Annals of Surgical Oncology Sign the Guestbook
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Swanson, R. S.
Right arrow Articles by Bland, K. I.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Swanson, R. S.
Right arrow Articles by Bland, K. I.
Related Collections
Right arrow Pathology
Annals of Surgical Oncology 10:65-71 (2003)
© 2003 Society of Surgical Oncology

ORIGINAL ARTICLES

The Prognosis of T3N0 Colon Cancer Is Dependent on the Number of Lymph Nodes Examined

Richard S. Swanson, MD, Carolyn C. Compton, MD, PhD, Andrew K. Stewart, MA and Kirby I. Bland, MD

From the National Cancer Data Base (RSS, CCC, AKS, KIB), American College of Surgeons, Chicago, Illinois; Department of Surgery, Brigham and Women’s Hospital, Boston, Massachusetts (RSS); Department of Pathology, McGill University, Montreal, Canada (CCC); American College of Surgeons, Chicago, Illinois (AKS); and Department of Surgery, University of Alabama, Birmingham, Alabama (KIB).

Correspondence: Address correspondence and reprint requests to: Richard S. Swanson, MD, Division of Surgical Oncology, Brigham and Women’s Hospital, 75 Francis St., Boston, MA 02115; Fax: 617-739-1728; E-mail: rswanson{at}partners.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: T3N0 colon cancer is the target of many adjuvant studies. Very few studies have examined the relationship of the number of lymph nodes examined to the prognosis of this stage. We examined data from the National Cancer Data Base (NCDB) to determine whether the number of examined lymph nodes is prognostic for T3N0 colon cancer.

Methods: A total of 35,787 prospectively collected cases of T3N0 colon cancer that were surgically treated and pathologically reported from 1985 to 1991 to the NCDB as T3N0M0 were analyzed.

Results: The 5-year relative survival rate for T3N0M0 colon cancer varied from 64% if 1 or 2 lymph nodes were examined to 86% if >25 lymph nodes were examined. Three strata of lymph nodes (1–7, 8–12, and >=13) distinguished significantly different observed 5-year survival rates.

Conclusions: These results demonstrate that the prognosis of T3N0 colon cancer is dependent on the number of lymph nodes examined. A minimum of 13 lymph nodes should be examined to label a T3 colon cancer as node negative. These data suggest that adjuvant trials for T3N0 colon cancer should stratify according to the number of lymph nodes examined.

Key Words: Colon cancer • T3N0 • Lymph nodes • Prognosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
For patients with suspected localized colon cancer, the most important determinant of survival is the presence or absence of metastases to regional lymph nodes. The number of lymph nodes that need to be examined and found to be free of metastases to confidently determine that a colon cancer is node negative has not been established. A recent report by Tepper et al.1 suggests that approximately 14 nodes need to be examined to define the nodal status of rectal cancer. The investigators retrospectively analyzed a prospective database for 1664 patients with rectal cancer who entered a randomized trial for multimodality treatment for rectal cancer. The report did not address patients with colon cancer.

Currently, patients with T3N1 disease are offered adjuvant chemotherapy after colectomy, whereas patients with T3N0 disease are not routinely offered adjuvant therapy. This management plan follows the recommendations of an National Institutes of Heath Consensus Conference.2 Thus, it is important to know the number of lymph nodes that need to be examined to label a colon cancer as node negative. This number has not been determined for colon cancer by examining a large data set with survival related to the number of lymph nodes examined.

Patients with T3N0 colon cancer are the target for adjuvant randomized studies in an effort to improve survival for this stage of colon cancer. If the prognosis of this stage varies as a function of the number of lymph nodes examined, then adjuvant studies for T3N0 colon cancer should be stratified according to the number of lymph nodes examined.

