Open Journal of Gastroenterology, 2013, 3, 217-222 OJGas
doi:10.4236/ojgas.2013.34036 Published Online August 2013 (http://www.scirp.org/journal/ojgas/)
The validity of predicting prognosis by the number of
lymph node metastases in node-positive colon cancer*
Kiichi Sugimoto, Masaya Kawai, Kazuhiro Takehara, Yoshihiko Tashiro, Shinya Munakata,
Kiichi Nagayasu, Koichiro Niwa, Shun Ishiyama, Hiromitsu Komiyama, Makoto Takahashi,
Yutaka Kojima, Michitoshi Goto, Yuichi Tomiki, Kazuhiro Sakamoto
Department of Coloproctological Surgery, Faculty of Medicine, Juntendo University, Tokyo, Japan
Received 22 May 2013; revised 22 June 2013; accepted 15 July 2013
Copyright © 2013 Kiichi Sugimoto et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
ABSTRACT
Background: We examined the possibility of predict-
ing prognosis by the number of lymph node metasta-
ses. Methods: Two hundred and forty-nine patients
with lymph node metastases who underwent curative
surgery for colon cancer were enrolled in this study.
We calculated cancer-specific survival according to
the number of lymph node metastases. Results: There
was a tendency toward better rates of cancer-specific
survivals among the patients with 1 LNM, compared
with those with 2 LNM (p = 0.07). When comparing
cancer-specific survival between the patients with 1, 2
- 3 and 4 or more lymph node metastases, cancer-
specific survival was well stratified (p < 0.0001). With
regard to stage classification, in the Japanese classi-
fication, there was a significant difference in cancer-
specific survival between Stages IIIa and IIIb (p <
0.0001). On the other hand, in the TNM classification,
cancer-specific survivals in Stages IIIA, IIIB and IIIC
were stratified into three groups with significant dif-
ferences (IIIA vs. IIIB; p = 0.007, IIIB vs. IIIC; p <
0.0001). Conclusion: It appeared to be valid to strat-
ify cancer-specific survival into three groups, i.e., the
patients with 1, 2 and 3 and 4 or more lymph node
metastases. This study was in favor of the TNM clas-
sification in which N category is classified by the
number of lymph node metastases.
Keywords: Colon Cancer; Lymph Node Metastasis;
Stage Classification; TNM Classification; Prognostic
Factors
1. INTRODUCTION
Colorectal cancer is a major cause of cancer death in the
United States and Japan, and its incidence is rapidly
increasing in Japan [1,2]. Several prognostic factors have
been evaluated in colorectal cancer [3-7]. Nodal involve-
ment is accepted as one of the important prognostic fac-
tors in colorectal cancer [8-10] and postoperative adju-
vant chemotherapy is recommended for node-positive
colorectal cancer [11,12]. In the United States the num-
ber of lymph node metastases (LNM) is regarded as an
important prognostic factor in node-positive colorectal
cancer and stage classification by the number of LNM
has been adopted in the TNM classification of malignant
tumors, 7th Edition [13]. In Japan, stage classification by
the distribution of LNM has been modified to that by the
number of LNM in order to also integrate with the TNM
classification in the Japanese classification of colorectal
carcinoma 2nd English Edition [14]. However, there have
been few reports regarding the validity of predicting
prognosis by the number of LNM in node-positive colon
cancer in Japan. We retrospectively examined the possi-
bility of predicting prognosis by the number of LNM and
considered the validity of stage classification in TNM
classification and Japanese classification.
2. METHODS
2.1. Patient Selection
Two hundred and forty-nine patients with LNM who
underwent curative surgery for colon cancer at our
department between January 1992 and December 2004
were enrolled in this study. We retrospectively reviewed
the database and medical records. All patients were
followed for 5 years after the operation. Cases with
multiple primary cancer, preoperative adjuvant therapy
and 11 or fewer dissected lymph nodes, and cases that
died because of non cancer-related causes were ex-
cluded from this study. The median observation period
*Conflict of interest statement: Authors have no conflict of interest.
