{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,13]],"date-time":"2026-03-13T05:37:54Z","timestamp":1773380274373,"version":"3.50.1"},"reference-count":47,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,11,15]],"date-time":"2021-11-15T00:00:00Z","timestamp":1636934400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,11,15]],"date-time":"2021-11-15T00:00:00Z","timestamp":1636934400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Universidad Publica de Navarra","award":["Proyecto J\u00f3venes Investigadores PJUPNA2018-11"],"award-info":[{"award-number":["Proyecto J\u00f3venes Investigadores PJUPNA2018-11"]}]},{"name":"Spanish Research Agency and Feder","award":["MTM2017-82553-R"],"award-info":[{"award-number":["MTM2017-82553-R"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The distribution of lip, oral cavity, and pharynx (LOCP) cancer mortality rates in small domains (defined as the combination of province, age group, and gender) remains unknown in Spain. As many of the LOCP risk factors are preventable, specific prevention programmes could be implemented but this requires a clear specification of the target population. This paper provides an in-depth description of LOCP mortality rates by province, age group and gender, giving a complete overview of the disease. This study also presents a methodological challenge. As the number of LOCP cancer cases in small domains (province, age groups and gender) is scarce, univariate spatial models do not provide reliable results or are even impossible to fit. In view of the close link between LOCP and lung cancer, we consider analyzing them jointly by using shared component models. These models allow information-borrowing among diseases, ultimately providing the analysis of cancer sites with few cases at a very disaggregated level. Results show that males have higher mortality rates than females and these rates increase with age. Regions located in the north of Spain show the highest LOCP cancer mortality rates.<\/jats:p>","DOI":"10.1038\/s41598-021-01765-7","type":"journal-article","created":{"date-parts":[[2021,11,15]],"date-time":"2021-11-15T11:03:36Z","timestamp":1636974216000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Estimating LOCP cancer mortality rates in small domains in Spain using its relationship with lung cancer"],"prefix":"10.1038","volume":"11","author":[{"given":"Garazi","family":"Retegui","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jaione","family":"Etxeberria","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mar\u00eda Dolores","family":"Ugarte","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2021,11,15]]},"reference":[{"key":"1765_CR1","doi-asserted-by":"publisher","first-page":"394","DOI":"10.3322\/caac.21492","volume":"68","author":"F Bray","year":"2018","unstructured":"Bray, F. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 68, 394\u2013424 (2018).","journal-title":"CA Cancer J. Clin."},{"key":"1765_CR2","doi-asserted-by":"publisher","first-page":"356","DOI":"10.1016\/j.ejca.2018.07.005","volume":"103","author":"J Ferlay","year":"2018","unstructured":"Ferlay, J. et al. Cancer incidence and mortality patterns in Europe: Estimates for 40 countries and 25 major cancers in 2018. Eur. J. Cancer 103, 356\u2013387 (2018).","journal-title":"Eur. J. Cancer"},{"key":"1765_CR3","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1186\/1471-2407-14-254","volume":"14","author":"D Seoane-Mato","year":"2014","unstructured":"Seoane-Mato, D. et al. Trends in oral cavity, pharyngeal, oesophageal and gastric cancer mortality rates in Spain, 1952\u20132006: An age-period-cohort analysis. BMC Cancer 14, 254 (2014).","journal-title":"BMC Cancer"},{"key":"1765_CR4","doi-asserted-by":"crossref","unstructured":"Cabanes, A. et\u00a0al. Cancer mortality trends in Spain: 1980\u20132007. Ann. Oncol. 