{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T17:58:01Z","timestamp":1781632681669,"version":"3.54.5"},"reference-count":45,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T00:00:00Z","timestamp":1781568000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003645","name":"National Cancer Center of Korea","doi-asserted-by":"crossref","award":["NCC-2610290-1"],"award-info":[{"award-number":["NCC-2610290-1"]}],"id":[{"id":"10.13039\/501100003645","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100003645","name":"National Cancer Center of Korea","doi-asserted-by":"crossref","award":["NCC-24H1720"],"award-info":[{"award-number":["NCC-24H1720"]}],"id":[{"id":"10.13039\/501100003645","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100003725","name":"National Research Foundation of Korea","doi-asserted-by":"crossref","award":["2022R1A2C2009971"],"award-info":[{"award-number":["2022R1A2C2009971"]}],"id":[{"id":"10.13039\/501100003725","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:sec id=\"sec001\">\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Gastric cancer (GC) is a global health concern, with incidence and mortality varying significantly across populations. The spatial heterogeneity of GC may reflect differences in prevention strategies and their effectiveness, highlighting the need to identify high-risk areas and their possible contributing factors.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec id=\"sec002\">\n                    <jats:title>Objective<\/jats:title>\n                    <jats:p>Leveraging the decline of GC incidence since 2012 affected by nationwide cancer prevention programs in South Korea, this study aimed to identify high- and low-risk clusters and explore the changes in spatial clusters of GC incidence between 2009\u20132013 and 2014\u20132018 before and after the decline, respectively. In addition, we identified geographic characteristics associated with cluster.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec id=\"sec003\">\n                    <jats:title>Method<\/jats:title>\n                    <jats:p>Using national cancer registry and geographic data across 243 districts, we performed spatial clustering analyses in each period. We identified the high- and low-risk areas as the overlapping clusters by two common clustering approaches of local Moran\u2019s I and Getis Ord Gi*. Then, we compared 23 geographic characteristics between high- and low-risk areas and two periods.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec id=\"sec004\">\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>The average GC incidence rate declined in both high- (96\u201379 per 100,000 people) and low-risk districts (73\u201361) between 2009\u20132013 and 2014\u20132018. While cluster locations remained stable, low-risk districts expanded notably (26\u201337) and high-risk districts slightly reduced (31\u201328). As opposed to little geographic characteristics that showed the significant difference between high- and low-risk areas in the early period, the later period gave large green space, frequent regular walking, and reduced self-related obesity in the low-risk area, in addition to sociodemographic advantages, compared to those in the high-risk area (p-value &lt;0.002).<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec id=\"sec005\">\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>Our findings suggest the potential effectiveness of lifestyle- and\/or environment-focused prevention for GC incidence and the need of locally-tailored strategies to reduce cancer burden.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1371\/journal.pone.0349384","type":"journal-article","created":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T17:27:32Z","timestamp":1781630852000},"page":"e0349384","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Spatio-temporal changes in clusters of gastric cancer incidence: The impact of nationwide cancer control programs in South Korea"],"prefix":"10.1371","volume":"21","author":[{"given":"Ji Hyun","family":"Kim","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Won Kyung","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeongseon","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7110-3395","authenticated-orcid":true,"given":"Sun-Young","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2026,6,16]]},"reference":[{"key":"pone.0349384.ref001","author":"J