IJE Advance Access first published online on January 16, 2007
This version published online on March 12, 2007
International Journal of Epidemiology, doi:10.1093/ije/dyl275
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Socioeconomic position and the risk of gastric and oesophageal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST)
1 Division of Clinical Epidemiology, Deutsches Krebsforschungszentrum, Heidelberg, Germany.
2 Department of Epidemiology, University Ulm, Ulm, Germany.
3 National Institute of Public Health and the Environment, Bilthoven, The Netherlands.
4 Department of Epidemiology, Catalan Institute of Oncology, Barcelona, Spain.
5 IRIS Research Center, Chiron Vaccines, Siena, Italy.
6 Cancer Research UK Epidemiology Unit, University of Oxford, UK.
7 Julius Center for Health Sciences and Primary Care, University Medical Center, Utrecht, Netherlands.
8 Department of Epidemiology. National Cancer Institute, Milan, Italy.
9 Cancer Epidemiology Department. University of Turin, Italy.
10 Molecular and Nutritional Epidemiology Unit, CSPO-Scientific Institute of Tuscany, Florence, Italy.
11 Dipartimento di Medicina Clinica e Sperimentale, Federico II University, Naples, Italy.
12 Cancer Registry, Azienda Ospedaliera "Civile - M.P.Arezzo", Ragusa, Italy.
13 Malmö Diet and Cancer Study, Lund University, Malmö, Sweden.
14 Department of Public Health and Clinical Medicine, Nutritional Research, University of Umeå, Sweden.
15 Department Medical Biosciences, Pathology, Umeå University, Sweden.
16 Andalusian School of Public Health, Granada, Spain.
17 Public Health Department of Guipuzkoa, San Sebastian, Spain.
18 Public Health Institute, Navarra, Spain.
19 Epidemiology Department, Murcia health Council, Murcia, Spain.
20 Dirección General de Salud Pública, Consejería de Salud y Servicios Sanitarios Asturias, Spain.
21 MRC Dunn Human Nutrition Unit, Cambridge, UK.
22 German Institute of Human Nutrition, Potsdam-Rehbücke, Germany.
23 Department of Clinical Epidemiology, Aalborg Hospital and Aarhus University Hospital.
24 Institute of Cancer Epidemiology, Danish Cancer Society, Copenhagen, Denmark.
25 INSERM, U 521, Institut Gustave Roussy, Villejuif, France.
26 Department of Hygiene and Epidemiology, Medical School, University of Athens, Greece.
27 Département de Pathologie Institut Gustave Roussy, Villejuif, France.
28 Institute of Molecular Pathology and Immunology of University of Porto (IPATIMUP) and Faculty of Medicine/H.S.Joao, Porto, Portugal.
29 Unit of Nutrition and Cancer, International Agency for Research on Cancer, Lyon, France.
30 Imperial College, London, UK.
* Corresponding author: Department of Epidemiology, University of Ulm, Helmholtzstr.22, 89081 Ulm, Germany. E-mail: gabriele.nagel{at}uni-ulm.de
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Abstract |
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Objectives To evaluate the association of socioeconomic position with adenocarcinoma of the oesophagus and stomach.
Methods The European Prospective Investigation into Cancer and Nutrition (EPIC) cohort comprises about 520 000 participants mostly aged 35–70 years. Information on diet and lifestyle was collected at recruitment. After an average follow-up of 6.5 years, 268 cases with adenocarcinoma of the stomach and 56 of the oesophagus were confirmed. We examined the effect of socioeconomic position on cancer risk by means of educational data and a computed Relative Index of Inequality (RII). In a nested case-control study, adjustment for Helicobacter pylori (H. pylori) infection was performed.
Results Higher education was significantly associated with a reduced risk of gastric cancer [vs lowest level of education, hazard ratio (HR): 0.64, 95% Confidence intervals (CI): 0.43–0.98]. This effect was more pronounced for cancer of the cardia (HR: 0.42, 95% CI: 0.20–0.89) as compared to non-cardia gastric cancer (HR: 0.66, 95% CI: 0.36–1.22). Additionally, the inverse association of educational level and gastric cancer was stronger for cases with intestinal (extreme categories, HR: 0.13, 95% CI: 0.04–0.44) rather than diffuse histological subtype (extreme categories, HR: 0.71 95% CI: 0.37–1.40). In the nested case-control study, inverse but statistically non-significant associations were found after additional adjustment for H. pylori infection [highest vs lowest level of education: Odds ratio (OR) 0.53, 95% CI: 0.24–1.18]. Educational level was non-significantly, inversely associated with carcinoma of the oesophagus.
Conclusion A higher socioeconomic position was associated with a reduced risk of gastric adenocarcinoma, which was strongest for cardia cancer or intestinal histological subtype, suggesting different risk profiles according to educational level. These effects appear to be explained only partially by established risk factors.
