Yonago Acta medica 2000;43:73–80

Clinicopathological Aspects of Gastric Carcinoma in the Remnant
StomachMasahide Ikeguchi, Shin-ichi Oka and Michio Maeta*
First Department of Surgery and *Department of Fundamental Nursing, Faculty of Medicine,
Tottori University, Yonago 683-0826, JapanThe clinicopathological differences between remnant gastric carcinoma (RGC) afterpartial gastrectomy for benign disease (RGC-BD) and RGC after partial gastrectomy
for gastric carcinoma (RGC-GC) were evaluated. The incidences of developing gastriccarcinomas in patients more than 10 years after partial gastrectomy for benign diseaseor for gastric carcinoma were compared with those of developing gastric carcinomas inpatients with colorectal carcinoma who were determined to have no malignant diseasein the stomach preoperatively. Next, we analyzed the clinicopathological differencesamong RGC-BD, RGC-GC and primary gastric carcinoma (PGC) in the upper third of
the stomach. RGC-BD was detected in 8 of 1,187 (0.7%) patients and RGC-GC was
detected in 19 of 764 (2.5%) patients. Among the controls, 7 of 226 (3.1%) patientsdeveloped gastric carcinoma. The estimated risk of developing of RGC-BD and RGCGC were 0.12 and 0.798. No difference was found among 18 patients with RGC-BD, 16
patients with RGC-GC and 229 patients with PGC in terms of patient age, histologic
type, tumor size and distribution of tumor stage. The 5-year survival rate for patientswith PGC (55%) was not different from that for patients with RGC-BD (43%) or thatfor patients with RGC-GC (65%). However, the interval between initial operation anddetection of RGCs was longer in RGC-BD than in RGC-GC (P = 0.004), and RGCs
were more frequently detected at the site of anastomosis in patients with RGC-BD (50%)
than in patients with RGC-GC (19%, P = 0.057). The incidence of developing RGCs
after partial gastrectomy for benign and malignant diseases was low. The histologic
type of tumors and tumor stages of RGC-GC were not different from those of RGCBD; however, RGC-GC developed within a short time and most lesions were at sites
remote from the anastomosis. These findings indicate that carcinogenesis of RGC-GC
appears to be different from that of RGC-BD.
Key words: partial gastrectomy for benign disease; partial gastrectomy for gastric carcinoma;
primary gastric carcinoma in the upper third of the stomach; prognosis; remnant gastric carcinoma

Carcinomas developing in the remnant stomach
after partial gastrectomy for benign gastroduodenal disease, such as gastric ulcer or duodenal
ulcer, have been intensively investigated inWestern countries (Kivilaakso et al., 1977;
Northfield and Hall, 1990). However, little data
exists on the group of patients who undergo apartial gastric resection for gastric carcinoma,
later developing the second primary lesion in

the gastric remnant. As a result of the increasing number of patients who have undergone
gastrectomy for early gastric cancer in Japan,
the incidence of developing second primary
gastric cancer in the remnant stomach has
increased (Furukawa et al., 1993; Isozaki et al.,1998). However, the clinicopathological difference between the 2 types of gastric carcinomas
which developed in the remnant stomach (after

Abbreviations: B-I, Billroth I; B-II, Billroth II; PGC, primary gastric carcinoma; RGC, remnant gastric carcinoma;
RGC-BD, RGC after partial gastrectomy for benign disease; RGC-GC, RGC after partial gastrectomy for gastriccarcinoma73