The number of lymph nodes examined depends on the number of regional lymph nodes present, the extent of surgery, and the technique of the pathologist who examines the tissue. As laparoscopic colon cancer surgery and sentinel node biopsies for colon cancer are being studied, it becomes increasingly important to know the "gold standard" as to the minimum number of lymph nodes that should be examined to accurately determine node negativity in T3N0 colon cancer. This study reviewed the large prospective database of the National Cancer Data Base (NCDB) to determine whether the prognosis of T3N0 colon cancer is related to the number of lymph nodes examined.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Patients with a diagnosis of primary colon cancer (International Classification of Diseases of Oncology, 2nd edition, site codes 18.0–18.9, excluding the appendix3) reported to the NCDB between 1985 and 1991 form the basis of this review. The scope and depth of the NCDB’s data collection activities have been previously described.4 Data collected by the NCDB allow analysis by each of the tumor, node, and metastasis elements of the American Joint Committee on Cancer staging schema, the total number of regional lymph nodes surgically removed and examined, and the corresponding number of dissected nodes pathologically determined to be positive for the presence of tumor. Case selection was further limited to patients who were pathologically determined to be T2N0, T3N0, T3N1, T3N2, and T3N3. All cases were staged according to either the 3rd or 4th edition of the American Joint Committee on Cancer staging manual (in particular, with these staging editions N1 = one to three positive lymph nodes; N2 = four or more positive lymph nodes; and N3 = central lymph nodes positive).5,6 In addition, only patients who received surgery as the first course of treatment were selected for review; patients who had radiotherapy were omitted. The NCDB does not routinely collect data on other prognostic factors, such as carcinoembryonic antigen level.

A standard statistical software package, SPSSTM (SPSS Inc., Chicago, IL), was used in analysis. The primary mode of analysis used for survival calculations was the 5-year relative survival rate, which is the observed survival rate divided by the survival expected of a cohort similar in age, ethnicity, and sex. This technique was complemented by use of the Kaplan-Meier technique. Linear regression techniques were used to evaluate observable patterns and to propose rationales for further stratification. Analysis of stratified variables used analysis of variance and the Bonferroni test for differences among means, where appropriate. Univariate survival calculations were performed with the Kaplan-Meier technique. Cox regression was used to estimate multivariate survival outcomes.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
Between 1985 and 1991, 35,787 cases of T3N0 and, for comparison purposes, 21,362 cases of T3N1–3 colon cancer were reported to the NCDB that were treated with surgery or surgery plus adjuvant chemotherapy as the initial course of treatment. The American Cancer Society estimated that there were 618,000 new colon cancer cases during this time period. The NCDB collected 260,939 colon cancer cases from 1985 to 1991; thus, the NCDB collected 42% of the American Cancer Society’s estimate. The average age of patients with T3N0 disease was 72 years; the average age for T3N1–3 patients was 70 years. The median follow-up times were 46.3 months for T3N0 cases and 29.1 months for T3N1–3 cases. The difference in the median follow-up times is a reflection of the survival experience of these two groups; only 11.6% of all cases were reported as lost to follow-up. The 5-year relative survival rates were 77% for T3N0 and 57% for T3N1 (Table 1). For comparison, the 5-year relative survival rate for 16,032 patients with T2N0 colon cancer reported to the NCDB between 1985 and 1991 was 87.1%.


View this table:
[in this window]
[in a new window]
  		TABLE 1. Five-year relative survival rates of T3 colon cancers
 
Men comprised 45.7% of the T3N0 patients. The mean numbers of lymph nodes removed from the right, transverse, and sigmoid colons were 13.3, 11.6, and 10.1, respectively. The median number of nodes removed for the entire T3N0 cohort was 9; the range was from 0 to >30. Tumor grades varied as follows: well differentiated, 11.8%; moderately differentiated, 66.5%; and poorly differentiated, 13.7%.

Only 7.0% of patients with T3N0 disease had chemotherapy after surgery. The survival rates for T3 patients treated with and without postoperative chemotherapy are listed in Table 2.


View this table:
[in this window]
[in a new window]
  		TABLE 2. Five-year relative survival rates of T3 colon cancer by first-course therapy
 
Examining the patients with T3N0 colon cancer demonstrates that the 5-year survival rate is clearly dependent on the number of lymph nodes examined. This is depicted in Table 3. If a patient has only one or two nodes examined, the 5-year relative survival rate (64%) is close to the survival rate for T3N1 (57%) disease but is statistically different. At the same time, the 5-year relative survival rate for T3N0 patients is 87% if >20 nodes are examined; this survival rate is the same as that for 16,032 patients with T2N0 disease (87.1%).


View this table:
[in this window]
[in a new window]
  		TABLE 3. Five-year survival rates of T3N0 colon cancers by the number of pathologically examined regional lymph nodes
 
To address the concern of the adequate staging of T3N0 patients, it was necessary to examine T3N-positive cases by stratifying patients by the number of nodes examined and the extent of regional nodal metastasis. Examining the proportion of cases that had at least one lymph node determined to be positive as a function of the number of nodes examined determined the minimum number of nodes needed to be examined to consider categorizing a tumor as node negative. An analysis of the average number of positive nodes found as a function of the number of nodes examined determined the adequate number of nodes removed before further nodal evaluation provided limited additional prognostic benefit.