21, iii14\u2013iii20 (2010).","DOI":"10.1093\/annonc\/mdq089"},{"key":"1765_CR5","doi-asserted-by":"publisher","first-page":"400","DOI":"10.1016\/j.oraloncology.2010.06.010","volume":"47","author":"M Bonifazi","year":"2011","unstructured":"Bonifazi, M. et al. Age-period-cohort analysis of oral cancer mortality in Europe: The end of an epidemic?. Oral Oncol. 47, 400\u2013407 (2011).","journal-title":"Oral Oncol."},{"key":"1765_CR6","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1186\/1471-2458-6-17","volume":"6","author":"G Lopez-Abente","year":"2006","unstructured":"Lopez-Abente, G. et al. Municipal distribution of bladder cancer mortality in Spain: Possible role of mining and industry. BMC Public Health 6, 17 (2006).","journal-title":"BMC Public Health"},{"key":"1765_CR7","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1136\/jech.2005.041491","volume":"61","author":"R Ramis-Prieto","year":"2007","unstructured":"Ramis-Prieto, R. et al. Modelling of municipal mortality due to haematological neoplasias in Spain. J. Epidemiol. Commun. Health 61, 165\u2013171 (2007).","journal-title":"J. Epidemiol. Commun. Health"},{"key":"1765_CR8","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1016\/j.envres.2017.03.009","volume":"156","author":"JA Ortega-Garc\u00eda","year":"2017","unstructured":"Ortega-Garc\u00eda, J. A. et al. Childhood cancer in small geographical areas and proximity to air-polluting industries. Environ. Res. 156, 63\u201373 (2017).","journal-title":"Environ. Res."},{"key":"1765_CR9","unstructured":"Instituto de Salud Carlos III. Servidor Interactivo de Informaci\u00f3n Epidemiol\u00f3gica (ARIADNA). http:\/\/ariadna.cne.isciii.es\/ (2004)."},{"key":"1765_CR10","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1111\/j.0006-341X.2001.00197.x","volume":"57","author":"C Dean","year":"2001","unstructured":"Dean, C., Ugarte, M. D. & Militino, A. F. Detecting interaction between random region and fixed age effects in disease mapping. Biometrics 57, 197\u2013202 (2001).","journal-title":"Biometrics"},{"key":"1765_CR11","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1191\/0962280205sm389oa","volume":"14","author":"L Held","year":"2005","unstructured":"Held, L., Nat\u00e1rio, I., Fenton, S. E., Rue, H. & Becker, N. Towards joint disease mapping. Stat. Methods Med. Res. 14, 61\u201382 (2005).","journal-title":"Stat. Methods Med. Res."},{"key":"1765_CR12","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1177\/0962280206071642","volume":"15","author":"L Held","year":"2006","unstructured":"Held, L., Graziano, G., Frank, C. & Rue, H. Joint spatial analysis of gastrointestinal infectious diseases. Stat. Methods Med. Res. 15, 465\u2013480 (2006).","journal-title":"Stat. Methods Med. Res."},{"key":"1765_CR13","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1111\/j.1467-9868.2008.00700.x","volume":"71","author":"H Rue","year":"2009","unstructured":"Rue, H., Martino, S. & Chopin, N. Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. J. R. Stat. Soc. Ser. B (Stat. Methodol.) 71, 319\u2013392 (2009).","journal-title":"J. R. Stat. Soc. Ser. B (Stat. Methodol.)"},{"key":"1765_CR14","unstructured":"Martino, S. & Rue, H. Implementing Approximate Bayesian Inference Using Integrated Nested Laplace Approximation: A Manual for the INLA Program (Department of Mathematical Sciences, NTNU, 2009)."},{"key":"1765_CR15","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1111\/1467-9868.00353","volume":"64","author":"DJ Spiegelhalter","year":"2002","unstructured":"Spiegelhalter, D. J., Best, N. G., Carlin, B. P. & Van Der Linde, A. Bayesian measures of model complexity and fit. J. R. Stat. Soc. Ser. B (Stat. Methodol.) 64, 583\u2013639 (2002).","journal-title":"J. R. Stat. Soc. Ser. B (Stat. Methodol.)"