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BMC Cancer
Published in: BMC Cancer 1/2014

Open Access 01-12-2014 | Research article

Trends in oral cavity, pharyngeal, oesophageal and gastric cancer mortality rates in Spain, 1952–2006: an age-period-cohort analysis

Authors: Daniel Seoane-Mato, Nuria Aragonés, Eva Ferreras, Javier García-Pérez, Marta Cervantes-Amat, Pablo Fernández-Navarro, Roberto Pastor-Barriuso, Gonzalo López-Abente

Published in: BMC Cancer | Issue 1/2014

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Abstract

Background

Although oral cavity, pharyngeal, oesophageal and gastric cancers share some risk factors, no comparative analysis of mortality rate trends in these illnesses has been undertaken in Spain. This study aimed to evaluate the independent effects of age, death period and birth cohort on the mortality rates of these tumours.

Methods

Specific and age-adjusted mortality rates by tumour and sex were analysed. Age-period-cohort log-linear models were fitted separately for each tumour and sex, and segmented regression models were used to detect changes in period- and cohort-effect curvatures.

Results

Among men, the period-effect curvatures for oral cavity/pharyngeal and oesophageal cancers displayed a mortality trend that rose until 1995 and then declined. Among women, oral cavity/pharyngeal cancer mortality increased throughout the study period whereas oesophageal cancer mortality decreased after 1970. Stomach cancer mortality decreased in both sexes from 1965 onwards. Lastly, the cohort-effect curvature showed a certain degree of similarity for all three tumours in both sexes, which was greater among oral cavity, pharyngeal and oesophageal cancers, with a change point in evidence, after which risk of death increased in cohorts born from the 1910-1920s onwards and decreased among the 1950–1960 cohorts and successive generations. This latter feature was likewise observed for stomach cancer.

