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10.1245/ASO.2003.01.012
Annals of Surgical Oncology 10:903-909 (2003)
© 2003 Society of Surgical Oncology
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ORIGINAL ARTICLES

Lymph Node Retrieval and Assessment in Stage II Colorectal Cancer: A Population-Based Study

F.C. Wright, MD, FRCSC, C.H. L. Law, MD, MPH, FRCSC, L. Last, CCRP, M. Khalifa, MD, PhD, FRCPC, A. Arnaout, MD, Z. Naseer, BSc, MSc, N. Klar, PhD, S. Gallinger, MD, MSc, FRCSC and A.J. Smith, MD, MSc, FRCSC

From the University of Toronto (FCW, CHLL, AA, AJS), Toronto, Ontario, Canada; Toronto Sunnybrook Regional Cancer Centre (CHLL, LL, MK, AJS), Toronto, Ontario, Canada; Cancer Care Ontario (ZN, NK), Toronto, Ontario, Canada; and Mount Sinai Hospital (SG), New York, New York.

Correspondence: Address correspondence and reprint requests to: A. J. Smith, MD, MSc, FRCSC, Toronto Sunnybrook Regional Cancer Centre, 2075 Bayview Ave., Toronto, Ontario, Canada M4N 3M5; Fax: 416-217-1338; E-mail: andy.smith{at}tsrcc.on.ca


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Adjuvant chemotherapy for patients with stage III (node-positive) colorectal cancer (CRC) reduces mortality by one third. Retrieval of an inadequate number of lymph nodes in the surgical specimen may result in incorrectly designating some patients as stage II (node negative), and consequently, such patients may not be offered appropriate chemotherapy. Recent National Cancer Institute guidelines suggest that a minimum of 12 nodes should be examined to ensure accurate staging.

Methods: This population-based study identified stage II (T3N0 and T4N0) CRC cases by using CRC pathology reports (1997–2000) from the Ontario Cancer Registry. Patients aged 19 to 75 years were identified, and demographic, surgical, pathologic, and hospital data were extracted. Factors relating to the number of lymph nodes assessed were examined.

Results: A total of 8848 CRC cases were reviewed, and 1789 stage II cases were identified. Seventy-three percent of cases were designated as node negative on the basis of assessment of <12 lymph nodes. Multivariate analysis showed that age, tumor size, specimen length, use of a pathology template, and academic status of the hospital were significant predictors of the number of lymph nodes assessed.

Conclusions: A subset of patients with CRC in Ontario were assigned stage II disease on the basis of examination of relatively few lymph nodes.

Key Words: Colorectal cancer • Staging • Lymph node assessment • Population study


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Colorectal cancer (CRC) is the second most common cause of cancer death in North America.1,2 At first presentation of disease, 36% of CRC patients have localized or node-negative disease (stages I and II), and 37% have regional or node-positive disease (stage III).3 It is critically important to accurately differentiate between these groups of patients because this has a significant effect on prognosis and treatment. Five-year survival for stage I CRC is 80%–85% and for stage II CRC is 70%–75%.4 In contrast, survival for stage III CRC is 45% with surgery alone.2,5 Adjuvant chemotherapy (5-fluorouracil and leucovorin) has been shown to improve survival by one third when administered to patients whose lymph nodes are involved with cancer.6,7

Adequate retrieval and assessment of colorectal mesenteric lymph nodes is critical to ensure that the lymph nodes do not contain metastatic disease. Failure to examine enough lymph nodes may result in a failure to identify patients in whom a relatively small fraction of the nodes are involved with cancer. Lymph node metastases may occur in patients regardless of the T stage and other pathologic factors.8

