Introduction

In 1963, the Japanese Research Society for Gastric Cancer launched a nationwide gastric cancer registry to collect details on the development and prevalence of the research on gastric cancer. This was the precursor of the Japanese Gastric Cancer Association (JGCA), and has been continued, with a decade of inactivity, to date by the JGCA [1,2,3,4,5]. A number of JGCA members voluntarily participate in this registry program. Surgical cases were registered in the JGCA first, and endoscopic cases were additionally registered from 2006. In 2018, 27,034 surgically treated patients were registered from 366 hospitals, and 8681 endoscopically treated patients were registered from 162 hospitals in the 2011 registry [1].

The National Clinical Database (NCD) of Japan was founded in April 2010 as a result of the participation of 10 surgical subspecialty academies associated with the board certification system [6, 7]. The NCD commenced data registration in 2011, and has since become a nationwide database covering more than 95% of the surgeries performed [8]. To date, more than 5200 facilities have enrolled in the NCD, with a registration of approximately 1,500,000 cases per year [9]. The NCD was built as a platform for surgical procedures to evaluating the practices and outcomes, and ultimately, provide better medical care. Additionally, some organ-specific cancer registries, such as those for pancreatic and breast cancer, were implemented to the NCD from the beginning, while hepatocellular cancer, urinary organ cancer, gastric cancer, and esophageal cancer were added later [10]. The Ministry of Health, Labour and Welfare has planned to construct databases of organ-specific cancer registries for patterns of care study and selected NCD as an organization of gastric cancer registry in 2017 [5]. In such a situation, the registration committee of the JGCA and NCD planned to apply the same registration items of the conventional JGCA gastric cancer registry to the NCD gastric cancer registry, which started in 2018. Concomitantly, the registration method was changed from a by-mail to a web-based entry system.

Because data registration in the NCD program that can collect more nationwide data than the conventional program has started, we herein report that gastric cancer registry has led to a better understanding of the real-world situation with respect to gastric cancer in Japan.

Methods

Data source

The registered gastric malignant tumors were primary gastric cancer, remnant gastric cancer, gastrointestinal stromal tumor, malignant lymphoma, and other malignant tumor, and were all treated in 2011. The registration data are listed in Table 1, and consist of the same 73 items as the JGCA registry program, including personal information, surgical results, histological diagnosis, final diagnosis, treatment, and follow-up information according to the Japanese Gastric Cancer Association classification (14th edition), UICC TNM classification (7th edition), and the Japanese gastric cancer treatment guidelines (2010) [11,12,13]. The data were registered in the NCD using a web-based data entry system, by uploading an exported data set registered in the JGCA program, by direct data entry as a result of a relationship with previously registered surgeries, or by direct data entry in an organ-specific cancer registry site. The NCD gastric cancer registration program was approved by the Institutional Review Board of the Graduate School of Medicine, Kobe University (No.180265).

Table 1 Registration data
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Statistical analysis

The collected data of primary gastric cancer patients were analyzed for 5 year survival rate considering various subgroups of prognostic factors, including patient characteristics, tumor status, and surgical procedure. The following data were calculated: total patients; direct death within 30 postoperative days; patients lost to follow-up within 5 years; survival rates by year; standard error of 5 year survival; 5 year survivors; death from gastric cancer, other cancer, other disease, and unknown cause; and recurrence site, such as local, lymph node metastasis, peritoneal metastasis, liver metastasis, and unknown site. The overall survival rates were calculated using the Kaplan–Meier method and were compared using the log-rank test. P values of < 0.05 were considered statistically significant. All statistical analyses were performed using SPSS Statistics 25.0 (IBM, USA).

Results

The data of 30,257 patients with malignant gastric tumors were enrolled from 501 hospitals in all 47 prefectures. The geographical distribution of the participating hospitals is illustrated in Fig. 1a. The median number of hospitals per prefecture was 7 (range 2–48). The composition of the enrolled data is shown in Fig. 1b. High-volume centers, recording more than 100 cases per year, accounted for 16.2% of all participating hospitals. Of 30,257 cases, 2656 cases (8.8%) without data entry approval and 325 cases (1.2%) without follow-up information were excluded. Additionally, 654 cases, including cases of remnant gastric cancer or other malignant tumor, cases with synchronous malignancy, non-surgical cases, and palliative surgery cases, were excluded. The remaining 26,622 patients were used for the analyses.

Fig. 1
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a Geographic distribution of the registered hospitals in 47 prefectures. b Patient volume in the participating hospital

