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Gastric Cancer

, Volume 14, Issue 4, pp 301–316 | Cite as

Gastric cancer treatment in Japan: 2008 annual report of the JGCA nationwide registry

  • Yoh Isobe
  • Atsushi Nashimoto
  • Kohei Akazawa
  • Ichiro Oda
  • Kenichi Hayashi
  • Isao Miyashiro
  • Hitoshi Katai
  • Shunichi Tsujitani
  • Yasuhiro Kodera
  • Yasuyuki Seto
  • Michio Kaminishi
Open Access
Special Article

Abstract

The Japanese Gastric Cancer Association (JGCA) started a new nationwide gastric cancer registry in 2008. Approximately 50 data items, including surgical procedures, pathological diagnoses, and survival outcomes, for 12004 patients with primary gastric cancer treated in 2001 were collected retrospectively from 187 participating hospitals. Data were entered into the JGCA database according to the JGCA Classification of gastric carcinoma, 13th edition and the International Union Against Cancer (UICC) TNM Classification of malignant tumors, 5th edition by using an electronic data collecting system. Finally, data of 11261 patients with gastric resection were analyzed. The 5-year follow-up rate was 83.5%. The direct death rate was 0.6%. TNM 5-year survival rates (5YSRs)/JGCA 5YSRs were 91.8/91.9% for stage IA, 84.6/85.1% for stage IB, 70.5/73.1% for stage II, 46.6/51.0% for stage IIIA, 29.9/33.4% for stage IIIB, and 16.6/15.8% for stage IV. The proportion of patients more than 80 years old was 7.0%, and their 5YSR was 48.7%. Compared to the JGCA archived data, though the follow-up rate needs to be improved, these data suggest that the postoperative results of patients with primary gastric carcinoma have improved in those with advanced disease and in the aged population in Japan.

Keywords

Gastric cancer Registry Survival rate Japan 

Introduction

From 1998, the Japanese Gastric Cancer Association (JGCA) began conducting a nationwide gastric cancer registration project by using electronic data collecting systems. Detailed survival analyses of 8851 patients with primary gastric cancer treated in 1991 were reported in 2006 [1]. However, this nationwide registry was suspended because of several issues such as the operation of the Act Concerning Protection of Personal Information, revision of the JGCA classification for gastric cancer, and rapid changes in the information technology (IT) environment at the member hospitals. After a period of 10 years in which the program was inactive, the registration committee of the JGCA started a new registration program to collect anonymized data simply, correctly, and quickly, in 2008 [2, 3]. Based on this program, we investigated the survival outcomes of patients with primary gastric cancer treated in 2001.

Subjects, materials, and methods

In the 2008 JGCA nationwide registration program, approximately 50 data items, including surgical procedures, pathological diagnoses, and prognoses, for patients with primary gastric carcinoma surgically treated in 2001 were collected retrospectively in 2008 by using custom-made software. This software could be downloaded from the JGCA website. The JGCA member hospitals could participate in this project voluntarily.

The registration data of this system are listed in Table 1. Definition and documentation of the items were based on the Japanese (JGCA) Classification of gastric carcinoma, 13th edition [4, 5] and the International Union Against Cancer (UICC) TNM Classification of malignant tumors, 5th edition [6]. These two classifications were not compatible with each other and items could not be converted automatically. The JGCA T-category was identical to the TNM classification. On the other hand, in the JGCA classification, peritoneal metastasis and liver metastasis were individually recorded as P- and H-categories, both of which could be translated into the M-category in the TNM classification. Intraoperative peritoneal washing cytology (CY) was an independent category in the JGCA classification. The JGCA N-category was defined by the anatomical extension of lymph node metastasis in association with the location of the primary tumor, while the TNM N-category was defined by number of metastatic regional lymph nodes. Items that are compatible in the JGCA classification and the TNM classification, and items that are not compatible are listed in Table 2 for convenience.
Table 1

Registration data

Category

Item

Personal information

Name of hospital, serial no., case no., ID no.a, age, sex

Follow-up

Date of follow-up, survival situation, causes of death

Surgery

Date of operation, approach, operative procedure, LN dissection (D), organs resected together with stomach, type of reconstruction

Pathology

Anatomical subsite, macroscopic type, size of tumor, histological type, depth of tumor invasion, ly, v, number of dissected LNs, number of metastatic LNs, N, PM/DM, CY

JGCA final diagnosis

Depth of tumor invasion, adjacent structure involved, fN, H, P, M, curability, stage

UICC TNM categories

T, N, M, stage

LN lymph node, ly lymphatic invasion, v venous invasion, N extent of LN metastasis (JGCA), PM/DM involvement of proximal and distal margin, CY peritoneal cytology, fN extent of LN metastasis (final diagnosis), H liver metastasis, P peritoneal metastasis, M distant metastasis, JGCA Japanese Gastric Cancer Association, UICC International Union Against Cancer

aID no. was not exported to the registration data set

Table 2

Compatibility to convert JGCA classification to TNM classification

Category

JGCA 13th ed.

