GRAPHICAL ABSTRACT

Key Message

• The COVID-19 pandemic disrupted cancer diagnosis and treatment, particularly for gastric cancer, where early diagnosis and timely treatment are critical for survival.

• Using age-specific gastric cancer mortality trends from 2015–2019, we estimated expected deaths during 2020–2023 and quantified excess mortality in Korea using P-scores.

• The pre-pandemic decline in age-standardized gastric cancer mortality slowed during the pandemic. Excess mortality increased from 3.8% in 2020 to 20.7% in 2023, with the largest increases observed among adults aged 60–79 years.

INTRODUCTION

The coronavirus disease 2019 (COVID-19) pandemic caused substantial disruptions in medical care for patients with cancer, including declines in screening, diagnosis, treatment, and outpatient visits [1,2]. These disruptions raised concerns about delayed detection and suboptimal cancer management, which may have led to more advanced stages at diagnosis and lower survival rates [3,4]. The magnitude of these effects is expected to vary across cancer types, with the greatest negative impact likely occurring in cancers for which timely detection is central to improving outcomes.

Gastric cancer, which ranks fifth globally in incidence and fourth in mortality [5], is particularly vulnerable to pandemic-related healthcare interruptions because long-term declines in gastric cancer mortality have been driven largely by widespread screening and timely treatment [6]. In East Asian countries with established national screening programs, such as Korea and Japan, screening participation declined during the pandemic [7-9], accompanied by an increase in late-stage diagnoses [10,11]. Similar patterns have been reported in many other countries [12].

Excess mortality provides a comprehensive measure of the overall impact of the pandemic by capturing deaths beyond the number expected under normal circumstances [13]. Although prior research has focused primarily on all-cause mortality, disease-specific excess mortality analyses are essential for identifying differential effects across conditions. For cancer, site-specific excess mortality assessments are particularly important because cancers differ substantially in their natural history, screening pathways, and treatment approaches.

Several studies have compared gastric cancer mortality or survival rates between the pre-pandemic and pandemic periods, but results have varied across countries [14-17]. Because these analyses did not account for long-term secular trends in gastric cancer mortality, which can differ substantially among countries and should be considered in formal excess mortality evaluations, their findings are difficult to interpret. In addition, many studies examined only the early phase of the pandemic when comparing outcomes with those in the pre-pandemic period. However, because the adverse effects of reduced screening and delayed diagnosis often take time to emerge, longer follow-up periods are needed.

Several statistical methods are available for estimating excess mortality. Studies that applied different approaches to estimate all-cause excess mortality in Korea reported broadly consistent results when the models accounted for changes in age structure and long-term mortality trends [18-20]. Importantly, complex statistical models do not necessarily yield valid estimates. For example, a global analysis comparing excess mortality across countries used an ensemble of 6 statistical models [21]. However, this study was widely criticized for producing implausible estimates in many countries because the estimated expected deaths deviated substantially from pre-pandemic trends in observed deaths [22,23]. These findings underscore the importance of graphical comparisons between estimated excess mortality and underlying pre-pandemic mortality trends.

Therefore, this study estimated excess mortality from gastric cancer in Korea from 2020 to 2023 using an age-adjusted linear regression approach previously applied in national analyses of all-cause excess mortality in Korea [19]. This method is intuitive and facilitates comparison with observed pre-pandemic mortality trends. Given the persistent pre-pandemic decline in gastric cancer mortality [24], we hypothesized that this downward trend would attenuate during the pandemic period.

MATERIALS AND METHODS

Data and study population

Data on the number of gastric cancer deaths, defined using International Classification of Diseases, 10th revision code C16, from 2015 to 2023 were obtained from Statistics Korea’s cause-of-death database [13]. Data on the registered resident population by 10-year age group, from 0–9 years to ≥90 years, were also obtained from the Korean Statistical Office [13].

Statistical analysis

Annual crude mortality rates and age-standardized mortality rates for gastric cancer per 100,000 population were first calculated from 2015 to 2023. Age standardization was performed using the 2019 population as the standard population. Excess mortality from gastric cancer was then estimated for each year from 2020 to 2023. Excess mortality was expressed as the P-score, defined as follows: P-score=[(observed deaths−expected deaths)/expected deaths]×100 [14]. Observed deaths corresponded to the recorded number of gastric cancer deaths during 2020–2023, whereas expected deaths were derived from age-specific mortality trends during the pre-pandemic reference period of 2015–2019, stratified by 10-year age group.

