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Gastric Cancer

, Volume 20, Issue 5, pp 834–842 | Cite as

Gastric cancer treated by endoscopic submucosal dissection or endoscopic mucosal resection in Japan from 2004 through 2006: JGCA nationwide registry conducted in 2013

  • Satoshi Tanabe
  • Shigeki Hirabayashi
  • Ichiro Oda
  • Hiroyuki Ono
  • Atsushi Nashimoto
  • Yoh Isobe
  • Isao Miyashiro
  • Shunichi Tsujitani
  • Yasuyuki Seto
  • Takeo Fukagawa
  • Souya Nunobe
  • Hiroshi Furukawa
  • Yasuhiro Kodera
  • Michio Kaminishi
  • Hitoshi Katai
Original Article

Abstract

Background

The Japanese Gastric Cancer Association (JGCA) initiated a new nationwide gastric cancer registry in 2008 and reported the treatment outcomes of patients with primary gastric cancer who underwent surgical therapy in 2001 and 2003. However, the outcomes of endoscopic therapy have not been reported yet.

Methods

The JGCA conducted a retrospective nationwide registry in 2013 to investigate the short-term and long-term outcomes of endoscopic mucosal resection or endoscopic submucosal dissection in patients with gastric cancer treated from January 2004 through December 2006. This registry used a computerized database with terminology in accordance with the JGCA classification (13th and 14th editions) and the Japanese Gastric Cancer Treatment Guidelines from 2010.

Results

Accurate data on 12,647 patients were collected from 126 participating hospitals and analyzed. The treatment procedure was endoscopic submucosal dissection in 81% of the patients and endoscopic mucosal resection in 19%. En bloc and R0 resections were achieved in 89% and 79% of the patients respectively. The total proportion of patients who underwent curative resection was 69.2%; 43.8% of patients underwent curative resection for absolute indication lesions, and 25.4% underwent curative resection for expanded indication lesions. Emergency surgery was performed to treat bleeding or perforation in very few patients (0.3% and 0.4% respectively). The 5-year follow-up rate after endoscopic resection was 70%. The 5-year overall survival rate was 91.6% in patients with absolute indications and 90.3% in patients with expanded indications after curative resection and 86.5% in patients who underwent noncurative resection. The 5-year disease-specific survival rates were 99.9%, 99.7%, and 98.7% in patients with absolute indications who underwent curative resection, patients with expanded indications who underwent curative resection, and patients who underwent noncurative resection respectively.

Conclusion

Endoscopic resection of gastric cancer resulted in favorable short-term and long-term outcomes nationwide in Japan. Further efforts to increase the follow-up rate are needed.

Keywords

Early gastric cancer Nationwide registry 5-year survival rate 5-year disease-specific survival rate 

Introduction

The Japanese Gastric Cancer Association (JGCA) reported the results of a nationwide gastric cancer registry in 2006 [1], 2011 [2], and 2013 [3]. The patients were restricted to those who underwent surgical therapy. Since then, remarkable progress has been made in endoscopic treatment of early gastric cancer, which is now performed in increasing numbers of patients. The conventional procedure of endoscopic mucosal resection (EMR) was used as the basis for the development of a procedure for endoscopic submucosal dissection (ESD) [4, 5], and the indications for endoscopic treatment have been expanded [6]. We report the short-term and long-term outcomes of registered patients with gastric cancer who underwent endoscopic treatment from 2004 through 2006.

Materials and methods

The Registration Committee of the JGCA requested hospitals affiliated with JGCA members to enroll consecutive patients with early gastric cancer who underwent EMR or ESD from January 2004 through December 2006. As shown in Table 1, the numbers of participating hospitals and enrolled patients have increased year by year. One hundred twenty-six hospitals participated, and 12,647 patients were enrolled during the 3 years. The Institutional Review Boards of each participating hospital approved the study protocol. In patients with multiple lesions, the main lesion was registered. The main lesion was defined by tumor depth. If multiple lesions had the same tumor depth, the main lesion was defined by tumor size. The tumor size was based on the histology results. Curability criteria were in accordance with the gastric cancer treatment guidelines described later. All tumors that were resected in a piecemeal fashion were classified as noncurative resection.
Table 1

Registered institutions and patients by year

 

Registered institutions

Registered patients

2004

89

3579

2005

99

4213

2006

108

4855

Total

126

12,647

This registry used a computerized database with terminology in accordance with the Japanese Classification of Gastric Carcinoma (13th and 14th editions) and the Japanese Gastric Cancer Treatment Guidelines from 2010.