TNM 5th ed.

Compatibility

T

1–4

0–4

Compatible

N

0

0

Identical

 

1–3

1–3

Incompatible

Ma

0

0

Compatible

 

1

1

Compatible

H

0

None

 
 

1

M1

Compatible

P

0

None

 
 

1

M1

Compatible

CY

0

None

 
 

1

None

 

Stage

IA

IA

Identical

 

IB, II, IIIA, IIIB, IV

IB, II, IIIA, IIIB, IV

Incompatible

Lymphatic invasion

ly0

L0

Identical

 

ly1–3

L1

Compatible

Venous invasion

v0

v0

Identical

 

v1–3

v1

Compatible

 

None

v2

 

Histological typing

Differentiated type

G1–2

Compatible

 

Undifferentiated type

G3–4

Compatible

Residual tumor

Resection A–C

R0–2

Incompatible

aJGCA M-category is defined as distant metastases other than peritoneal, liver, or cytological metastases

After the patients’ data were entered with the data entry software, the patients’ names and other personal information were removed from the exporting data set for privacy protection. A compact disk containing the linkable anonymous data was then mailed to the JGCA data center, located at Niigata University Medical and Dental Hospital. The accumulated data of the patients were reviewed and analyzed by the JGCA registration committee. One- to 5-year survival rates (5YSRs) were calculated for various subsets of prognostic factors by the Kaplan–Meier method. Deaths of any cause observed during 5 postoperative years were counted as events in the survival analysis. SPSS Ver. 15 software (SPSS, Chicago, IL, USA) was used for statistical analyses. This nationwide registration program was approved by the ethics committee of the JGCA.

Results

The data were collected from 187 participating hospitals across the country. The geographical distribution of the registered patients among Japan’s 47 prefectures is illustrated in Fig. 1. More than 1000 patients per year were registered in the prefectures of Tokyo and Osaka; on the other hand, the number of registered patients was less than 100 in 15 prefectures. The hospital volumes in the participating hospitals are indicated in Fig. 2. The median hospital volume was 66 patients per year.
Fig. 1

Geographical distribution of the registered patients

Fig. 2

Hospital volumes in the 187 participating hospitals

Data of 13067 patients who had undergone surgery in 2001 for primary gastric tumors were eventually accumulated. Of these, 88 patients with benign tumor or non-epithelial tumor were excluded from the analysis. Ninety-four patients who received endoscopic mucosal resection were also excluded. Data of 881 patients lacked essential items. Consequently, data of the remaining 12004 patients were used for the final analysis.

The results are shown in Tables 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, and 28; data in these Tables are for the total number of patients, survival rates by year, standard error of 5YSR, direct death within 30 postoperative days, numbers lost to follow-up within 5 years, 5-year survivors, and main causes of death (such as local and/or lymph node metastasis, peritoneal metastasis, liver metastasis, distant metastasis, recurrence at unknown site, other cancer and other disease). Figures 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, and 14 show cumulative survival curves of patients stratified by essential categories.
Table 3

Survival outcomes of primary cancer

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Primary cancer

12004

86.4

78.7

74.1

71.1

69.1

0.4

95

1976

6588

309

1266

374

183

349

162

530

267

SE standard error, 5YSR 5-year survival rate, DD direct death, Lost to follow up lost to follow-up within 5 years, Alive 5-year survivors, L local recurrence and/or lymph node metastasis, P peritoneal metastasis, H liver metastasis, M distant metastasis, R recurrence at unknown site, OC other cancer, OD other disease, UK unknown