M. Ikeguchi et al.

tients who underwent partial gastrectomy for
benign diseases was 282 months (range: 0–480
months) and that of the 1,497 patients who
underwent partial gastrectomy for gastriccarcinoma was 144 months (range: 0–469
months). The follow-up records of patientswere obtained from our hospital and from affiliated hospitals. For the controls, we investigated
the incidence of occurrence of gastric carcinoma in 516 patients (297 males, 219 females;mean age, 60 years; age range, 22–91 years) withcolorectal carcinoma who underwent colorectal
resection between 1960 and 1985 in our
hospital. These 516 patients were confirmed tohave no gastric carcinomas in the stomach prior
to colorectal operation by the upper barium gastrointestinal series or by the endoscopic studies.
They were followed up at our hospital till theend of 1999. The mean follow-up period ofthese 516 patients was 121 months (range: 0–473 months).
Between 1960 and 1993, 23 patients with
RGC after partial gastrectomy for benign disease (RGC-BD) and 37 patients with RGC afterpartial gastrectomy for gastric carcinomas(RGC-GC) were treated in our hospital. In the
23 patients with RGC-BD, the first gastrectomies for 6 patients were performed in our hospital and those for the remaining 17 patients weredone in other hospitals. In the 37 patients with
RGC-GC, the first gastrectomies for 18 patientswere performed in our hospital and those for theremaining 19 patients were done in other hospitals. In order to analyze the clinicopathologicaldifferences between RGC-BD and RGC-GC,
we excluded 26 patients (RGC-BD: 5 patientsand RGC-GC: 21 patients) whose interval period between the initial gastrectomy and the detection of carcinoma in the remnant stomach
was less than 10 years from our study; we could
not negate the possibility that some cancer
could have already developed in the upper thirdof the stomach at the time of distal partial
gastrectomy for benign disease or for malignant
disease, and was overlooked at the time of theinitial operation, nor could we negate the possibility of cancer recurrence in the remnant
stomach after distal partial gastrectomy for gastric carcinoma. Kidokoro et al. (1985) reported

partial gastrectomy for benign disease and afterpartial gastrectomy for gastric carcinoma) has
not been well discussed.
In this study, we designed 2 studies to determine the difference between these 2 types ofgastric carcinomas in the remnant stomach(remnant gastric carcinoma, RGC). First, wefollowed patients who had undergone distal
partial gastrectomy for benign disease or for
gastric carcinoma at our hospital, and compared
the incidences of developing gastric carcinomas
in the remnant stomachs. Next, we analyzed theclinicopathological differences between the 2types of RGCs gastrectomized in our hospital.
Also, we compared the clinicopathological dataof patients with RGC with that of patients withprimary gastric carcinoma (PGC) whichdeveloped in the upper third of the stomach.

Materials and Methods

Study design
In order to analyze the incidence of developing
gastric carcinoma in the remnant stomach, we
studied 2,880 patients (2,045 males, 835 females; mean age, 53.9 years; age ranges, 15–88
years) who underwent distal partial gastrectomy between 1960 and 1985 in our hospital.
Billroth I (B-I) reconstruction was performed in
1,717 patients and Billroth II (B-II) reconstruction was performed in 1,163 patients. Distal
partial gastrectomy was performed for benign
disease in 1,383 patients (1,072 males, 311 females; mean age, 49.6 years; age range, 15–86
years). Benign gastroduodenal diseases in
1,383 patients included gastric ulcer (839), duodenal ulcer (273), polyp (150), gastritis (99) andbenign submucosal tumor (22). Distal partial
gastrectomy was performed for gastric carcinoma in 1,497 patients (973 males, 524 females;mean age, 58 years; age range, 21–88 years).
Tumor stages for these patients included Stages
IA (498), IB (222), II (249), IIIA (204), IIIB
(155) and IV (169). These 2,880 patients were
followed till the end of 1999. The mean followup period was 210 months (range: 0–480 months).
The mean follow-up period of the 1,383 pa74

Gastric carcinoma in the remnant stomachthat the recurrence of gastric carcinoma usuallyoccurred within 10 years regardless of the initial stage of disease. To eliminate these possibilities, an interval of more than 10 years is required between the initial partial gastrectomy
and the detection of carcinoma in the remnant
stomach (Takeda et al., 1992). Thus, RGCs
(RGC-BD: 18 patients and RGC-GC: 16 patients) found after more than 10 years from initial gastrectomy are likely to represent true newneoplasms. As a control group for RGC, 299
patients with PGC located in the upper third of
the stomach who underwent gastrectomy
between 1960 and 1993 were investigated.

