Abstract

Background

Gastric cancer is a major health problem worldwide, with a high incidence among older adults. Given the aging overall population, it was crucial to understand the current burden and prospective trend of older gastric cancer. This study aimed to analyze the temporal trends of the incidence, mortality, and survival of older gastric cancer in the highest gastric cancer risk area in China from 2010 to 2019, and to predict the future burden of older gastric cancer up to 2024.

Methods

The study was conducted in Gansu province, an area characterized by the highest gastric cancer incidence and mortality in China. The registration data of gastric cancer incidence and mortality from 2010 to 2019 were pooled from registries in the Gansu Cancer Registration System, while survival data were collected from the First Hospital of Lanzhou University, Lanzhou University Second Hospital, and Gansu Cancer Hospital. Chinese standard population in 2000 and the Segi’s world standard population were applied to calculate the age-standardized rate. Joinpoint regression was used to analyze the average annual percentage change (AAPC) in cancer incidence and mortality. Autoregressive Integrated Moving Average (ARIMA) models were employed to generate forecasts for incidence and mortality from 2020 to 2024.

Results

Based on registry data from 2010 to 2019, the incidence and mortality rates of gastric cancer among older adults remained stable. The incidence rates declined from 439.65 per 100,000 in 2010 to 330.40 per 100,000 in 2019, with an AAPC of -2.59% (95% confidence interval[CI], -5.14 to 0.04, P = 0.06). Similarly, the mortality rate changed from 366.98 per 100,000 in 2010 to 262.03 per 100,000 in 2019, with an AAPC of -2.55% (95% CI, -8.77–4.08%, P = 0.44). In the hospital-based cohort, the decline in survival rates was reported among older patients with gastric cancer in the highest gastric cancer risk area in China, with the 3-year overall survival (OS) decreasing from 58.5% (95% CI, 53.5–63.2%) in 2010 to 34.4% (95%CI, 32.1–36.7%) in 2019, and the 3-year progression-free survival (PFS) decreasing from 51.3% (95%CI, 47.5–55.1%) in 2010 to 34.2% (95%CI, 32.0–36.3%) in 2019, respectively. Moreover, forecasts generated by ARIMA models revealed a significant decline in the incidence and mortality of older gastric cancer in China from 2020 to 2024. Specifically, the incidence rate of older gastric cancer was expected to decrease from 317.94 per 100,000 population in 2020 to 205.59 per 100,000 population in 2024, while the anticipated mortality rate was estimated to decrease from 222.52 per 100,000 population in 2020 to 186.22 per 100,000 population in 2024.

Conclusion

From 2010 to 2019, the incidence and mortality of older gastric cancer remained stable in the highest gastric cancer risk area in China, while the survival rates showed a decline. Based on the ARIMA models, it was anticipated that there might be a continued decline in older gastric cancer incidence and mortality in the highest-risk area in China over the next five years.

Introduction

The worldwide burden of cancer was rapidly increasing as people lived longer and reached older ages [1, 2]. Among the five most prevalent cancers worldwide, gastric cancer ranks fifth, with over 58% of newly diagnosed cases occurring in individuals aged 65 years and older [3]. Notably, China bears a significant burden of gastric cancer, accounting for 42% of global cases [4].

Gansu was the province with the highest incidence and mortality of gastric cancer in China, with the incidence of 79.04 per 100,000 and the mortality of 60.33 per 100,000 in 2016 [5]. There has been an increase in the number of people aged 65 years and older in Gansu province over the past few years, with an increase from 8.23% in 2010 to 13.44% in 2022 [6]. Li et al. [7] reported that the incidence and mortality rates of gastric cancer have increased from 2003 to 2012 in Wuwei, Gansu province. However, the comprehensive analysis of incidence and mortality of gastric cancer among older adults in Gansu province was still lacking. Nevertheless, the survival trends of older patients with gastric cancer in the highest gastric cancer risk area in China remained to be elucidated.

Based on the registration data and hospital-based data, this study was conducted to examine trends of the incidence, mortality, and survival of older gastric cancer in the highest gastric cancer risk area in China from 2010 to 2019, as well as to predict the future cancer burden up to 2024, which may provide valuable information for the adjustment of health policies and optimization of medical resources.

