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Annals of Surgical Oncology 10:213-218 (2003)
© 2003 Society of Surgical Oncology

ORIGINAL ARTICLES

Accuracy of Determining Nodal Negativity in Colorectal Cancer on the Basis of the Number of Nodes Retrieved on Resection

Natalie E. Joseph, MD, Elin R. Sigurdson, MD, PhD, Alexandra L. Hanlon, PhD, Hao Wang, MS, Robert J. Mayer, MD, John S. MacDonald, MD, Paul J. Catalano, ScD and Daniel G. Haller, MD

From the Department of Surgical Oncology (NEJ, ERS) and Division of Population Science and the Department of Biostatistics (ALH, HW), Fox Chase Cancer Center, Philadelphia, Pennsylvania; Cancer and Leukemia Group B (RJM), Boston, Massachusetts; Southwest Oncology Group (JSM), Philadelphia, Pennsylvania; Dana-Farber Cancer Institute (PJC), Boston, Massachusetts; and Eastern Cooperative Oncology Group (DGH), Philadelphia, Pennsylvania.

Correspondence: Address correspondence and reprint requests to: Elin R. Sigurdson, MD, PhD, Department of Surgical Oncology, Fox Chase Cancer Center, 7701 Burholme Avenue, Philadelphia, PA 19111; Fax: 215-728-2773; E-mail: e_sigurdson{at}fccc.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Correct determination of nodal status is pivotal to accurate staging and predicting survival.

Methods: This is a secondary analysis of INT0089, an intergroup trial of adjuvant chemotherapy for high-risk stage II and III colon cancer. A subset of patients was studied who underwent right or left hemicolectomy and from whom at least 10 lymph nodes were examined. A mathematical model was created to estimate the probability of a true negative result on the basis of the number of nodes examined. The number of nodes needed to predict nodal negativity with 85%, 50%, and 25% probability on the basis of tumor stage was calculated.

Results: In this analysis, 1585 patients were studied. The average number of nodes removed at surgery was comparable between treatment groups at 18.5 (median of 16 in all groups). With this model, when 18 nodes are removed at resection, there is a <25% probability of true node negativity in T1/T2 tumors, whereas <10 nodes need to be examined in T3 and T4 tumors to achieve the same probability.

Conclusions: Tumor stage and the number of nodes retrieved at resection influence the accuracy of determining nodal status in colon cancer. Most patients are understaged. Underestimating nodal stage may influence decisions regarding adjuvant therapy, as well as overall prognosis.

Key Words: Lymph node status • Colon cancer • Survival • 5-fluorouracil chemotherapy • Prognostic factors


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Colorectal cancer is the third most common cancer and the second leading cause of death from cancer in the United States. The single most important determinant of prognosis for those patients with otherwise localized disease is the presence or absence of nodal metastases. This is demonstrated by the fact that 5-year survival decreases from approximately 80% in patients with stage II colon cancer to 50% with the presence of nodal involvement.1 In addition to having great prognostic significance, correctly defining the nodal status has a direct effect on therapy. Although surgery remains the mainstay of treatment, adjuvant chemotherapy has a proven survival benefit in patients with stage III (node-positive) colon cancer, and more aggressive regimens are being instituted for those patients deemed to be at high risk for recurrence.2 Results of studies over the last decade have confirmed the benefits of using various 5-fluorouracil–based chemotherapy regimens to decrease recurrence and improve patient survival.3,4

For these reasons, staging accuracy bears great importance. Many studies have been performed to determine the optimal number of lymph nodes that need to be examined to accurately stage colon cancer. These results are variable, suggesting that anywhere from 6 to 17 nodes need to be examined.5–7 The two main factors contributing to the high degree of variability are the extent of surgical resection performed and the extent of pathologic examination conducted. In addition, the number of lymph nodes may vary from person to person. Principles of surgical resection for colorectal cancer dictate en-bloc removal of the cancer with adequate proximal and distal margins and inclusion of the regional mesenteric lymphatics following anatomical landmarks. Despite these guidelines, differences in technique may account for differences in lymph node recovery.8 The number of nodes identified may also vary greatly depending on the extent and method of pathologic examination. Scott and Grace9 demonstrated that the total number of lymph nodes recovered from a colon specimen increased by 50% when a method of fat clearance was used in addition to standard dissection techniques. Other studies have clearly demonstrated that more lymph node metastases were identified when more lymph nodes were examined.6