This nationwide registration program was approved by the Ethics Committee of the JGCA.

Results

Table 2 shows the characteristics of the patients and lesions. The mean age was 71 years. Men accounted for 76% of the registered patients. The endoscopic treatment procedure was ESD in 10,259 patients (81.1%), EMR in 2355 patients (18.6%), and other procedures in 30 patients (0.2%). The gastric status was an intact stomach in 96% of the patients, but some patients had a remnant stomach after gastrectomy or a reconstructed gastric tube after esophagectomy. More than 80% of the lesions were located in the region from the middle to the lower part of the stomach. The largest proportion of lesions was located along the lesser curvature of the stomach. With regard to the macroscopic type, 50% of the lesions were depressed type, 40% were elevated type, and 9% were mixed type. Histologically, 95% of the lesions were differentiated-type cancer. The median tumor diameter was 15 mm and the tumor diameter ranged from 0.5 to 169 mm. The depth of tumor invasion extended to the mucosa in 84.1% of the patients, and was less than 500 μm from the muscularis mucosae in 7.9% of the patients and 500 μm or more from the muscularis mucosae in 7.2% of the patients. With regard to lymphovascular invasion, 4.5% of the patients had lymphatic invasion and 2.3% had venous invasion. Ulcers (including open ulcers and ulcer scars) were found in 10.5% of the patients.
Table 2

Patient (n = 12,647) and lesion characteristics

 

Number or value

Percentage

Age (years)

 Mediana

71 (18–96), 12,644

>99.9

 Missing data

3

<0.1

Sex

 Male

9585

75.8

 Female

3062

24.2

Method of endoscopic resection

 ESD

10,259

81.1

 EMR

2355

18.6

 Other

30

0.2

 Missing data

3

<0.1

Treatment history

 Primary treatment

12,298

97.2

 Posttreatment

349

2.8

Gastric status

 Intact stomach

12,196

96.4

 Remnant stomach after gastrectomy

356

2.8

 Gastric tube after esophagectomy

92

0.7

 Missing data

3

<0.1

Tumor location

 Three gastric regions

  Upper

2251

17.8

  Middle

4889

38.7

  Lower

5502

43.5

  Missing data

5

<0.1

 Four parts of the gastric circumference

  Lesser curvature

5346

42.3

  Greater curvature

2268

17.9

  Anterior wall

2327

18.4

  Posterior wall

2702

21.4

  Missing data

4

<0.1

Macroscopic type

 Depressed

6378

50.4

 Elevated

5014

39.6

 Mixed

1157

9.1

 Undetermined

93

0.7

 Missing data

5

<0.1

Histological type

 pap

428

3.4

 tub1

10,048

79.4

 tub2

1648

13.0

 por

198

1.6

 sig

234

1.9

 muc

10

0.1

 Other

52

0.4

 Undetermined

29

0.2

Tumor size (mm)

 Mediana

15.0 (0.5–169.0), 12,424

98.2

 Missing data

223

1.8

Depth of invasion

 M

10,639

84.1

 SM1

1005

7.9

 Deeper than or equal to SM2

914

7.2

 Other

15

0.1

 Undetermined

70

0.6

 Missing data

4

<0.1

Lymphatic invasion

 Negative

11,956

94.5

 Positive

566

4.5

 Undetermined

119

0.9

 Missing data

6

<0.1

Venous invasion

 Negative

12,234

96.7

 Positive

287

2.3

 Undetermined

120

0.9

 Missing data

6

<0.1

Ulcer findings

 Absent

11,084

87.6

 Present

1325

10.5

 Undetermined

231

1.8

 Missing data

7

0.1

EMR endoscopic mucosal resection, ESD endoscopic submucosal dissection, M intramucosa, muc mucinous adenocarcinomapap papillary adenocarcinoma, por poorly differentiated adenocarcinoma, SM1 depth of invasion less than 500 μm from the muscularis mucosae, SM2 depth of invasion 500 μm or more from the muscularis mucosae, tub1 well-differentiated tubular adenocarcinoma, tub2 moderately differentiated tubular adenocarcinoma, sig signet ring cell carcinoma