Methods

Study population and data source

In this study, both cancer registration data and hospital-based data in the area with the highest cancer risk in China were used to evaluate the older gastric cancer burden and temporal trends from 2010 to 2019. The incidence and mortality rates of older gastric cancer were pooled from registries in the Gansu Cancer Registration System. Until now, 23 cancer registration sites in Gansu Province reported the 2019 cancer registration data, which covering 36.96% of the province’s population. Gastric cancer was identified by the International Classification of Diseases for Oncology, third edition (ICD-O-3)-tomography (ICD-O-3-T) codes of C16.0-C16.9. Population data were obtained from the data on the total number of residents, gender and age group composition collected annually by local public security departments and statistical departments. Furthermore, survival data of older gastric cancer patients were collected from the First Hospital of Lanzhou University, Lanzhou University Second Hospital, and Gansu Cancer Hospital. The endpoints under consideration in this study were Progress-Free Survival (PFS) and Overall Survival (OS). PFS was delineated as the duration from the date of diagnosis until the occurrence of recurrence, metastasis, or death. Conversely, OS was defined as the time interval from the initiation of diagnosis to the event of death under any circumstance. Enrollment criteria included individuals aged 65 years and older, born and resided in Gansu province, and without a previous cancer diagnosis, except for gastric cancer.

Quality control

The data quality of Gansu Cancer Registry Center was assessed according to the criteria set out in the Guidebook for Cancer Registration in China [8] and the International Center for Research on Cancer (IARC)/The relevant requirements of the International Association for Cancer Registries (IACR) on registration quality [9, 10]. The reliability, completeness, and validity of the data were evaluated according to the main indicators such as the proportion of pathological diagnoses (MV%), the proportion of only death certificates (DCO%), and the death/morbidity ratio (M/I). Finally, the MV%, DCO%, and M/I of the aggregated cancer registry regions included in the analysis were 60.31%, 2.13%, and 0.56, respectively. MSFoxPro, MS-Excel, SAS 9.4, and IARC/IACR’s IARC crgTools software were used [11] to review and evaluate registration and hospital data.

Statistical analysis

The data of each cancer registration site that met the quality control standards of cancer registration were merged and analyzed. The incidence and mortality of older gastric cancer in the highest gastric cancer risk area of China were stratified by area (urban or rural) and gender. According to the National Cancer Center, cities above prefecture level are considered urban areas while counties or county-level cities are considered rural areas. Chinese standard population in 2000 and the Segi’s world standard population were respectively used to calculate the Chinese age-standardized incidence/mortality rate (ASIRC/ASMRC) and the world age-standardized mortality rate (ASIRW/ASMRW). The average annual percent change (AAPC) for the period of 2010–2019 was calculated using the Joinpoint Regression Program to assess changing trends in the incidence and mortality of older gastric cancer. Survival analyses were calculated with the log-rank regression. The Chi-squared test was performed to compare the difference between registration data and hospital-based data. The Autoregressive Integrated Moving Average (ARIMA) model was a useful tool for assessing the impact of large-scale interventions, and it’ s objective was to enhance the predictive accuracy over more rudimentary regression models by characterizing the auto-correlation present within the data, identifying trends, and subsequently integrating this information into the forecast. By incorporating the onset and death time of each older gastric cancer case, while considering variables such as age, gender, geographical location, and seasonal patterns, ARIMA models were employed to generate forecasts for incidence and mortality of older gastric cancer from 2020 to 2024. The stability and reliability of the model were assessed using the mean square error (MSE). The above analysis was conducted using SAS software (Version 9.4), Python software (Version 3.8.1), and Joinpoint Trend Analysis Software (Version 4.9.1.0).