Expected deaths were estimated in 3 steps. First, linear regression was applied to age-specific mortality rates from 2015 to 2019 to predict age-specific rates for 2020–2023. Second, the predicted age-specific rates were multiplied by the corresponding age-specific population sizes for each year. Third, the resulting age-specific expected death counts were summed to obtain total expected deaths for each year.

P-scores were calculated for the total population and separately for men and women using the same approach. Age-specific P-scores were also estimated for 3 age groups: 20–59, 60–79, and ≥80 years. These broader age categories were selected to reduce instability caused by small numbers of deaths in narrower age bands. However, because individuals aged ≥40 years are eligible for the national gastric cancer screening program in Korea, additional results are presented after further stratifying the 20–59-year age group at age 40. The 95% confidence intervals (CIs) for P-scores were calculated using the standard normal approximation for Poisson-distributed death counts. Analyses were performed using Microsoft Excel (Microsoft Corp., Redmond, WA, USA) and SPSS version 25.0 (IBM Corp., Armonk, NY, USA).

Ethics statement

This study used publicly available data and did not require approval from the institutional review board.

RESULTS

Figure 1 presents trends in crude and age-standardized mortality rates for gastric cancer from 2015 to 2023. The dotted lines represent a visual extension of the linear downward trends observed during 2015–2019, extended into 2020–2023. These lines provide an illustrative visual guide rather than exact projections derived from the fitted regression equations. Before the pandemic, both crude and age-standardized mortality declined steadily, with a sharper decline in the age-standardized rate, consistent with rapid population aging in Korea. Although mortality continued to decline during the pandemic, the pace of decline progressively attenuated, with this attenuation becoming more pronounced each year.

Table 1 presents observed deaths, expected deaths, and excess mortality, expressed as P-scores, for gastric cancer during the pandemic period. P-scores were +3.8% in 2020, +5.5% in 2021, +10.6% in 2022, and +20.7% in 2023, indicating a gradual and substantial increase in excess mortality over time, with the highest level observed in 2023. These results closely correspond to the visual patterns shown in Figure 1. When stratified by gender, excess mortality was consistently higher among women than among men. Among men, P-scores were +2.2%, +3.7%, +8.8%, and +13.2% from 2020 to 2023, respectively, whereas the corresponding values among women were +8.1%, +5.2%, +14.7%, and +22.7%.

Figure 2 presents age-specific gastric cancer mortality trends across 3 age groups. When the pre-pandemic linear trends from 2015 to 2019 were extended into the pandemic period, the 60–79-year age group showed a marked weakening of the previously declining mortality trend. In the ≥80-year group, which had the highest mortality, rates continued to decline through 2022 but shifted upward in 2023. In contrast, no meaningful excess mortality was observed among individuals aged 20–59 years.

Table 2 summarizes observed deaths, expected deaths, and excess mortality by age group. The most pronounced excess mortality occurred among adults aged 60–79 years, with P-scores of +9.7% in 2020, +15.1% in 2021, +32.6% in 2022, and +46.6% in 2023. Among those aged ≥80 years, excess mortality increased only in 2023, reaching +12.8%. Consistent with the visual patterns, no statistically meaningful excess mortality was detected among individuals aged 20–59 years. However, when the 20–59-year age group was further stratified at age 40, P-scores among individuals aged 20–39 years were +33.8%, +38.4%, +92.9%, and +143.4% from 2020 to 2023, respectively, and remained statistically significant despite wide confidence intervals. In contrast, the corresponding values among those aged 40–59 years were +1.2%, −5.6%, −8.3%, and −3.1%.

DISCUSSION

This study demonstrated that the COVID-19 pandemic adversely affected gastric cancer mortality in Korea. Although gastric cancer mortality continued its long-term decline from 2015 to 2023, the pace of decline weakened during the pandemic period, resulting in measurable excess mortality. Consistent with this pattern, P-scores increased steadily from the first year of the pandemic and continued to rise through 2023.

Age-stratified analyses showed that excess mortality was most pronounced among individuals aged 60–79 years, whereas it remained minimal among those younger than 60 years. Among adults aged ≥80 years, excess mortality was not evident from 2020 to 2022, but a notable increase emerged in 2023. In this oldest age group, the previously declining mortality trend reversed and shifted upward in 2023. When stratified by gender, excess mortality was more evident among women than among men.