aThe range is given in parentheses

Short-term outcomes of endoscopic resection

With regard to short-term outcomes (Table 3), the en bloc resection rate was 89.3%. Horizontal margins were negative in 81.6% of patients, and vertical margins were negative in 94.5%. The rate of en bloc resection with negative margins was 78.9%. The total proportion of patients who underwent curative resection was 69.2%; 43.8% of patients underwent curative resection for absolute indication lesions, and 25.4% underwent curative resection for expanded indication lesions. Noncurative resection was performed in 3704 patients (29.3%). Of the patients who underwent noncurative resection, 63.2% received no additional treatment, 25.2% underwent surgical gastrectomy, and 3.2% underwent additional endoscopic resection. Endoscopic ablation was performed in 155 patients (4.2%). Emergency surgery was performed to treat bleeding in 38 patients (0.3%) and perforation in 45 patients (0.4%). The short-term outcomes are shown according to the method of endoscopic treatment in Table 4. The rate of en bloc resection was significantly higher for ESD (94.5%) than for EMR (66.8%; p < 0.01). The rate of complete en bloc resection was significantly higher for ESD (86.0%) than for EMR (48.2%; p < 0.01). The curative resection rate for absolute indication lesions and expanded indication lesions combined was significantly higher for ESD (75.1%) than for EMR (43.7%; p < 0.01). The rate of emergency surgery for complications did not differ significantly between ESD and EMR (0.3% vs 0.4% for bleeding and 0.3% vs 0.4% for perforation).
Table 3

Short-term outcomes (n = 12,647 patients)

 

Number

Percentage

Resection type

 En bloc resection

11,296

89.3

 Fractional resection

1347

10.7

 Resection not possible

3

<0.1

 Missing data

1

<0.1

Horizontal margin involvement

 Negative

10,319

81.6

 Positive

950

7.5

 Undetermined

1365

10.8

 Missing data

13

0.1

Vertical margin involvement

 Negative

11,951

94.5

 Positive

382

3.0

 Undetermined

302

2.4

 Missing data

12

0.1

En bloc resection with negative margins

 Fulfilled

9975

78.9

 Not fulfilled

2669

21.1

 Missing data

3

<0.1

Curability

 Curative resection for absolute indication lesions

5544

43.8

 Curative resection for expanded indication lesions

3210

25.4

 Noncurative resection

3704

29.3

 Undetermined

189

1.5

Additional treatment for noncurative resection

 No treatment

2342

63.2

 Surgical gastrectomy

933

25.2

 Repeated endoscopic resection

118

3.2

 Endoscopic ablation

155

4.2

 Other

89

2.4

 Missing data

67

1.8

Emergency operation for bleeding

 Operated on

38

0.3

 Not operated on

12,608

99.7

 Missing data

1

<0.1

Emergency operation for perforation

 Operated on

45

0.4

 Not operated on

12,602

99.6

Table 4

Short-term outcomes according to the method of endoscopic resection

 

ESD (n = 10,259)

EMR (n = 2355)

p

Number

Percentage

Number

Percentage

Resection type

<0.01

 En bloc resection

9698

94.5

1573

66.8

 

 Fractional resection

557

5.4

781

33.2

 

  Resection not possible

2

<0.1

0

0

 

 Missing data

2

<0.1

1

<0.1

 

Horizontal margin involvement

<0.01

 Negative

9116

88.9

1181

50.1

 

 Positive

494

4.8

451

19.2

 

 Undetermined

645

6.3

714

30.3

 

 Missing data

4

<0.1

9

0.4

 

Vertical margin involvement

<0.01

 Negative

9783

95.4

2138

90.8

 

 Positive

298

2.9

84

3.6

 

 Undetermined

175

1.7

124

5.3

 

 Missing data

3

<0.1

9

0.4

 

En bloc resection with negative margins

<0.01

 Fulfilled

8819

86.0

1134

48.2

 

 Not fulfilled

1438

14.0

1220

51.8

 

 Missing data

2

<0.1

1

<0.1

 

Curability

<0.01

 Curative resection for absolute indication lesions

4648

45.3

879

37.3

 

 Curative resection for expanded indication lesions

3056

29.8

150

6.4

 

 Noncurative resection

2413

23.5

1279

54.3

 

 Undetermined

142

1.4

47

2.0

 