Table 4

Survival outcomes of resected cases and unresected cases

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Resected cases

11261

88.6

80.9

76.2

73.0

70.9

0.4

63

1877

6354

267

1040

357

161

298

155

501

251

Unresected cases

350

23.0

9.8

7.1

5.6

5.3

1.3

20

40

14

32

176

12

13

43

0

10

10

Table 5

Survival outcomes by sex

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Male

7828

88.4

80.7

75.6

72.3

70.0

0.5

47

1314

4348

190

646

299

112

205

138

403

173

Female

3419

88.9

81.1

77.5

74.6

73.0

0.8

16

562

1997

76

392

58

49

93

17

97

78

Table 6

Survival outcomes by age

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

<40

257

89.9

82.0

80.3

79.4

78.4

2.7

0

40

165

3

30

2

8

4

1

0

4

40–59

3232

92.5

86.6

83.1

80.6

79.3

0.7

12

516

2095

60

274

58

48

66

13

54

48

60–79

6924

87.9

80.1

74.9

71.6

69.2

0.6

37

1129

3818

186

651

259

91

182

135

322

151

≧80

788

78.5

64.3

58.6

53.1

48.7

2.0

14

178

256

18

84

35

13

29

6

123

46

Table 7

Survival outcomes by tumor location

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

U

2399

86.0

76.7

71.3

67.5

65.3

1.0

13

370

1258

69

237

107

49

75

32

134

68

M

4351

92.2

87.1

83.3

80.8

78.9

0.6

23

760

2741

65

260

90

43

84

65

161

82

L

3936

89.4

81.4

77.1

74.2

71.9

0.7

21

685

2230

108

309

141

52

99

55

176

81

Whole

532

63.7

44.7

33.7

25.8

23.4

2.0

6

56

104

23

230

17

17

34

3

28

20

U upper third, M middle third, L lower third of stomach

Table 8

Survival outcomes by macroscopic type

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Type 0

6085

97.5

95.7

93.7

91.8

90.3

0.4

12

1143

4401

20

45

23

23

32

100

217

81

Type 1

318

79.1

66.7

61.7

56.5

54.6

2.9

4

49

136

12

18

28

7

14

7

36

11

Type 2

1419

84.8

73.0

66.5

62.5

59.7

1.4

11

220

669

58

127

126

29

59

10

81

40

Type 3

2151

76.5

60.8

52.4

47.8

45.1

1.1

21

306

760

119

425

152

62

124

25

112

66

Type 4

779

62.1

41.9

30.0

23.4

20.4

1.5

10

65

133

37

363

11

31

54

7

35

43

Type 5

340

86.8

74.3

67.4

62.6

59.5

2.8

4

48

166

13

49

16

7

15

4

15

7

Table 9

Survival outcomes by histological diagnosis

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

pap

364

85.8

75.1

70.4

67.5

65.1

2.6

3

64

185

11

27

23

6

13

8

23

4

tub1

2752

95.2

91.1

87.9

85.3

83.5

0.7

5

519

1818

30

55

42

16

36

51

137

48

tub2

2997

89.2

81.4

76.3

73.1

70.6

0.9

20

537

1651

64

207

156

46

74

45

160

57

por1

1476

82.5

72.4

67.8

64.9

63.7

1.3

14

238

737

53

174

82

30

40

14

69

39

por2

1903

81.4

69.7

63.4

59.5

56.6

1.2

15

244

886

75

401

34

44

86

19

59

55

sig

1325

93.2

88.0

84.5

81.2

79.4

1.2

4

217

855

17

108

2

14

32

12

30

38

muc

231

81.5

68.8

60.4

53.7

51.2

3.4

1

24

100

9

54

5

1

10

3

19

6

Adenosquamous carcinoma

6

50.0

33.3

33.3

16.7

16.7

15.2

0

0

1

0

2

2

0

0

1

0

0

Squamous cell carcinoma

5

60.0

30.0

0.0

0.0

0.0

0.0

0

1

0

2

1

0

1

0

0

0

0

Miscellaneous carcinoma

45

65.2

53.1

48.1

45.6

45.6

7.7

0

4

18

2

8

7

2

2

0

1

1

Pap papillary adenocarcinoma, tub1 tubular adenocarcinoma, well-differentiated type, tub2 tubular adenocarcinoma, moderately differentiated type, por1 poorly differentiated adenocarcinoma, solid type, por2 poorly differentiated adenocarcinoma, non-solid type, sig signet-ring cell carcinoma, muc mucinous adenocarcinoma

Table 10

Survival outcomes by histological differentiation

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Differentiated type

6113

91.7

85.4

81.2

78.3

76.1

0.6

28

1120

3654

105

289

221

68

123

104

320

109

Undifferentiated type

4935

84.9

75.4

70.1

66.6

64.6

0.7

34

723

2578

154

737

123

89

168

48

177

138

Other type

144

81.6

75.3

71.9

68.4

68.4

4.1

1

29

74

6

12

11

4

2

1

3

2

Table 11

Survival outcomes by venous invasion (v)

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

v0

6453

95.4

91.5

88.6

86.2

84.5

0.5

23

1228

4304

54

258

59

36

70

101

260

83

v1

2601

84.5

72.7

66.6

62.2

59.7

1.0

17

352

1276

103

365

115

53

112

29

127

69

v2

1347

75.7

59.8

50.4

45.8

42.6

1.4

17

168

463

71

271

95

44

74

16

84

61

v3

539

59.4

44.5

35.7

32.2

30.8

2.1

5

69

128

30

123

85

23

34

4

21

22

Table 12

Survival outcomes by lymphatic invasion (ly)