Figure 1 shows the proportion of cases, stratified by the number of nodes examined, that had at least one positive node reported. Standard regression analysis and the Chow test (P < .0001) determined that the rate of decline in the proportion of cases with at least one positive node for every additional node examined was different when seven or fewer nodes were examined (-3.18) than when more than eight nodes were examined (-.74). This would suggest that once eight nodes are examined, additional nodal dissection is associated with declining marginal returns and that this number may represent the minimum number of nodes required to determine node negativity.



View larger version (15K):
[in this window]
[in a new window]
  		FIG. 1. Proportion of T3N0 colon cancer cases with at least one positive regional lymph node, by the number of regional lymph nodes examined.

 
Figure 2 shows the average number of positive nodes found given the number of nodes examined. The results of analysis of variance indicate that to maximize the number of positive nodes found in a sample, >12 nodes should be examined. The Bonferroni statistic tests for significant differences between the mean number of positive nodes found in each group of nodes examined. It was determined that little additional benefit was derived from evaluation of >13 nodes. In other words, the average yield of positive nodes did not significantly increase once 13 nodes were examined, and this number of nodes may represent the number necessary to adequately stage a tumor.



View larger version (16K):
[in this window]
[in a new window]
  		FIG. 2. Mean number of positive regional lymph nodes identified in surgically resected T3N1–3 colon cancer specimens, by the number of regional lymph nodes pathologically examined.

 
These 2 analytic reviews suggest that <=7 nodes are inadequate to assign node-negative status (pN0) to a T3 colon cancer and that as many as 13 nodes are required to adequately stage a tumor. Stratifying the T3N0 cohort of patients by the number of nodes examined (1–7, 8–12, >=13) shows significantly different 5-year relative survival rates of 69.3%, 77.5%, and 84.5%, respectively. These data are depicted in Fig. 3.



View larger version (28K):
[in this window]
[in a new window]
  		FIG. 3. Five-year relative survival rate, with upper (UL) and lower (LL) confidence intervals, of surgically resected T3N0 colon cancers, by the number of regional lymph nodes pathologically examined.

 
Use of observed 5-year survival rates rather than relative 5-year survival rates demonstrated different rates for the three strata of examined lymph nodes: 49.8% for 1 to 7 lymph nodes, 56.2% for 8 to 12 lymph nodes, and 63.4% for >=13 lymph nodes (P < .0001). These data are shown in Fig. 4. The mean time of observed survival was 67 months for patients with 1 to 7 nodes examined (95% confidence interval [CI], 65–68); 74 months for 8 to 12 nodes (95% CI, 73–76); and 83 months for >=13 nodes (95% CI, 82–85).



View larger version (18K):
[in this window]
[in a new window]
  		FIG. 4. Kaplan-Meier 5-year survival curves of surgically resected T3N0 colon cancers, by the number of regional lymph nodes pathologically examined.

 
A Cox proportional hazards analysis was performed to evaluate further prognostic factors in the survival of patients with reported T3N0 colon cancer. Tumor grade (well or moderately differentiated vs. poorly differentiated or undifferentiated), tumor location (right, transverse, or sigmoid colon), and treatment modality (surgery alone vs. surgery and adjuvant chemotherapy) were not significant contributors to the model. Patient age and the number of nodes examined were found to be significant variables (Table 4). Patient age was the strongest covariate, with patients aged 60 to 69, 70 to 79, and >=80 years 1.5, 2.2, and 3.8 times, respectively, more likely to die (at any time within 5 years of diagnosis) than patients under the age of 60 years. The extent of nodal examination was found to be the other strong contributor to the model. Increased nodal detection was associated with decreasing hazard ratios. When compared with cases with 1 to 7 nodes examined, the examination of 8 to 12 nodes reduced a patient’s hazard to .81, and taking >=13 nodes reduced it further to .68.