Given the implications of understaging patients with colorectal cancer, this study aimed to identify the minimum number of nodes that need to be examined in a colon cancer specimen to accurately determine negative nodal status. This will enable us to identify all patients who will benefit from adjuvant chemotherapy and to improve survival in this group.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
This is a secondary analysis of INT0089, a large prospective multicenter trial conducted by the Eastern Cooperative Oncology Group in conjunction with the Southwest Oncology Group and the Cancer and Leukemia Group B. This trial was designed to evaluate the effects of modulation of 5-fluorouracil with both levamisole and leucovorin in high-risk stage II and III colon cancer in the adjuvant setting. This is the largest prospective database for stage II and III colon cancer. Survival was found to be similar in all four arms of the study; therefore, these patients could be analyzed as a single group.

Patients were eligible for the study if they had histological proof of adenocarcinoma of the colon, complete surgical resection of the tumor with no evidence of residual gross microscopic disease, and evidence of poor prognosis (i.e., nodal involvement, serosal penetration, perforation, or obstruction). Patients were ineligible for the study if they had distant disease, prior therapy with 5-fluorouracil, prior chemotherapy or radiotherapy for the same disease, another malignancy within the 3 years before the study, or any other major illnesses that precluded them from receiving chemotherapy. All patients underwent standard surgical resection of their disease. They were then entered onto the study and randomized to one of four treatment arms between postoperative days 21 and 35 (Table 1). After completion of chemotherapy, patients were followed up every 3 months for 1 year and then every 6 months. After 5 years, follow-up was on an annual basis.


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  		TABLE 1. Treatment regimen
 
A mathematical model was used to estimate the true underlying number of involved mesenteric lymph nodes in patients undergoing right or left hemicolectomy.10 This model relies on two quantities:

  1. The probability of having M involved nodes, q(M), where q(M) = (number of patients with M involved nodes)/(total number of patients in group).
  2. The probability of m nodes observed positive in a sample size of n resected, P(n,m,N,M). N represents the total number of lymph nodes with M nodes positive. P(n,m,N,M) is obtained from the hypergeometric distribution, where equation


    		(1)

The estimation of the first quantity, q(M), is accomplished for patients with T1/T2, T3, and T4 tumors separately. Patients with at least 10 lymph nodes examined were used to estimate the probability of having M involved lymph nodes.

The average total number of lymph nodes was assumed to be 44 in the right colon and 46 in the left colon. These numbers were obtained from the average number of lymph nodes seen in a study by Herrera-Ornelas.11

The mathematical model was used to estimate the probability that the number of nodes observed positive is actually representative of the true underlying number of nodes positive. These probabilities are based on observed sampling combinations and thus rely on the Bayes theorem. More specifically, r(M,n,m) is the probability of a patient’s having M involved nodes after m nodes are observed positive in a sample of n resected: equation


(2)

For example, to estimate the probability associated with M = 3 when three nodes are observed positive in six dissected, one would calculate equation


(3)


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Data from 3557 patients were available for review. Of those patients, 146 were excluded because of incomplete data regarding the number of lymph nodes. Of the remaining patients, we selected a subset who had undergone either right or left hemicolectomy and from whom at least l0 lymph nodes had been examined. These 1585 patients comprise the basis of our analysis. These specific groups were chosen as an attempt to decrease surgical variability because these resections are anatomically well defined. Demographics for the study population are listed in Table 2. Patients were comparable with respect to sex. Eighty-five percent of the study population was white. The most common pathology was adenocarcinoma (88%). Sixty-seven percent were moderately differentiated, 24% poorly differentiated, and 9% well differentiated. Sixty percent underwent right hemicolectomy and 40% left hemicolectomy. Eighty-one percent of the total study population was node positive. More than 50% of the patients undergoing either right or left hemicolectomy were tumor stage T3 and node positive (Figs. 1 and 2). Figures 3 and 4 show the distributions of the number of nodes examined for node-negative and node-positive patients, respectively. There was no difference in the number of nodes examined between these two groups (mean for both was 18.5). The number of nodes needed to predict nodal negativity with 85%, 50%, and 25% probability on the basis of their tumor stage is listed in Tables 3 and 4. Patients with T1 and T2 tumors need to have 36 nodes examined to have a 50% probability that they are node negative, whereas <10 nodes would have to be examined in a patient with a T4 tumor to have the same probability of being node negative.