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

ly0

4783

97.2

95.3

93.3

91.4

89.9

0.5

11

956

3389

10

48

23

11

35

80

177

54

ly1

2604

92.4

86.1

81.1

77.7

75.1

0.9

13

398

1606

51

187

84

36

37

40

115

50

ly2

2047

80.7

65.8

58.4

53.3

50.5

1.2

22

271

834

102

346

134

53

103

17

123

64

ly3

1481

65.2

45.4

36.3

31.6

29.4

1.3

16

194

334

95

438

110

57

110

13

77

53

Table 13

Survival outcomes by depth of invasion

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

pT1(M)

3071

98.1

96.9

95.0

93.5

92.2

0.5

5

606

2248

7

4

4

1

7

53

98

43

pT1(SM)

2662

97.5

95.0

93.1

90.9

89.1

0.6

6

500

1898

11

16

19

11

16

51

109

31

pT2(MP)

1071

93.4

88.7

84.0

80.9

78.3

1.3

3

183

675

13

23

31

19

22

17

68

20

pT2(SS)

1695

87.0

74.7

67.6

63.2

60.6

1.2

17

262

817

67

148

122

48

65

20

99

47

pT3(SE)

2278

69.7

50.9

41.3

35.8

33.0

1.0

26

264

601

132

712

140

72

148

10

102

97

pT4(SI)

417

57.7

38.1

30.0

26.0

22.8

2.2

5

45

77

36

134

39

8

40

4

24

10

p pathological finding, M mucosa or muscuralis musoca, SM submucosa, MP muscularis propria, SS subserosal, SE serosa, SI adjacent structures

Table 14

Survival outcomes by pT classification

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

pT1

5733

97.8

96.0

94.1

92.3

90.8

0.4

11

1106

4146

18

20

23

12

23

104

207

74

pT2

2766

89.5

80.1

74.0

70.1

67.5

0.9

20

445

1492

80

171

153

67

87

37

167

67

pT3

2278

69.7

50.9

41.3

35.8

33.0

1.0

26

264

601

132

712

140

72

148

10

102

97

pT4

417

57.7

38.1

30.0

26.0

22.8

2.2

5

45

77

36

134

39

8

40

4

24

10

Table 15

Survival outcomes by lymph node metastasis (pN)

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

pN0

6508

97.0

94.7

92.5

90.6

89.0

0.4

22

1240

4616

18

95

38

16

44

109

248

84

pN1

2274

84.7

72.3

66.2

61.3

58.3

1.1

12

322

1074

78

309

139

46

99

23

118

66

pN2

1703

72.1

52.8

41.4

35.8

33.4

1.2

19

224

439

103

442

135

69

109

13

100

69

pN3

421

53.8

33.1

25.8

22.0

17.4

1.9

4

33

61

60

136

37

28

35

3

13

15

Table 16

Survival outcomes by liver metastasis (fH)

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

fH0

10665

89.9

82.6

78.1

74.9

72.7

0.5

55

1806

6171

249

956

216

143

268

144

482

230

fH1

305

42.6

24.6

15.3

12.2

11.8

2.0

7

28

28

8

48

130

15

25

5

10

8

f final finding

Table 17

Survival outcomes by peritoneal metastasis (fP)

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

fP0

10301

91.2

84.5

80.0

76.9

74.8

0.4

49

1771

6131

232

628

322

143

245

148

468

213

fP1

658

49.0

27.0

19.3

14.7

12.4

1.4

11

64

66

24

363

30

15

49

1

21

25

Table 18

Survival outcomes by peritoneal cytology (CY)

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

CY0

4109

88.6

78.9

73.0

68.9

66.4

0.8

24

671

2157

135

403

184

82

120

56

185

116

CY1

651

51.6

29.1

18.2

14.9

12.3

1.4

4

73

60

23

338

35

15

62

4

25

16

Table 19

Survival outcomes by distant metastasis (fM)

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

fM0

10752

89.4

82.0

77.3

74.2

72.1

0.5

59

1817

6159

233

932

331

140

278

149

479

234

fM1

215

46.7

27.3

23.6

19.7

18.0

2.8

3

21

30

25

72

15

16

16

2

14

4

Table 20

Survival outcomes by JGCA stage

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Stage IA

4997

98.2

96.7

94.9

93.2

91.9

0.4

11

983

3646

6

11

8

3

14

87

181

58

Stage IB

1459

96.4

93.0

90.1

87.4

85.1

1.0

7

267

993

9

28

13

11

15

28

78

17

Stage II

1237

93.0

85.0

79.7

75.7

73.1

1.3

7

196

736

26

70

44

24

38

14

65

24

Stage IIIA

975

85.8

71.2

61.2

55.2

51.0

1.7

9

143

395

47

137

50

32

53

6

61

51

Stage IIIB

562

76.6

55.3

43.9

36.0

33.4

2.1

5

63

153

48

141

31

24

40

2

36

24

Stage IV

1649

53.9

32.2

22.4

18.3

15.8

1.0

22

161

206

122

626

199

62

135

11

71

56

Table 21

Survival outcomes by JGCA stage (4 classifications)