Because Korea’s national gastric cancer screening program begins at age 40, the 20–59-year age group was further stratified at age 40. In these analyses, individuals aged 20–39 years exhibited the highest excess mortality, with a steadily increasing trend throughout the pandemic, whereas those aged 40–59 years showed estimates closer to the null or even negative excess mortality. However, findings for the 20–39-year age group should be interpreted with caution because the number of observed deaths was small. Although stratification at age 40 is clinically relevant, interpretations based on broader age groups may be more appropriate in the present study.

To our knowledge, no previous studies have applied formal excess mortality analyses that account for long-term trends in gastric cancer mortality. Existing studies have instead relied largely on comparisons of mortality or survival outcomes between the pre-pandemic and pandemic periods without formal excess mortality methods, yielding heterogeneous results across countries. For example, studies from Japan and Portugal reported decreased survival or increased mortality during the pandemic [14,15], whereas studies from Israel and Spain found no meaningful change in gastric cancer mortality [16,17]. These mixed findings suggest that pandemic-related effects on gastric cancer outcomes differed across countries.

Despite the high incidence of gastric cancer in Korea, widespread screening programs that detect precursor lesions and early-stage tumors have contributed to relatively high 5-year survival rates [25]. Accordingly, disruptions in access to diagnostic and treatment services during the pandemic would be expected to increase excess mortality [9,10]. Although delayed diagnosis and suboptimal treatment both contribute to gastric cancer mortality, their relative influence likely differed across phases of the pandemic. In the early period, such as 2020, disruptions in treatment may have played a greater role in increasing excess mortality. Over time, however, the cumulative effects of delayed screening and postponed diagnostic evaluations would be expected to exert an increasingly substantial impact.

However, a study of Korean adults aged 40–74 years reported a surge in gastric cancer screening, particularly endoscopy, in 2021 after screening rates declined in 2020 [26]. Therefore, delayed diagnosis and suboptimal treatment may not fully explain the progressive increase in excess mortality from 2020 to 2023. Additional factors may also have contributed to excess gastric cancer mortality, although these factors remain unclear.

This study has several limitations. First, although excess mortality was estimated using death certificate data, misclassification of cause of death during the pandemic cannot be ruled out. Previous reports have documented substantial inaccuracies in cause-of-death certification during this period [27]. Such misclassification likely led to underestimation rather than overestimation of gastric cancer mortality because patients with underlying conditions were frequently coded as COVID-19 deaths if they tested positive by polymerase chain reaction. Second, excess mortality estimates can vary depending on the statistical methods used and the choice of reference period. However, prior studies of all-cause excess mortality in Korea have reported relatively consistent results when accounting for age structure and long-term mortality trends [18-20]. Notably, gastric cancer mortality declined steadily from 1999 to 2022, with a steeper decline in earlier years [24]. Consequently, using a longer pre-pandemic reference period would likely produce higher excess mortality estimates than those reported in the present study. Third, excess mortality estimates for subgroups with low gastric cancer mortality may be unstable because of small numbers of deaths. In particular, the markedly elevated excess mortality among individuals aged 20–39 years warrants cautious interpretation. Fourth, although this study included 4 years of data after the onset of the pandemic, the full impact of delayed diagnosis may not yet be evident because these effects can take longer to manifest.

In summary, excess gastric cancer mortality increased steadily from 2020 to 2023, with the greatest impact observed among individuals aged 60–79 years. Given the central importance of early detection and prompt treatment for gastric cancer outcomes, these findings suggest that pandemic-related disruptions adversely affected cancer control efforts. Because the consequences of delayed screening may take years to fully emerge, continued long-term surveillance of mortality trends is essential. Identifying subgroups with disproportionately high excess mortality will also be important for guiding targeted strategies to protect patients with cancer during future public health emergencies.

Data availability

NOTES

Conflict of interest

The authors have no conflicts of interest to declare for this study.

Funding

None.

Acknowledgements

None.

Author contributions

Conceptualization: Lee DH. Data curation: Kim G. Formal analysis: Kim G. Funding acquisition: None. Methodology: Lee DH. Visualization: Kim G. Writing – original draft: Kim G. Writing – review & editing: Shin JY, Lee YM, Lee DH.

Figure 1.

