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Annals of Surgical Oncology 9:1010-1016 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

The Prognostic Significance of Lymph Node Size in Patients With Squamous Esophageal Cancer

Dipok Kumar Dhar, MD, Mitsuo Tachibana, MD, Naoko Kinukawa, PhD, Maruyama Riruke, MD, Hitoshi Kohno, MD, Alex G. Little, MD and Naofumi Nagasue, MD

From the Second Department of Surgery (MT, HK, NN) and Department of Central Pathological Laboratory (MR), Shimane Medical University, Izumo, Japan; Department of Medical Information Science (NK), Faculty of Medicine, Kyushu University, Fukuoka-shi, Japan; and Department of Surgery (AGL), University of Nevada, School of Medicine, Las Vegas, Nevada.

Correspondence: Address correspondence and reprint requests to: Dipok Kumar Dhar, MD, Second Department of Surgery, Shimane Medical University, Izumo 693-8501, Japan; Fax: 81-853-202229; E-mail: nigeka33{at}shimane-med.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The prognosis of patients with esophageal cancer remains dismal, and their care poses a great challenge of customizing therapeutic strategies for individual patients. Lymph node staging is still less than ideal in esophageal cancer patients. Therefore, we investigated a new approach to lymph node analysis.

Methods: One hundred eighty-seven patients curatively resected for squamous cell cancer of the esophagus were studied. The long diameter of the largest metastatic lymph node (MLN) was measured on a histopathologic slide and was considered as the MLN size.

Results: Patient survival decreased with each millimeter increment in MLN size. By using MLN size as the lymph node classification criterion, patients with MLN <10 mm had both a significantly better overall and cancer-specific survival than those with MLN >=10 mm. Patients with fewer than four MLNs were separated into prognostic groups according to the MLN size. Among the several prognostic factors, MLN size remained the strongest independent predictor of survival by multivariate analysis. This nodal analysis allowed stratification of patients into four stages with distinctly different survivals.

Conclusions: This approach supplements traditional nodal staging strategies and therefore has potential for guiding the development of treatment strategies in this carcinoma.

Key Words: Esophageal carcinoma • Staging • Prognosis • Metastatic lymph node size • Metastatic lymph node number


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The treatment of esophageal cancer patients poses a major clinical challenge.1,2 Early-stage disease has a better prognosis than advanced-stage disease with extensive lymph node (LN) metastasis.3,4 Regional LN metastasis still remains one of the most important prognostic factors in this carcinoma.5,6

Proper staging is a prerequisite for designing therapeutic strategies for individual patients. Tumor staging is a standardized common language that facilitates comparison of treatment results from different institutions and also enables clinicians to predict prognosis. In an effort to promote uniform cancer staging, the International Union Against Cancer (UICC) and the American Joint Committee on Cancer recommended the first tumor-node-metastasis classification in 1958. Subsequent refinements have attempted to improve the predictability of prognosis and reproducibility.

The T category of the tumor-node-metastasis classification was improved by using the depth of wall penetration instead of tumor length.7 LN staging is still less than ideal. Previously, it was thought that once the regional LNs were involved, the prognosis was dismal. However, a certain number of patients with shallow tumor, a limited number of metastatic regional LNs, or both have an improved prognosis after a curative resection with lymphadenectomy.5,6,8 Therefore, further stratification of the N category would be useful. Although the pN classification in patients with gastric and colon carcinomas is divided into prognostically different groups in the revised tumor-node-metastasis classification (1997),9 this is yet to be settled in esophageal carcinoma patients. In this study, we set out to analyze a very simple way to stage metastatic LNs (MLNs) in esophageal carcinoma patients by measuring the long axis of the largest MLN on histopathologic specimens.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Between February 1981 and December 1999, we studied 187 patients with squamous cell carcinoma of the esophagus who underwent a curative resection at Shimane Medical University. Of these patients, 16 (9%) were women and 171 (91%) were men; their ages ranged from 46 to 83 years. All patients underwent a standardized one-stage esophagectomy with extensive lymphadenectomy, as described previously.10 Gastrointestinal continuity was restored mostly by a gastric and in some cases by a colonic interposition. Immediately after resection, all specimens were opened in the operating room and photographed for documentation. In suspected cases of positive resection margin, specimens were sent to the pathology department for frozen sections to rule out the involvement of the resection margin. The location of dissected LNs was identified by the attending surgeon, and collected LNs were aliquoted in formalin for subsequent pathologic examination. According to a prospective protocol, all LNs were cut at several levels, including the long axis, and embedded in paraffin; sections were taken for hematoxylin and eosin staining. An experienced pathologist checked all of these slides and delivered the final comment about the metastatic status of the LNs. To determine the size of the largest and/or metastatic node, all histopathologic slides were scrutinized under a light microscope, and the long diameter was measured by placing a measure directly on the histopathologic slide.