},{"key":"1765_CR16","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1016\/j.neunet.2009.08.002","volume":"23","author":"S Watanabe","year":"2010","unstructured":"Watanabe, S. Equations of states in singular statistical estimation. Neural Netw. 23, 20\u201334 (2010).","journal-title":"Neural Netw."},{"key":"1765_CR17","doi-asserted-by":"publisher","first-page":"359","DOI":"10.1198\/016214506000001437","volume":"102","author":"T Gneiting","year":"2007","unstructured":"Gneiting, T. & Raftery, A. E. Strictly proper scoring rules, prediction, and estimation. J. Am. Stat. Assoc. 102, 359\u2013378 (2007).","journal-title":"J. Am. Stat. Assoc."},{"key":"1765_CR18","first-page":"1","volume":"32","author":"D Simpson","year":"2017","unstructured":"Simpson, D., Rue, H., Riebler, A., Martins, T. G. & S\u00f8rbye, S. H. Penalising model component complexity: A principled, practical approach to constructing priors. Stat. Sci. 32, 1\u201328 (2017).","journal-title":"Stat. Sci."},{"key":"1765_CR19","doi-asserted-by":"publisher","first-page":"749","DOI":"10.1007\/s00477-017-1405-0","volume":"32","author":"T Goicoa","year":"2018","unstructured":"Goicoa, T., Adin, A., Ugarte, M. D. & Hodges, J. S. In spatio-temporal disease mapping models, identifiability constraints affect PQL and INLA results. Stochastic Environ. Res. Risk Assess. 32, 749\u2013770 (2018).","journal-title":"Stochastic Environ. Res. Risk Assess."},{"key":"1765_CR20","unstructured":"R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2019)."},{"key":"1765_CR21","doi-asserted-by":"publisher","first-page":"170","DOI":"10.1016\/S1368-8375(99)00084-6","volume":"36","author":"LA Moreno-L\u00f3pez","year":"2000","unstructured":"Moreno-L\u00f3pez, L. A. et al. Risk of oral cancer associated with tobacco smoking, alcohol consumption and oral hygiene: A case-control study in Madrid. Spain. Oral Oncol. 36, 170\u2013174 (2000).","journal-title":"Spain. Oral Oncol."},{"key":"1765_CR22","doi-asserted-by":"publisher","first-page":"1194","DOI":"10.1093\/jnci\/91.14.1194","volume":"91","author":"SS Hecht","year":"1999","unstructured":"Hecht, S. S. Tobacco smoke carcinogens and lung cancer. JNCI J. Natl. Cancer Inst. 91, 1194\u20131210 (1999).","journal-title":"JNCI J. Natl. Cancer Inst."},{"key":"1765_CR23","doi-asserted-by":"publisher","first-page":"494","DOI":"10.1002\/ijc.2910590411","volume":"59","author":"DM Parkin","year":"1994","unstructured":"Parkin, D. M., Pisani, P., Lopez, A. D. & Masuyer, E. At least one in seven cases of cancer is caused by smoking. Global estimates for 1985. Int. J. Cancer 59, 494\u2013504 (1994).","journal-title":"Int. J. Cancer"},{"key":"1765_CR24","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1097\/00008469-200302000-00009","volume":"12","author":"E Fern\u00e1ndez","year":"2003","unstructured":"Fern\u00e1ndez, E. et al. Prevalence of cigarette smoking by birth cohort among males and females in Spain, 1910\u20131990. Eur. J. Cancer Prevent. 12, 57\u201362 (2003).","journal-title":"Eur. J. Cancer Prevent."},{"key":"1765_CR25","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1136\/tobaccocontrol-2014-051892","volume":"25","author":"U Bilal","year":"2016","unstructured":"Bilal, U. et al. Gender equality and smoking: A theory-driven approach to smoking gender differences in Spain. Tobacco Control 25, 295\u2013300 (2016).","journal-title":"Tobacco Control"},{"key":"1765_CR26","first-page":"14","volume":"120","author":"E Fern\u00e1ndez","year":"2003","unstructured":"Fern\u00e1ndez, E. et al. Prevalencia del consumo de tabaco en Espa\u00f1a entre 1945 y 1995. Reconstrucci\u00f3n a partir de las Encuestas Nacionales de Salud. Med. Cl\u00edn. 120, 14\u201316 (2003).","journal-title":"Med. Cl\u00edn."