View this table:
[in this window]
[in a new window]
  		TABLE 4. Cox proportional hazards model: T3N0 colon cancers
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
We examined >35,000 cases of T3N0 colon cancer to determine the relationship between the number of lymph nodes examined in colonic resection specimens from cancer-directed surgery to 5-year survival rates. The source of the data was the NCDB. The NCDB collected >260,000 cases of colon cancer from 1985 to 1991 from 1,644 hospitals. These cases represent >42% of estimated colon cancer cases in the United States during this time period. The large number of cases and the representation from all types of hospitals in all 50 states suggest that the data are relevant to and broadly representative of current medical practice. The reliability of the data rests on the established Cancer Program of the Commission on Cancer of the American College of Surgeons. This program audits individual cancer programs on a periodic basis. Cases submitted to the NCDB from Commission on Cancer–approved programs represent a convenience sample of incident cancer diagnosis. On aggregate, however, descriptions of patient and tumor characteristics and treatment patterns with NCDB data differ only marginally from those described with use of data from population-based data sets.7

The results of this study suggest that (1) the number of lymph nodes examined is a prognostic variable for patients with T3N0 colon cancer; (2) examination of <8 lymph nodes is inadequate to assign node-negative status (pN0) to a T3 colon cancer; (3) >=13 lymph nodes should be examined to label a T3 colon cancer truly node negative; (4) adjuvant studies should consider stratifying T3N0 colon cancer patients on the basis of the number of lymph nodes examined; and (5) age is a prognostic variable for this group. Given the results of other, smaller studies, the results of this study are not surprising. They further confirm the importance of the adequacy of lymph node examination in the surgical resection specimen.

At least 4 recent studies suggest that 13 to 17 lymph nodes should be examined to stage colorectal cancer. Scott and Grace8 used a fat-clearance technique on 103 specimens of colon or rectal cancer. They found that 94% of node-positive tumors were correctly identified after examination of 13 lymph nodes. Goldstein et al.9 reviewed 750 specimens of colorectal cancer collected over 40 years. They suggested that at least 17 lymph nodes should be examined to stage colorectal cancers. Wong et al.10 retrospectively reviewed 196 patients who had surgery for colorectal cancer. They compared their data with NCDB data and concluded that 14 lymph nodes should be examined to accurately stage colorectal cancer. Tepper et al.1 retrospectively reviewed data from a relatively large (1664 patients) prospective rectal cancer trial. They also concluded that 14 lymph nodes should be examined to define nodal status accurately. Our data generally agree with the data in these reports; however, our report specifically suggests that examining <8 lymph nodes is inadequate for staging, whereas examination of >13 lymph nodes has very little additional benefit.

Why does the prognosis of T3N0 colon cancer depend on both the age of the patient and the number of lymph nodes examined? The significance of age is not clear from this analysis, but it may be related to comorbid disease. The NCDB did not collect data related to comorbid disease during the time of this study; thus, relating age to comorbid disease is speculation at best. However, the relationships of age, comorbidity, and mortality with treatment for colon cancer have been recognized previously.12 The importance of comorbidity for cancer treatment survival has prompted the NCDB to develop methods to collect these data.13

The number of lymph nodes examined depends on the number of lymph nodes present, the extent of the dissection by the surgeon, and the extent of the examination of the tissue by the pathologist. Certainly, with the resection of >35,000 apparent T3N0 colon cancers, it would be reasonable to assume that there may be some variability in the extent of the dissection by different surgeons. The differing amounts of mesenteric tissue and lymph nodes removed by different surgeons might explain some, but probably not all, of the widely variable (0 to >30) number of lymph nodes examined in these 35,000 specimens. It also would be reasonable to assume that different pathologists use different techniques and degrees of diligence in examining specimens for lymph nodes. Certainly, it would be interesting to have data about the size and location of the lymph nodes. Are the larger nodes truly those that are easier to find, and are they associated more often with reactive hyperplasia? The NCDB does not have data to address this possibility. To reduce the variation in the pathologist’s examination, the College of American Pathologists recently recommended that all grossly negative or equivocal lymph nodes be submitted in their entirety for microscopic examination. If fewer than 12 to 15 nodes are found after gross examination, the College of American Pathology suggests that the use of additional techniques, such as fat clearing, may be considered to identify lymph nodes.8,1,14 In hospitals where the lymph node count is frequently low, using the recommendations noted previously by the College of American Pathology might determine whether it is the surgeon or the pathologist who is responsible for the low lymph node count. Certainly, if a pathologist re-examines the mesentery with a fat-clearing technique and does not find 13 lymph nodes, it would seem that the mesenteric resection was inadequate.