The UICC (1997) staging system was used for tumor classification. All patients with node-positive disease received adjuvant therapy. The follow-up was complete in all patients, with a median follow-up period of 40 months. Data obtained at regular follow-up visits at the outpatient department were stored in a database specially designed for the esophageal cancer patients. An update inquiry about the status of all surviving patients was made by telephone call in October 1999.

Correlation between LN size and survival was analyzed by the Spearman rank correlation test. The survival rates were calculated by the Kaplan-Meier method, and the statistical significance between groups was determined by the log-rank test. Independent variables predicting survival were evaluated by a stepwise multivariate survival analysis (Cox’s proportional hazards model). The BMDPTM (2L program) statistical package (BMDP, Los Angeles, CA) and Statview 4.5JTM (Abacus Concepts, Berkeley, CA) were used for data analysis.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
At the last follow-up (complete in all patients), 107 patients had died. Of these, 42 patients died as a result of recurrence of their disease; out of them, 16 (38%) patients had failure in the locoregional area, and in 26 (62%) patients, distant metastasis occurred. The average number of dissected LNs was 40 (range, 6 to 107), and the average number of MLNs was 4.2 (range, 1 to 24). Of 187 curatively resected cases, 94 (50.8%) had MLNs. The long diameter was considered as the MLN size, and the size of MLNs varied from 3 to 30 mm, with an average of 12.6 mm. After serial analysis at different cutoff points, 10 mm was found to be the most appropriate cutoff point for MLN size, with the strongest predictability of prognosis. According to this cutoff point, patients with MLNs were divided into two groups. In 32 (34%) patients, the largest MLN was <=9 mm, and they were classified as pn1. Sixty-two (66%) patients had MLNs >=10 mm and were classified as pn2. Distribution of these nodal groups according to the T stage is shown in Fig. 1. Patients with pn1 disease were evenly distributed among the four T stages, and a stepwise increase in the frequency of pn2 disease was noticed with the advancement of the T stages.



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  		FIG. 1. Percent distributions of the new nodal status classification according to the tumor (T) stage are shown. Advancement of the nodal stage was noticed with increasing depth of penetration.

 
A significant positive correlation was detected between the size and number of MLNs (P = .0002; {rho} = 40.0; Spearman rank correlation test) (Fig. 2a). Both 5-year overall survival (OS) and cancer-specific survival (CSS) rates decreased with each increment in the MLN size (Fig. 2b).



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  		FIG. 2. A significant positive correlation was noticed between metastatic lymph node (MLN) size and number (a) (P = .0002; {rho} = 40.0). Stepwise decreases in the 5-year overall and cancer-specific survival rates were noticed with each increment in the MLN size (b).

 
The 5-year OS and CSS are shown in Fig. 3. According to our nodal classification, there were significant differences in OS and CSS between patients with pn0 and pn1 disease (P = . 0083, CSS; P = . 0187, OS) and between pn1 and pn2 disease (P = .0021, CSS; P = .0048, OS). This size cutoff point of 10 mm had the strongest predictability of survival after a serial bisection at different cutoff points. Similarly, the number of MLNs had a significant effect on OS and CSS, with a worse survival in patients with four or more MLNs than in those with three or fewer MLNs (P = .0096, CSS; P = .0114, OS). Out of 55 patients with <=3 MLNs, 25 patients had pn1 disease (MLN size <=9 mm), and 30 patients had pn2 disease (MLN size >=10 mm). Among these patients, the 5-year CSS was significantly worse in those with pn2 disease than with pn1 disease (30.1% vs. 81.7%, respectively; P = .0041, log-rank test), and the 5-year OS difference approached significance (50.1% vs. approximately 24.2%; P = .081) (Fig. 3c). However, when the patients with pn2 disease were assessed by the number of MLNs, there was no difference in survival between the two groups (P = .4052, log-rank test) (data not shown).



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  		FIG. 3. Cancer-specific and overall survivals according to metastatic lymph node (MLN) size (a and a') and number (b and b') are shown. Patients with three or fewer MLNs are further stratified by the MLN size (c and c').

