the findings of our study do represent US community standards.

Despite the recent 1997 AJCC/UICC recommendations, two thirds of gastric cancer patients in the United States undergo inadequate LNE. Both surgical undertreatment and incomplete pathologic examination likely contribute to this problem. Comprehensive fat-clearing techniques may improve the lymph node yield in gastric cancer dissections,25,26 but such techniques have rarely been used clinically. The observations reported in our study must be considered in the design and analysis of future surgical and adjuvant gastric cancer clinical trials. Further research must evaluate factors associated with increased lymph node retrieval and must assess intervention strategies to ensure proper surgical care and pathologic assessment. Adequate training of surgeons and pathologists may improve gastric cancer staging in the United States. Such efforts may be facilitated by the Society of Surgical Oncology and the College of American Pathologists. Individual institutions and some SEER registries have demonstrated that adequate lymph node evaluation for gastric cancer is feasible in the United States. In addition, each surgeon should review and orient gross specimens with consulting surgical pathologists to ensure adequate lymph node evaluation. Finally, physicians must consider referring patients with gastric cancer to high-volume centers of excellence that have experienced surgeons and pathologists.


   ACKNOWLEDGMENTS
 
The authors thank Dr. Mary Knatterud for her helpful editorial suggestions. Supported, in part, by the University of Minnesota Comprehensive Cancer Center. Both authors are supported by University of Minnesota Cancer Center Clinical Scholar Awards. N.N.B. is supported by an American Society of Clinical Oncology Career Development Award.

Received for publication March 1, 2005. Accepted for publication July 20, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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