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The 5 year survival rate (5YSR) of all patients with primary gastric cancer was 68.4% (Fig. 2a). With the exclusion of 1123 unresected cases, 189 atypically surgical procedure cases, and 4 unknown cases, the 5YSR was 71.3%, and the 30 day operative mortality rate was 0.41% in the 25,306 resected cases (Fig. 2b). Analyses of various subgroups for patient demographics and gastric cancer characteristics were performed for resected cases (Table 2). Patients aged ≥ 80 years old comprised 15.6% of the population, and their 5YSR was 49.6%, whereas that of patients aged 40‒59 years old was 82.9% (P < 0.001) (Fig. 2c). The proportion of male patients was 68.9%, and their 5YSR was lower than that of female patients (69.1% vs. 74.8%, P < 0.001) (Fig. 2d). With regards to the primary tumor, tumors in the upper-third of the stomach with esophageal invasion accounted for 23.4%, and the 5YSR (63.3%) of these cases was lower than the cases with tumors located at the middle-third (76.6%) and lower-third and duodenum (70.3%) (P < 0.001) (Fig. 2e). The 5YSR of type 4 tumor was remarkably low at 25.2%, and the 28.3% of this tumor had peritoneal recurrence (Fig. 2f). With regards to histological classification, the proportion of undifferentiated tumor types, including poorly differentiated adenocarcinoma, signet-ring cell carcinoma, and mucinous adenocarcinoma was 45.9%, and their 5YSR was lower than that of differentiated type tumors, such as papillary adenocarcinoma and tubular adenocarcinoma (66.8% vs. 74.4%, P < 0.001) (Fig. 2g). Early gastric cancer (pT1) accounted for 48.2%, the 5YSR was 88.7%, and death from gastric cancer was only 0.25% (Fig. 2h, i). Progression of venous invasion and lymphatic invasion were associated with poor prognosis (Fig. 2j, k). The proportion of cases that were negative for lymph node metastasis was 59.8%, and their 5YSR was 85.5% (Fig. 2l). In cases with non-curative factors, the presence of distant metastasis, peritoneal metastasis, positive peritoneal lavage cytology, and liver metastasis showed similar 5YSRs (Fig. 2m–p). The 5YSRs of patients stratified by pathological stage were 89.6% for stage IA, 83.8% for stage IB, 77.3% for stage IIA, 69.1% for stage IIB, 58.7% for stage IIIA, 44.1% for stage IIIB, 30.1% for stage IIIC, and 13.4% for stage IV (Fig. 2q, r). The results for surgical procedure and outcome are shown in Table 3. The groups classified based on surgical procedure had various tumor characteristics and survival differences among procedure groups were not precisely evaluated. Laparoscopic surgery was performed in 31.1%. Thoraco-laparotomy, which was performed for tumors with esophageal invasion, accounted for only 0.6%. Distal gastrectomy accounted for 59.6% and total gastrectomy was performed in 32.9%. D2 lymph node dissection was carried out for 43.6% of all resected patients, and had a low incidence of direct death at 0.25%. Combined resection was performed in 31.5% of all cases. R0 resection was achieved for 89.9%, and the 5YSR was 77.0% (Fig. 3). The predominant site of recurrence after R0 resection was the peritoneum, followed by the liver and distant lymph nodes.

Table 2 Gastric cancer characteristics
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Fig. 2
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Kaplan–Meier survival curves of patients stratified to various subsets of prognostic factors for patient demographics and tumor characteristics. a All patients with primary gastric cancer, b resected cases and unresected cases, c age category, d sex, e tumor location, f macroscopic type, g histological classification, h depth of tumor invasion, i depth of subclassification of submucosa, j lymphatic invasion, k venous invasion, l lymph node metastasis, m distant metastasis, n peritoneal metastasis, o peritoneal cytology, p liver metastasis, q stage, and r stage (IV classification)

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Table 3 Surgical outcomes
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Fig. 3
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Kaplan–Meier survival curves of patients stratified to residual tumor

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Discussion

The initial NCD gastric cancer registry collected 30,257 surgically treated cases from 501 hospitals in all 47 prefectures. The 55,278 stomach cancer surgeries, including total gastrectomy, distal gastrectomy, proximal gastrectomy, pylorus preserving gastrectomy, segmental gastrectomy, and local gastrectomy (including wedge resection), were recorded in the NCD database at 2011 [9]. In the NCD gastric cancer registry, the 24,539 resected cases with the above procedures covered 44.4% of stomach surgeries. The number of enrolled cases in gastric cancer registry accounted for less than half of stomach surgeries in NCD. The difficulty in achieving complete enumeration of all cancer patients is a major issue in organ-specific cancer registries. So far, the conventional JGCA registry has been voluntarily supported by the hospitals to which JGCA members belong, and so the increase in the number of participating hospitals has limitations. The launch of the NCD cancer registry has been widely announced to all hospitals that participated in the NCD surgery registry, as well as the 199 hospitals (39.7%) that newly participated in the initial NCD gastric cancer registry in addition to 302 conventional hospitals (60.3%). The NCD database showed high similarity to the conventional JGCA registry database [1]. The NCD cancer registry, which used a new registry system, demonstrated the validity of database construction. The NCD registry can be expected to expand the range of the gastric cancer registry and increase the number of hospitals participating in the cancer registry.

Another issue raised in the initial registry was the quality assurance of the registration data. An audit of the registration data of the gastroenterological surgeries in the NCD was started in 2015, and high accuracy of data entry has been proved through quality verification [14]. With regards to gastric cancer registry in the NCD, registrants failed to finish or approve data entry in 8.8% of all recorded cases, and did not enter follow-up data in 1.2% of the approved cases. These data deficiencies are also a limitation of this study. An entry system needs to become well known and should be modified for its easy-to-use application through validation by an audit. The complementary integration and reorganization of registry systems between organ-specific cancer registries containing detailed data about tumor status and other cancer registries containing prognostic information is required for conducting an accurate and reliable nationwide cancer database. If all the above-mentioned surgeries registered in the NCD are enrolled in the gastric cancer registry and provided prognostic information, complete enumeration of all stomach surgeries patients is possible.

In conclusion, the NCD registry system of gastric cancer demonstrated the validity of database construction. This program is expected to provide a new comprehensive cancer database integrating patient demographics, oncological features, and therapeutic outcomes with the optimization of data entry system. Therefore, the NCD registry system may offer useful information to further develop gastric cancer research, and provide high-quality treatment.