},{"key":"1765_CR27","unstructured":"Sociedad Espa\u00f1ola de Oncolog\u00eda M\u00e9dica. Las cifras del c\u00e1ncer en Espa\u00f1a 2020. https:\/\/seom.org\/seomcms\/images\/stories\/recursos\/Cifras_del_cancer_2020.pdf (2020)."},{"issue":"2","key":"1765_CR28","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1016\/j.arbres.2020.04.025","volume":"57","author":"L Cayuela","year":"2021","unstructured":"Cayuela, L. et al. The beginning of the trend change in lung cancer mortality trends in Spain, 1980\u20132018. Arch. Bronconeumol. (Engl Ed). 57(2), 115\u2013121. https:\/\/doi.org\/10.1016\/j.arbres.2020.04.025 (2021).","journal-title":"Arch. Bronconeumol. (Engl Ed)."},{"key":"1765_CR29","doi-asserted-by":"publisher","first-page":"160","DOI":"10.1002\/ijc.25019","volume":"127","author":"W Garavello","year":"2010","unstructured":"Garavello, W. et al. The oral cancer epidemic in central and eastern Europe. Int. J. Cancer 127, 160\u2013171 (2010).","journal-title":"Int. J. Cancer"},{"key":"1765_CR30","first-page":"6502","volume":"50","author":"S Franceschi","year":"1990","unstructured":"Franceschi, S. et al. Smoking and drinking in relation to cancers of the oral cavity, pharynx, larynx, and esophagus in northern Italy. Cancer Res. 50, 6502\u20136507 (1990).","journal-title":"Cancer Res."},{"key":"1765_CR31","doi-asserted-by":"publisher","first-page":"878","DOI":"10.1093\/ije\/20.4.878","volume":"20","author":"SY Choi","year":"1991","unstructured":"Choi, S. Y. & Kahyo, H. Effect of cigarette smoking and alcohol consumption in the aetiology of cancer of the oral cavity, pharynx and larynx. Int. J. Epidemiol. 20, 878\u2013885 (1991).","journal-title":"Int. J. Epidemiol."},{"key":"1765_CR32","doi-asserted-by":"publisher","first-page":"2548","DOI":"10.3390\/ijerph16142548","volume":"16","author":"GA Fernandes","year":"2019","unstructured":"Fernandes, G. A., Algranti, E., Concei\u00e7\u00e3o, G. M. D. S., W\u00fcnsch\u00a0Filho, V. & Toporcov, T. N. Lung cancer mortality trends in a Brazilian city with a long history of asbestos consumption. Int. J. Environ. Res. Public Health 16, 2548 (2019).","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"1765_CR33","doi-asserted-by":"publisher","first-page":"e007384","DOI":"10.1136\/bmjopen-2014-007384","volume":"5","author":"L Van den Borre","year":"2015","unstructured":"Van den Borre, L. & Deboosere, P. Enduring health effects of asbestos use in Belgian industries: A record-linked cohort study of cause-specific mortality (2001\u20132009). BMJ Open 5, e007384 (2015).","journal-title":"BMJ Open"},{"key":"1765_CR34","doi-asserted-by":"publisher","first-page":"742","DOI":"10.1016\/j.scitotenv.2019.06.259","volume":"688","author":"Y Zhu","year":"2019","unstructured":"Zhu, Y. et al. Internal biomarkers and external estimation of exposure to polycyclic aromatic hydrocarbons and their relationships with cancer mortality in a high cancer incidence area. Sci. Total Environ. 688, 742\u2013750 (2019).","journal-title":"Sci. Total Environ."},{"key":"1765_CR35","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1007\/s00420-011-0683-y","volume":"85","author":"S Paget-Bailly","year":"2012","unstructured":"Paget-Bailly, S., Cyr, D. & Luce, D. Occupational exposures to asbestos, polycyclic aromatic hydrocarbons and solvents, and cancers of the oral cavity and pharynx: A quantitative literature review. Int. Arch. Occup. Environ. Health 85, 341\u2013351 (2012).","journal-title":"Int. Arch. Occup. Environ. Health"},{"key":"1765_CR36","doi-asserted-by":"publisher","first-page":"324","DOI":"10.1093\/eurpub\/cku145","volume":"25","author":"P Cui","year":"2015","unstructured":"Cui, P., Huang, Y., Han, J., Song, F. & Chen, K. Ambient particulate matter and lung cancer incidence and mortality: A meta-analysis of prospective studies. Eur. J. Public Health 25, 324\u2013329 (2015).","journal-title":"Eur. J. Public Health"},{"key":"1765_CR37","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1136\/jim-2016-000263","volume":"67","author":"YH Chu","year":"2019","unstructured":"Chu, Y. H. et al. Association between fine particulate matter and oral cancer among Taiwanese men. J. Invest. Med. 67, 34\u201338 (2019).","journal-title":"J. Invest. Med."