Ferlay","year":"2024"},{"issue":"3","key":"pone.0349384.ref002","first-page":"209","article-title":"Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries","volume":"71","author":"H Sung","year":"2021","journal-title":"CA Cancer J Clin"},{"issue":"10","key":"pone.0349384.ref003","article-title":"Global burden and trends in incidence, mortality, and disability of stomach cancer from 1990 to 2017","volume":"12","author":"Y Qin","year":"2021","journal-title":"Clin Transl Gastroenterol"},{"issue":"5","key":"pone.0349384.ref004","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1136\/gutjnl-2019-320234","article-title":"Is gastric cancer becoming a rare disease? A global assessment of predicted incidence trends to 2035","volume":"69","author":"M Arnold","year":"2020","journal-title":"Gut"},{"issue":"10125","key":"pone.0349384.ref005","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1016\/S0140-6736(17)33326-3","article-title":"Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): analysis of individual records for 37\u2008513\u2008025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries","volume":"391","author":"C Allemani","year":"2018","journal-title":"Lancet"},{"key":"pone.0349384.ref006","author":"Organisation for Economic Co-operation and Development","year":"2022"},{"key":"pone.0349384.ref007","doi-asserted-by":"crossref","first-page":"101404","DOI":"10.1016\/j.eclinm.2022.101404","article-title":"The current and future incidence and mortality of gastric cancer in 185 countries, 2020\u201340: a population-based modelling study","volume":"47","author":"E Morgan","year":"2022","journal-title":"EClinicalMedicine"},{"issue":"3","key":"pone.0349384.ref008","doi-asserted-by":"crossref","first-page":"221","DOI":"10.5230\/jgc.2021.21.e27","article-title":"Korean Gastric Cancer Association-led nationwide survey on surgically treated gastric cancers in 2019.","volume":"21","author":"Information Committee of the Korean Gastric Cancer Association","year":"2021","journal-title":"J Gastric Cancer"},{"issue":"1","key":"pone.0349384.ref009","first-page":"26","article-title":"Epidemiology of gastric cancer: global trends, risk factors and prevention","volume":"14","author":"P Rawla","year":"2019","journal-title":"Prz Gastroenterol"},{"issue":"2","key":"pone.0349384.ref010","doi-asserted-by":"crossref","first-page":"330","DOI":"10.4143\/crt.2022.128","article-title":"Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2019","volume":"54","author":"MJ Kang","year":"2022","journal-title":"Cancer Res Treat"},{"issue":"5","key":"pone.0349384.ref011","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1093\/jjco\/hyn026","article-title":"Cancer control activities in the Republic of Korea","volume":"38","author":"K-Y Yoo","year":"2008","journal-title":"Jpn J Clin Oncol"},{"issue":"1","key":"pone.0349384.ref012","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1186\/s12885-019-5726-x","article-title":"Geospatial analyses identify regional hot spots of diffuse gastric cancer in rural Central America","volume":"19","author":"RL Dominguez","year":"2019","journal-title":"BMC Cancer"},{"issue":"12","key":"pone.0349384.ref013","doi-asserted-by":"crossref","first-page":"1187","DOI":"10.3748\/wjg.v28.i12.1187","article-title":"Epidemiology of stomach cancer","volume":"28","author":"M Ilic","year":"2022","journal-title":"World J Gastroenterol"},{"issue":"4","key":"pone.0349384.ref014","doi-asserted-by":"crossref","first-page":"4555","DOI":"10.1007\/s10708-023-10864-z","article-title":"Spatial and temporal analysis of gastric cancer incidence in northwest Iran","volume":"88","author":"M Soleimani","year":"2023","journal-title":"GeoJournal"},{"key":"pone.0349384.ref015","doi-asserted-by":"crossref","first-page":"116841","DOI":"10.1016\/j.envres.2023.116841","article-title":"Role of geographic characteristics in the spatial cluster detection of cancer: evidence in South Korea, 1999\u20132013","volume":"236","author":"I Song","year":"2023","journal-title":"Environ Res"},{"issue":"4","key":"pone.0349384.ref016","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.4143\/crt.2017.411","article-title":"Geographical variations and trends in major cancer incidences throughout Korea during 1999-2013","volume":"50","author":"Y-J Won","year":"2018","journal-title":"Cancer Res Treat"},{"issue":"16","key":"pone.0349384.ref017","doi-asserted-by":"crossref","first-page":"17418","DOI":"10.1002\/cam4.6365","article-title":"Changes