rected survival rates were used; that is, only
deaths caused by gastric carcinoma were regarded as outcome events, and all other deaths
were considered censored events. Differences
between survival distributions were tested forstatistical significance by log rank analysis. All
statistical analyses were performed using the
StatView-5.0 software package for Macintosh(Abacus Concepts Inc., Berkeley, CA). P values
less than 0.05 were considered to be statisticallysignificant.

Clinicopathological and statistical analysis

The incidence of developing gastric carcinoma in the remnant stomach

Clinicopathological factors were determined inaccordance with criteria from the Japanese Research Society for Gastric Cancer (1999). Histological classifications of tumors followed thecriteria established by Laurén (1965). The chisquare test and Fisher’s exact probability test
were used to compare the distribution of individual variables among the groups. Differencesin the numerical data (patient age and tumorsize) among the groups were evaluated by the
Mann-Whitney U test or by the Kruskal-Wallis
test. The survival distributions were estimatedusing the method of Kaplan and Meier. Cor-In the 2,880 patients who underwent distal partial gastrectomy between 1960 and 1985, 36 patients (RGC-BD: 8 patients and RGC-GC: 28
patients) developed gastric carcinoma in theirremnant stomach by the end of 1999. The intervals between initial partial gastrectomy and detection of RGC for these 36 patients are shownin Table 1. The mean interval between initial
operation and the detection of RGC of the 8 patients with RGC-BD was 178 months (125–228
months) and that of the 28 patients with RGCGC was 142 months (22–271 months). Of the2,880 patients, 1,951 patients (1,187 patientsfor benign diseases and 764 patients for gastriccarcinomas) survived more than 10 years afterpartial gastrectomy. Newly developed gastriccarcinomas in the remnant stomach more than
10 years after initial operation were detected in
8 of 1,187 (0.7%) patients for benign diseases
and in 19 of 764 (2.5%) patients for gastric carcinomas. Among the 516 colorectal carcinoma
patients (control patients), 226 patients were
followed up more than 10 years after surgery
and 7 patients (3.1%) were found to have gastric carcinoma. The details of the incidence ofdeveloping RGCs after partial gastrectomy are
shown in Table 2. In our case-control study,
estimated risks (odds ratios) of the developmentof RGCs after partial gastrectomy for benign
diseases and for gastric carcinomas were low(0.212 and 0.798, Table 2).

Results

Table 1. The interval (in years) between
primary operation and detection of RGC in
36 patients
Year after
gastric resection

Number of patients with
RGC-BD
RGC-GC

< 4
0
5
5 – 9
0
4
10 – 144
11
15 – 19
4
5
20 ≤
0
3
Total
8
28
RGC, remnant gastric carcinoma; RGC-BD, RGC
detected after distal partial gastrectomy for benign
gastroduodenal disease; RGC-GC, RGC detected
after distal partial gastrectomy for gastric carcinoma.

75

M. Ikeguchi et al.

Table 2. The incidence of developing gastric carcinoma in the remnant stomach more than
10 years after partial gastrectomy
Initial operation for

Total numberof patients

Number of patients†(%)

Odds ratio[95% confidence limit]

Benign gastroduodenal disease
Total
1187
8 (0.8)*0.212 [0.083–0.539]
Operative procedure
Billroth I
902
7 (0.8)****
Billroth II285
1 (0.4)*****
Gastric carcinoma
Total
764
19 (2.5)**
0.798 [0.332–1.919]
Operative procedure
Billroth I
469
12 (2.6)******
Billroth II295
7 (2.4)*******
Control group226
7 (3.1)***
1.00† Patients with newly developed gastric carcinoma in the remnant stomach.
Control group: patients with colorectal carcinoma who were followed up for more than 10 years aftercolorectal operation.
Statistically significant differences were observed between * and ** (P = 0.001) and between * and *** (P= 0.001).
No significant differences were detected between ** and *** (P = 0.614), between **** and ***** (P =0.444) or between ****** and ******* (P = 0.873).