Conclusions

While the similarities of the cohort effects in oral cavity/pharyngeal, oesophageal and gastric tumours support the implication of shared risk factors, the more marked changes in cohort-effect curvature for oral cavity/pharyngeal and oesophageal cancer could be due to the greater influence of some risk factors in their aetiology, such as smoking and alcohol consumption. The increase in oral cavity/pharyngeal cancer mortality in women deserves further study.
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Literature
1.
Ferlay J, Shin H-R, Bray F, Forman D, Mathers C, Parkin DM: Globocan 2008: Cancer Incidence and Mortality Worldwide. IARC CancerBase No. 10. 2010, Lyon, France: International Agency for Research on Cancer
2.
Sant M, Allemani C, Santaquilani M, Knijn A, Marchesi F, Capocaccia R: EUROCARE-4. Survival of cancer patients diagnosed in 1995–1999. Results and commentary. Eur J Cancer. 2009, 45: 931-991. 10.1016/j.ejca.2008.11.018.CrossRefPubMed
3.
Zigon G, Berrino F, Gatta G, Sánchez M-J, van Dijk B, Van Eycken E, Francisci S: Prognoses for head and neck cancers in Europe diagnosed in 1995–1999: a population-based study. Ann Oncol. 2011, 22: 165-174. 10.1093/annonc/mdq306.CrossRefPubMed
4.
De Angelis R, Sant M, Coleman MP, Francisci S, Baili P, Pierannunzio D, Trama A, Visser O, Brenner H, Ardanaz E, Bielska-Lasota M, Engholm G, Nennecke A, Siesling S, Berrino F, Capocaccia R: EUROCARE-5 Working Group: Cancer survival in Europe 1999–2007 by country and age: results of EUROCARE–5-a population-based study. Lancet Oncol. 2014, 15: 23-34. 10.1016/S1470-2045(13)70546-1.CrossRefPubMed
5.
6.
Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JWW, Comber H, Forman D, Bray F: Cancer incidence and mortality patterns in Europe: Estimates for 40 countries in 2012. Eur J Cancer. 2013, 49: 1374-1403. 10.1016/j.ejca.2012.12.027.CrossRefPubMed
7.
Smith EM, Rubenstein LM, Haugen TH, Pawlita M, Turek LP: Complex etiology underlies risk and survival in head and neck cancer human papillomavirus, tobacco, and alcohol: a case for multifactor disease. J Oncol. 2012, 2012: 571862-CrossRefPubMedPubMedCentral
8.
D’Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM, Westra WH, Gillison ML: Case–control study of human papillomavirus and oropharyngeal cancer. N Engl J Med. 2007, 356: 1944-1956. 10.1056/NEJMoa065497.CrossRefPubMed
9.
Pennathur A, Gibson MK, Jobe BA, Luketich JD: Oesophageal carcinoma. Lancet. 2013, 381: 400-412. 10.1016/S0140-6736(12)60643-6.CrossRefPubMed
10.
González CA, Agudo A: Carcinogenesis, prevention and early detection of gastric cancer: where we are and where we should go. Int J Cancer. 2012, 130: 745-753. 10.1002/ijc.26430.CrossRefPubMed
11.
La Vecchia C, Tavani A, Franceschi S, Levi F, Corrao G, Negri E: Epidemiology and prevention of oral cancer. Oral Oncol. 1997, 33: 302-312. 10.1016/S1368-8375(97)00029-8.CrossRefPubMed
12.
Levi F, Lucchini F, Negri E, Boyle P, La Vecchia C: Cancer mortality in Europe, 1990–1994, and an overview of trends from 1955 to 1994. Eur J Cancer. 1999, 35: 1477-1516. 10.1016/S0959-8049(99)00154-9.CrossRefPubMed
13.
Macfarlane GJ, Boyle P, Evstifeeva TV, Robertson C, Scully C: Rising trends of oral cancer mortality among males worldwide: the return of an old public health problem. Canc Causes Contr. 1994, 5: 259-265. 10.1007/BF01830246.CrossRef
14.
La Vecchia C, Lucchini F, Negri E, Levi F: Trends in oral cancer mortality in Europe. Oral Oncol. 2004, 40: 433-439. 10.1016/j.oraloncology.2003.09.013.CrossRefPubMed
15.
Garavello W, Bertuccio P, Levi F, Lucchini F, Bosetti C, Malvezzi M, Negri E, La Vecchia C: The oral cancer epidemic in central and eastern Europe. Int J Cancer. 2010, 127: 160-171. 10.1002/ijc.25019.CrossRefPubMed
16.
Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, Jiang B, Goodman MT, Sibug-Saber M, Cozen W, Liu L, Lynch CF, Wentzensen N, Jordan RC, Altekruse S, Anderson WF, Rosenberg PS, Gillison ML: Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol. 2011, 29: 4294-4301. 10.1200/JCO.2011.36.4596.CrossRefPubMedPubMedCentral
17.
Bosetti C, Levi F, Ferlay J, Garavello W, Lucchini F, Bertuccio P, Negri E, La Vecchia C: Trends in oesophageal cancer incidence and mortality in Europe. Int J Cancer. 2008, 122: 1118-1129.CrossRefPubMed
18.
Aragonés N, Pollán M, Rodero I, López-Abente G: Gastric cancer in the European Union (1968–1992): mortality trends and cohort effect. Ann Epidemiol. 1997, 7: 294-303. 10.1016/S1047-2797(97)00002-1.CrossRefPubMed