Trends in crude and age-standardized mortality rates for gastric cancer in Korea, 2015–2023. The blue solid line represents the crude mortality rate, and the red solid line represents the age-standardized mortality rate. The dotted lines depict an illustrative extension of the 2015–2019 linear trends into 2020–2023. The 2019 population was used as the standard population for calculating age-standardized mortality.

Figure 2.

Trends in age-specific gastric cancer mortality rates in Korea, 2015–2023 (A) 20-59 years, (B) 60-79 years, and (C) ≥80 years. The red solid lines represent age-specific mortality rates. The dotted lines depict a visual continuation of the 2015–2019 linear trends into 2020–2023.

REFERENCES

• 1. Chen RC, Haynes K, Du S, Barron J, Katz AJ. Association of cancer screening deficit in the United States with the COVID-19 pandemic. JAMA Oncol 2021;7:878-884. https://doi.org/10.1001/jamaoncol.2021.0884ArticlePubMedPMC
• 2. Richards M, Anderson M, Carter P, Ebert BL, Mossialos E. The impact of the COVID-19 pandemic on cancer care. Nat Cancer 2020;1:565-567. https://doi.org/10.1038/s43018-020-0074-yArticlePubMedPMC
• 3. Al-Quteimat OM, Amer AM. The impact of the COVID-19 pandemic on cancer patients. Am J Clin Oncol 2020;43:452-455. https://doi.org/10.1097/COC.0000000000000712ArticlePubMedPMC
• 4. Moraliyage H, De Silva D, Ranasinghe W, Adikari A, Alahakoon D, Prasad R, et al. Cancer in lockdown: impact of the COVID-19 pandemic on patients with cancer. Oncologist 2021;26:e342-e344. https://doi.org/10.1002/onco.13604Article
• 5. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021;71:209-249. https://doi.org/10.3322/caac.21660Article
• 6. Zhang X, Li M, Chen S, Hu J, Guo Q, Liu R, et al. Endoscopic screening in Asian countries Is associated with reduced gastric cancer mortality: a meta-analysis and systematic review. Gastroenterology 2018;155:347-354. https://doi.org/10.1053/j.gastro.2018.04.026Article
• 7. Fujita M, Nagashima K, Suzuki K, Kasai T, Hashimoto H, Yamaguchi K, et al. Changes in the number of cancer diagnosis practices due to the COVID-19 pandemic: interrupted time-series analysis using the National Database of Japan. J Cancer Res Clin Oncol 2023;149:6023-6033. https://doi.org/10.1007/s00432-022-04557-2ArticlePubMedPMC
• 8. Park H, Seo SH, Park JH, Yoo SH, Keam B, Shin A. The impact of COVID-19 on screening for colorectal, gastric, breast, and cervical cancer in Korea. Epidemiol Health 2022;44:e2022053. https://doi.org/10.4178/epih.e2022053ArticlePubMedPMC
• 9. Suh MA, Park SB, Kwak MS, Yoon JY, Cha JM. Impact of the COVID-19 pandemic on esophagogastroduodenoscopy and gastric cancer claims in South Korea: a nationwide, population-based study. Yonsei Med J 2023;64:549-557. https://doi.org/10.3349/ymj.2023.0074ArticlePubMedPMC
• 10. Hong M, Choi M, Lee J, Kim KH, Kim H, Lee CK, et al. Impact of coronavirus disease 2019 on gastric cancer diagnosis and stage: a single-institute study in South Korea. J Gastric Cancer 2023;23:574-583. https://doi.org/10.5230/jgc.2023.23.e36ArticlePubMedPMC
• 11. Kuzuu K, Misawa N, Ashikari K, Kessoku T, Kato S, Hosono K, et al. Gastrointestinal cancer stage at diagnosis before and during the COVID-19 pandemic in Japan. JAMA Netw Open 2021;4:e2126334. https://doi.org/10.1001/jamanetworkopen.2021.26334ArticlePubMedPMC
• 12. Herrera-Kok JH, Parmar C, Bangash AH, Samadov E, Demirli Atici S, Cheruvu CV, et al. Global impact of COVID-19 pandemic on gastric cancer patients. Eur J Surg Oncol 2023;49:876-877. https://doi.org/10.1016/j.ejso.2023.02.016ArticlePubMedPMC