Results

Trends in the incidence of older gastric cancer from 2010 to 2019

TableÌý1; Fig.Ìý1 set out the estimated number of new older gastric cancer cases and the incidence of older gastric cancer during 2010–2019. Overall, the incidence, ASIRC, ASIRW of older gastric cancer in the highest gastric cancer risk area in China were observed to decline from in 439.65 per 100,000, 427.39 per 100,000, 422.18 per 100,000 in 2010 to 330.40 per 100,000, 334.38 per 100,000, and 326.27 per 100,000 in 2019, respectively. However, the results of AAPCs showed no statistic difference for the changing trends of incidence (AAPCs of − 2.59% (95% CI: -5.14 to 0.04%, P = 0.06) in the crude incidence, AAPCs of − 2.32% (95% CI: -5.02 to 0.46%, P = 0.10) in ASIRC, AAPCs of − 2.56% (95% CI: -5.23 to 0.18, P = 0.07) in ASIRW, respectively.). After stratified by sex and area, the incidence of older male gastric cancer was higher than these in females (male to female ratio ranging from 2.90 to 3.73). The incidence of older gastric cancer was also higher in urban areas than rural areas (urban to rural ratio ranging from 1.01 to 1.72), except the incidence in 2012 (urban to rural ratio: 0.75). Moreover, except the crude incidence trends of older female patients with gastric cancer (AAPCs of − 3.12% (95% CI: -6.00% to -0.15%, P = 0.04), no statistical significance were observed in other subgroups of older gastric cancer (AAPCs of − 3.64% (95% CI: -8.02–0.94%), P = 0.12 in males, AAPCs of − 2.58% (95% CI: -5.77–0.72%), P = 0.12 in urban areas, and AAPCs of − 3.15% (95% CI: -8.68–2.72%), P = 0.25 in rural areas, respectively.).

Table 1 Estimated numbers of new older gastric cancer cases and the incidence in the highest gastric cancer risk area in China, 2010 to 2019 (per 100,000 population)

Fig. 1

Time-trends of incidence for the older gastric cancer cases in the highest gastric cancer risk area in China, 2010 to 2019. A: the incidence of older gastric cancer; B: ASIRC of older gastric cancer; C: ASIRW of older gastric cancer; D: the incidence of male older gastric cancer; E: ASIRC of male older gastric cancer; F: ASIRW of male older gastric cancer; G: the incidence of female older gastric cancer; H: ASIRC of female older gastric cancer; I: ASIRW of female older gastric cancer

Trends in the mortality of older gastric cancer from 2010 to 2019

As shown in TableÌý2; Fig.Ìý2, a declining trend was observed in the mortality, ASMRC, and ASMRW of older individuals with gastric cancer in the region of highest prevalence in China from 2010 to 2019 (the mortality 366.98 per 100,000 in 2010 to 262.03 per 100,000 in 2019, ASMRC 342.28 per 100,000 in 2010 to 266.53 per 100,000 in 2019, and ASMRW 330.17 per 100,000 in 2010 to 253.78 per 100,000 in 2019, respectively.), despite the absence of statistically significant differences (AAPCs of − 2.55% (95% CI: −8.77–4.08%, P = 0.44) in the crude mortality, AAPCs of − 2.52% (95% CI: −9.34–4.82%, P = 0.49) in ASMRC, AAPCs of − 2.76% (95% CI: −8.91–3.81%, P = 0.40) in ASMRW). After stratified by sex and area, the mortality of older male gastric cancer was higher than these in females (male to female ratio ranging from 2.04 to 3.85). Moreover, the mortality of older gastric cancer was also higher in urban areas than rural areas (urban to rural ratio ranging from 1.05 to 2.43), except the incidence in 2012 (urban to rural ratio: 0.97). In addition, there were no significant mortality trends in all subgroups of older gastric cancer, with AAPCs of − 4.93% (95%CI:-11.62 to 2.26, P = 0.17) in males, AAPCs of − 3.05% (95%CI:-8.82 to 3.08, P = 0.28) in females, AAPCs of − 2.86% (95%CI:-9.23 to 3.95, P = 0.40) in urban areas, and AAPCs of − 1.45% (95%CI:-6.51 to 3.89, P = 0.54) in rural areas, respectively.

Table 2 Estimated numbers of older gastric cancer deaths and the mortality in the highest gastric cancer risk area in China, 2010 to 2019 (per 100,000 population)

Fig. 2

Time-trends of mortality for the older gastric cancer in the highest gastric cancer risk area in China, 2010 to 2019. A: the mortality of older gastric cancer; B: ASMRC of older gastric cancer; C: ASMRW of older gastric cancer; D:the mortality of male older gastric cancer; E: ASMRC of male older gastric cancer; F: ASMRW of male older gastric cancer; G: the mortality of femal older gastric cancer; H: ASMRC of femal older gastric cancer; I: ASMRW of femal older gastric cancer