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Stage I

6456

97.8

95.8

93.8

91.9

90.3

0.4

18

1250

4639

15

39

21

14

29

115

259

75

Stage II

1237

93.0

85.0

79.7

75.7

73.1

1.3

7

196

736

26

70

44

24

38

14

65

24

Stage III

1537

82.4

65.4

54.9

48.2

44.5

1.3

14

206

548

95

278

81

56

93

8

97

75

Stage IV

1649

53.9

32.2

22.4

18.3

15.8

1.0

22

161

206

122

626

199

62

135

11

71

56

Table 22

Survival outcomes by TNM stage

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Stage IA

4795

98.2

96.7

94.8

93.1

91.8

0.4

11

951

3489

6

11

9

3

13

81

175

57

Stage IB

1495

95.9

92.5

89.4

86.9

84.6

1.0

7

290

995

11

29

19

8

19

28

77

19

Stage II

1333

92.1

84.2

77.4

72.9

70.5

1.3

10

201

769

34

92

45

28

47

13

77

27

Stage IIIA

874

83.6

67.3

57.6

51.6

46.6

1.8

7

134

318

51

138

58

21

49

9

51

45

Stage IIIB

352

76.2

51.4

38.6

32.3

29.9

2.6

3

39

85

35

101

20

14

20

1

21

16

Stage IV

1638

55.3

33.2

23.9

19.0

16.6

1.0

21

157

219

120

605

186

79

128

11

68

65

Table 23

Survival outcomes by TNM stage (4 classifications)

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Stage I

6290

97.7

95.7

93.5

91.7

90.1

0.4

18

1241

4484

17

40

28

11

32

109

252

76

Stage II

1333

92.1

84.2

77.4

72.9

70.5

1.3

10

201

769

34

92

45

28

47

13

77

27

Stage III

1226

81.4

62.7

52.1

46.0

41.8

1.5

10

173

403

86

239

78

35

69

10

72

61

Stage IV

1638

55.3

33.2

23.9

19.0

16.6

1.0

21

157

219

120

605

186

79

128

11

68

65

Table 24

Survival outcomes by approaches

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Laparotomy

10532

88.3

80.4

75.6

72.4

70.2

0.5

59

1757

5869

251

1002

345

154

289

147

487

231

Thoraco-laparotomy

112

70.5

56.0

47.6

43.7

40.7

4.7

3

8

39

14

19

11

6

7

0

4

4

Laparoscopic

396

99.2

98.9

98.6

97.7

97.4

0.9

0

87

300

0

0

0

0

1

2

3

3

Others

2

100.0

50.0

50.0

50.0

50.0

35.4

0

0

1

0

0

0

0

0

0

1

0

Table 25

Survival outcomes by operative procedures

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Distal gastrectomy

6684

91.6

85.5

81.6

79.1

77.2

0.5

33

1173

4096

133

412

191

75

129

90

267

118

Total gastrectomy

3377

80.0

67.5

60.6

56.1

53.7

0.9

25

512

1427

124

612

154

75

155

32

179

107

Proximal gastrectomy

446

95.2

90.0

88.3

84.3

82.3

1.9

1

60

312

4

9

6

11

6

9

21

8

Pylorus-preserving

277

96.7

95.2

94.4

92.0

90.4

1.8

2

32

220

1

2

3

0

2

5

6

6

Local excision/segmental resection

339

95.1

94.1

89.1

84.9

82.7

2.2

2

69

218

4

4

2

0

5

10

20

7

Mucosal resection

138

94.4

89.5

84.3

80.8

78.0

3.8

0

31

81

1

1

1

0

1

9

8

5

Table 26

Survival outcomes by lymph node dissection (D)

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

D0

812

79.1

72.7

69.2

65.1

63.7

1.8

8

153

394

17

85

25

4

30

28

52

24

D1

2371

85.1

76.9

72.9

70.4

68.3

1.0

19

340

1326

48

236

83

31

74

46

137

50

D1+α

1368

91.3

85.8

82.2

79.6

77.5

1.2

5

292

799

26

69

40

15

28

17

68

14

D1+β

605

94.8

90.7

87.2

84.9

83.5

1.6

2

122

391

5

25

10

5

6

5

26

10

D2

5403

90.7

82.8

77.5

74.0

71.8

0.6

28

840

3147

134

523

166

81

142

53

183

134

D3

391

78.9

62.7

54.6

50.5

46.8

2.6

0

30

161

30

82

23

18

15

2

20

10

α, Lymph node No. 7 irrespective of the location of lesions, and additionally No. 8a in patients with lesions located in the lower third of the stomach; β, Lymph nodes No. 7, 8a, 9