• 13. Ioannidis JP. Over- and under-estimation of COVID-19 deaths. Eur J Epidemiol 2021;36:581-588. https://doi.org/10.1007/s10654-021-00787-9ArticlePubMedPMC
• 14. Morais S, Antunes L, Rodrigues J, Fontes F, Bento MJ, Lunet N. The impact of the COVID-19 pandemic on the short-term survival of patients with cancer in Northern Portugal. Int J Cancer 2021;149:287-296. https://doi.org/10.1002/ijc.33532ArticlePubMedPMC
• 15. Shigenobu Y, Miyamori D, Ikeda K, Yoshida S, Kikuchi Y, Kanno K, et al. Assessing the influence of the COVID-19 pandemic on gastric cancer mortality risk. J Clin Med 2024;13:715. https://doi.org/10.3390/jcm13030715ArticlePubMedPMC
• 16. Roura P, Puigoriol E, Altimiras J, Batiste-Alentorn E, Dégano IR. Trend and joinpoint analysis of cancer incidence and 1-year mortality in north-east Spain 2005-2020. Cancers (Basel) 2023;15:5527. https://doi.org/10.3390/cancers15235527Article
• 17. Abu-Freha N, Hizkiya R, Abu-Abed M, Michael T, Jacob BM, Rouvinov K, et al. The impact of the COVID-19 pandemic on colorectal and gastric cancer diagnosis, disease stage and mortality. Front Med (Lausanne) 2022;9:954878. https://doi.org/10.3389/fmed.2022.954878ArticlePubMedPMC
• 18. Han C, Jang H, Oh J. Excess mortality during the coronavirus disease pandemic in Korea. BMC Public Health 2023;23:1698. https://doi.org/10.1186/s12889-023-16546-2ArticlePubMedPMC
• 19. Im SJ, Shin JY, Lee DH. Excess deaths in Korea during the COVID-19 pandemic: 2020-2022. J Prev Med Public Health 2024;57:480-489. https://doi.org/10.3961/jpmph.24.254ArticlePubMedPMC
• 20. Jang M, Kim S, Choi S, Ryu B, Choi SY, Choi S, et al. Estimating excess mortality during the COVID-19 pandemic between 2020-2022 in Korea. J Korean Med Sci 2024;39:e267. https://doi.org/10.3346/jkms.2024.39.e267ArticlePubMedPMC
• 21. COVID-19 Excess Mortality Collaborators. Estimating excess mortality due to the COVID-19 pandemic: a systematic analysis of COVID-19-related mortality, 2020-21. Lancet 2022;399:1513-1536. https://doi.org/10.1016/S0140-6736(21)02796-3ArticlePubMedPMC
• 22. Schöley J, Karlinsky A, Kobak D, Tallack C. Conflicting COVID-19 excess mortality estimates. Lancet 2023;401:431-432. https://doi.org/10.1016/S0140-6736(23)00116-2ArticlePubMedPMC
• 23. Bager P, Nielsen J, Bhatt S, Nielsen LB, Krause TG, Vestergaard LS, et al. Conflicting COVID-19 excess mortality estimates. Lancet 2023;401:432-433. https://doi.org/10.1016/S0140-6736(23)00115-0ArticlePubMedPMC
• 24. Park KB, Kang MJ, Ha J, Park EH, Yun EH, Kim HJ, et al. Epidemiology of gastric cancer in Korea (1999-2022): incidence, survival, and 5-year conditional relative survival. J Gastric Cancer 2026;26:4-15. https://doi.org/10.5230/jgc.2026.26.e13Article
• 25. GBD 2017 Stomach Cancer Collaborators. The global, regional, and national burden of stomach cancer in 195 countries, 1990-2017: a systematic analysis for the Global Burden of Disease study 2017. Lancet Gastroenterol Hepatol 2020;5:42-54. https://doi.org/10.1016/S2468-1253(19)30328-0ArticlePubMedPMC
• 26. Lee K, Suh M, Jun JK, Choi KS. Impact of the COVID-19 pandemic on gastric cancer screening in South Korea: results from the Korean National Cancer Screening Survey (2017-2021). J Gastric Cancer 2022;22:264-272. https://doi.org/10.5230/jgc.2022.22.e36ArticlePubMedPMC
• 27. Prahlow JA, VanderVeen MH, Storer JD. Cremation permit review and COVID-19 death certificates. Am J Forensic Med Pathol 2023;44:90-96. https://doi.org/10.1097/PAF.0000000000000814ArticlePubMedPMC

Figure & Data

References

Citations

Citations to this article as recorded by