19.
Bosetti C, Bertuccio P, Malvezzi M, Levi F, Chatenoud L, Negri E, La Vecchia C: Cancer mortality in Europe, 2005–2009, and an overview of trends since 1980. Ann Oncol. 2013, 24: 2657-2671. 10.1093/annonc/mdt301.CrossRefPubMed
20.
Osmond C, Gardner MJ: Age, period and cohort models applied to cancer mortality rates. Stat Med. 1982, 1: 245-259. 10.1002/sim.4780010306.CrossRefPubMed
21.
Holford TR: Understanding the effects of age, period, and cohort on incidence and mortality rates. Annu Rev Public Health. 1991, 12: 425-457. 10.1146/annurev.pu.12.050191.002233.CrossRefPubMed
22.
Breslow NE: Extra-Poisson variation in Log-linear models. Appl Stat. 1984, 33: 38-44. 10.2307/2347661.CrossRef
23.
Muggeo VM: Estimating regression models with unknown break-points. Stat Med. 2003, 22: 3055-3071. 10.1002/sim.1545.CrossRefPubMed
24.
Muggeo VM: Segmented: segmented relationships in regression models. R package version 0.1-4. 2004
25.
Regidor E, Gutiérrez-Fisac JL, De Los Santos Ichaso M, Fernández E: Trends in principal cancer risk factors in Spain. Ann Oncol. 2010, 21 (3): iii37-iii42.PubMed
26.
Aragonés N, Goicoa T, Pollán M, Militino AF, Pérez-Gómez B, López-Abente G, Ugarte MD: Spatio-temporal trends in gastric cancer mortality in Spain: 1975–2008. Canc Epidemiol. 2013, 37: 360-369. 10.1016/j.canep.2013.03.009.CrossRef
27.
Hashibe M, Brennan P, Chuang S-C, Boccia S, Castellsague X, Chen C, Curado MP, Dal Maso L, Daudt AW, Fabianova E, Fernandez L, Wünsch-Filho V, Franceschi S, Hayes RB, Herrero R, Kelsey K, Koifman S, La Vecchia C, Lazarus P, Levi F, Lence JJ, Mates D, Matos E, Menezes A, McClean MD, Muscat J, Eluf-Neto J, Olshan AF, Purdue M, Rudnai P, et al: Interaction between tobacco and alcohol use and the risk of head and neck cancer: pooled analysis in the International Head and Neck Cancer Epidemiology Consortium. Cancer Epidemiol Biomarkers Prev. 2009, 18: 541-550. 10.1158/1055-9965.EPI-08-0347.CrossRefPubMedPubMedCentral
28.
Anantharaman D, Marron M, Lagiou P, Samoli E, Ahrens W, Pohlabeln H, Slamova A, Schejbalova M, Merletti F, Richiardi L, Kjaerheim K, Castellsague X, Agudo A, Talamini R, Barzan L, Macfarlane TV, Tickle M, Simonato L, Canova C, Conway DI, McKinney PA, Thomson P, Znaor A, Healy CM, McCartan BE, Hashibe M, Brennan P, Macfarlane GJ: Population attributable risk of tobacco and alcohol for upper aerodigestive tract cancer. Oral Oncol. 2011, 47: 725-731. 10.1016/j.oraloncology.2011.05.004.CrossRefPubMed
29.
Correa P, Houghton J: Carcinogenesis of Helicobacter pylori. Gastroenterology. 2007, 133: 659-672. 10.1053/j.gastro.2007.06.026.CrossRefPubMed
30.
González CA, López-Carrillo L: Helicobacter pylori, nutrition and smoking interactions: their impact in gastric carcinogenesis. Scand J Gastroenterol. 2010, 45: 6-14. 10.3109/00365520903401959.CrossRefPubMed
31.
Marur S, D’Souza G, Westra WH, Forastiere AA: HPV-associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol. 2010, 11: 781-789. 10.1016/S1470-2045(10)70017-6.CrossRefPubMed
32.
Fakhry C, Westra WH, Li S, Cmelak A, Ridge JA, Pinto H, Forastiere A, Gillison ML: Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J Natl Cancer Inst. 2008, 100: 261-269. 10.1093/jnci/djn011.CrossRefPubMed
33.
Fakhry C, Gillison ML: Clinical implications of human papillomavirus in head and neck cancers. J Clin Oncol. 2006, 24: 2606-2611. 10.1200/JCO.2006.06.1291.CrossRefPubMedPubMedCentral
34.
Hammarstedt L, Lindquist D, Dahlstrand H, Romanitan M, Dahlgren LO, Joneberg J, Creson N, Lindholm J, Ye W, Dalianis T, Munck-Wikland E: Human papillomavirus as a risk factor for the increase in incidence of tonsillar cancer. Int J Cancer. 2006, 119: 2620-2623. 10.1002/ijc.22177.CrossRefPubMed
35.
Attner P, Du J, Näsman A, Hammarstedt L, Ramqvist T, Lindholm J, Marklund L, Dalianis T, Munck-Wikland E: The role of human papillomavirus in the increased incidence of base of tongue cancer. Int J Cancer. 2010, 126: 2879-2884.PubMed
36.
Näsman A, Attner P, Hammarstedt L, Du J, Eriksson M, Giraud G, Ahrlund-Richter S, Marklund L, Romanitan M, Lindquist D, Ramqvist T, Lindholm J, Sparén P, Ye W, Dahlstrand H, Munck-Wikland E, Dalianis T: Incidence of human papillomavirus (HPV) positive tonsillar carcinoma in Stockholm, Sweden: an epidemic of viral-induced carcinoma?. Int J Cancer. 2009, 125: 362-366. 10.1002/ijc.24339.CrossRefPubMed
37.