(total gastrectomy: 12 and proximal gastrectomy: 6). The postoperative mortality rates of the
3 groups were not significantly different (Table
3). Among patients who underwent resection of
the stomach, 8 patients with RGC-BD, 4 patients with RGC-GC and 107 patients with PGC
had died from gastric carcinoma by the end of
1999. The 5-year survival rate for the 299
patients with PGC was 55%, while that for the
15 patients with RGC-BD was 43%, and that forthe 13 patients with RGC-GC was 65%, asestimated by the Kaplan-Meier method. No
statistically significant difference was foundamong the 3 survival curves by the log rank test
(P = 0.548, Fig. 1).

Clinicopathological differences between
RGCs and PGC in the upper third of thestomachClinicopathological findings of 18 patients with
RGC-BD, 16 patients with RGC-GC and 299
patients with PGC are shown in Table 3. No statistically significant differences were observed
among the 3 groups (as assessed in terms ofpatient age, histologic type, tumor size and distribution of histologic stage). Remnant gastrectomy was performed for 28 patients (RGC-BD:
15 and RGC-GC: 13). Because of distantmetastases or the degree of advancement ofgastric carcinomas, gastrectomy could not be
performed in 6 patients with RGC (RGC-BD: 3
and RGC-GC: 3). The resectability rate of
RGC-BD was 83% and that of RGC-GC was
81%. Partial remnant gastrectomy was performedfor 2 patients and total remnant gastrectomy
was done for the remaining 26 patients with
RGC. In the 299 patients with PGC, total gastrectomy was performed for 173, and proximal
gastrectomy for the remaining 126 patients.
One patient with RGC-BD and 18 patients with
PGC died from postoperative complications

Pathological differences between RGCBD and RGC-GC
The initial operative procedure and histologic
type of tumor of patients with RGC-BD were
not different from those of patients with RGCGC. However, the interval between the initial
operation and detection of RGCs was longer in
RGC-BD than in RGC-GC (P = 0.004). According to our classification of the location of
RGCs (Ikeguchi et al., 1994), RGCs were more
76

Gastric carcinoma in the remnant stomach

Table 3. Clinicopathological differences among RGC-BD, RGC-GC and PGC
RGC-BD[18]

RGC-GC
[16]

PGC
[299]

P

Age (mean, year)
63.7
64.3
59.4
0.098
GenderMale/female
16/2
8/8
204/95
0.05
Histologic type
Diffuse type/intestinal type
8/10
9/7
172/127
0.557
Tumor size (mean, cm)
6.2
6.1
7.1
0.374
Stage
IA
3
6
59
IB
2
2
26
II
3
1
54
0.569
IIIA
1
2
60
IIIB
4
1
36
IV
5
4
64
Operative mortality (%)
1/15 (6.7)
0/13 (0)18/299 (7.9)
0.655[ ], number of patients.
PGC, primary gastric carcinoma located in the upper third of the stomach; RGC, remnant gastric carcinoma;
RGC-BD, RGC after partial gastrectomy for benign disease; RGC-GC, RGC after partial gastrectomy for
gastric carcinoma.

frequently detected at the site of anastomosis inpatients with RGC-BD (50%) than in patientswith RGC-GC (19%, P = 0.057, Table 4).
Moreover, 10 of 12 tumors (83%) located at theanastomotic site were the diffuse type while, incontrast, only 7 of 22 tumors (32%) located atother sites were the diffuse type. The difference
was significant (P = 0.004). However, no significant correlations were detected between

initial operative procedures (B-I or B-II) andthe location of RGCs (P = 0.799) or between
initial operative procedures and the histologic
types of tumors (P = 0.492). The interval between the initial operation and detection of
RGCs of 12 tumors located at the anastomoticsite (mean: 232 months) was longer than that of
22 tumors located at other sites (mean: 205
months, P = 0.027). Based on these results,(%)

Survival rate

100
80
60
40
20
0
0

50

100 150 200

250 300 350

Time after operation

400

450
(month)Fig. 1. Survival curve for 299 patients with PGC ( — ), for 15 patients with RGC-BD ( — ) and for
13 patients with RGC-GC ( — ) are shown. No statistically significant difference was found among the
3 survival curves by the log rank test (P = 0.548).

