ORIGINAL ARTICLE
Stage Migration Effect on Survival in Gastric Cancer Surgery
With Extended Lymphadenectomy
The Reappraisal of Positive Lymph Node Ratio as a Proper N-Staging
Seong-Ho Kong, MD, MS,
∗
Hyuk-Joon Lee, MD, PhD,
∗
† Hye Seong Ahn, MD, MS,
∗
Jong-Won Kim, MD,
∗
Woo Ho Kim, MD, PhD,†‡ Kuhn Uk Lee, MD, PhD, FACS,
∗
and Han-Kwang Yang, MD, PhD, FACS
∗
†
Objective: The purpose of this study is to analyze the relationship between
the number of examined lymph nodes (NexLN) and survival in gastric cancer
and to determine whether the metastatic/examined lymph node ratio (LN ratio)
system can compensate for the shortcomings of the UICC/AJCC staging.
Methods: Prospective data of 8949 primary T1-T4a gastric cancer patients
who underwent curative surgery were reviewed. The patients were stratified
by T-stage and grouped according to NexLN; 1 to 14 exLN denoted the first
group and every subsequent 10 LNs thereafter. Numbers of LN and 5-year
survival rates were analyzed according to NexLN. “The NR-staging system”
was generated using 0.2 and 0.5 as the cut-off values of LN ratio and then
compared with UICC/AJCC stages.
Results: The proportion of advanced N-stage increased with NexLN. Survival
and the LN ratio were constant regardless of NexLN when combining all N0-
N3b patients, however, T2/3 and T4a patients showed an increasing tendency
toward survival in N1/2 and N3a as NexLN increased, mainly due to a stage
migration effect. The LN ratio system showed better patterns of distribution
of the LN stage and survival graph. The power of the differential staging of
the LN ratio system was fortified with higher NexLN.
Conclusion: The relationship between NexLN and survival is probably af-
fected by stage migration in a high-volume gastric cancer center. The LN ratio
system could be a better option to compensate for this effect, and the value of
the prognosis prediction in this system increases with a higher NexLN.
(Ann Surg 2012;255:50–58)
L
ymph node (LN) dissection is crucial in gastric cancer surgery
for treatment and staging. However, the extent of LN dissection
represented by D0, D1, D2, and D3 in the Japanese classification
is very complicated and has variations in each category.
1
The num-
ber of the examined LN (exLN) has instead been used as a simpler
indicator of the extent of LN dissection. Smith et al
2
reported a ther-
apeutic benefit of a high number of exLN using SEER data, and the
UICC/AJCCTNM classification required a minimum of 15 exLN for
adequate N staging.
3
Studies using the number of exLN as an indica-
tor of the extent of LN dissection have been performed in breast and
colon cancer.
4–8
In general, Eastern doctors believe in the therapeutic benefits
of extended LN dissection and try to obtain as many LN as possible
From the
*
Department of Surgery; †Cancer Research Institute; and ‡Department
of Pathology, Seoul National University College of Medicine, Seoul, Korea.
Disclosure: We have no commercial sponsorship for this study. All the authors of
this study including Seong-Ho Kong, Hyuk-Joon Lee, Hye Seong Ahn, Jong-
Won Kim, Woo Ho Kim, Kuhn Uk Lee and Han-Kwang Yang do not have any
financial interest or conflict with any industries or parties.
Reprints: Hyuk-Joon Lee, MD, PhD, Department of Surgery and Cancer Research
Institute Seoul National University College of Medicine, Seoul, Korea, 101
Daehang-Ro, Jongno-Gu, Seoul 110-744, Korea. E-mail: appe98@snu.ac.kr.
Copyright C 2011 by Lippincott Williams & Wilkins
ISSN: 0003-4932/11/25501-0050
DOI: 10.1097/SLA.0b013e31821d4d75
during surgery.
9,10
However, many Western doctors regard the num-
ber of metastatic LN simply as an index of the tumor burden and
instead highlight the negative effects of extended LN dissection.
11,12
Too many exLN are also believed to produce a significant stage
migration,
13
so it tends to be only small number of LNs are examined
in Western institutes.
2,14,15
However, it is still uncertain whether a
large number of exLN contributes to stage migration or rather to an
accurate assessment of the LN metastatic status; the optimal number
of exLN that provides a survival benefit and/or accurate staging is
also unknown.
On the other hand, the large proportion of patients with poor
survival rates and less than 15 exLN suggests that the ratio of the
number of metastasized LN to the number of exLN (LN ratio) should
be used in Western countries.
14–18
However, the LN ratio system
has not been universally accepted, especially by Eastern institutions
in which most cases have sufficient number of exLN for the present
staging system. A few studies have described the usefulness of the LN
ratio system in Korea and Japan,
19,20
and about 13% of the operations
in Japan were reported to have less than 15 exLN.
21
It is worthwhile
to validate the value of the LN ratio for the patients with sufficient
number of exLN in Eastern institutions if the survival rate is greatly
affected by the number of exLN.
The purpose of this study was to analyze the effect of the
number of exLN on survival in gastric cancer patients in an Eastern
high-volume gastric cancer center. The LN ratio system was also val-
idated regarding the necessity and the appropriateness of LN staging
compared with UICC/AJCC staging for the patients with high-yield
exLN.
PATIENTS AND METHODS
A prospectively collected database of 10,492 gastric cancer
patients who underwent gastric resection with curative intent at the
Seoul National University Hospital (SNUH) from 1991 to 2006 was
reviewed. Cases with the following characteristics were excluded:
recurrent cancer, residual stomach cancer, concurrent malignancy in
other organs, preoperative chemotherapy, R1 or R2 resection, direct
invasion of adjacent organs and missing exLN data. In total, 8949
patients were selected (Fig. 1).
For the overall survival, the 2007 update of the database of
the National Statistical Office of Korea, which records all deaths of
Korean people, was accessed.
The distribution of the number of patients was shown in
Figure 2 when grouped according to every 5 exLN. To avoid small
numbers in each group, the first group comprised patients with 1 to
14 exLN and the other groups were composed of every subsequent
10 exLN. The extent of LN dissection was mainly planned by pre-
operative assessment of the depth of the tumor to form the basis of
the stratification as follows: mucosa and submucosa, muscularis pro-
pria and subserosa, and serosa infiltration. These correspond to T1,
T2/3 and T4a in the 7th edition of the UICC/AJCC staging man-
ual, respectively.
22
The standard surgical strategy employed at the
Copyright © 2011 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
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