Table 27

Survival outcomes by involvement of the resection margins

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

PM− and DM−

10550

89.5

82.3

77.7

74.6

72.5

0.5

56

1784

6086

232

881

338

136

258

143

466

226

PM+ and/or DM+

332

58.5

39.4

32.2

24.5

22.3

2.4

6

34

59

22

119

12

19

31

5

20

11

PM proximal margin, DM distal margin

Table 28

Survival outcomes by curative potential of gastric resection

 

No. of patients

Postoperative survival rate (%)

SE of 5YSR

DD

Lost to follow up

Alive

Main cause of death

1 year

2 year

3 year

4 year

5 year

L

P

H

M

R

OC

OD

UK

Resection A

7038

97.5

94.9

92.5

90.4

88.7

0.4

20

1309

5006

41

72

52

31

49

108

271

99

Resection B

2593

85.0

70.7

62.1

56.3

53.1

1.0

20

364

1108

121

380

151

72

119

31

157

90

Resection C

1420

50.3

28.7

19.7

15.5

13.4

1.0

22

145

145

98

567

152

55

128

10

65

55

Resection A, no residual disease with high probability of cure satisfying all of the following conditions: T1 or T2; N0 treated by D1, 2, 3 resection or N1 treated by D2, 3 resection; M0, P0, H0, CY0, and proximal and distal margins >10 mm; Resection B, no residual disease but not fulfilling criteria for “Resection A”; Resection C, definite residual disease

Fig. 3

Kaplan–Meier survival for all 12004 patients with primary gastric cancer. 5YSR 5-year survival rate

Fig. 4

Kaplan–Meier survival for resected cases and unresected cases

Fig. 5

Kaplan–Meier survival of the resected cases stratified by sex

Fig. 6

Kaplan–Meier survival of the resected cases stratified by age

Fig. 7

Kaplan–Meier survival of the resected cases stratified by tumor location. W whole stomach, M middle third, L lower third, U upper third of stomach

Fig. 8

Kaplan–Meier survival of the resected cases stratified by macroscopic type

Fig. 9

Kaplan–Meier survival of the resected cases stratified by depth of tumor invasion. M mucosa or muscuralis mucosa, SM submucosa, MP muscularis propria, SS subserosal, SE serosa, SI adjacent structures

Fig. 10

Kaplan–Meier survival of the resected cases stratified by pT classification

Fig. 11

Kaplan–Meier survival of the resected cases stratified by lymph node metastasis

Fig. 12

Kaplan–Meier survival of the resected cases stratified by Japanese Gastric Cancer Association (JGCA) stage

Fig. 13

Kaplan–Meier survival of the resected cases stratified by TNM stage

Fig. 14

Kaplan–Meier survival of the resected cases stratified by curative potential of gastric resection. Resection A, no residual disease with high probability of cure satisfying all of the following conditions: T1 or T2; N0 treated by D1, 2, 3 resection or N1 treated by D2, 3 resection; M0, P0, H0, CY0, and proximal and distal margins >10 mm; Resection B, no residual disease but not fulfilling criteria for “Resection A”; Resection C, definite residual disease

The 5YSR in the 12004 patients with primary gastric cancer was 69.1% (Table 3; Fig. 3). Within 5 postoperative years, 1976 patients were lost to follow-up; the follow-up rate was 83.5%. Of the 12004 patients, 11261 underwent gastric resection; 350 were unresected; and in 393 the type of surgery was not specified. Accordingly, the resection rate was 97.0% (11261/11611). Sixty-three of the 11261 patients who had undergone gastrectomy died within 30 postoperative days; the direct death rate was 0.6% (Table 4; Fig. 4).

The most frequent cause of death in patients who had received gastrectomy was peritoneal metastasis (n = 1040), followed, in descending order, by other diseases (n = 501), liver metastasis (n = 357), recurrence at an unknown site (n = 298), and local recurrence including node metastasis (n = 267).

The proportion of male patients was 69.6% and their 5YSR was lower than that of female patients (P < 0.01; Table 5; Fig. 5). The proportion of patients who were more than 80 years old was 7.0%, and their 5YSR was 48.7% (Table 6; Fig. 6). Upper-third gastric cancer accounted for 21.4% of the cases, and the 5YSR (65.3%) of patients with cancer at this site was lower than that for the middle- and lower-third cancers (P < 0.001; Table 7; Fig. 7). The proportion of patients with type 4 cancer was 7.0%, and their 5YSR was markedly low, at 20.4% (P < 0.001; Table 8; Fig. 8). In regard to the histological type, the 5YSR of patients with undifferentiated type, including poorly differentiated adenocarcinoma, signet-ring cell carcinoma, and mucinous adenocarcinoma, was 64.6%. The undifferentiated type showed a poorer prognosis than the differentiated type (P < 0.001; Tables 9, 10). The grade of venous invasion (v0–v3) and that of lymphatic invasion (ly0–ly3) showed significant correlations with prognosis (P < 0.001; Tables 11, 12).