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  		TABLE 2. Demographics of study population
 


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  		FIG. 1. Right colectomy node status according to stage.

 


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  		FIG. 3. Number of nodes examined in node-negative patients.

 

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  		TABLE 3. Number of nodes to accurately predict nodal negativity
 


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  		FIG. 2. Left colectomy node status according to stage.

 


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  		FIG. 4. Number of nodes examined in node-positive patients.

 

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  		TABLE 4. Number of nodes to accurately predict nodal negativity
 
Overall survival for the six groups is listed in Table 5. Five-year survival was better in T1/T2 compared with T3/T4. There was a significant difference in 10-year survival in early-stage left-colon cancers, but this is probably due to the small numbers in this group and not a real finding. Kaplan-Meier curves of overall and disease-free survival by the number of nodes examined are presented in Figs. 5 and 6, respectively. In node-negative patients, when >30 nodes were examined, the 5- and 8-year overall survival rates were 100% and 92%, respectively, compared with when <30 nodes were examined, when 5- and 8-year survival rates decreased to 80% and 72% (P = .03). Similarly, disease-free survival was 91% and 87% at 5 and 8 years, respectively, when >30 nodes were examined. These rates decreased to 78% and 74% when <30 nodes were examined (P = .09).


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  		TABLE 5. Overall survival by tumor stage
 


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  		FIG. 5. Overall survival in node-negative patients.

 


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  		FIG. 6. Disease-free survival in node-negative patients.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Determining lymph node status is pivotal to the staging of colorectal cancer. Having an early-stage cancer should imply a good prognosis, but despite this, the outcome for stage II colon cancer remains variable. Studies have demonstrated that up to 20% of these patients die from local recurrence or distant disease within 5 years of their diagnosis,12 the implication being that a large percentage of these patients are understaged and might have benefited from adjuvant therapy. In studies of lymph nodes from patients with stage II colon cancer, Liefers et al.13 demonstrated micrometastatic disease in 54% patients that had previously been described as being node negative with carcinoembryonic antigen–specific reverse transcriptase-polymerase chain reaction. There was also a statistically significant difference in 5-year survival between those patients with micrometastases and those without.

The reasons for understaging may be multifactorial, in part because of variation in surgical technique, aggressiveness of pathologic analysis, or both. In a review of outcomes in cancer surgery, it has become increasingly apparent that sound surgical technique and experience clearly influence outcome in breast, pancreatic, gastric, and colorectal cancer.14–16 In this study, we attempted to decrease the surgical variability by limiting our study population to patients who had operations that are anatomically the most well defined.

Many studies have commented on the limitations of conventional methods of pathologic analysis of lymph nodes. Techniques such as fat clearance have been shown to detect greater rates of metastases, particularly in small regional nodes (<4–5 mm).17 These constitute the majority of metastatic nodes detected after colon resection and have the same prognostic implications as do larger nodes.18

This study is the largest review of the role of the number of lymph nodes examined on staging accuracy in colon cancer. Earlier analysis of this cohort of patients demonstrated that examining more nodes was associated with increased survival in both node-negative and node-positive patients.19 This suggested that when more nodes were analyzed, patients were more likely to be accurately staged. Furthermore, in the node-positive group, this may be further interpreted as those patients with a more thorough lymph node dissection having less residual disease and, thus, a better outcome. These findings were supported by Tepper et al.20 in a study of 1664 high-risk rectal cancer patients. They demonstrated a decrease in the 5-year relapse rate and a corresponding increase in 5-year survival in patients from whom >14 nodes were analyzed. Given these findings, we attempted to investigate the minimum number of nodes that need to be examined to enable us to say with high probability that a patient is node negative and, second, to see how this affects outcome. Our results are similar in that the more nodes examined, the better the survival. With our mathematical model, the number of nodes needed to accurately predict nodal negativity was significantly higher than in other series, particularly in early-stage cancers. This could be explained by the facts that this is a larger patient population than many of the other studies and that there are a higher percentage of node-positive patients because we selected from a high-risk population. The probability of nodal negativity correlated with tumor stage in that node-negative status could be predicted more accurately with fewer nodes examined in the more advanced cancers. In our own series, an average of 18 nodes was recovered from each specimen. Our data suggest that >40 nodes would need to be examined in a patient with an early-stage (T1/T2) cancer for the probability to be 85% that the patient is node negative. With 18 nodes, the probability is only 25% of being truly node negative. For T3 and T4 tumors, 40 and 30 nodes, respectively, need to be examined to achieve an 85% probability of being node negative. When 18 lymph nodes are examined, the probability of being truly node negative is >25% for T3 tumors and >50% for T4 tumors. On the basis of this analysis, a strong effort must be made to improve surgical technique and our methods of pathologic analysis.