77

M. Ikeguchi et al.

Table 4. Clinicopathological differences between RGC-BD and RGC-GC
RGC-BD[18]

RGC-GC[16]

P

Reconstruction of initial operation
Billroth I/Billroth II
8/10
10/6
0.292
Histologic type
Diffuse type/intestinal type
8/10
9/7
0.472
Interval between initial operation and detection of RGC(mean, month)
265
167
0.004
Location of tumor
Anastomotic site/other site
9/9
3/13
0.057
[ ], number of patients.
RGC, remnant gastric carcinoma; RGC-BD, RGC after partial gastrectomy for benign disease; RGC-GC,
RGC after partial gastrectomy for gastric carcinoma.

cheese and traditional foods were reported asrisk factors in the development of gastric carcinoma (Buiatti et al., 1991; La Vecchia et al.,1995). Geographical variance and dietarydifferences between Japanese and European
people need to be correlated with the incidenceof RGC-BD.
To date, RGC-GC has not been thoroughly
discussed. In investigating RGC-GC, the possibility of overlooking multiple synchronous
small carcinomas in the remnant stomach or the
possibility of cancer recurrence in the remnant
stomach has been considered major difficulties.
Overlooking small carcinomas in the remnant
stomach at the time of initial partial gastrectomy has also been a problem in investigating
RGC-BD. Many reports from Western countries have required that the interval between theinitial operation and detection of RGC should
be more than 5 years to avoid these possibilities(Luukkonen et al., 1990; Pointner et al., 1994).
Kosaka et al. (1990) reported that the rate ofoccurrence of synchronous multiple gastric carcinomas was 5.8% by macroscopic examination, though the rate increased to 13.2% after
microscopic examination of the stomach.
Kodera et al. (1995) reported that in only 53%
of patients with synchronous multiple gastriccarcinomas, the lesions were detected before
operation. Moreover, they concluded thatoverlooking one or more microscopic neoplastic lesions might result in the development ofcancer of the gastric remnant within 10 years
after initial partial gastrectomy for benign or

RGC-BD seems to develop frequently at theanastomotic site and its development seems totake longer than that of RGC-GC.

Discussion
The partial distal gastrectomy for benign gastroduodenal diseases has been considered to bea risk factor of developing RGC. However,whether gastric resection implies an increased
risk for carcinoma remains a matter of dispute.
Tersmette et al. (1991) calculated the estimatedrisk of developing RGC after distal partial
gastrectomy for benign gastroduodenal diseases
from reports previously published. According
to their data, the estimated risk ranged from 0.2
to 4.4, and they reported that the weighted mean
relative risk of RGC-BD in Japan was 0.28; significantly lower than that of RGC-BD in
Europe (1.66). In our case-control study, theestimated risk (odds ratios) of developing RGC
after partial gastrectomy for benign diseases
was 0.212. Tersmette et al. (1991) reported thata very high incidence of primary gastric cancer
in Japan statistically resulted in a decreased risk
for RGC-BD. On the other hand, primary gastric cancer has been much less common in
Europe, thus the risk of RGC-BD relatively increased. Interestingly, Harrison et al. (1997)
reported that total caloric intake increased therisk of developing gastric carcinoma and that
dietary fiber intake decreased this risk. In Italy,high intake of meat, salted fish, seasoned78