Published Online August 2013 in SciRes. http://www.scirp.org/journal/ojgas

K. Sugimoto et al. / Open Journal of Gastroenterology 3 (2013) 217-222 218
was 8.6 years (range: 0.2 - 14.6 yeras).
2.2. Clinicopathological Analysis
We first calculated cancer-specific survival according to
the number of LNM in order to examine whether or not
stratification of the prognosis by the number of LNM is
appropriate. Secondly, clinicopathological factors, such
as age, gender (male/female), location (proximal/distal),
invasion depth (TNM classification: T1-T3/T4), differ-
entiation (well differentiated adenocarcinoma/others),
lymphatic invasion (none-mild/moderate-severe), venous
invasion (none-mild/moderate-severe), preoperative serum
CEA, the number of dissected lymph nodes, the number
of LNM and survival data were analyzed to determine
prognostic factors related to cancer-specific survival.
Finally, we considered the differences between the TNM
classification and the Japanese classification.
2.3. Pathological Examination
All specimens were examined in the following manner:
After resection of the primary tumor, the excised speci-
men was opened on the antimesenteric side by the sur-
geon. The surgeon identified the lymph nodes, isolated
them, and recorded both their number and distribution.
After formalin fixation, the specimens and lymph nodes
were examined by the pathologist.
2.4. Follow-Up Program
All patients were followed for 5 years after the opera-
tion. During the first 3 years, patients were followed
every 3 months with clinical assessment and measure-
ment of serum carcinoembryonic antigen, and every 3 - 6
months with chest X-ray and abdominal ultrasonography
or computed tomography. For the remaining 2 years, all
tests were performed every 6 months. Colonoscopy was
performed 1 year after the operation and every 2 years
for the next 4 years.
2.5. Statistical Analysis
Discrete variables were compared using Fisher’s exact
probability test and continuous variables were compared
using the Mann-Whitney U-test. Clinicopathological fac-
tors, for which there was a significant difference in the
univariate analysis, were used as covariables for the mul-
tivariate analysis. For the multivariate analysis, the Cox
proportional-hazard model was used with the Hazard
ratio as a measure of association by applying a stepwise
procedure. The survival rate was calculated using the
Kaplan-Meier method and univariate analyses were per-
formed using the log-rank test. Data were statistically
analyzed using JMP 9.0.2 software (SAS Institute Inc.,
Cary, NC, USA). Differences were considered statisti-
cally significant at p < 0.05. Values are expressed as
median (min. - max.).
3. RESULTS
3.1. The Stratification of Cancer-Specific
Survival According to the Number of Lymph
Node Metastases
Cancer-specific survival according to the number of
LNM is shown in Figure 1. Cancer-specific survival of
the patients with 5 or 7 LNM was better than those with
4 or 6 LNM. With the exception of those cases, cancer-
specific survival was worse as the number of LNM in-
creased. When comparing cancer-specific survival ac-
cording to the number of LNM, there was a tendency
toward better rates of cancer-specific survivals among
the patients with 1 LNM, compared with those with 2
LNM (p = 0.07) (Table 1). There were no significant dif-
ferences in cancer-specific survival between the patients
with 3 or more LNM. Next, we examined whether or not
stratification of the cancer-specific survival according to
the number of LNM was possible. When dividing the
number of LNM into groups (i.e., 2/3≤, 2 - 3/4≤, 2 - 4/5≤,
etc.), except for the patients with one LNM, among
whom cancer-specific survival was better, there were sig-
nificant differences in cancer-specific survival between
groups (i.e., 2 - 3/4≤, 2 - 4/5≤, 2 - 5/6≤) (p = 0.007,
Figure 1. Cancer-specific survival according to number of
lymph node metastases.