The reason the number of lymph nodes examined relates to prognosis probably does not relate to differences in surgical technique that directly affect survival. It is more likely that the reason that examining more lymph nodes is associated with a better prognosis is that staging is improved; examining more lymph nodes probably results in identifying patients with lymph node metastases who otherwise would have been falsely labeled as node negative. There is at least one study that substantiates this possibility. Investigators in Japan used mutant-allele–specific amplification (MASA) to identify mutations in K-ras and p53 in 120 colorectal cancers that were considered lymph node negative. Somatic mutations were identified by MASA in 71 tumors. Lymph nodes of these 71 patients were examined by MASA to detect the specific mutations found in the primary tumors. Of 37 patients with lymph nodes that were negative by standard hematoxylin and eosin analysis but positive for the specific mutation by MASA, 27 had tumor recurrence within 5 years of surgery; none of the 34 patients who had lymph nodes that were negative by MASA had a recurrence.15

The adequacy of lymph node examination for T3 colon cancer has several important implications for patients. First, patients with T3N1 colon cancer are routinely offered postoperative adjuvant chemotherapy, whereas those patients with T3N0 colon cancer are not2,16; thus, it is important to know who is truly node negative before recommending against postoperative adjuvant chemotherapy. Second, as trials evolve to examine newer adjuvant therapy for node-negative disease, such as the National Cancer Institute–sponsored trial for monoclonal antibody 17-1a for T3–4N0 colon cancer, it is important to ensure that prognostic variables are correctly stratified. From the data presented in this article, it would be reasonable to stratify T3N0 patients into one of three strata on the basis of the number of nodes examined. Third, laparoscopic colectomy for colon cancer is being examined and might become an accepted surgical procedure for colon cancer. To assess this technique, it will be important to know what number of lymph nodes should be examined after an open or laparoscopic colectomy. Fourth, sentinel node biopsies have become routine for breast cancer and melanoma. This technique is being examined in several centers for colon cancer. To evaluate the sentinel node technique for colon cancer, it will be important to know the minimum number of lymph nodes that should be examined for a patient with colon cancer.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
Through the examination of a large prospective database with >35,000 cases of T3N0 colon cancer, it seems that to confidently diagnose node negativity (pN0) in T3 colon cancer, at least 13 lymph nodes need to be examined. The survival rate of T3N0 colon cancer patients relates to the number of nodes examined, and three strata of examined nodes (1–7, 8–12, and >=13) may be useful in the design of future adjuvant trials for T3N0 colon cancer. Finally, age is a prognostic factor in the survival of patients with T3N0 colon cancer; this finding argues for prospective collection and analysis of comorbidity data that might be the reason that age seems important prognostically.


   Footnotes
 
Presented at the 54th Annual Meeting of the Society of Surgical Oncology, Washington, DC, March 17, 2001.

A retrospective examination of the large prospective National Cancer Data Base suggests that at least 13 lymph nodes should be examined to label a T3 colon cancer as node negative. Further, adjuvant studies regarding T3N0 colon cancer should consider stratifying according to three strata of numbers of lymph nodes examined: 1 to 7, 8 to 12, and >=13.

Received for publication March 17, 2001. Accepted for publication August 21, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