 
A stepwise multivariate analysis was performed to determine the independence and relative strength of other prognostic factors, adjusting for the number and size of MLNs and T stage in the node-positive patients. The criterion to enter a variable into the Cox model was set as P < .1. The following variables were entered into the survival analysis: age, sex, tumor size, histopathologic type, lymphatic invasion, venous invasion, amount of intraoperative blood loss, LN ratio, number of MLNs, and size of MLNs. Among the several prognostic indicators, MLN size was the strongest independent predictor of survival and remained significant in stepwise multivariate survival analysis with Cox’s proportional hazards model (P = .0021; hazard ratio [HR], 4.5322) (Table 1). The number of MLNs and the amount of intraoperative blood loss remained independent prognostic factors along with the MLN size only when multiple cutoff points for MLN size (10 and 12 mm) and amount of intraoperative blood loss were included in a forward stepwise analysis model. However, the HR for MLN size was almost three times higher than that for the number of MLNs (HR 8.39 for MLN size, 3.43 for MLN number, and 1.57 for blood loss) (data not shown). Similarly, when the OS was encountered as the end point of the disease outcome, MLN size (P < .0001; HR, 1.647) remained the strongest independent predictor of prognosis, followed by the T stage (P = .0011; HR, 1.413). No other factors had an independent influence on the OS.


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  		TABLE 1. Multivariate analysis of prognostic factors
 
With the MLN size as the criterion for nodal classification, patients were grouped into a modified tumor-node-metastasis classification system, as shown in Table 2. To simplify this classification, only patients with distant visceral metastasis were considered to have pM1 disease. We considered all LNs, including the cervical and celiac nodes (nonregional nodes according to the present UICC tumor-node-metastasis classification), as regional. Therefore, of 31 patients with nonregional LN metastasis (M1a and M1b) according to the UICC tumor-node-metastasis system, 7 patients are in the pn1 category, and 24 patients are in the pn2 group. Also, we placed T2N0 patients in stage I instead of stage II, as has been previously recommended by several authors.5,11 A comparison of the stage and distribution of patients according to the UICC tumor-node-metastasis classification and our classification is shown in Table 3. Patients were evenly distributed in stages I through IV, with 79 patients in stage I, 32 patients in stage II, and 38 patients each in stages III and IV. There were significant differences in CSS between stage I and II (P = .0021; log-rank test), stage II and III (P = .0347; log-rank test), and stage III and IV (P = .0376; log-rank test) (Fig. 4a). A similar effect of this new staging was noticed on OS, with significant differences between stages I and II (P = .0105) and III and IV (P = .0238); however, there was no significance between stages II and III (P = .4636). CSS curves according to the present UICC tumor-node-metastasis classification are shown in Fig. 4b. There were no significant differences between stages IIa and IIb or between stages III and IV.


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  		TABLE 2. Definitions of the current and revised stages
 

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  		TABLE 3. Distribution of patients according to the UICC TNM and the new TNM classification is shown
 


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  		FIG. 4. Cancer-specific and overall survivals according to the new staging incorporating the metastatic lymph node size as the nodal stage (a and a') and the International Union Against Cancer tumor-node-metastasis (b and b') stages are shown.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Esophageal cancer staging is always changing and has undergone several revisions with the emergence of new prognostic factors. The results of this study suggest that careful estimation of the MLN size on histopathologic slides may supplement current staging and help us to stratify esophageal cancer patients into prognostically different groups, and they thus may help clinicians to tailor treatment.

Regional LNs serve as the primary barrier to the systemic spread of cancer cells. Recent advancements in understanding of the immunological and biological aspects of cancer cell behavior indicate that cancer cells fight the immune competent cells largely by the Fas/FasL system and overcome the host immune surveillance.12 Recently, several authors concluded that in a proper classification of cancer, in addition to the anatomical extent of the disease as adopted in the tumor-node-metastasis classification, biological and molecular factors also should be emphasized.13,14 There are several such factors, and it is very difficult to choose a particular one for use in cancer staging. However, this might be accomplished by considering the net cancer growth inside the regional LNs, which might serve as an indicator of the balance between tumor aggressiveness and the host immune status. This is suggested by our finding that the incidence of pn2 disease (MLN size of >=10 mm) increased proportionately with advancement of the depth of penetration of the esophageal wall (Fig. 1).