K. Sugimoto et al. / Open Journal of Gastroenterology 3 (2013) 217-222 219
p = 0.03, p = 0.02, respectively) (Table 2). Among them,
the p-value was lowest in comparison of the cancer-spe-
cific survival between the patients with 2 - 3 and 4 or
more LNM. Therefore, when comparing cancer-specific
survival between the patients with 1, 2 - 3 and 4 or
more LNM, cancer-specific survival was well stratified
(p < 0.0001) (Figure 2).
3.2. Prognostic Factors for 5-Year Survival
There were 76 patients (30.5%) in the non-survivor
group. In univariate analysis of the non-survivor group
compared with the 5-year survivor group, there were
significantly more patients with invasion depth (T4) (p =
0.0001), lymphatic invasion (moderate-severe) (p =
0.003), venous invasion (moderate-severe) (p = 0.0002)
and the number of LNM (p < 0.0001) (Table 3). With
respect to the other clinicopathological factors, there
were no significant differences between the two groups.
According to the multivariate analysis using these clini-
copathological factors, invasion depth (T4) (p = 0.004,
Odds ratio = 2.43), venous invasion (moderate-severe) (p
= 0.04, Odds ratio = 1.98) and the number of LNM (p =
0.0007, Odds ratio = 1.19) were significant independent
Figure 2. Stratification of the cancer-specific survival accord-
ing to the number of lymph node metastases.
Table 1. Differences in cancer-specific survival according to
number of lymph node metastases.
No. of lymph
node metastases No. of patients 5-year cancer specific survival (%) p-value
1 111 87.4
2 42 71.4
3 28 67.9
4 19 47.4
5 9 55.6
6 9 44.4
≥7 31 51.6
Total 249
Table 2. Stratification of the cancer-specific survival according
to the number of lymph node metastases except for the patients
with one lymph node metastasis.
No. of lymph node
metastases No. of patients 5-year cancer-specific survival (%) p-value
2 42 71.4
≥3 96 55.2
0.05
2 - 3 70 70.0
≥4 68 50.0
0.007
2 - 4 89 65.2
≥5 49 51.0
0.03
2 - 5 98 64.3
≥6 40 50.0
0.02
2 - 6 107 62.6
≥7 31 51.6
0.07
Table 3. Prognostic factors for 5-year cancer-specific survival
in univariate analysis.
Clinico-
pathological
factor Category 5-year
survivor group
(n = 173)
Non-survivor
group
(n = 76) p-value
Age 64 (30 - 90) 66.5 (44 - 89)0.08
Male 95 44
Gender
Female 78 32
0.68
Proximal66 26
Location
Distal 107 50
0.57
T1 - T3 122 33
Invasion depth
T4 51 43
0.0001
Well diff.
adenoca. 79 27
Differentiation
Others 94 49
0.16
None-mild68 15
Lymphatic
invasion Moderate
severe 173 61
0.003
None - mild113 30
Venous
invasion Moderate
severe 60 46
0.0002
Preoperative
serum CEA
(μg/dl)
3.8
(0.6 - 1034)
6.8
(1.1 - 44.6)0.09
No. of dissected
lymph nodes 19 (3 - 74)
17
(6 - 108) 0.21
No. of
lymphnode
metastases
1
(1 = 17)
3
(1 - 19) <0.0001
Present 138 56
Postoperative
adjuvant
chemotherapy Absent 35 20
0.32
0.07
0.69
0.16
0.70
0.50
0.80

K. Sugimoto et al. / Open Journal of Gastroenterology 3 (2013) 217-222 220
prognostic factors (Table 4).
3.3. Comparisons between the TNM
Classification and the Japanese
Classification Systems
Each of the classification systems is shown in Figure 3.