Previous investigators have addressed the question of how many lymph nodes need to be assessed to define node negativity in a CRC specimen. The minimum adequate number ranges between 12 and 20.9–13 It is important to note that it has been found that inadequate lymph node assessment affects survival in stage II CRC.14–16 Despite this, many centers do not assess the suggested number of lymph nodes needed to confidently determine whether a specimen is node negative.14,17,18 In this population-based study, we assessed the adequacy of lymph node assessment in stage II CRC in the province of Ontario, Canada, from 1997 to 2000.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
This study was composed of stage II (T3N0M0 and T4N0M0) CRC patients aged 19 to 75 years residing in Ontario (population, 11.8 million), Canada, between July 1, 1997, and June 30, 2000.19 This time period was selected because many of these cases have also been registered in the Ontario Familial Colorectal Cancer Registry, a member of the National Institutes of Health Cooperative Family. Pathology reports were collected by the Ontario Cancer Registry as described previously.20 All cases with disease that did not penetrate the muscularis propria (T1 and T2) and cases with positive lymph nodes (stage III), distant metastases, or both were excluded. Clinical and pathologic data were extracted, including patient age, sex, type of colorectal resection, number of lymph nodes assessed, specimen length, tumor size, and stage. In addition, the hospital where the colorectal resection was performed, its academic status, and whether a pathology template was used when reporting the CRC specimen were noted.

Type of Colorectal Resection
Colorectal specimens were subdivided into right colon resections (includes right colon to transverse colon), left colon (includes mid transverse to sigmoid), and rectal (low anterior and abdominal perineal) resections. Cases in which the resection was smaller than a typical oncological resection were coded within the category that was deemed most appropriate; e.g., an ileocolic resection for a cecal cancer was coded as a right colon resection. Cases with positive margins were excluded.

Number of Lymph Nodes Assessed
The number of lymph nodes assessed was retrieved from the diagnosis section or the tumor template in the pathology report. Because at the time of pathologic grossing of the specimen, identification of pericolic lymph nodes could be inaccurate, the number of lymph nodes stated in the macroscopic description component of the pathology report was disregarded. When the lymph node status was reported as negative, but the actual number of lymph nodes assessed was not recorded, the number of lymph nodes was designated as "missing." Lymph node–clearing techniques were not documented in the individual pathology reports. However, in a separate study of Ontario pathologists, we found that 20% had used chemical clearing techniques, whereas 80% used simple manual lymph node–clearing techniques (Wright et al., unpublished data, 2003).

Specimen Length
This variable was used as a crude surrogate for the extent of surgical resection.21–23 There is no dependable method to ascertain the extent of a lymphadenectomy from the pathology reports alone.

Hospital Academic Status
The site where surgery was performed was categorized into either an academic or nonacademic hospital. An academic hospital was defined as a hospital where both pathology and surgical residents did rotations during their training.

Hospital CRC Case Volume
The number of stage II resections was used as a surrogate for the overall number of CRC resections performed at a given institution.

Pathology Template
A pathology template was defined as a standardized, succinct format used to report key pathologic variables whether they were positive or negative. To qualify as a template, the summary had to include a minimum of (1) histological diagnosis (e.g., adenocarcinoma), (2) depth of invasion (T stage, Dukes’ stage, or depth of penetration through the bowel wall), and (3) the lymph node status (e.g., zero of eight nodes positive for cancer). A wide range of templates reflecting a range of level of detail was observed.

Statistical Analysis
Statistical analysis was performed by using descriptive analyses that are based on comparisons of mean and median lymph node counts per patient. Statistical inferences concerning lymph node counts per patient were conducted with the generalized estimating equations extension of Poisson regression24 fit via PROC GENMOD of the computer package SAS (SAS Institute, Cary, NC).25 Poisson regression is used to model count data (i.e., the number of nodes per patient). Regression coefficients from this model estimate the log of the ratio of the average number of nodes obtained per patient for a unit change in the covariate. The generalized estimating equations extension allows adjustment for variation in surgical practice patterns among hospitals.26 Failure to account for such variation tends to result in P values that are too small and confidence intervals that are too narrow. Age, tumor size, specimen length, and number of cases per hospital were treated as continuous predictors. The relative average number of nodes for age was calculated by using 10-year increases; for tumor size, 10-cm increases; specimen length, 10-cm increases; and number of hospital cases, 10-case increases. P values were considered significant at .05 and were two tailed.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Pathology reports from 8848 patients with CRC who were treated between June 30, 1997, and June 30, 2000, were reviewed. The population was composed mostly of patients aged 19 to 75 years, although a few cases of older patients were reviewed and excluded. Of all cases, 1789 (20.2%) were diagnosed as having stage II (node negative, transmural CRC) disease and were between 19 and 75 years of age. Ninety-nine hospitals performed colorectal surgery in Ontario from 1997 to 2000. Of these hospitals, 17 were classified as academic and 82 as nonacademic institutions. The average number of stage II CRC surgeries performed over the 3-year period was 29.2 for academic centers and 15.9 for nonacademic centers.