},{"key":"1765_CR38","unstructured":"Cuartas, J. Cien a\u00f1os de la Gran Guerra, la contienda que encumbr\u00f3 a Asturias. La Nueva Espa\u00f1a (2014)."},{"key":"1765_CR39","unstructured":"Fern\u00e1ndez\u00a0Mateo, I. El sector de la miner\u00eda en Espa\u00f1a:? llega el fin del carb\u00f3n nacional? (Final-degree project (Director: Antonio Javier Ramos Llanos), Universidad Pontificia Comillas, 2015)."},{"key":"1765_CR40","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.lungcan.2008.02.004","volume":"62","author":"M Hendryx","year":"2008","unstructured":"Hendryx, M., ODonnell, K. & Horn, K. Lung cancer mortality is elevated in coal-mining areas of Appalachia. Lung Cancer 62, 1\u20137 (2008).","journal-title":"Lung Cancer"},{"key":"1765_CR41","doi-asserted-by":"publisher","first-page":"243","DOI":"10.4081\/gh.2010.204","volume":"4","author":"M Hendryx","year":"2010","unstructured":"Hendryx, M., Fedorko, E. & Anesetti-Rothermel, A. A geographical information system-based analysis of cancer mortality and population exposure to coal mining activities in West Virginia, United States of America. Geospatial Health 4, 243\u2013256 (2010).","journal-title":"Geospatial Health"},{"key":"1765_CR42","unstructured":"Carreras, A. & Tafunell, X. Estad\u00edsticas hist\u00f3ricas de Espa\u00f1a, siglos XIX-XX (Fundaci\u00f3n BBVA\/BBVA Foundation, 2006)."},{"key":"1765_CR43","unstructured":"Barranco, A.\u00a0P. Estad\u00edsticas hist\u00f3ricas sobre el sector industrial, minero y energ\u00e9tico en Andaluc\u00eda: siglo XX (Instituto de Estad\u00edstica de Andaluc\u00eda, 2005)."},{"key":"1765_CR44","unstructured":"Ramos, P.\u00a0G. Impacto del consumo de tabaco en Extremadura. Ph.D. thesis, Universidad de Extremadura (2010)."},{"key":"1765_CR45","doi-asserted-by":"publisher","first-page":"340","DOI":"10.1016\/j.oraloncology.2008.05.018","volume":"45","author":"S Petti","year":"2009","unstructured":"Petti, S. Lifestyle risk factors for oral cancer. Oral Oncol. 45, 340\u2013350 (2009).","journal-title":"Oral Oncol."},{"key":"1765_CR46","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1097\/00008469-200302000-00005","volume":"12","author":"J Lissowska","year":"2003","unstructured":"Lissowska, J. et al. Smoking, alcohol, diet, dentition and sexual practices in the epidemiology of oral cancer in Poland. Eur. J. Cancer Prevent. 12, 25\u201333 (2003).","journal-title":"Eur. J. Cancer Prevent."},{"key":"1765_CR47","unstructured":"Gobierno de Espa\u00f1a: Ministerio de Sanidad. Encuesta domiciliaria sobre alcohol y drogas en espa\u00f1a (EDADES), 1995\u20132007. https:\/\/pnsd.sanidad.gob.es\/home.htm."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-01765-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-01765-7","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-01765-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,3]],"date-time":"2022-12-03T17:35:37Z","timestamp":1670088937000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-01765-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,15]]},"references-count":47,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["1765"],"URL":"https:\/\/doi.org\/10.1038\/s41598-021-01765-7","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,15]]},"assertion":[{"value":"15 April 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 November 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 November 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"22273"}}