Additional treatment for noncurative resection

<0.01

 No treatment

1421

58.9

913

71.4

 

 Surgical gastrectomy

787

32.6

145

11.3

 

 Repeated endoscopic resection

51

2.1

65

5.1

 

 Endoscopic ablation

62

2.6

93

7.3

 

 Other

32

1.3

56

4.4

 

 Missing data

60

2.5

7

0.5

 

Emergency operation for bleeding

0.226

 Operated on

28

0.3

10

0.4

 

 Not operated on

10,231

99.7

2345

99.6

 

 Missing data

0

0

0

0

 

Emergency operation for perforation

0.540

 Operated on

35

0.3

10

0.4

 

 Not operated on

10,224

99.7

2345

99.6

 

EMR endoscopic mucosal resection, ESD endoscopic submucosal dissection

Long-term outcomes of endoscopic resection

The 5-year follow-up rate after endoscopic resection was 70%. Figure 1 shows the 5-year overall survival rates according to curability. The 5-year overall survival rate was 91.6% after curative resection of absolute indication lesions and 90.3% after curative resection of expanded indication lesions, as compared with 86.5% after noncurative resection, which was slightly lower. Figure 2 shows the disease-specific survival rates according to curability. The 5-year disease-specific survival rate was 99.9% after curative resection of absolute indication lesions and 99.7% after curative resection of expanded indication lesions, indicating good outcomes. In patients who underwent noncurative resection, the 5-year disease-specific survival rate was 98.7%, indicating good outcomes.
Fig. 1

Overall survival according to curability

Fig. 2

Disease-specific survival according to curability

Discussion

EMR [7] was developed in the 1980s as an endoscopic treatment for early gastric cancer. The development of EMR made possible the endoscopic resection of small differentiated mucosal carcinomas measuring 2 cm or less in diameter. However, EMR often had to be performed in a piecemeal fashion because of technical limitations [8], and histopathological evaluation was difficult in an appreciable number of patients. In the late 1990s, ESD was developed to make possible the en bloc resection of larger lesions [4] and rapidly became popular. Gotoda et al. [6] attempted to expand the clinical indications for ESD in accordance with the positioning of ESD in clinical trials. However, the long-term outcomes of ESD for expanded indication lesions remain unclear. Although ESD has several advantages, such as a high rate of en bloc resection and accurate histopathological assessment, it also has drawbacks when compared with EMR, including a higher incidence of complications such as posttreatment bleeding and perforation [9]; moreover, a longer time is required to master the technique for ESD as compared with that for EMR.

Oda et al. [10] retrospectively studied 714 patients who underwent endoscopic resection of early gastric cancer in 11 Japanese hospitals in 2001. During the study, EMR was performed in more than half of the patients (EMR in 411 patients and ESD in 303 patients). In the present study, we compiled data on patients who underwent endoscopic treatment of early gastric cancer in more than 100 Japanese hospitals from 2004 through 2006. To our knowledge, studies of a similar size have not been reported previously. ESD for treatment of early gastric cancer was approved for coverage by the Japanese National Health Insurance in April 2006 and was soon performed in more than 80% of patients, indicating its rapid acceptance. ESD is thus considered a very therapeutically useful procedure.

With regard to short-term outcomes, the rates of en bloc resection and complete en bloc resection achieved by ESD (95% and 86% respectively) were significantly higher than those achieved by EMR (67% and 48% respectively). The rate of conversion to open surgery because of complications such as bleeding and perforation did not differ between ESD and EMR. The incidences of late bleeding and perforation have been reported to be higher for ESD than for EMR [9], but some studies found no difference in complication rates between ESD and EMR after the procedure for ESD had been technically mastered [11, 12]. In our study, the proportions of patients who had serious complications requiring surgery did not differ significantly between ESD and EMR.

With regard to long-term outcomes according to curability, several studies have reported highly favorable 5-year overall and disease-specific survival rates in patients with early gastric cancer who underwent curative ESD [13, 14]. In our study, the 5-year disease-specific survival rate was nearly 100% in patients who underwent curative resection for absolute indication lesions or expanded indication lesions. In studies comparing ESD with surgery, the overall survival rate after ESD was similar to that after surgery, and the benefit of ESD as compared with surgery included fewer late complications and a shorter hospital stay [15, 16].