Survival of older gastric cancer from 2010 to 2019

Based on the three high-volume gastric cancer cohorts in the highest gastric cancer risk area in China(Supplementary TableÌý1, Supplementary TablesÌý2, and Supplementary TableÌý3), the survival of older gastric cancer patients during 2010–2019 was shown in TableÌý3; Fig.Ìý3. Overall, the median OS and PFS were observed to be 34.0 and 33.0 months, and the 3-year OS and the 3-year PFS were 46.9%(95%CI: 45.1–48.8%), 45.8%(95%CI: 44.0–47.7%), respectively. Following stratification by pTNM stage, older patients exhibited the 3-year OS of 83.7%, 65.9%, 47.2% and 15.7% for pTNM stages I, II, III, and IV, respectively. Similarly, the 3-year PFS for older patients with pTNM stages I, II, III, and IV were 82.9%, 64.7%, 45.0% and 14.7%, respectively. A higher survival rate was detected in female compared to male patients (the 3-year OS 45.5% (95%CI: 43.4–47.6%) in male, 51.8% (95%CI: 48.0–55.8%) in female, respectively). Moreover, the survival trends of older gastric cancer were observed to decrease during the period of 2010 to 2019 (As shown in Fig.Ìý3). In detail, the 3-year OS decreased from 58.5% in 2010 to 34.4% in 2019, while the 3-year PFS decreased from 51.3% in 2010 to 34.2% in 2019. When the survival trend was stratified by sex, the relative decrease was greater among male than female.

Table 3 A. Survival rates of older gastric cancer patients at different ages in the highest gastric cancer risk area in China, 2010 to 2019. B. Survival rates of older gastric cancer patients at different pathological TNM stage in the highest gastric cancer risk area in China, 2010 to 2019

Fig. 3

Time-trends of survival for the older gastric cancer cases in the highest gastric cancer risk area in China, 2010 to 2019. A: Overall survival; B: Progression-free survival

ARIMA models of older gastric cancer from 2020 to 2024

The ARIMA models of future trends in older gastric cancer incidence and mortality through 2024 in the highest gastric cancer risk area in China were presented in Fig.Ìý4. According to this graph, it could be observed that the projected incidence and mortality were expected to exhibit a continued decline between 2020 and 2024. The incidence rate of older gastric cancer in 2024 were expected to decrease to 205.59 per 100,000 (MES: 31.55), and the mortality rate in 2024 were expected to decrease to 186.22 per 100,000 (MES: 39.87).

Fig. 4

ARIMA models for the older gastric cancer in the highest gastric cancer risk area in China, 2020 to 2024. A: Projection of incidence; B: Projections of mortality

Discussion

Gansu Province was located in the northwest of China and had a population of 24.65Ìýmillion in 2023. In recent years, Gansu Province has experienced an increase in the aging population, with an increase from 8.23% in 2010 to 13.65% in 2023. Gastric cancer ranks first in incidence rate and mortality rate among all malignancies in Gansu province [7]. Gansu Central Cancer Registry was first established in 2005 to monitor the cancer burden and provide a decision-making basis for cancer control and prevention policies [12]. There are currently 23 cancer registries establised in Gansu Province covering 86 counties and districts, accounting for about 36.96% of the total population, which might accurately reflect cancer incidence and mortality for the whole province [13].

This study presented a comprehensive analysis of time-trends in the incidence, mortality, and survival of older gastric cancer in Gansu province from 2010 to 2019, and forecast gastric cancer burden of older individuals through 2024. Several key observations could be derived from our study. First, the trends of incidence and mortality of older gastric cancer remained stable from 2010 to 2019, while the survival exhibited a decline. Second, the incidence and mortality of older gastric cancer in Gansu province were projected to decrease to 205.59 per 100,000 (95%CI: 175.3 per 100000 to 235.88 per 100000) and 186.22 per 100,000 (95%CI: 106.93 per 100000 to 265.51 per 100000) by 2024.