There was a high incidence of early-stage cancer, as indicated in Tables 13 and 14 and Figs. 9 and 10. The proportion of pathological T1 (pT1; mucosal or submucosal) cancer was 51.2%. The 5YSR of this population was 90.8%, and the primary cause of death was not cancer recurrence (n = 96), but other diseases (n = 207).

Peritoneal washing cytology (CY) was carried out for 3481 of 5857 patients with T2, T3, and T4 cancer (59.4%). The 5YSR of cytology-positive patients (CY1) was 12.3%, which corresponded with that of the patients with peritoneal metastasis (P1) (Tables 17, 18).

The 5YSRs of the patients stratified by the JGCA staging system were 91.9% for stage IA, 85.1% for stage IB, 73.1% for stage II, 51.0% for stage IIIA, 33.4% for stage IIIB, and 15.8% for stage IV. These JGCA 5YSRs seemed to correlate well with the TNM 5YSRs (Tables 20, 21, 22, 23; Figs. 12, 13).

In regard to the operative procedure, the proportion of patients who underwent laparoscopic gastrectomy was 3.6%, and their 5YSR was 97.4%. Laparoscopic surgery was carried out mainly in patients with early gastric cancer. Only 1.0% of the patients were treated by thoraco-laparotomy, and their 5YSR was 40.7%. Thoraco-laparotomy was carried out in patients with gastric cardia cancer invading the esophagus (Table 24). Thirty percent of the patients underwent total gastrectomy, and their 5YSR was 53.7%. The proportion of patients treated by modified surgery such as proximal gastrectomy, pylorus-preserving gastrectomy, segmental gastrectomy, and local resection was 9.4% (Table 25). D0, D1, D1+α, and D1+β dissections were carried out in 7.4, 21.7, 12.5, and 5.5% of the patients, respectively. According to the JGCA gastric cancer treatment guidelines [7, 8], D1+α dissection with modified gastrectomy was indicated for T1(M)N0 tumors and T1(SM)N0 differentiated tumors <1.5 cm in diameter, while D1+β dissection with modified gastrectomy was indicated for T1(SM)N0 undifferentiated tumors, T1(SM)N0 differentiated tumors larger than 1.6 cm, T1(M)N1 tumors, and T1(SM)N1 tumors <2.0 cm. D0 and D1 dissections were carried out mainly in patients with non-curative factors or poor surgical risks. D2 lymph node dissection was carried out in 49.3% of the patients and the risk of direct death in those with D2 gastrectomy was 0.5% (28/5403; Table 26).

The curative potential of gastric resection was an important prognostic factor. The proportion of patients with a high probability of cure (resection A) was 63.7%, and their 5YSR was 88.7%. On the other hand, the proportion of patients with definite residual tumor (resection C) was 12.8%, and their 5YSR was 13.4% (Table 28; Fig. 14).

Discussion

The data presented in this report were collected from 187 hospitals in Japan. The number of new patients who were diagnosed with gastric cancer in 2001 was estimated to be 107726 [9]. Accordingly, the 11261 patients registered by this program corresponded to approximately 10% of the population affected by gastric cancer in Japan. Even though these patients may not represent the average features of gastric cancer, this article is considered to be the largest report for the past 10 years clarifying the trends of gastric cancer.

The reliability of the results in this report depends on the quality of data accumulated in the JGCA database. As the algorithms of the JGCA staging system were rather complicated, the error checking system on the data entry screen did not work perfectly. In several categories, such as lymph node metastasis (N), the JGCA code could not convert to the TNM code automatically. A few “bugs” in the software were revealed just after we had analyzed thousands of data records. Therefore, the registration committee had to make great efforts to cleanse and validate the raw data sent to the data center from participating hospitals.

As compared with our archived data of 7935 patients treated in 1991 [1], though the proportions of each stage were similar, the direct death rate had significantly improved, dropping from 1.0 to 0.6% (P < 0.001); the proportion of patients aged more than 80 years old had increased, from 4.5 to 7.0% (P < 0.001); and the 5YSR of stage IV had improved, from 9.0 to 15.8% (P < 0.05). These data suggest that, in this decade, the treatment results may have improved in patients with advanced disease and in older patients.