in spatial clusters of cancer incidence and mortality over 15\u2009years in South Korea: implication to cancer control","volume":"12","author":"CT Nguyen","year":"2023","journal-title":"Cancer Med"},{"issue":"2","key":"pone.0349384.ref018","doi-asserted-by":"crossref","first-page":"312","DOI":"10.4143\/crt.2025.264","article-title":"Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2022","volume":"57","author":"EH Park","year":"2025","journal-title":"Cancer Res Treat"},{"key":"pone.0349384.ref019","author":"National Cancer Center"},{"issue":"1","key":"pone.0349384.ref020","doi-asserted-by":"crossref","first-page":"69","DOI":"10.15531\/ksccr.2016.7.1.69","article-title":"Vulnerable homogeneous hotspot areas of the industrial sector for the climate change - focused on mitigation and adaptation perspective -","volume":"7","author":"EJ Yoon","year":"2016","journal-title":"J Clim Change Res"},{"issue":"5","key":"pone.0349384.ref021","doi-asserted-by":"crossref","first-page":"1659","DOI":"10.1080\/19475705.2015.1084542","article-title":"Applying spatial clustering analysis to a township-level social vulnerability assessment in Taiwan","volume":"7","author":"W-Y Lin","year":"2015","journal-title":"Geomatics, Natural Hazards and Risk"},{"issue":"2","key":"pone.0349384.ref022","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1111\/j.1538-4632.1995.tb00338.x","article-title":"Local indicators of spatial association\u2014LISA","volume":"27","author":"L Anselin","year":"1995","journal-title":"Geograph Anal"},{"key":"pone.0349384.ref023","volume-title":"The ESRI guide to GIS analysis, volume 2: spatial measurements and statistics","author":"A Mitchell","year":"2021"},{"issue":"13","key":"pone.0349384.ref024","doi-asserted-by":"crossref","first-page":"6277","DOI":"10.3390\/ijerph20136277","article-title":"A Systematic Review of Areal Units and Adjacency Used in Bayesian Spatial and Spatio-Temporal Conditional Autoregressive Models in Health Research","volume":"20","author":"ZT Tessema","year":"2023","journal-title":"Int J Environ Res Public Health"},{"issue":"4","key":"pone.0349384.ref025","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1111\/j.1538-4632.1995.tb00912.x","article-title":"Local spatial autocorrelation statistics: distributional issues and an application","volume":"27","author":"JK Ord","year":"1995","journal-title":"Geogr Anal"},{"key":"pone.0349384.ref026","article-title":"Regional disparities in major cancer incidence in South Korea, 1999\u20132018","volume":"45","author":"EH Park","year":"2023","journal-title":"Epidemiol Health"},{"key":"pone.0349384.ref027","doi-asserted-by":"crossref","DOI":"10.1002\/9781119558378","volume-title":"Introduction to meta-analysis","author":"M Borenstein","year":"2021","edition":"2"},{"issue":"1","key":"pone.0349384.ref028","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4143\/crt.2014.204","article-title":"Trends in cancer screening rates among Korean men and women: results of the Korean National Cancer Screening Survey, 2004-2013","volume":"48","author":"M Suh","year":"2016","journal-title":"Cancer Res Treat"},{"issue":"5","key":"pone.0349384.ref029","doi-asserted-by":"crossref","DOI":"10.1053\/j.gastro.2018.07.017","article-title":"Effects of organized colorectal cancer screening on cancer incidence and mortality in a large community-based population","volume":"155","author":"TR Levin","year":"2018","journal-title":"Gastroenterology"},{"issue":"1","key":"pone.0349384.ref030","first-page":"327","article-title":"Midcourse evaluation of the second-term 10-year plan for cancer control in Korea","volume":"12","author":"MA Han","year":"2011","journal-title":"Asian Pac J Cancer Prev"},{"issue":"6","key":"pone.0349384.ref031","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1097\/JSM.0000000000000316","article-title":"Physical activity and gastric cancer risk: a systematic review and meta-analysis","volume":"26","author":"T Psaltopoulou","year":"2016","journal-title":"Clin J Sport Med"},{"key":"pone.0349384.ref032","author":"World Cancer Research Fund International","year":"2018"},{"issue":"1","key":"pone.0349384.ref033","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1002\/ijc.21822","article-title":"A prospective study of dietary salt intake and gastric cancer incidence in a defined Japanese population: the Hisayama study","volume":"119","author":"K