In 2019, the ASIRW and ASMRW of gastric cancer among older individuals in Gansu province was 334.38 per 100,000 and 326.27 per 100,000, which was lower than the corresponding rates of 422.18 per 100,000 for ASIRW and 330.17 per 100,000 for ASMRW in 2010. Generally, it was widely thought that the decline in incidence and mortality attributable to the decrease in risk factors for gastric cancer. Helicobacter pylori (Hp) infection has been proven to play an important role in gastric carcinogenesis [14, 15]. Intervention study indicated that the eradication of Hp has been shown to reduce the risk of early gastric cancer by nearly 50% [16]. Thus, the decline in Hp prevalence in Gansu province in recent decades might resulted in the decreasing of gastric cancer incidence among older individuals [17]. Furthermore, environmental factors such as diet, smoking, diabetes, and metabolism diseases also play significant roles in gastric cancer development [18,19,20,21]. Recently, the promotion of healthy lifestyles including a balanced diet, low salt diet, smoking cessation and alcohol restriction in Gansu province might led to the decline of incidence and mortality of older gastric cancer [22].

From 2010 to 2019, the present study revealed the decreased survival rates among older gastric cancer patients in Gansu province, with the reduction of 24.1% in the 3-year overall survival rates and the decrease of 11.0 months in median survival. In general, the decline in survival rates among older patients in Gansu province might be partially attributed to the rise of average diagnosis age, which increased from 69 in 2010 to 72 in 2019. Multiple studies suggested that advanced age was associated with a poor prognosis in gastric cancer [23,24,25,26,27,28]. This correlation might be attributed to the reduced organ function, pharmacokinetic and pharmacodynamic variability, as well as the presence of severe comorbidities in older patients [28]. Moreover, our findings showed that there has been a rise in the percentage of older gastric cancer with pTNM stage IV, which increased from 8.33% in 2010 to 13.15% in 2019. As for the pathological TNM II/III, there was a decline from 27.78 to 20.28%, from 52.78 to 44.87%, respectively. In addition, the percentage of perioperative chemotherapy in older patients with local advanced gastric cancer decreased from 73.68% in 2010 to 52.77% in 2019, which might play a role in the survival decline of older patients in Gansu province.

Significantly higher incidence and mortality rates of older gastric cancer were observed in males compared to females in Gansu province. The reason for this discrepancy was not immediately clear. Several studies found that estrogen was associated with lowered risk of gastric cancer incidence and mortality among women [29, 30]. Larsson et al. [31] showed that the risk factors of gastric cancer, like Hp infection or alcohol drinking, were more prevalent in males than females. Furthermore, our study revealed a notable disparity in the prevalence of gastric cancer among older individuals in the urban and rural areas, potentially attributable to the comparatively limited economic status, inadequate healthcare facilities, and deficient public health consciousness prevalent in rural areas. The highlighted health disparities emphasize the urgency of establishing effective referral channels and developing user-friendly treatment technologies in low-health resource areas to enhance healthcare accessibility and efficacy.

One of the main strengths of this study was the combination of registration data and hospital-based data, enabling the systematic exploration of the incidence, mortality, and survival rates of older gastric cancer in the highest gastric cancer risk area in China. Another strength was that we firstly established the cancer burden model for older gastric cancer, which potentially offering valuable insights for regional gastric cancer prevention and treatment. However, when interpreting the findings of this study, several potential limitations needed to be considered. Firstly, the incidence and mortality data were estimated from cancer registration, which covered 36.96% of the total population in Gansu Province. Nevertheless, at this level of coverage, population-based cancer registration was thought to be able to provide scientific information for developing cancer control policies [12]. Secondly, some variables including the anatomical site, and cause specific survival were not included in our analysis, which might limit our ability to conduct further analyses.

Conclusion

From 2010 to 2019, the incidence and mortality of older gastric cancer remained stable, while the survival rates showed decline in the highest gastric cancer risk area in China. Moreover, the ARIMA models showed the sustained decline in the incidence and mortality of gastric cancer among older individuals over the next five years. More measures and strategies were expected to be proposed for the prevention, early diagnosis, and treatment improvement of older gastric cancer in the highest gastric cancer risk area in China.

Contributors

The conception and design: Penghui Niu, Mingyan He, Quanlin Guan, Dongbing Zhao, Yingtai Chen, Yumin Li, Yuqin Liu; Study material or patients: Fan Zhang, Deyuan Ma, Xiadong Zhou, Yitong Zhu, Lulu Zhao, Xiaoyi Luan, Wanqing Wang; Collecting and/or assembling data: Xiaojie Zhang, Xiaoyi Luan, Xue Han; Data analysis and interpretation: Penghui Niu, Lulu Zhao; Writing: Penghui Niu, Lulu Zhao, Deyuan Ma, Xiadong Zhou.