However, these data were retrospectively collected, 7 years after surgery. We had legal difficulties in registering personal information, which was essential for long-term and prospective follow-up. The overall follow-up rate in our program was 83.5%, as already mentioned. A lower follow-up rate is generally considered to show misleading results of higher survival rates in patients with advanced disease. The Japanese Association of Clinical Cancer Centers (consisting of 25 cancer center hospitals) has reported that their follow-up rate was 98.5%, and the 5YSRs of 9980 patients who underwent surgery from 1997 to 2000 were 90.4% for TNM stage I, 67.8% for stage II, 43.3% for stage III, and 9.3% for stage IV [10]. On the other hand, our 5YSR in stage IV patients was 16.6% (Table 23). We might have overestimated our 5YSR in stage IV patients, but we found that the follow-up rate increased as the stage advanced; the follow-up rate of stage IV patients was 90.4% (Table 29). Of the 187 participating hospitals, 114 hospitals achieved high follow-up rates of 90% or more for stage IV patients. Therefore, the 5-year follow-up rates and 5YSRs in these 114 hospitals were calculated for reference. The mean follow-up rate for stage IV patients in these 114 selected hospitals was 97.7% and their 5YSR was 15.9% (Table 30). These data suggest that the lower follow-up rate in our program may not have serious effects on the 5YSRs. Although the correlation between follow-up rate and survival rate is complicated, we need to greatly improve our follow-up system to evaluate our survival rates more accurately.
Table 29

Five-year follow-up rates stratified by TNM stage

 

No. of patients

Lost to follow up

FUR (%)

Stage I

6290

1241

80.3

Stage II

1333

201

84.9

Stage III

1226

173

85.9

Stage IV

1638

157

90.4

Total

10487

1772

83.1

FUR 5-year follow-up rate

Table 30

Follow-up rates and survival rates stratified by TNM stage in 187 participating hospitals and 114 selected hospitals

TNM stage

187 Participating hospitals

114 Selected hospitals

No. of patients

FUR (%)

5YSR (%)

No. of patients

FUR (%)

5YSR (%)

Stage IA

4795

80.2

91.8

3401

84.0

91.3

Stage IB

1495

80.6

84.6

1000

84.2

82.5

Stage II

1333

84.9

70.5

938

89.6

70.3

Stage IIIA

874

84.7

46.6

608

93.1

45.2

Stage IIIB

352

88.9

29.9

243

93.8

30.8

Stage IV

1638

90.4

16.6

1196

97.7

15.9

The 114 hospitals were selected on the criterion of achieving high follow-up rate of 90% or more for stage IV patients

This is the first nationwide report in which the JGCA refers to peritoneal washing cytology (CY). CY was conducted in 3481 (59.4%) of 5857 patients with T2, T3, or T4 cancer. The 5YSR of CY-positive (CY1) patients was 12.3% and their 5YSR was as poor as that of patients with peritoneal metastasis (P1; 12.4%). Although CY was not carried out commonly in 2001, it was regarded as a significant and independent prognostic factor.

The JGCA restarted a nationwide registration program after an inactive period of 10 years. The most urgent priority of this program was to report detailed 5YSRs in patients who had received a gastrectomy. Therefore, the structure of the database was required to be simple and the number of registration items was kept to a minimum. We are now planning to register more items concerning remnant gastric cancer, chemotherapy, and endoscopic submucosal dissection by upgrading the data entry software. We will continue our efforts to collect qualified data annually.

Notes

Acknowledgments

The JGCA Registration Committee appreciates very much the great effort of member hospitals in registering accurate and detailed data for this project. We also wish to thank Ms. Yoshimi Sugamura, Niigata University Medical and Dental Hospital, for her valuable assistance.

Open Access

This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

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Copyright information

© The Author(s) 2011

Authors and Affiliations

  • Yoh Isobe
    • 1
  • Atsushi Nashimoto
    • 2
  • Kohei Akazawa
    • 3
  • Ichiro Oda
    • 4
  • Kenichi Hayashi
    • 5
  • Isao Miyashiro
    • 6
  • Hitoshi Katai
    • 7
  • Shunichi Tsujitani
    • 8
  • Yasuhiro Kodera
    • 9
  • Yasuyuki Seto
    • 10
  • Michio Kaminishi
    • 11
  1. 1.Department of SurgeryNational Hospital Organization Tokyo Medical CenterTokyoJapan
  2. 2.Department of SurgeryNiigata Cancer Center HospitalNiigataJapan
  3. 3.Department of Medical InformaticsNiigata University Medical and Dental HospitalNiigataJapan
  4. 4.Endoscopy DivisionNational Cancer Center HospitalTokyoJapan
  5. 5.Department of SurgeryYamagata Prefectural Kahoku HospitalYamagataJapan
  6. 6.Department of SurgeryOsaka Medical Center for Cancer and Cardiovascular DiseasesOsakaJapan
  7. 7.Department of SurgeryNational Cancer Center HospitalTokyoJapan
  8. 8.Department of Surgery and Science, Graduate School of Medical ScienceKyushu UniversityFukuokaJapan
  9. 9.Department of SurgeryNagoya University School of MedicineNagoyaJapan
  10. 10.Department of Gastrointestinal Surgery, Graduate School of MedicineUniversity of TokyoTokyoJapan
  11. 11.Department of SurgeryShowa General HospitalTokyoJapan

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