Separation of node-positive esophageal cancer patients into prognostically distinct groups would be useful. Including our report, several carefully performed studies from Japan and several Western series have looked at substaging patients according to the number of MLNs, as is performed in gastric and colon cancer patients.11,15,16 The notion of pN classification by the number of MLNs was originally proposed by Skinner et al.6 and was subsequently supported by many authors.17 Roder et al.18 and others proposed using the LN ratio of the number of MLNs to the number of collected LNs. Similarly, in our study of curatively resected esophageal cancer patients, both the number of MLNs and the LN ratio were significant indicators of prognosis; however, when entered into the multivariate analysis along with the MLN size, both were eliminated from the stepwise multivariate analysis because of their comparatively low predictability of prognosis compared with the MLN size. It is worth mentioning that patients with three or fewer MLNs could be further divided into prognostically significant groups according to MLN size, with a 5-year CSS of 81.7% for patients with pn1 disease and 30.1% in those with pn2 disease. Indeed, with each millimeter increment in the MLN size, the CSS was decreased proportionately. This observation is supported by Ide et al.,19 who reported that patients with positive LNs larger than 10 mm had a significantly poorer prognosis, although they did not mention whether the measurement was performed on a pathologic specimen or on histological slides.

Accurate preclinical staging in gastrointestinal tumors is needed to tailor the treatment in individual patients, in whom the greatest benefit would result with minimum risk. At present, most of this treatment policy is based on the T and M categories of the tumor-node-metastasis classification as assessed by computed tomography scanning and endoscopic ultrasonogram (EUS). Recent advancements in imaging techniques, e.g., positron emission tomographic scan and EUS, could detect the presence of MLNs with high accuracy.20 This detection rate could be further increased; Reed et al.21 reported excellent staging results with EUS-guided needle biopsies of suspected celiac LNs, with a sensitivity of 72% and specificity of 97%. From this point of view, use of MLN size may enable us to accurately perform preclinical staging and thus would help in designing treatment before the operation.

In our study, there were no significant differences in patient survival between current stages IIa and IIb or between III and IV. Similar results are reported by other authors.22 An accurate pathologic tumor-node-metastasis staging should stratify patients into homogenous prognostic groups. By using the MLN size, patients were stratified into four groups, with statistical significance in survival between each of the four stages. Also, the numbers of patients in stages II and III were less than in stages I and IV (70 and 117, respectively). Previously, several authors concluded that the T2N0 patients were better classified under stage I; we concur with them that these patients have an excellent prognosis, and we grouped them under stage I.5,11 There is a long-standing controversy over whether patients with nonregional LN metastasis should be considered as stage IV.23 According to our nodal classification, most (24 of 31; 77%) of the patients with M1a or M1b disease were grouped under the pn2 stage and were placed in stages III (11 of 24; 46%) and IV (13 of 24; 54%). This again represents the unique ability of the MLN size to predict prognosis without separating nodes into regional or nonregional compartments.

In conclusion, the MLN size is determined by a simple procedure and stratifies patients with squamous cell carcinoma of the esophagus into prognostic groups. It remains to be clarified whether a similar classification will work in patients with esophageal adenocarcinoma. In a preliminary unpublished work, we found that this classification seems to be effective in patients with other gastrointestinal adenocarcinomas, including stomach and colon cancers. This classification may help clinicians to tailor treatment before operation; however, it needs to be confirmed in other studies before any definite conclusion is made.


   Acknowledgments
 
The authors thank Prof. Yoshiaki Nose of the Department of Medical Information Science, Faculty of Medicine of Kyushu University, for his kind help in statistical evaluation and Miki Asazu for excellent technical assistance.


   Footnotes
 
Dr. Dhar was also a visiting scholar at the University of Nevada, Las Vegas, Nevada.

The metastatic lymph node size, as determined on a hematoxylin and eosin–stained histopathologic slide, was found to be a significant prognostic indicator in squamous cell carcinoma of the esophagus. This approach supplements traditional nodal staging strategies and therefore has potential for guiding the development of treatment strategies in this carcinoma.

Received for publication April 2, 2002. Accepted for publication August 12, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  6. Skinner DB, Ferguson MK, Soriano A, Little AG, Staszak VM. Selection of operation for esophageal cancer based on staging. Ann Surg 1986; 204: 391–401.[Medline]
  7. Hermanek P, Sobin LH, eds. TNM Classification of Malignant Tumours. 4th ed. New York: Springer, 1987: 40–2.
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  12. Shibakita M, Tachibana M, Dhar DK, et al. Prognostic significance of Fas and Fas ligand expressions in human esophageal cancer. Clin Cancer Res 1999; 5: 2464–9.[Abstract/Free Full Text]
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  14. Wang LS, Chow KC, Chi KH, et al. Prognosis of esopha-geal squamous cell carcinoma: analysis of clinicopatholo-gical and biological factors. Am J Gastroenterol 1999; 94: 1933–40.[CrossRef][Medline]
  15. Tachibana M, Kinugasa S, Dhar DK, et al. Prognostic factors after extended esophagectomy for squamous cell carcinoma of the thoracic esophagus. J Surg Oncol 1999; 72: 88–93.[Medline]
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