  1. Tepper JE, O’Connell MJ, Niedzwiecki D, et al. Impact of number of nodes retrieved on outcome in patients with rectal cancer. J Clin Oncol 2001; 19: 157–63.[Abstract/Free Full Text]
  2. National Institutes of Health Consensus Statement. Adjuvant Therapy for Patients With Colon and Rectum Cancer. Bethesda, MD: National Institutes of Health, 1990.
  3. Percy C, Van Holten V, Muir C. International Classification of Diseases of Oncology. 2nd ed. Geneva: World Health Organization, 1990.
  4. Stewart AK, Bland KI, McGinnis LS, Morrow M, Eye HJ. Clinical highlights from the National Cancer Data Base, 2000. CA J Clin 2000; 50: 171–83.[Abstract]
  5. Beahrs OH, Myers MH, Hutter RVP, Kennedy BJ, eds. Manual for Staging of Cancer: American Joint Committee on Cancer. 3rd ed. Philadelphia: Lippincott, 1988.
  6. Beahrs OH, Henson DE, Hutter RVP, Kennedy BJ, eds. Manual for Staging of Cancer: American Joint Committee on Cancer. 4th ed. Philadelphia: Lippincott, 1992.
  7. Mettlin CJ, Menck HR, Winchester DP, Murphy GP. A comparison of breast, colorectal, lung, and prostate cancers reported to the National Cancer Data Base and the Surveillance, Epidemiology, and End Results Program. Cancer 1997; 79: 2052–6.[CrossRef][Medline]
  8. 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]
  9. Goldstein NS, Sanford W, Coffey M, Layfield LJ. Lymph node recovery from colorectal resection specimens removed for adenocarcinoma. Trends over time and a recommendation for a minimum number of lymph nodes to be recovered. Am J Clin Pathol 1996; 106: 209–16.[Medline]
  10. Wong JH, Severino R, Honnebier B, 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]
  11. Deleted in proof.
  12. Yancik R, Wesley MN, Ries LAG, et al. Comorbidity and age as predictors of risk for early mortality of male and female colon carcinoma patients: a population-based study. Cancer 1998; 82: 2123–34.[CrossRef][Medline]
  13. Wingo PA, Luke E, O’Brien K, et al. Population-based patterns of care studies: collaboration among state cancer registries, the American College of Surgeons, and the American Cancer Society. J Registry Manage 2001; 28: 5–16.
  14. Compton C, Fielding L, Burgart L, et al. Prognostic factors in colorectal cancer: College of American Pathologists consensus statement 1999. Arch Pathol Lab Med 2000; 124: 979–94.[Medline]
  15. Hayashi N, Ito I, Yanagisawa A, et al. Genetic diagnosis of lymph-node metastasis in colorectal cancer. Lancet 1995; 345: 1257–9.[CrossRef][Medline]
  16. Moertel CG, Fleming TR, MacDonald JS, et al. Fluorouracil plus levamisole as effective adjuvant therapy after resection of stage III colon carcinoma: a final report. Ann Intern Med 1995; 122: 321–6.[Abstract/Free Full Text]



This article has been cited by other articles:


Home page
 Arch SurgHome page
F. F. Attiyeh
Is Laparoscopic Colectomy a Good Operation for Colon Cancer?
Arch Surg, March 1, 2009; 144(3): 290 - 291.
[Full Text] [PDF]

Home page
 JAMAHome page
S. A. Waldman, T. Hyslop, S. Schulz, A. Barkun, K. Nielsen, J. Haaf, C. Bonaccorso, Y. Li, and D. S. Weinberg
Association of GUCY2C Expression in Lymph Nodes With Time to Recurrence and Disease-Free Survival in pN0 Colorectal Cancer
JAMA, February 18, 2009; 301(7): 745 - 752.
[Abstract] [Full Text] [PDF]

Home page
 JNCI J Natl Cancer InstHome page
K. Y. Bilimoria, D. J. Bentrem, A. K. Stewart, M. S. Talamonti, D. P. Winchester, T. R. Russell, and C. Y. Ko
Lymph Node Evaluation as a Colon Cancer Quality Measure: A National Hospital Report Card
J Natl Cancer Inst, September 17, 2008; 100(18): 1310 - 1317.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Surg. Oncol.Home page
J. Wang, J. M. Hassett, M. T. Dayton, and M. N. Kulaylat
Lymph Node Ratio: Role in the Staging of Node-Positive Colon Cancer
Ann. Surg. Oncol., June 1, 2008; 15(6): 1600 - 1608.
[Abstract] [Full Text] [PDF]

Home page
 J Oncol PractHome page
T. Grote, A. H. Hughes, C. C. Rimmer, D. A. Less, A. P. Abernethy, and Multidisciplinary Gastrointestinal Tumor Board, De
Targeting Lymph Node Retrieval and Assessment in Stage II Colon Cancer: A Quality Outcome Community-Based Cancer Center Study
J. Oncol. Pract, March 1, 2008; 4(2): 55 - 58.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Surg. Oncol.Home page
K. Y. Bilimoria, A. K. Stewart, D. P. Winchester, and C. Y. Ko
The National Cancer Data Base: A Powerful Initiative to Improve Cancer Care in the United States
Ann. Surg. Oncol., March 1, 2008; 15(3): 683 - 690.
[Full Text] [PDF]