Lymph node retrieval from colon cancer specimens is variable and highly dependent on technique. Many studies have shown that with conventional methods, only a percentage of lymph nodes are retrieved from pathologic specimens. Alternative methods such as fat clearance, although effective, are time consuming, expensive, and largely impractical. Molecular techniques of detecting micrometastatic disease may also enable us to detect disease in patients otherwise thought to be node negative, but these may also not be possible in all clinical settings.

Sentinel lymph node mapping has well-documented application in the management of melanoma and breast cancer. There has been increasing interest in extending this technique to colorectal cancer. A number of studies have effectively demonstrated that this is a feasible, safe technique in colorectal cancer.21,22 Additionally, as many as 18% to 25% of patients have been upstaged from stage II to stage III after metastatic disease was detected in the sentinel node.23,24 The advantage is that a more focused pathologic examination can be performed on the few nodes that are identified as sentinel lymph nodes by using techniques such as immunohistochemistry and polymerase chain reaction. As in melanoma and breast cancer, the accuracy of the technique can be expected to improve with experience.

The results of this study have important implications in the management of patients with early-stage disease. Every effort should be made surgically to perform the most thorough nodal dissection to optimize surgical outcome. More importantly, a thorough pathologic assessment of the nodal status has a substantial effect on determining further therapy and prognosis in this patient population. Using standard techniques, we may be grossly understaging a subset of node-negative patients, thus accounting for the relapse rate seen in this population. Every effort must be made to standardize our surgical and pathologic approach in these patients to further improve outcome.


   Footnotes
 
A secondary analysis of INT0089, a trial of adjuvant therapy in high-risk colon cancer, was performed. A mathematical model was created to estimate the probability of correctly determining nodal status on the basis of the number of lymph nodes examined after surgical resection.

Received for publication March 15, 2002. Accepted for publication October 8, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  7. Wong JH, Severino R, Honnebier MB, Tom P, Namiki TS. Number of nodes examined and staging accuracy in colorectal carcinoma. J Clin Oncol 1999; 17: 2896–900.[Abstract/Free Full Text]
  8. Reinbach DH, McGregor JR, Murray GD, O’Dwyer PJ. Effect of the surgeon’s specialty interest on the type of resection performed for colorectal cancer. Dis Colon Rectum 1994; 37: 1020–3.[CrossRef][Medline]
  9. Scott KWM, Grace RH. Detection of lymph node metastases in colorectal carcinoma before and after fat clearance. Br J Surg 1989; 76: 1165–7.[Medline]
  10. Kiricuta CI, Tausch J. A mathematical model of axillary lymph node involvement based on 1446 complete axillary dissections in patients with breast carcinoma. Cancer 1992; 69: 2496–501.[CrossRef][Medline]
  11. Herrera-Ornelas L. Metastases in small lymph nodes from colon cancer. Arch Surg 1987; 122: 1253–6.[Abstract]
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  13. Liefers G, Cleton-Jansen A, van de Velde CJ, et al. Micrometastases and survival in stage II colorectal cancer. N Engl J Med 1998; 339: 223–8.[Abstract/Free Full Text]
  14. Giacomantonia CA, Temple WJ. Quality of cancer surgery: challenges and controversies. Surg Oncol Clin North Am 2000; 9: 51–60.[Medline]
  15. Saettler EB, Temple WJ. The surgeon as a prognostic factor in the management of pancreatic cancer. Surg Oncol Clin North Am 2000; 9: 133–42.[Medline]
  16. Hartgrink HH, Bonenkamp HJ, van de Velde CJH. Influences of surgery on outcomes in gastric cancer. Surg Oncol Clin North Am 2000; 9: 97–117.[Medline]
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  19. Le Voyer TE, Sigurdson ER, Hanlon AL, et al. Colon cancer survival is associated with increasing number of lymph nodes analyzed. A secondary survey of INT-0089 (abstract). Proc Am Soc Clin Oncol 2000; 925.
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