Shikata","year":"2006","journal-title":"Int J Cancer"},{"key":"pone.0349384.ref034","doi-asserted-by":"crossref","first-page":"801228","DOI":"10.3389\/fnut.2021.801228","article-title":"Dietary salt intake and gastric cancer risk: a systematic review and meta-analysis","volume":"8","author":"B Wu","year":"2021","journal-title":"Front Nutr"},{"issue":"5","key":"pone.0349384.ref035","doi-asserted-by":"crossref","first-page":"1289","DOI":"10.3945\/ajcn.2009.28732","article-title":"Gastric cancer and salt preference: a population-based cohort study in Korea","volume":"91","author":"J Kim","year":"2010","journal-title":"Am J Clin Nutr"},{"issue":"2","key":"pone.0349384.ref036","doi-asserted-by":"crossref","first-page":"189","DOI":"10.7856\/kjcls.2021.32.2.189","article-title":"Predictive analysis of food behavior and related factors using spatial analysis: based on community health survey data 2016","volume":"32","author":"S-M Jeong","year":"2021","journal-title":"Korean J Commun Living Sci"},{"issue":"3","key":"pone.0349384.ref037","doi-asserted-by":"crossref","first-page":"57","DOI":"10.16879\/jkca.2019.19.3.057","article-title":"Analysis of association between cancer incidence and geographical and environmental characteristics using spatial statistical techniques","volume":"19","author":"S-H Lee","year":"2019","journal-title":"J Korean Cartogr Assoc"},{"issue":"3","key":"pone.0349384.ref038","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1007\/s10389-009-0306-1","article-title":"Socioeconomic inequalities in cancer incidence and mortality\u2014a spatial analysis in Bremen, Germany","volume":"18","author":"A Eberle","year":"2010","journal-title":"J Public Health"},{"issue":"4","key":"pone.0349384.ref039","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1158\/1055-9965.EPI-16-0925","article-title":"GPS-based exposure to greenness and walkability and accelerometry-based physical activity","volume":"26","author":"P James","year":"2017","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"key":"pone.0349384.ref040","doi-asserted-by":"crossref","first-page":"156180","DOI":"10.1016\/j.scitotenv.2022.156180","article-title":"Exposure to greenspace and cancer incidence, prevalence, and mortality: a systematic review and meta-analyses","volume":"838","author":"MJ Zare Sakhvidi","year":"2022","journal-title":"Sci Total Environ"},{"issue":"3","key":"pone.0349384.ref041","doi-asserted-by":"crossref","first-page":"775","DOI":"10.31557\/APJCP.2019.20.3.775","article-title":"Risk factors of gastric cancer in high-risk region of China: a population-based case-control study","volume":"20","author":"P Chen","year":"2019","journal-title":"Asian Pac J Cancer Prev"},{"issue":"11","key":"pone.0349384.ref042","doi-asserted-by":"crossref","first-page":"2527","DOI":"10.1007\/s11606-023-08094-7","article-title":"Habitually skipping breakfast is associated with the risk of gastrointestinal cancers: evidence from the kailuan cohort study","volume":"38","author":"T Liu","year":"2023","journal-title":"J Gen Intern Med"},{"key":"pone.0349384.ref043","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.maturitas.2018.05.001","article-title":"Eating habits and behaviors of older people: where are we now and where should we go?","volume":"114","author":"M Yannakoulia","year":"2018","journal-title":"Maturitas"},{"issue":"2","key":"pone.0349384.ref044","article-title":"Seroprevalence of Helicobacter pylori in Korea: a multicenter, nationwide study conducted in 2015 and 2016","volume":"23","author":"JH Lee","year":"2018","journal-title":"Helicobacter"},{"issue":"10","key":"pone.0349384.ref045","article-title":"Trends in the seroprevalence of Helicobacter pylori infection and its putative eradication rate over 18 years in Korea: a cross-sectional nationwide multicenter study","volume":"13","author":"SH Lim","year":"2018","journal-title":"PLoS One"}],"container-title":["PLOS One"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0349384","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T17:27:51Z","timestamp":1781630871000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0349384"}},"subtitle":[],"editor":[{"given":"Jie","family":"Yang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026,6,16]]},"references-count":45,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2026,6,16]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0349384","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,16]]}}}