Home page
 Ann. Surg. Oncol.Home page
S. H. Baik, N. K. Kim, K. Y. Lee, S. K. Sohn, C. H. Cho, M. J. Kim, H. Kim, and R. K Shinn
Factors Influencing Pathologic Results after Total Mesorectal Excision for Rectal Cancer: Analysis of Consecutive 100 Cases
Ann. Surg. Oncol., March 1, 2008; 15(3): 721 - 728.
[Abstract] [Full Text] [PDF]

Home page
 JAMAHome page
K. Y. Bilimoria, A. K. Stewart, S. B. Edge, and C. Y. Ko
Lymph Node Examination Rate, Survival Rate, and Quality of Care in Colon Cancer
JAMA, February 27, 2008; 299(8): 896 - 896.
[Full Text] [PDF]

Home page
 Ann. Surg. Oncol.Home page
S. J. Lim, B. W. Feig, H. Wang, K. K. Hunt, M. A. Rodriguez-Bigas, J. M. Skibber, V. Ellis, K. Cleary, and G. J. Chang
Sentinel Lymph Node Evaluation Does Not Improve Staging Accuracy in Colon Cancer
Ann. Surg. Oncol., January 1, 2008; 15(1): 46 - 51.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Surg. Oncol.Home page
M. B. Slidell, D. C. Chang, J. L. Cameron, C. Wolfgang, J. M. Herman, R. D. Schulick, M. A. Choti, and T. M. Pawlik
Impact of Total Lymph Node Count and Lymph Node Ratio on Staging and Survival after Pancreatectomy for Pancreatic Adenocarcinoma: A Large, Population-Based Analysis
Ann. Surg. Oncol., January 1, 2008; 15(1): 165 - 174.
[Abstract] [Full Text] [PDF]

Home page
 Clin. Cancer Res.Home page
C. C. Compton
Optimal Pathologic Staging: Defining Stage II Disease
Clin. Cancer Res., November 15, 2007; 13(22): 6862s - 6870s.
[Abstract] [Full Text] [PDF]

Home page
 JAMAHome page
S. L. Wong, H. Ji, B. K. Hollenbeck, A. M. Morris, O. Baser, and J. D. Birkmeyer
Hospital Lymph Node Examination Rates and Survival After Resection for Colon Cancer
JAMA, November 14, 2007; 298(18): 2149 - 2154.
[Abstract] [Full Text] [PDF]

Home page
 GutHome page
E. J A Morris, N. J Maughan, D. Forman, and P. Quirke
Who to treat with adjuvant therapy in Dukes B/stage II colorectal cancer? The need for high quality pathology
Gut, October 1, 2007; 56(10): 1419 - 1425.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Surg. Oncol.Home page
S. L. Chen and A. J. Bilchik
Resecting Lymph Nodes in Colon Cancer: More than a Staging Operation?
Ann. Surg. Oncol., August 1, 2007; 14(8): 2175 - 2176.
[Full Text] [PDF]

Home page
 Arch SurgHome page
J. S. Tomlinson, S. Jain, D. J. Bentrem, E. G. Sekeris, M. A. Maggard, O. J. Hines, H. A. Reber, and C. Y. Ko
Accuracy of Staging Node-Negative Pancreas Cancer: A Potential Quality Measure
Arch Surg, August 1, 2007; 142(8): 767 - 774.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Surg. Oncol.Home page
H.-Y. Lee, H.-J. Choi, K.-J. Park, J.-S. Shin, H.-C. Kwon, M.-S. Roh, and C. Kim
Prognostic Significance of Metastatic Lymph Node Ratio in Node-Positive Colon Carcinoma
Ann. Surg. Oncol., May 1, 2007; 14(5): 1712 - 1717.
[Abstract] [Full Text] [PDF]

Home page
 CA Cancer J ClinHome page
B. M. Wolpin, J. A. Meyerhardt, H. J. Mamon, and R. J. Mayer
Adjuvant Treatment of Colorectal Cancer
CA Cancer J Clin, May 1, 2007; 57(3): 168 - 185.
[Abstract] [Full Text] [PDF]

Home page
 JNCI J Natl Cancer InstHome page
R. Ricciardi and N. N. Baxter
Association Versus Causation Versus Quality Improvement: Setting Benchmarks for Lymph Node Evaluation in Colon Cancer
J Natl Cancer Inst, March 21, 2007; 99(6): 414 - 415.
[Full Text] [PDF]