Lymph Node Assessment
Of the 1789 eligible cases, it was not stated in 94 (5.3%) how many lymph nodes were assessed. Analyses of lymph node counts were therefore limited to the 1695 cases that had such information. For these cases, a median of 8 (range, 0–65) lymph nodes were assessed to render a diagnosis of stage II (node-negative) CRC. More importantly, 73% of these stage II specimens had fewer than 12 lymph nodes assessed (Fig. 1). In 4% of these cases, there were zero nodes assessed. In these cases, there was usually a notation that the pathologist searched unsuccessfully for lymph nodes.



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  		FIG. 1. Number of lymph nodes assessed in stage II colorectal cancer cases in Ontario between 1997 and 2000. ({blacksquare}) Cases in which the number of lymph node assessed was >12. () Cases in which the number of lymph node assessed was <12.

 
Univariate Analysis of Factors Affecting Lymph Node Assessment
Significant factors that affected lymph node retrieval included age, tumor size, specimen length, use of a pathology template, and academic status of the hospital. Factors that were not significant were patient sex, tumor stage, and hospital CRC case volume (Table 1; Fig. 2). In addition, we separately examined the effect of the number of cases per surgeon on average lymph node retrieval and found no statistically significant association. Of note, there was a weak association between specimen length and tumor size (correlation = .13; P < .0001). This suggests that there was a somewhat increased tendency to larger resections in patients with large tumors.


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  		TABLE 1. Univariate analysis of factors affecting lymph node assessment in stage II (node-negative) colorectal cancer in Ontario (1997–2000)
 


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  		FIG. 2. Scattergram demonstrating the distribution of academic and nonacademic hospitals in Ontario and the case volume and average number of lymph nodes reported in determining a diagnosis of node-negative colon cancer. The lines represent regression and analyses showing the relationship between the number of cases performed at each hospital and the relationship to the average number of lymph nodes assessed in academic and nonacademic hospitals.

 
Multivariate Analysis
Significant factors associated with improved lymph node retrieval included young age, increased tumor size, increased specimen length, use of a pathology template, and having surgery performed at an academic center (Table 2). The number of cases per hospital was associated with a significant decrease in the number of lymph nodes assessed on multivariate analysis, although this effect was of marginal statistical significance.


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  		TABLE 2. Multivariate analysis of factors affecting lymph node assessment in stage II (node-negative) colorectal cancer in Ontario (1997–2000)
 
Patient Population in Academic Versus Nonacademic Hospitals
The patient populations were reviewed in both academic and nonacademic hospitals. There was no difference in age, sex, tumor size, or tumor stage between these two groups. There was a trend toward a shorter specimen length in cases from nonacademic hospitals (P = .076; Table 3).


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  		TABLE 3. Patient characteristics in academic versus nonacademic hospitals
 
Number of Lymph Nodes Assessed in Academic Versus Nonacademic Hospitals
There were 438 (28.6% of total) stage II CRC resections performed in academic centers and 1095 (71.4% of total) in nonacademic hospitals from 1997 to 2000. Academic hospitals identified significantly more lymph nodes in all types of resections compared with nonacademic centers (Table 4). Of note, there was a trend toward shorter resection specimens in the nonacademic centers, but it was not possible to determine accurately whether there were a larger number of nononcological colorectal resections in this group (e.g., ileocolic resections for cecal cancer). Also, it was not possible to accurately determine whether the grossing of specimens was consistently performed by pathology residents, pathology assistants, or pathologists in these two groups of hospitals.


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  		TABLE 4. Lymph node assessment of patients treated in academic versus nonacademic centers
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Adequate lymph node assessment is a critical component in staging CRC because of its direct effect on prognosis and treatment. This is especially important because of the difference in prognosis for node-positive CRC (5-year survival of approximately 45%) and node-negative CRC (5-year survival of approximately 80%).4 Moreover, adjuvant chemotherapy has been shown to significantly improve survival by one third (up to 65% 5-year survival in stage III CRC).5,6

In clinical practice, there are both surgical and pathologic barriers to accurately staging patients with CRC. Surgeons must provide pathologists with an adequate specimen composed of the segment of bowel containing the tumor and an adequate amount of lymph node–bearing mesentery. The ideal extent of bowel resection is defined by excising the blood supply and lymphatics at the level of the origin of the primary feeding vessel.13 If the colorectal specimen is inadequate, then no matter how assiduously the pathologist examines the specimen, he or she will be unsuccessful in identifying an adequate number of lymph nodes. In this study, more lymph nodes were found and assessed as the specimen length increased. This is consistent with the principle that the surgeon must perform an adequate surgical resection, including the main lymphovascular supply to the bowel, to provide the pathologist with enough lymph nodes to dissect. Nonetheless, specimen length as a surrogate marker for an adequate resection is limited in its ability to reflect the surgeon’s attention to an adequate lymphadenectomy.

Lymph nodes can be difficult to identify in the pathology suite. Malignant lymph nodes are frequently <5 mm in size.4 A number of techniques—including fat clearance with xylene and alcohol, lymph node–revealing solution (e.g., Carnoy’s solution), an increased use of pathology assistants, and the use of a pathology template—have all been suggested as improving lymph node assessment.9,17,27–29 In 4% of cases included in this study, the pathologist was unable to find any lymph nodes. The size and morphology of lymph nodes are modified by immune responses. Distension and prominence of the lymphatic sinusoids, called sinus histiocytosis, may represent a host immune response against neoplastic cell products. This is a common phenomenon seen in lymph nodes draining cancer and leads to lymph node enlargement, even in the absence of metastatic spread. Mesenteric lymph node sinus histiocytosis in resected specimens for CRC has been previously documented.30,31 Larger tumors are expected to provide a more intense antigenic immune challenge to the draining lymph nodes, making them more visible to the examining pathologist. This could explain the association noted in this series between larger tumor size and higher counts of lymph nodes. Of note, depth of invasion (T3 vs. T4) did not affect the extent of lymph node assessment.

It has been shown that an inadequate assessment of lymph nodes can negatively affect survival in CRC.14–16 Caplin et al.15 reported that overall survival was diminished in patients with stage II disease with fewer than seven lymph nodes examined compared with patients with stage II disease and seven or more lymph nodes examined (5-year survival, 49% vs. 68%). Law et al.14 also confirmed that an inadequate assessment of lymph nodes negatively affects survival for patients with stage II CRC. The Law et al. patient cohort was also divided into two groups: those with specimens with fewer than seven nodes examined (group 1) and those with seven or more nodes examined (group 2). The 3-year survival of patients comprising group 1 was 72.7%, compared with 89.8% in group 2. It is hypothesized that some patients with designated stage II disease and few nodes examined have a poor survival because they likely have understaged stage III (node-positive) disease; i.e., the tumor’s capacity to metastasize was unrecognized. On a larger scale, Prandi et al.16 reviewed 3648 patients on the Intergruppo Italiano Terapia Adiuvante Carcinoma Del Colon multicenter trial testing adjuvant therapy for Dukes’ B and C (stage II and III) colon cancer. This group also found that stage B patients with fewer than seven nodes examined had a shorter overall survival than stage B patients with seven or more nodes assessed. The outcome of patients with stage III CRC was not affected by the number of nodes recovered. This group suggested that perhaps patients with stage II disease and fewer than seven nodes examined should be given chemotherapy because of the distinct possibility that they have been understaged. In a previous study, we showed that the pattern of failure in stage II CRC patients with low lymph node counts is mainly characterized by an increase in cases with distant disease, especially hepatic metastases.14 However, in the same study, locoregional recurrence did not differ among patients with low or high lymph node counts, suggesting that there may have been equivalent mesenteric dissection but inadequate lymph node retrieval from the CRC specimen in the pathology lab. This again supports the hypothesis that a subset of patients with stage II CRC and low numbers of lymph nodes examined actually have stage III, or node-positive, disease.

The National Cancer Institute recommends that a minimum of 12 lymph nodes should be assessed to accurately stage patients with CRC.13 In our study, we found that 73% of patients in Ontario with stage II CRC had fewer than 12 lymph nodes assessed. This suggests that a subset of patients in Ontario assigned stage II disease could have been erroneously understaged and could have not been offered appropriate chemotherapy.

In this population-based study, use of a pathology template was associated with an increased number of lymph nodes examined. Pathology templates were first suggested to be of benefit in 1996 in ensuring that important pathologic characteristics of a CRC specimen were included in the pathology report.32 Follow-up studies found that the use of template pro formas increased the rate of clinically significant data items being included to 100%.33 Finally, a pathology template or protocol has been suggested as a reliable tool by the Cancer Committee of the College of American Pathologists for pathologists to communicate with clinicians treating a patient with CRC about prognostically important characteristics of the CRC specimen.4,34,35 We have recently shown that in a single center, lymph node counts can be increased by using a multifaceted change initiative directed at both pathologists and surgeons.36 A key part of this plan included the development and use of a pathology template. We hypothesize that the implementation of a pathology template reflects the culture (or commitment to quality) of a hospital to ensuring that a standardized, reproducible approach to treating and assessing CRC patients exists.

Pathology reports from academic hospitals included more lymph nodes than those from nonacademic hospitals, although the patient populations were not different between these two types of institutions. It is possible that in academic centers there are increased resources available to provide quality multidisciplinary cancer care and that this is reflected by an increased number of lymph nodes examined. A higher volume of cases per hospital was associated with a statistically significant decrease in the number of lymph node examined in multivariate analysis. However, in univariate analysis, an increased number of colorectal cases had no effect on the number of lymph nodes assessed. We cannot explain why there was a decrease in the number of lymph nodes examined in multivariate, but not in univariate, analysis as cases increased. We suggest that this finding emphasizes that a commitment to provide quality cancer care needs to be consciously made at an administrative level by providing adequate resources. In particular, pathology assistants have been demonstrated to identify more lymph nodes than residents or busy staff pathologists.29 Our data suggest that a higher volume of cases does not necessarily mean that a higher quality of care is being provided, at least at the level of lymph node reporting in CRC (Fig. 2). Although some studies show that increased surgical volume is associated with improved outcomes in CRC, other reports have not found this to be the case.37

The inadequacy of lymph node assessment in both academic and nonacademic centers across Ontario may be ameliorated via a multifaceted education plan with the end point of improved staging and patient care in CRC. If staging CRC is improved, then more node-positive patients may be offered the benefits of adjuvant chemotherapy. We developed an educational pilot study in late 1999 to improve our low lymph node assessment rate in our academic center.36 Our multifaceted education program spanned 16 weeks and included a review of the literature, a retreat, informal discussions among opinion leaders in pathology and surgery, and development of a pathology template. Before this time, the median number of lymph nodes assessed in stage II CRC was 7. At a 2-year follow-up, the CRC lymph node counts improved to a median of 17. It is important to note that among patients treated with curative intent, the percentage of lymph node–positive cancers increased from 30.8% before the intervention to 35.3% afterward. Although not yet statistically significant (P = .29), this trend is expected to become significant with time. It is hoped that the durable success at improving lymph node counts at our center, after a relatively short intervention period, could serve as a model for a larger province-wide intervention. Because 73% of patients in Ontario were assigned stage II disease on the basis of fewer than 12 lymph nodes being assessed, we propose a multifaceted education program directed at both surgeons and pathologists that is aimed at improving lymph node examination across Ontario in both academic and nonacademic centers.


   ACKNOWLEDGMENTS
 
The acknowledgments are available online at www.annalssurgicaloncology.org.

Supported by the National Cancer Institute, National Institutes of Health (RFA CA-95-011), and through cooperative agreements with the Ontario Registry for Studies of Familial Colorectal Cancer (U01CA 74783). The content of this article does not necessarily reflect the views or policies of the National Cancer Institute or any of the collaborating centers in the Cancer Family Registries (CFR), nor does mention of trade names, commercial products, or organizations imply endorsement by the US government or the CFR.


   FOOTNOTES
 
Adequate lymph node retrieval is important for accurate staging and management in colorectal cancer. We assessed lymph node retrieval in Ontario from 1997 to 2000 and found that 73% of patients had fewer than 12 lymph nodes assessed when assigned stage II (node-negative) disease.

Received for publication January 15, 2003. Accepted for publication May 22, 2003.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Pathology practice patterns affect lymph node evaluation and outcome of colon cancer: a population-based study
Ann. Onc., December 1, 2006; 17(12): 1803 - 1809.
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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]

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