Gastric carcinoma in the remnant stomach

malignant conditions. Thus, in the study, toavoid the possibility of overlooking microscopic gastric carcinoma and to avoid the possibilityof recurrence of carcinoma, we required 10
years or more for the interval between the initial
partial gastrectomy and the detection of carcinoma in the remnant stomach. In the present
study, the estimated risk of developing metachronous gastric carcinoma in the remnant
stomach after partial gastrectomy for gastriccarcinoma was 0.798.
Some reports have estimated the risk ofdeveloping RGC based on the mortality rate
(Luukkonen et al., 1990) or the incidence rate
(Domellöf and Janunger, 1977) for gastric carcinoma in their countries (cohort studies). We
conducted a hospital-based case-control study.
As a control group, we selected patients withcolorectal carcinoma. The possibility of selection bias in terms of the control group should beconsidered in any hospital-based study compared with a population-based study. Moreover,
our control patients were not matched with patients who underwent partial gastrectomy interms of age and sex. However, hospital-based
individuals generally provide higher compliance and accuracy of information. We checked
the control patients, who were determined tohave no gastric carcinomas in their stomachs,
before colorectal operation and they were followed up for a long time at our hospital. The
clinical records of the control patients could beobtained every year and the incidence of developing gastric carcinoma could be accurately
calculated.
What is the difference between RGC-BD
and RGC-GC? Histologic distribution andstage distribution were not significantly different among the RGC-BD, RGC-GC and PGCgroups. Moreover, the prognosis of patients operated on for RGC-BD was not different fromthat of patients operated on for RGC-GC orfrom that of patients with PGC. The same result
was obtained by Kodera et al. (1996). Althoughno significant difference was found, RGCs
located in the anastomotic area were frequently
detected in RGC-BD, while, in contrast, RGCs
located in other sites were frequently found in
RGC-GC. The interval between the initial op-

eration and detection of RGC was longer in
RGC-BD than in RGC-GC. Moreover, 83% of
tumors located at the anastomotic site were thediffuse type, while only 32% of tumors locatedat other sites were the diffuse type (P = 0.004).
The interval between the initial operation anddetection of RGCs of tumors located at theanastomotic site was longer than that of tumors
located at other sites (P = 0.027). These findings indicate that the carcinogenesis of RGCGC is in some regard different from that of
RGC-BD.
In the previous study, we investigated theproliferative activity of normal gastric mucosa
adjacent to carcinoma in 13 patients with RGC
by flow cytometry (Ikeguchi et al., 1995). We
reported that the percentages of the S + G2M
phase of the normal mucosa in anastomoticareas from 5 patients with RGC-BD was significantly higher than those from 8 patients with
RGC-GC. Assad and Eastwood (1980) reported that epithelial proliferation, assessed in biopsies morphologically, was increased significantly in the fundic mucosa of patients after
antrectomy, as compared to the fundic mucosa
of normal controls. These findings indicate thatthe increase in proliferation of cells in the mucosa of the remnant stomach is closely related
to the extent of exposure of the gastric mucosa
to the duodenal contents. Duodenogastric bilereflux after distal partial gastrectomy was foundto induce carcinoma at the anastomotic site inanimal experiments (Nishidoi et al., 1984).
Dysplasia, intestinal metaplasia and atrophy ofthe normal mucosa have frequently been observed at the anastomotic area of the remnant
stomach (Offerhaus et al., 1989). These changes
in the gastric mucosa, considered to be theresult of duodenogastric reflux into the remnant
stomach, have been suggested to be the initialsigns of developing RGC-BD. In contrast, developing RGC-GC has the characteristics ofmultifocal cancer; it develops relatively quickly
and most lesions are located at sites remotefrom the anastomosis.
To realize the carcinogenesis of RGC, further investigations about the normal epitheliumof the gastric remnant are necessary.

79M. Ikeguchi et al.

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Received April 28, 2000; accepted May 15, 2000
Corresponding author: Dr. Masahide Ikeguchi

80