Outcomes in patients with expanded indication lesions have been sporadically reported by various groups of investigators, and many studies showed no difference in outcomes in comparison with patients who had absolute indication lesions [14, 17, 18]. These studies were conducted in relatively small numbers of patients at single centers. In our study, 5 (0.16%) of 3056 patients with expanded indication lesions that were curatively resected by ESD died of gastric cancer. In another multicenter collaborative study that we conducted, 6 (0.14%) of 4202 patients with expanded indication lesions had metastatic recurrence [19]. Prospective studies of expanded indication lesions, including the JCOG0607 study [20], the JCOG1009 study [21], and the J-WEB/EGC study [22], have been conducted, and the results of these studies are awaited.

The results of previous studies suggest that expanded indication lesions might be associated with extremely low risks of metastatic recurrence and death from gastric cancer. Kikuchi et al. [23] reported that 3 (0.35%) of 851 patients with early gastric cancer died after surgical therapy, indicating that surgery is also associated with a certain level of risk. Given this background, endoscopic therapy is considered one of the treatment options for expanded indication lesions provided that informed consent is obtained from patients after they are given an adequate explanation about the risk of metastatic recurrence, albeit the incidence is less than 1%.

This is the first time the results of a nationwide study performed by the JGCA that analyzed the outcomes of endoscopic treatment of early gastric cancer have been reported. We compiled and analyzed data on more than 12,000 patients from 126 Japanese hospitals. Our results indicate that endoscopic treatment had good short-term and long-term outcomes in patients with early gastric cancer. The present study was performed during the shift from EMR to ESD and compared the treatment outcomes of these procedures. We therefore consider our results to be valuable. Future participation of more hospitals in nationwide registration may allow various new findings, including the long-term outcomes of patients with expanded indication lesions, to be obtained. On the other hand, the proportion of patients who could be followed up for at least 5 years was only 70%, which was not satisfactory. We will attempt to increase the follow-up rate in future studies and thereby report more accurate results.

Notes

Acknowledgements

The Japanese Gastric Cancer Association Registration Committee is indebted to the great efforts of the member hospitals in registering accurate and detailed data for this project.

Compliance with ethical standards

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1964 and later versions.

Conflict of interest

The authors declare that they have no conflict of interest

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Copyright information

© The International Gastric Cancer Association and The Japanese Gastric Cancer Association 2017

Authors and Affiliations

  • Satoshi Tanabe
    • 1
  • Shigeki Hirabayashi
    • 2
  • Ichiro Oda
    • 3
  • Hiroyuki Ono
    • 4
  • Atsushi Nashimoto
    • 5
  • Yoh Isobe
    • 6
  • Isao Miyashiro
    • 7
  • Shunichi Tsujitani
    • 8
  • Yasuyuki Seto
    • 9
  • Takeo Fukagawa
    • 10
  • Souya Nunobe
    • 11
  • Hiroshi Furukawa
    • 12
  • Yasuhiro Kodera
    • 13
  • Michio Kaminishi
    • 14
  • Hitoshi Katai
    • 10
  1. 1.Research and Development Center for New Medical FrontiersKitasato University School of MedicineSagamiharaJapan
  2. 2.Department of Medical InformaticsNiigata University Medical and Dental HospitalNiigataJapan
  3. 3.Endoscopy DivisionNational Cancer Center HospitalTokyoJapan
  4. 4.Endoscopy DivisionShizuoka Cancer CenterShizuokaJapan
  5. 5.Department of SurgeryNiigata Cancer Center HospitalNiigataJapan
  6. 6.Department of SurgeryNational Hospital Organization Tokyo Medical CenterTokyoJapan
  7. 7.Department of SurgeryOsaka Medical Center for Cancer and Cardiovascular DiseasesOsakaJapan
  8. 8.Tottori University Hospital Cancer CenterYonagoJapan
  9. 9.Department of Gastrointestinal Surgery, Graduate School of MedicineUniversity of TokyoTokyoJapan
  10. 10.Gastric Surgery DivisionNational Cancer Center HospitalTokyoJapan
  11. 11.Department of Gastroenterological SurgeryCancer Institute Ariake HospitalTokyoJapan
  12. 12.Department of SurgeryKinki University HospitalOsakaJapan
  13. 13.Department of SurgeryNagoya University School of MedicineNagoyaJapan
  14. 14.Department of SurgeryShowa General HospitalTokyoJapan

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