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Objective: In Korea and Japan, early gastric cancer (EGC) accounts for >50% of all gastric cancers. Here, we propose recommendations for the
optimal distance from the tumor to the resection margins when evaluating EGC.
Summary of Background Data: There are very few guidelines regarding the distance from the EGC tumor to the resection margins.
Methods: We evaluated 2,081 patients who underwent gastrectomy for EGC between January 1989 and May 2000. We subdivided tumors according
to the distance from the proximal margin: 1, >1, 10, >10, 30, or >30 mm.
Results: Three of ve patients demonstrating distances 1 mm between the tumor and gross proximal margin were microscopically positive. No
patients with gross proximal margins >1, 10, >10, or 30 mm were microscopically positive. There were no statistical differences in rates of
microscopically positive margin, reresection, or reoperation between groups (P > 0.05). In addition, there were statistical differences in terms of
tumor recurrence and diseaserelated death between groups (P > 0.05).
Conclusions: When the resection margins are clear, we propose that margins >1 mm are adequate for EGC gastrectomy.
INTRODUCTION
Early gastric cancer (EGC) is dened by the Japanese Society of
Gastroenterological Endoscopy as conned to either the mucosa or
submucosa, irrespective of lymph node metastasis [1]. In Korea and
Japan, >50% of all gastric cancers are EGC [2,3]. However, there
are very few published guidelines on the resection margins for EGC.
Based on a Medline search, only two articles recommend resection
margins [4,5]. Bozzetti et al. evaluated 343 patients with gastric cancer
(including advanced cancer), specically referencing the distance from
the outline of the grossly assessed tumor and other macroscopic and
microscopic features. They reported that proximal and distal inltration
distances >3 cm did not occur in lesions conned to the mucosa,
submucosa, or muscularis [5]. However, that study was reported
30 years ago and may not accurately reect gastric cancer today.
According to the 2010 Japanese gastric cancer treatment guidelines
(version 3), gross resection margins 2 cm should be obtained for T1
tumors [4]. However, these guidelines do not cite any clinical studies,
making it difcult to assess reliability.
In our current study, we evaluate the incidence of positive resection
margins on microscopy and tumor recurrence, taking into account the
gross distance from the tumor to the resection margins. The purpose of
this study was to recommend the appropriate gross distances from the
tumor to the resection margins in EGC patients.
*Correspondence to: Correspondence to: Byung Sik Kim, MD, PhD, 3881,
Pungnap 2 dong, SongpaGu, Seoul 138736, Korea. Fax: 8224749027.
Email: bskim@amc.seoul.kr
Received 10 May 2013; Accepted 10 October 2013
DOI 10.1002/jso.23483
Published online 19 November 2013 in Wiley Online Library
(wileyonlinelibrary.com).
199
RESULTS
No.
2,081
Percent
100
1,374
707
66.0
34.0
1,893
188
91.0
9.0
1,306
634
141
2,081
2,081
62.8
30.5
6.8
100
100
1,039
1,042
49.9
50.1
1,744
120
217
83.8
5.8
10.4
1,077
1,024
51.8
48.2
1,827
254
87.8
12.2
1,884
197
90.5
9.5
1,983
98
95.3
4.7
2,010
71
96.6
3.4
Mean SD
54.9 11.5
30.3 18.8
52.3 27.5
DISCUSSION
The negative effect of positive resection margin on patient survival
has been the subject of many studies [814]. Most such reports describe
a positive resection margin as a negative prognostic factor in patients
with EGC with or without lymph node metastasis [810,13,14].
However, a positive resection margin is not a prognostic factor in
patients with aggressivestage gastric cancer or lymph node
metastasis [8,11,14,15]. Therefore, multiple operations are required
by patients with nonaggressive gastric cancer in order to obtain
microscopically negative resection margins [811,13]. Sun et al. [15]
reported that patients with advanced cancer are more likely to die of
carcinomatosis or disseminated disease than anastomotic recurrence.
Sano and Mudan [11] recommends patients with >N3 nodal
involvement should not undergo multiple operations in order to
obtain microscopically negative margins.
Cho et al. [8] attributed their low rate of positive margins (98% R0
rate; determined using microscopy) to surgical expertise, preoperative
endoscopic assessment, and the routine examination of frozen sections.
In our present study, ve patients (0.23%) demonstrated microscopically
positive resection margins. However, frozen sections, which
demonstrate higher accuracy, were not used to assess two patients.
Cho et al. and the Japanese gastric cancer treatment guidelines
recommend preoperatively marking the tumor border using clips
when the tumor border is unclear; according to their biopsy results, this
helps determine the best resection line [4,15]. In fact, it is difcult to
identify tumor lesions through a small opening in the stomach during
operations when the tumor is small with an unclear border. In two of ve
patients with microscopic residual tumors, the operator did not identify a
denite tumor lesion during surgery. These two tumor lesions were
located in the remnant stomach, and total gastrectomies were
subsequently performed on these two patients. If these two patients
had received preoperative endoscopic evaluation with clipping at the
proximal border, a negative resection margin would have been obtained
and additional gastrectomies would have been avoided.
There are very few denitive guidelines in the clinical literature that
recommend distances from the tumor to the resection margin. Of 48
patients who had gross distances 10 mm to the proximal resection
margin, we identied three patients with microscopically positive
resection margins. These three patients underwent multiple resections
TABLE II. Clinicopathologic Characteristics and Outcomes According to Gross Distance From the Proximal Resection Margin
Distance from proximal resection margin (mm)
Characteristics
Age (years)
Sex
Male
Female
Depth of invasion
Mucosa
Submucosa
Macroscopic finding
Superficial
Protruded
Excavated
Retrieved lymph nodes (no.)
Lymph node metastasis
No
Yes
Microscopically positive margin
No
Yes
Reresection or reoperation
No
Yes
Tumor recurrence, n (%)
No
Yes
Diseaserelated death, n (%)
>30 (n 1,533)
Pvalue
53.7 14.3
53.5 12.1
55.4 11.2
NS
NS
28
15
324
176
1018
515
18
25
253
247
764
769
39
1
3
24.3 12.1
409
33
58
25.3 13.2
1291
86
156
24.4 12.5
36
7
45
56
1343
190
43
0
499
1
1632
1
43
0
499
1
1632
1
42
1 (2.3%)
2 (4.6%)
469
30 (6%)
26 (5.2%)
1467
67 (4.4%)
57 (3.7%)
NS
NS
NS
NS
NS
NS
NSa
NSa
Gross findings
Superficial flat
Superficial Elevated
Superficial flat
Superficial flat
Superficial flat
Yes
No
Yes
No
Yes
No
No
Yes
No
Yes
(180)
(185)
(180)
(157)
(157)
f/u, followup.
Fig. 1. Tumor recurrence and diseaserelated survival curves determined using the KaplanMeier method. There are no signicant differences
between the resection margin subgroups (P > 0.05). A: >1 and 10 mm. B: >10 and 30 mm. C: >30 mm.
Journal of Surgical Oncology
201
30
40
1
1
1
Gross findings
Superficial depressed
Superficial flat
Superficial depressed
Superficial flat
Superficial flat
Yes
Yes
Yes
Yes
No
No
No
No
No
No
(187)
(186)
(180)
(180)
(157)
f/u, followup.
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