Home page
 JNCI J Natl Cancer InstHome page
G. J. Chang, M. A. Rodriguez-Bigas, J. M. Skibber, and V. A. Moyer
Lymph Node Evaluation and Survival After Curative Resection of Colon Cancer: Systematic Review
J Natl Cancer Inst, March 21, 2007; 99(6): 433 - 441.
[Abstract] [Full Text] [PDF]

Home page
 CA Cancer J ClinHome page
S. L. Chen, D. M. Iddings, R. P. Scheri, and A. J. Bilchik
Lymphatic Mapping and Sentinel Node Analysis: Current Concepts and Applications
CA Cancer J Clin, September 1, 2006; 56(5): 292 - 309.
[Abstract] [Full Text] [PDF]

Home page
 Ann OncolHome page
I Chau and D Cunningham
Adjuvant therapy in colon cancer--what, when and how?
Ann. Onc., September 1, 2006; 17(9): 1347 - 1359.
[Abstract] [Full Text] [PDF]

Home page
 JCOHome page
P. M. Johnson, G. A. Porter, R. Ricciardi, and N. N. Baxter
Increasing Negative Lymph Node Count Is Independently Associated With Improved Long-Term Survival in Stage IIIB and IIIC Colon Cancer
J. Clin. Oncol., August 1, 2006; 24(22): 3570 - 3575.
[Abstract] [Full Text] [PDF]

Home page
 JCOHome page
C. E. Desch, A. B. Benson III, M. R. Somerfield, P. J. Flynn, C. Krause, C. L. Loprinzi, B. D. Minsky, D. G. Pfister, K. S. Virgo, N. J. Petrelli, et al.
Colorectal Cancer Surveillance: 2005 Update of an American Society of Clinical Oncology Practice Guideline
J. Clin. Oncol., November 20, 2005; 23(33): 8512 - 8519.
[Abstract] [Full Text] [PDF]

Home page
 Arch SurgHome page
J. H. Wong, D. S. Johnson, D. Hemmings, A. Hsu, T. Imai, and G. T. Tominaga
Assessing the Quality of Colorectal Cancer Staging: Documenting the Process in Improving the Staging of Node-Negative Colorectal Cancer
Arch Surg, September 1, 2005; 140(9): 881 - 887.
[Abstract] [Full Text] [PDF]

Home page
 JNCI J Natl Cancer InstHome page
N. N. Baxter, D. J. Virnig, D. A. Rothenberger, A. M. Morris, J. Jessurun, and B. A. Virnig
Lymph Node Evaluation in Colorectal Cancer Patients: A Population-Based Study
J Natl Cancer Inst, February 2, 2005; 97(3): 219 - 225.
[Abstract] [Full Text] [PDF]

Home page
 CA Cancer J ClinHome page
C. C. Compton and F. L. Greene
The Staging of Colorectal Cancer: 2004 and Beyond
CA Cancer J Clin, November 1, 2004; 54(6): 295 - 308.
[Abstract] [Full Text] [PDF]

Home page
 JNCI J Natl Cancer InstHome page
J. B. O'Connell, M. A. Maggard, and C. Y. Ko
Colon Cancer Survival Rates With the New American Joint Committee on Cancer Sixth Edition Staging
J Natl Cancer Inst, October 6, 2004; 96(19): 1420 - 1425.
[Abstract] [Full Text] [PDF]

Home page
 JCOHome page
A. B. Benson III, D. Schrag, M. R. Somerfield, A. M. Cohen, A. T. Figueredo, P. J. Flynn, M. K. Krzyzanowska, J. Maroun, P. McAllister, E. Van Cutsem, et al.
American Society of Clinical Oncology Recommendations on Adjuvant Chemotherapy for Stage II Colon Cancer
J. Clin. Oncol., August 15, 2004; 22(16): 3408 - 3419.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Surg. Oncol.Home page
S. Saha, A. G. Dan, A. J. Bilchik, Y. Kitagawa, E. Schochet, S. Choudhri, L. T. Saha, D. Wiese, D. Morton, and M. Kitajima
Historical Review of Lymphatic Mapping in Gastrointestinal Malignancies
Ann. Surg. Oncol., March 1, 2004; 11(3_suppl): 245S - 249S.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Swanson, R. S.
Right arrow Articles by Bland, K. I.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Swanson, R. S.
Right arrow Articles by Bland, K. I.
Related Collections
Right arrow Pathology

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS