Number of lymph nodes examined and associated clinicopathologic factors in colorectal carcinoma.
Abstract: Context.--Nodal metastasis is one of the most important prognostic factors in colorectal carcinoma. The number of lymph nodes recovered and examined in resection specimens has been recently shown to be critical for proper staging and is associated with survival.

Objective.--To assess the clinicopathologic factors that may be associated with the number of lymph nodes harvested from surgical resections.

Design.--Clinicopathologic factors of 434 consecutive cases of colorectal cancers treated by surgical resection from a single tertiary medical center were retrospectively reviewed and correlated with number of lymph nodes recovered.

Results.--Our data show that patient age, tumor location, and length of resected bowel segment were associated with number of lymph nodes harvested in surgical resections of colorectal cancer. The average number of lymph nodes was 18.2 and 17.8 for patients younger than 50 years and aged 50 through 60 years, respectively, whereas it was 14.4, 15.1, and 14.9 for patients aged 61 through 70 years, 71 through 80 years, and 80 years and older, respectively. More lymph nodes were present in resection specimens of cecum/ascending colon and descending colon cancers than in those of transverse colon, sigmoid colon, and rectal cancers. There was a linear increase in number of lymph nodes examined with increasing length of bowel resection specimens. In multivariate regression analysis, the factors that remained independent predictors of removal of 12 or more lymph nodes from resection specimens were tumor location and length of resected bowel segment.

Conclusions.--The number of lymph nodes obtained in resection specimens for colorectal cancer was significantly associated with the length of resected segments of bowel, patient age, and location of the tumor.
Article Type: Report
Subject: Colorectal cancer (Diagnosis)
Colorectal cancer (Prognosis)
Colorectal cancer (Care and treatment)
Lymph nodes (Health aspects)
Pathologists (Practice)
Pathology (Practice)
Authors: Shen, Steven S.
Haupt, Bisong X.
Ro, Jae Y.
Zhu, Jijiang
Bailey, H. Randoph
Schwartz, Mary R.
Pub Date: 05/01/2009
Publication: Name: Archives of Pathology & Laboratory Medicine Publisher: College of American Pathologists Audience: Academic; Professional Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2009 College of American Pathologists ISSN: 1543-2165
Issue: Date: May, 2009 Source Volume: 133 Source Issue: 5
Topic: Event Code: 200 Management dynamics
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 230152000
Full Text: Colorectal carcinoma is the second most common cause of cancer deaths in the United States. (1) The most important prognostic factor in colorectal carcinoma is the nodal status at the time of surgical treatment. The 5-year survival rate for stages I and II colorectal carcinomas is greater than 75%. With nodal metastasis, the 5-year survival rate drops dramatically to from 40% to 60%. (2) The presence of nodal metastasis is one of the key determining factors for undergoing postoperative adjuvant therapy and is also a key factor in predicting disease-free and longterm survival. (3-5)

The standard treatments of stages I and II colon cancer are surgical removal of the cancer with clear surgical margins and adequate regional lymph node dissection. For stages II and III rectal cancers, neoadjuvant chemoradiation is indicated. Additional treatment with chemotherapy or radiotherapy is often the standard treatment of stages III and IV colorectal cancers. It is still controversial whether chemotherapy should be selectively added for certain patients with stage II colon cancer and high risk factors, such as poorly differentiated tumors, tumor perforation, and limited number of lymph nodes examined. A growing body of evidence suggests that the prognosis of certain patients with stage II cancer and unfavorable prognostic factors can be improved by adjuvant chemotherapy. (6,7)

Accurate staging is critical for the appropriate management of patients with colorectal cancer. The number of lymph nodes harvested and examined from a resected colorectal specimen is a key factor for accurate staging and has also been shown to be associated with survival. (8-11) However, the number of lymph nodes examined varies tremendously among patients. (12,13) Some studies have suggested that a minimum of 12 negative lymph nodes are needed for adequately staging a node-negative colorectal cancer and this number is recommended by a National Cancer Institute guideline. (14,15) Furthermore, the minimal number of lymph nodes examined is now being used by some third-party payers as quality of surgery or pay-for-performance indicator.

However, the number of lymph nodes recovered and examined pathologically is a combination of many hostspecific, disease-specific, surgical, and pathologic procedural factors. The purpose of this study was to assess the clinicopathologic factors that may have an impact on the number of lymph nodes harvested from surgical resections of colorectal cancer.

MATERIALS AND METHODS

A total of 434 consecutive colorectal cancer cases were reviewed, for which resection specimens were collected from 2002 to 2007 at an academic tertiary referral hospital in Houston, Texas. Colectomies that were associated with inflammatory bowel disease and familial polyposis syndromes were excluded from this study. Other exclusion criteria included noninvasive malignant polyps, nonprimary colorectal carcinomas, gastrointestinal stromal or other mesenchymal tumors, tumors other than conventional colorectal adenocarcinoma or mucinous carcinoma, and tumors with unspecified location. All slides from each case were reviewed by at least 1 of 3 pathologists (S.S.S., B.X.H., J.Y.R.) to confirm the diagnoses, including histologic type and grade as well as depth of invasion. Clinical and pathologic parameters including basic demographic information, such as age and sex, tumor location, length of resected bowel specimen, total number of lymph nodes, and number of positive lymph nodes were obtained from the pathology database or patient chart review. Tumor locations were divided into cecum and ascending colon, transverse colon, descending colon, sigmoid colon, and rectum. The colorectal specimens were processed and examined according to standard procedure. For smaller tumors (<2 cm), the entire tumor was submitted for pathologic examination. For larger tumors, multiple sections (at least 1 section per cm) with deepest invasion were submitted for examination. Dissection of lymph nodes was performed with manual dissection methods, by either pathologists' assistants or pathology residents, with close supervision by pathologists or pathologists' assistants. No chemical clearing agent was used for nodal dissection. Tumor stage was based on TNM staging system and American Joint Committee on Cancer's AJCC Cancer Staging Manual (6th edition, 2002). (16) Tumors were graded as well differentiated (less than 5% solid), moderately differentiated (5% to 50% solid), and poorly differentiated (more than 50% solid) adenocarcinomas primarily on the basis of relative proportion of gland formation and solid components. Circumscription, presence of a well-defined capsule and subcapsular sinuses, and subserosal or mesenteric fat location were required for identification of lymph nodes. Subserosal or mesenteric nodules that were entirely replaced by metastatic carcinoma were counted as positive lymph nodes if the nodules had smooth and rounded contours with configuration of lymph nodes. The surgeons who performed the colorectal resection were divided into 2 groups: group 1 consisted of surgeons who had specialized colorectal oncologic fellowship training and group 2 was composed of general surgeons.

All of the aforementioned parameters were incorporated into a database with institutional review board approval. Categoric variables such as sex, tumor location, grade, and nodal status were summarized by frequencies and percentages. Quantitative variables such as age and number of lymph nodes were summarized as mean and standard deviation. One-way analysis of variance (ANOVA) was used to compare a continuous variable among more than 2 groups. Student t test was used to compare continuous variables between 2 groups. Multivariate logistic regression analysis was performed to determine the factors that are associated with the harvest of 12 or more lymph nodes for pathologic examination. Statistical analysis was performed with SPSS for Windows (Version 13.0; SPSS Inc, Chicago, Ill).

RESULTS

Table 1 summarizes the clinicopathologic data of the 434 patients with colorectal adenocarcinoma. The total number of lymph nodes and positive lymph nodes separated by age groups are shown in Table 2. As expected, the lengths of the resected bowel specimens among different age groups were very similar. However, the average number of lymph nodes recovered from the 2 groups of patients younger than 60 years was 18.2 and 17.8, which was significantly higher than that from the 3 older age groups (P = .001). Of note, the average number of positive lymph nodes in the 2 younger age groups (4.64 and 2.84) was also significantly higher than that in the 3 older age groups (1.97, 1.85, and 1.22).

The length of the resected bowl segments for cecum/ ascending colon, sigmoid colon and rectal cancers was similar (23.2, 20.1, and 24 cm), but the average total number of lymph nodes for cecum/ascending colon cancers was 17.8, significantly higher than for sigmoid colon (14.3, P < .001) and rectal cancers (13.7, P = .001). Tumors in the descending colon and transverse colon were much less frequent than tumors in the cecum/ascending colon and sigmoid colon (Table 3). Resection specimens for descending colon were longer than resection specimens from the remainder of the bowel, with an average length of 29.2 cm (P = .002). Significantly more lymph nodes were recovered from cancers in the descending colon than from other sites. Notably, the number of positive lymph nodes for sigmoid cancer was significantly greater than that for cecum/ascending colon cancer (P = .03). No difference in the number of positive lymph nodes was observed between all other tumor locations.

There was no significant difference in the length of resected bowel segments among different stages of colorectal cancer. The total number of lymph nodes increased slightly with advancing stages of cancer, with 13.6, 14.8, 16.2, and 18.1 nodes associated with T1, T2, T3, and T4 tumors, respectively, but with no significant difference between the groups (P = .08). There was a strong positive correlation between average number of positive lymph nodes and advancing tumor stages (P < .001) (Table 4).

Table 5 summarizes the relationship of length of resected bowel specimen and number of lymph nodes recovered with patient sex, tumor histology, tumor grade, and surgeon stratified by specialty training. There was no difference between the sexes for average length of resected bowel specimen or total number of lymph nodes recovered. Neither were there any differences for length of resected specimen and total number of lymph nodes between the 2 surgeon groups separated by subspecialty surgery training and volume of surgery. The average resected bowel specimen was slightly longer (24.2 vs. 21.8 cm) and the number of lymph nodes was higher (17.5 vs. 15.4) in conventional adenocarcinoma than in mucinous adenocarcinoma, but with no statistical significance (P = .08). While the average length of resection specimen was similar among tumors with different degrees of differentiation, there appeared to be a slightly higher number of lymph nodes recovered from poorly differentiated carcinomas than from well-differentiated and moderately differentiated adenocarcinomas. However, no significant statistical difference was observed (P = .09).

A univariate and multivariate logistic regression analysis was performed to analyze the significance of each clinicopathologic factor, including patient age, sex, tumor histology, tumor location, depth invasion, liver metastasis, length of resected bowel specimen, and surgeon training in predicting recovery of 12 or more lymph nodes from the resection specimens (Table 6). Tumor location, bowel specimen length, and histologic subtype were significantly associated with recovery of 12 or more lymph nodes in the univariate analysis. However, in multivariate analysis, the factors that remained strong predictors of the recovery of 12 or more lymph nodes were tumor location and bowel specimen length. All other factors, including patient sex, patient age, histologic subtype, tumor grade, depth of invasion, liver metastasis, or surgeon stratified by specialty surgery training, were not significant predictive factors of the recovery of at least 12 lymph nodes from resection specimens.

To further delineate the relationship between the length of resected bowel specimen and number of lymph nodes recovered, we calculated the total number of lymph nodes recovered in 6 groups stratified by length of resected specimen. There was a linear trend toward increasing numbers of lymph nodes recovered in longer resection specimens (Figure). The average number of lymph nodes recovered was 11 for bowel resection specimens measuring less than 10 cm and increased to 18.3 for specimens longer than 30 cm.

COMMENT

The number of lymph nodes examined in resection specimens for invasive colorectal cancer has become a very important issue for the proper management of patients. It provides not only information for proper staging and triage of patients for adjuvant therapy, but is also associated with overall survival. Therefore, the absolute number of lymph nodes has been used as an indicator for quality of surgery. In this study, we investigated a number of clinicopathologic factors that may have an impact on the total number of lymph nodes recovered. Our data demonstrate that the number of lymph nodes obtained during colorectal cancer resection is most significantly associated with tumor location (right-sided vs left-sided cancer), patient age, and length of resected bowel specimen; the latter is a critical factor that had not been adequately addressed in the literature.

One of the strengths of our study is that all the data were obtained from a single tertiary medical center with a strong colorectal cancer program. The surgical procedures were performed by experienced surgeons with either colorectal oncologic specialty training or specialty interest in colorectal surgery. Pathologic examination of the colorectal specimens was performed by either pathologists' assistants or residents who were closely supervised by attending pathologists or pathologists' assistants. This fact was reflected in the relatively longer resected segments of bowel obtained (average length, 22.2 cm) and in the higher proportion of specimens (67.1%) with 12 or more lymph nodes (average number of lymph nodes, 15.7) in this study than in previously published studies. The number of lymph nodes retrieved from colorectal cancer resections at our institution is substantially higher than that reported in the National Cancer Data Base (NCDB) and in a population-based study. (17,18) Although several studies have shown that specialty training and academic hospital setting are associated with a higher number of lymph nodes recovered, (18-20) we did not observe any difference in length of bowel specimen resected and total number of lymph nodes harvested in procedures performed by general or board-certified colorectal surgeons.

[GRAPHIC OMITTED]

Several studies have shown that tumor location is significantly associated with the number of lymph nodes in resection specimens; specifically, more lymph nodes are usually obtained from right-sided colon cancers than from left-sided colon cancers, and the lowest number is from rectal cancers. (21-24) Our results are similar and show that more lymph nodes were consistently recovered from resection specimens of cecum/ascending colon and descending colon cancers, and fewer were recovered from resections of transverse colon, sigmoid colon, and rectal cancers. The reasons for this difference are still not fully understood. The literature indicates that more numerous intermediate nodes can be found in and around the ileocecal region than in the mid-, left, and sigmoid colon. This may partially explain generally higher lymph node yield in right-sided hemicolectomy specimens than in left-sided colon resection specimens. In addition, difficulties in lymph node recovery from rectal resection specimens are well known. Cawthorn et al (25) found that lymph node metastases in the supralevator part of the mesorectum may be difficult to identify by manual dissection.

The number of lymph nodes harvested is associated with the age of the patients. (18,26,27) The older the patient, the fewer the number of lymph nodes recovered. It is well known that reactive lymph nodes are enlarged and more easily identified than "normal" lymph nodes. Leibl et al (23) reported that the median lymph node yield in standardized tumor-free specimens obtained during autopsies was 13 lymph nodes, compared with 20.5 when diverticula were present and more than 30 in specimens with chronic inflammation or from patients with systemic infections, which reflects normal human immunologic response to insults. For older individuals, both the immunologic reaction to cancers and inflammatory process might be reduced. The perception that older or high-risk patients do not tolerate extensive resections as well as younger patients may potentially limit surgeons from performing a thorough procedure. This is not the case in our series (Table 2). While the average lengths of resected bowel specimens were almost identical throughout the age decades, we observed a significant decrease in the number of lymph nodes recovered beginning at 60 years of age. It is noteworthy that the percentage of sigmoid colon cancer was significantly higher for patients who were older than 60 years than for patients who were younger than 60 years (50% vs 32.8%) (S. S. Shen, unpublished data, 2008). This may explain why a patient's age was not retained as a significant factor in multivariate analysis.

One limitation of this study was the fact that accurate information regarding neoadjuvant therapy for all patients with rectal cancer was not available for evaluation. During this study period, many patients may have received neoadjuvant therapy, which has been shown to be associated with lower number of lymph nodes recovered in resection specimens. (28)

One of the important conclusions from this study is that the length of resected bowel specimen is a strong predictor of lymph nodes recovered. The location of the bowel resection may be a confounding factor, but predictive value of bowel specimen length for number of lymph nodes recovered retained significance in multivariate analysis. Similar conclusions were reported only from population based studies. (19,20) However, length of resected bowel specimen as an independent predictor of number of lymph nodes harvested had not been previously addressed. Intuitively, a longer segment of resected bowel will have more pericolonic and mesenteric lymph nodes. This is consistent with the principle that the surgeon must perform a surgical resection, including removing an adequate segment of bowel and the main lymphovascular supply to the resected segment.

In conclusion, lymph node harvest in patients with colorectal cancer is highly variable and determined by multiple factors. Adequate nodal staging is critical for the care of patients with colorectal cancer and is a shared responsibility of surgeons and pathologists. It is the responsibility of surgeons to perform adequate surgery, and it is the responsibility of pathologists to ensure that a diligent effort is made to maximize lymph node retrieval to appropriately stage colorectal cancer and treat affected patients. It is important to consider all clinicopathologic factors when using absolute number of lymph nodes as sole criterion for determining the adequacy of nodal dissection.

References

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(14.) Sobin LH, Greene FL. TNM classification: clarification of number of regional lymph nodes for pNo. Cancer. 2001;92:452.

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(16.) Greene FL, Fage DL, Fleming ID, et al. AJCC Cancer Staging Manual. 6th ed. New York, NY: Springer-Verlag; 2002:127-138.

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(19.) Johnson PM, Malatjalian D, Porter GA. Adequacy of nodal harvest in colorectal cancer: a consecutive cohort study [discussion in J Gastrointest Surg. 2002;6:889-890]. J Gastrointest Surg. 2002;6:883-888.

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(21.) Canessa CE, Badia F, Fierro S, Fiol V, Hayek G. Anatomic study of the lymph nodes of the mesorectum. Dis Colon Rectum. 2001;44:1333-1336.

(22.) Topor B, Acland R, KolodkoV, Galandiuk S. Mesorectal lymph nodes: their location and distribution within the mesorectum. Dis Colon Rectum. 2003;46: 779-785.

(23.) Leibl S, Tsybrovskyy O, Denk H. How many lymph nodes are necessary to stage early and advanced adenocarcinoma of the sigmoid colon and upper rectum? Virchows Arch. 2003;443:133-138.

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(26.) Smith JJ, Tekkis PP, Thompson MR, Stamatakis JD, for the Association of Coloproctology ofGreatBritain and Ireland.Predicting the rightnumber oflymph nodes--the ACPGBI lymph node harvest model. In: Report of the ACPGBI Bowel Cancer Study; 2004:50-58.

(27.) Bilimoria KY, Stewart AK, Palis BE, Bentrem DJ, Talamonti MS, Ko CY. Adequacy and importance of lymph node evaluation for colon cancer in the elderly. J Am Coll Surg. 2008;206:247-254.

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Steven S. Shen, Bisong X. Haupt, Jae Y. Ro, Jijiang Zhu, H. Randoph Bailey, Mary R. Schwartz,

Accepted for publication August 21, 2008.

From the Department of Pathology, The Methodist Hospital and Research Institute, Weill Medical College of Cornell University, Houston, Tex (Drs Shen and Ro); and the Departments of Pathology (Drs Haupt, Zhu, and Schwartz) and the Division of Colon and Rectal Surgery, Department of Surgery (Dr Bailey), The Methodist Hospital, Houston, Tex.

The authors have no relevant financial interest in the products or companies described in this article.

This work was presented at the College of American Pathologists Annual Meeting, San Diego, Calif, September 2006.

Reprints: Steven S. Shen, MD, PhD, Department of Pathology, M244A, The Methodist Hospital and Research Institute, Weill Medical College of Cornell University, 6565 Fannin Street, Houston, TX 77030 (e-mail: stevenshen@tmhs.org).
Table 1. Clinicopathologic Data of Patients With
Colorectal Adenocarcinoma

                                      No. (%) of Cases
Sex
  Male                                   241 (55.5)
  Female                                 193 (44.5)

Age y
  [less than or equal to]50               44 (10.1)
  >50 and [less than or equal to]60       82 (18.9)
  >60 and [less than or equal to]70      109 (25.1)
  >70 and [less than or equal to]80      117 (27.0)
  >80                                     82 (18.9)

Tumor location
  Cecum/ascending colon                  161 (37.1)
  Transverse colon                        22 (5.1)
  Descending colon                        15 (3.5)
  Sigmoid colon                          167 (38.5)
  Rectum                                  69 (15.9)

Depth of invasion
  T1                                      46 (10.6)
  T2                                     104 (24.0)
  T3                                     254 (58.5)
  T4                                      30 (6.9)

Histologic type
  NOS *                                  367 (84.6)
  Mucinous                                67 (15.4)

Histologic grade
  Well differentiated                     36 (8.3)
  Moderately differentiated              325 (74.9)
  Poorly differentiated                   73 (16.8)

Number of lymph nodes
  Mean                                  15.7
  Median                                  15
  [greater than or equal to] 12          291 (67.1)
  <12                                    143 (32.9)

Node positive
  Yes                                    206 (47.4)
  No                                     228 (52.5)

Distant metastasis
  Yes                                     33 (7.6)
  No                                     401 (92.4)

* NOS, not otherwise specified.

Table 2. Relationship of Patient Age With Bowel Specimen Length,
Number of Lymph Nodes, and Number of Positive Lymph Nodes

                              Resected Specimen
                                  Length, cm
                     No. of
Age group, y         Cases    Mean [+ or -] SD

<50                    40     21.3 [+ or -] 9.9

>50 and [less than     82     20.7 [+ or -] 7.6
or equal to] 60

>60 and [less than    109     22.6 [+ or -] 8.9
or equal to] 70

>70 and [less than    117     22.8 [+ or -] 10.9
or equal to] 80

>80                    82     22.2 [+ or -] 9.1

                     No. of Lymph Nodes

Age group, y         Mean [+ or -] SD

<50                  18.2 [+ or -] 12.6

>50 and [less than   17.8 [+ or -] 9.5
or equal to] 60

>60 and [less than   14.4 [+ or -] 8.0 ([dagger])
or equal to] 70

>70 and [less than   15.1 [+ or -] 7.2 ([dagger])
or equal to] 80

>80                  14.9 [+ or -] 7.4 ([dagger])

                     No. of Positive
                      Lymph Nodes

Age group, y         Mean [+ or -] SD

<50                  4.64 [+ or -] 9.67 *

>50 and [less than   2.84 [+ or -] 4.14
or equal to] 60

>60 and [less than   1.97 [+ or -] 3.51
or equal to] 70

>70 and [less than   1.85 [+ or -] 3.20
or equal to] 80

>80                  1.22 [+ or -] 2.66

* P = .03 compared with age >50 and [less than or equal to] 60
and P < .001 compared with age >60. ([dagger]) P = .002 compared
with age [less than or equal to] 60.

Table 3. Relationship of Tumor Location With Bowel Specimen Length,
Number of Lymph Nodes, and Number of Positive Lymph Nodes

                                 Resected Specimen
                                   Length, cm
                        No. of
Location                Cases    Mean [+ or -] SD

Cecum/ascending colon    161     23.2 [+ or -] 9.4
Transverse colon          22     20.3 [+ or -] 10.2
Descending colon          15     29.2 [+ or -] 11.8 ([dagger])
Sigmoid colon            167     20.1 [+ or -] 8.8
Rectum                    69     24.0 [+ or -] 6.5
Total                    434     22.2 [+ or -] 9.1

                                              No. of Positive
                        No. of Lymph Nodes      Lymph Nodes

Location                Mean [+ or -] SD      Mean [+ or -] SD

Cecum/ascending colon   17.8 [+ or -] 7.9 *   1.8 [+ or -] 3.6
Transverse colon        14.5 [+ or -] 7.0     2.0 [+ or -] 5.2
Descending colon        19.0 [+ or -] 12.5    2.0 [+ or -] 4.1
Sigmoid colon           14.3 [+ or -] 9.4     2.9 [+ or -] 5.6 *
Rectum                  13.7 [+ or -] 6.6     1.9 [+ or -] 3.2
Total                   15.7 [+ or -] 8.6     2.2 [+ or -] 4.5

* P < .001 and P = .001 compared with tumors from sigmoid colon
and rectum, respectively.

([dagger]) P = .002 compared with other locations.

([double dagger]) P = .03 compared with cecum/ascending colon cancer.

Table 4. Relationship of Depth of Invasion (T Stage)
With Bowel Specimen Length, Number of Lymph
Nodes, and Number of Positive Lymph Nodes

                    Resected Specimen
Depth of   No. of   Length, cm          No. of Lymph Nodes
Invasion   Cases    Mean [+ or -] SD    Mean [+ or -] SD *

T1           46     22.4 [+ or -] 8.7   13.6 [+ or -] 6.8
T2          104     22.2 [+ or -] 9.3   14.8 [+ or -] 7.2
T3          254     22.0 [+ or -] 9.1   16.2 [+ or -] 9.1
T4           30     23.2 [+ or -] 9.5   18.1 [+ or -] 10.6

Depth of   No. of Positive Lymph Nodes
Invasion   Mean [+ or -] SD ([dagger])

T1             0.2 [+ or -] 0.6
T2             0.6 [+ or -] 1.6
T3             2.9 [+ or -] 5.1
T4             4.8 [+ or -] 6.4

* P = .08 between different T-stage tumors.

([dagger]) P < .001 between different T-stage tumors.

Table 5. Relationship of 4 Study-Defined
Clinicopathologic Factors With Bowel Specimen
Length and Number of Lymph Nodes Harvested *

                       Resected Specimen         No. of
              No. of      Length, cm           Lymph Nodes
Factor        Cases    Mean [+ or -] SD     Mean [+ or -] SD

Sex
  Male         241     22.3 [+ or -] 8.8    15.7 [+ or -] 8.8
  Female       193     22.1 [+ or -] 9.4     5.7 [+ or -] 8.5

Histology
  NOS           67     24.2 [+ or -] 10.7   17.5 [+ or -] 8.7
  Mucinous     367     21.8 [+ or -] 8.7    15.4 [+ or -] 8.6

Tumor grade
  G1            36     23.3 [+ or -] 10.9   14.4 [+ or -] 9.1
  G2           325     22.1 [+ or -] 9.1    15.4 [+ or -] 8.1
  G3            73     22.0 [+ or -] 8.3    17.6 [+ or -] 10.3

Surgeon
  Group 1      182     22.1 [+ or -] 10.0   15.8 [+ or -] 8.3
  Group 2      252     22.2 [+ or -] 8.5    15.6 [+ or -] 8.9

* NOS indicates not otherwise specified; Group 1, colorectal
surgeons; and Group 2, general surgeons.

Table 6. Univariate and Multivariate Logistic Regression Analysis
of Clinicopathologic Factors for Predicting Recovery
of 12 Lymph Nodes or More From Specimens of Colorectal Resection *

                                Univariate

Factor                   RR      95% CI        P

Patient age              0.995   0.980-1.010   .48
Patient sex              1.025   0.685-1.534   .90
Histologic type          0.487   0.260-0.912   .03
Histologic grade         1.008   0.672-1.512   .97
Tumor location           0.749   0.656-0.855  <.001
Specimen length          1.035   1.010-1.060   .005
Depth of invasion (pT)   1.137   0.878-1.474   .33
Liver metastasis         1.338   0.605-2.960   .47
Surgeon                  0.880   0.586-1.323   .54

                                Multivariate

Factor                   RR      95% CI        P

Patient age              0.983   0.967-1.000    .05
Patient sex              0.918   0.600-1.404    .69
Histologic type          0.585   0.301-1.136    .11
Histologic grade         0.991   0.631-1.558    .97
Tumor location           0.706   0.606-0.822   <.001
Specimen length          1.033   1.008-1.060    .01
Depth of invasion (pT)   1.125   0.835-1.517    .44
Liver metastasis         1.111   0.467-2.642    .81
Surgeon                  1.252   0.789-1.987    .34

* RR indicates relative risk; CI, confidence interval; and
pT, pathologic stage of primary tumor.
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