In the Japanese classification, N1 is defined as metastasis
in 1 to 3 pericolic/perirectal or intermediate lymph nodes;
N2 is defined as metastasis in 4 to more pericolic/peri-
rectal or intermediate lymph nodes, and N3 is defined as
metastasis in the main or lateral lymph nodes. Moreover,
N1 is defined as Stage IIIa, and N2 and N3 are defined as
Stage IIIb independent of invasion depth. On the other
hand, in the TNM classification, N1a is defined as meta-
stasis in one regional lymph node; N1b is defined as
metastasis in 2 - 3 regional lymph nodes; N2a is defined
as metastasis in 4 - 6 regional lymph nodes, and N2b is
defined as metastasis in 7 or more regional lymph nodes.
Moreover, by combining these N categories with inva-
sion depth, the patients with LNM are further divided
into three groups, i.e., IIIA, IIIB and IIIC. Cancer-spe-
cific survival in each N category is shown in Figure 4
and survival for each stage classification is presented in
Figure 5. With respect to the classifications by N cate-
gory, in the Japanese classification, cancer-specific sur-
Figure 3. Comparisons between the TNM classification and the
Japanese classification systems. (a) Japanese classification of
Coloretal Carcinoma. 2nd English Edition; (b) TNM classifica-
tion of Malignant Tumours, 7th Editon.
Table 4. Prognostic factors for 5-year cancer-specific survival
in multivariate analysis.
Clinicopathological
factors p-valueOdds ratio 95% confidence interval
Invasion depth (T4) 0.004 2.43 1.33 - 4.43
Lymphatic invasion
(moderate - severe) 0.37 1.40 0.67 - 2.95
Venous invasion
(moderate - severe) 0.04 1.98 1.03 - 3.80
No. of lymph node
metastases 0.0007 1.19 1.07 - 1.31
Figure 4. Cancer-specific survival in each N category. (a) Ja-
panese classification of Coloretal Carcinoma. 2nd English Edi-
tion; (b) TNM classification of Malignant Tumours, 7th Editon.
Figure 5. Cancer-specific survival for each stage classification.
(a) Japanese classification of Coloretal Carcinoma, 2nd English
Edition; (b) TNM classification of Malignant Tumours, 7th
Edition.
vival in N1 was significantly better than that in N2 or N3
(p < 0.0001). However, cancer-specific survival in N2
was nearly equal to that in N3 and there was no sig-
nificant difference between N2 and N3 (p = 0.79). On the
other hand, in the TNM classification, cancer-specific
survival in N1a was significantly better than that in N1b
(p = 0.02), and that in N1b was significantly better than
that in N2a (p = 0.02). However, there was no significant
difference in cancer-specific survival between N2a and
N2b (p = 0.76). With regard to stage classification, in the
Japanese classification, there was a significant difference
in cancer-specific survival between Stages IIIa and IIIb
(p < 0.0001). On the other hand, in the TNM classi-
fication, cancer-specific survival in Stages IIIA, IIIB and
IIIC were stratified into three groups with significant
differences (IIIA vs. IIIB; p = 0.007, IIIB vs. IIIC; p <
0.0001). The 5-year cancer-specific survival in Stage
IIIA was 96.4%, and was considered to be extremely
good.

K. Sugimoto et al. / Open Journal of Gastroenterology 3 (2013) 217-222 221
4. DISCUSSION
LNM is an important determinant of prognosis in pa-
tients with colorectal cancer, as acknowledged in both
the Japanese and TNM classification systems. In the
TNM classification, the N category is classified by the
number of LNM. The validity of the stage classification,
which consists of the number of LNM and invasion
depth, was confirmed by inspection of a database of
more than 100,000 colorectal cancer patients [15]. How-
ever, because this inspection was based on surgical out-
comes in the United States, it was not clear whether or
not the stage classification would be useful in Japan.
Moreover, in the Japanese classification, the conven-
tional classification by the distribution of LNM was mo-
dified to take into account the number of LNM, in order
to integrate with TNM classification. Therefore, we in-
vestigated the validity of predicting prognosis based on
the number of LNM in node-positive colon cancer.