International Agency for Research on Cancer: Human Papillomaviruses. IARC Monographs Volume 90. 2007, Lyon, France: IARC
38.
International Agency for Research on Cancer: A Review of Human Carcinogens: Biological Agents. IARC Monographs Volume 100 - Part B. 2012, Lyon, France: IARC
39.
Anantharaman D, Gheit T, Waterboer T, Abedi-Ardekani B, Carreira C, McKay-Chopin S, Gaborieau V, Marron M, Lagiou P, Ahrens W, Holcátová I, Merletti F, Kjaerheim K, Talamini R, Simonato L, Castellsague X, Macfarlane TV, Biggs A-M, Thakker N, Znaor A, Thomson P, Canova C, Conway DI, Healy CM, Tommasino M, Pawlita M, Brennan P: Human Papillomavirus Infections and Upper Aero-Digestive Tract Cancers: The ARCAGE Study. J Natl Cancer Inst. 2013, 105: 536-545. 10.1093/jnci/djt053.CrossRefPubMed
40.
Veldhuijzen NJ, Snijders PJ, Reiss P, Meijer CJ, van de Wijgert JH: Factors affecting transmission of mucosal human papillomavirus. Lancet Infect Dis. 2010, 10: 862-874. 10.1016/S1473-3099(10)70190-0.CrossRefPubMed
41.
Bosch FX, Lorincz A, Muñoz N, Meijer CJLM, Shah KV: The causal relation between human papillomavirus and cervical cancer. J Clin Pathol. 2002, 55: 244-265. 10.1136/jcp.55.4.244.CrossRefPubMedPubMedCentral
42.
Gillison ML, Broutian T, Pickard RKL, Tong Z, Xiao W, Kahle L, Graubard BI, Chaturvedi AK: Prevalence of oral HPV infection in the United States, 2009–2010. JAMA. 2012, 307: 693-703. 10.1001/jama.2012.101.CrossRefPubMed
43.
Bruni L, Diaz M, Castellsagué X, Ferrer E, Bosch FX, de Sanjosé S: Cervical human papillomavirus prevalence in 5 continents: meta‒analysis of 1 million women with normal cytological findings. J Infect Dis. 2010, 202: 1789-1799. 10.1086/657321.CrossRefPubMed
44.
Kreimer AR, Bhatia RK, Messeguer AL, González P, Herrero R, Giuliano AR: Oral human papillomavirus in healthy individuals: a systematic review of the literature. Sex Transm Dis. 2010, 37: 386-391.PubMed
45.
De Sanjose S, Almirall R, Lloveras B, Font R, Diaz M, Muñoz N, Català I, Meijer CJLM, Snijders PJF, Herrero R, Bosch FX: Cervical human papillomavirus infection in the female population in Barcelona, Spain. Sex Transm Dis. 2003, 30: 788-793. 10.1097/01.OLQ.0000080177.82204.E0.CrossRefPubMed
46.
De Vuyst H, Clifford G, Li N, Franceschi S: HPV infection in Europe. Eur J Cancer. 2009, 45: 2632-2639. 10.1016/j.ejca.2009.07.019.CrossRefPubMed
47.
De Sanjose S, Cortés X, Méndez C, Puig-Tintore L, Torné A, Roura E, Bosch FX, Castellsague X: Age at sexual initiation and number of sexual partners in the female Spanish population. Eur J Obstet Gynecol Reprod Biol. 2008, 140: 234-240. 10.1016/j.ejogrb.2008.04.005.CrossRefPubMed
48.
Zandberg DP, Bhargava R, Badin S, Cullen KJ: The role of human papillomavirus in nongenital cancers. CA Cancer J Clin. 2013, 63: 57-81. 10.3322/caac.21167.CrossRefPubMed
49.
Aragonés N, Izarzugaza MI, Ramos M, Chirlaque MD, Almar E, Martínez C: Trends in oesophago-gastric cancer incidence in Spain: analysis by subsite and histology. Ann Oncol. 2010, 21 (3): iii69-iii75.PubMed
50.
Sitas F, Egger S, Urban MI, Taylor PR, Abnet CC, Boffetta P, O’Connell DL, Whiteman DC, Brennan P, Malekzadeh R, Pawlita M, Dawsey SM, Waterboer T, on behalf of the InterSCOPE Collaboration: InterSCOPE study: associations between esophageal squamous cell carcinoma and human papillomavirus serological markers. J Natl Cancer Inst. 2012, 104: 147-158. 10.1093/jnci/djr499.CrossRefPubMedPubMedCentral
51.
Brown LM: Helicobacter pylori: epidemiology and routes of transmission. Epidemiol Rev. 2000, 22: 283-297. 10.1093/oxfordjournals.epirev.a018040.CrossRefPubMed
52.
Pérez-Gómez B, Aragonés N, Pollán M, Suárez B, Lope V, Llácer A, López-Abente G: Accuracy of cancer death certificates in Spain: a summary of available information. Gac Sanit. 2006, 20 (Suppl 3): 42-51.CrossRefPubMed
53.
Grupo de trabajo de la Ponencia y Registro de Vacunaciones: Virus del Papiloma Humano. Situación Actual, Vacunas y Perspectivas de su Utilización. 2007, Madrid: Ministerio de Sanidad y Consumo
Metadata
Title
Trends in oral cavity, pharyngeal, oesophageal and gastric cancer mortality rates in Spain, 1952–2006: an age-period-cohort analysis
Authors
Daniel Seoane-Mato
Nuria Aragonés
Eva Ferreras
Javier García-Pérez
Marta Cervantes-Amat
Pablo Fernández-Navarro
Roberto Pastor-Barriuso
Gonzalo López-Abente
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2014
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-14-254

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