In this study, cancer-specific survival decreased as the
number of LNM increased. There was a tendency toward
better rates of cancer-specific survivals among the pa-
tients with 1 LNM, compared with those with 2 LNM.
This was consistent between classification systems, in
that the 1 LNM would be classified into N1a in TNM
classification and reflected that the prognoses among the
patients with 1 LNM were good. Because the prognoses
of the patients with 1 LNM were good, we examined the
stratification of cancer-specific survival according to the
number of LNM among the patients with 2 or more
LNM. Consequently, the stratification of cancer-specific
survival between two groups, i.e., the patients with of 2
and 3 LNM and those with 4 or more was the most ideal
for stage classification. This result was consistent with
the TNM classification, in which the patients with 4 or
more LNM were classified into N2. Therefore, it appears
to be valid that cancer-specific survival should be stra-
tified into three groups, i.e., the patients with 1 LNM,
those with 2 and 3 and those with 4 or more. On the
other hand, cancer-specific survival among the patients
with 7 or more LNM was better than those with 4 or 6. It
would appear that sufficient investigation on the patients
with 4 or 5 or 6 LNM was not possible, due to the small
number of such patients; this would appear to be a limi-
tation of conducting this type of investigation in a single
institution.
Based upon the multivariate analysis, invasion depth
(T4), venous invasion and the number of LNM were
significant, independent prognostic factors. Some authors
have reported that the number of LNM was an indepen-
dent prognostic factor in multivariate analysis [16-18].
Invasion depth and the number of LNM were also inde-
pendent prognostic factors in this study. Therefore, this
result was consistent in that the stage classifications, i.e.,
the Japanese classification and the TNM classification,
consider invasion depth and the number of LNM.
In comparison of the Japanese and TNM classification
systems, the TNM classification appears to be more com-
plicated than the Japanese classification. The reason is
because the grades of invasion depth and the number of
LNM are subdivided in the TNM classification. Conse-
quently, there are many substages and the intervals be-
tween cancer-specific survival in each stage are becom-
ing narrower. Because overlaps and inversions are often
recognized in cancer-specific survival, predictions of
prognosis that are indicated by each stage are vague [19].
On the other hand, the patients in T1-T2N1 and T1N2a
are classified into Stage IIIA in the TNM classification,
and the patients in Stage IIIA have a good prognosis
[12,20]. In other words, these patients with a good prog-
nosis can be distinguished from the patients in Stage III
who have a poor prognosis by using the TNM classifica-
tion. When considering the indication and protocol of
postoperative adjuvant chemotherapy in Stage III, it ap-
pears necessary to distinguish the patients in Stage IIIA
from those in Stage III. In this study, the 5-year cancer-
specific survival was 96.4% and was extremely good. On
the other hand, the stage classification by using the num-
ber of LNM was introduced in order to integrate with the
TNM classification when revising the Japanese classifi-
cation. However, the concept of distribution of LNM was
left in category N3 of the Japanese classification. In
other words, metastasis in the main or lateral lymph
nodes is defined as N3 regardless of the number of LNM.
This is because N category in the Japanese classification
is designed to indicate the extent of lymph node dis-
section during the operation, as well as predictions of
prognosis. Therefore, in this point the Japanese classifi-
cation is quite distinct from the TNM classification. In
this study, there was no significant difference between
category N2 and N3, and this study was in favor of the
TNM classification in which the N category is classified
by the number of LNM. However, there were only
eighteen patients in N3 in this study and further research
is needed to evaluate this properly. Indeed, Kobayashi et
al. [21] reported that the distribution and the number of
LNM represented an important index of prognosis in pa-
tients with colon cancer. In this study, those data were
examined in a single institute, and only a small number
of patients were enrolled in this study. Therefore, further
investigation using a greater sample population through-
out Japan will be necessary.
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