Keywords Socioeconomic position, gastric cancer, Helicobacter pylori, EPIC
Accepted 9 November 2006
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Introduction |
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Over the past few decades, the incidence rate of gastric cancer has declined. However, it remains among the most common cancer sites world-wide.1,2 In some countries, an increase in adenocarcinomas of the oesophagus, gastric cardia and the gastro-oesophageal junction (GEJ) was noticed.3 It has been suggested that these three cancer sites form a single disease entity,3 since they share the same epidemiological risk factors that are associated with a specific diet (low fruit and vegetable consumption), smoking habits, obesity, gastro-esophageal reflux disease and physical inactivity seen as typical for a western lifestyle.4,5
Socioeconomic inequalities were shown to be strongly associated with mortality and morbidity.6–9 The risk of gastric and oesophageal cancers has also been associated with a lower socioeconomic position as measured by educational level,10–14 occupation12,14 or income.10,15 The infection with Helicobacter pylori (H. pylori) bacterium is positively associated with gastric cancer. Since this infection is frequently acquired in childhood, education as a marker for childhood socioeconomic position may be of particular interest.16 Most of these studies were case-control studies; however cohort studies have also found a higher educational level to be associated with a lower gastric cancer risk.10,12
The pathways through which the socioeconomic position influences gastric cancer risk are not established, but are likely to reflect differences in smoking,17 diet4,18 and infection with H. pylori.19 Chronic gastritis is another potential risk factor for gastric cancer.20,21 There is some evidence that the magnitude of these risk factors may differ by anatomical subtype.3
The aim of this study was to examine the association between socioeconomic position and the risk of adenocarcinomas of the stomach and oesophagus in the European Prospective Investigation into Cancer and Nutrition (EPIC), after taking into account other identified risk factors. H. pylori seroprevalence was assessed in a nested case-control study. In addition, differential effects by anatomical subsites and histological subtypes of gastric cancer were investigated.
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Material and methods |
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Study subjects
EPIC is a multicentre prospective cohort study designed to investigate the relation between diet, lifestyle factors and risk of cancer. Approximately 520 000 subjects, mainly aged between 35 and 70 years, were recruited in 10 European Countries (Denmark, France, Germany, Greece, Italy, The Netherlands, Norway, Spain, Sweden and the United Kingdom) between 1992 and 2000.
The study subjects were largely recruited from the general population residing in a given geographical area. Exceptions were the French cohort (members of the school health insurance and University employees), the Utrecht and the Florence cohorts (women attending breast cancer screening), part of the Italian and Spanish cohort (blood donors and their spouses), and most of the Oxford cohort (vegetarian volunteers and healthy eaters), details of which are provided elsewhere.22,23 In brief, eligible subjects were invited to participate in the study by mail or by personal contact. Those who accepted gave informed consent and completed a lifestyle and dietary questionnaire. The majority of subjects also provided a blood specimen and had anthropometric measurements taken. Educational level was reported from 460 648 participants (7250 participants with missing data and 10 443 participants with non-assigned education were excluded). Furthermore, the Norwegian subcohort (n = 35 229) was excluded due to the short follow-up and small number of incident cases, leaving 425 613 subjects (287 038 of whom were women) for the present analysis.
Since the French subcohort of 64 692 women consisted of educational employees only, this subcohort was only excluded from the analysis of the Relative Index of Inequality (RII), leaving 360 651 subjects (222 074 women) for this investigation.
Diet and lifestyle questionnaires
Habitual diet over the previous 12 months was measured at recruitment by a country-specific validated self- or interviewer-administered questionnaire. Most centres adopted a self-administered questionnaire, which comprised between 84 and 266 food items. Some centres additionally used 7- or 14-day dietary records. Lifestyle data were derived from questions on education, occupation, lifetime smoking and alcohol consumption, reproductive history, medical history and physical activity.
End points
Incident cancer cases were identified by population-based cancer registries (Denmark, Italy, The Netherlands, Spain, Sweden and the United Kingdom) or by active follow-up (France, Germany and Greece). Follow-up began at the date of recruitment and ended at either the date of diagnosis of gastric or oesophageal cancer, death or date of the last complete follow-up. A total of 400 incident stomach cancer and 67 oesophageal cancer cases had been reported to the central database at the International Agency for Research on Cancer (IARC) for the period up to December 1999, or September 2002, depending on the study centre. Cancer of the stomach included cancers coded as C16 according to the 10th Revision of the International Statistical Classification of Diseases, Injuries and Causes of Death (ICD). Validation of the diagnosis and classification of the tumours (according to ICD-O2 classification) was carried out by a panel of pathologists, details of which have been reported elsewhere.23
We excluded cases of gastric lymphomas (n = 26), gastric stump tumours (n = 5), other non-adenocarcinoma cases (n = 11), and other unspecified tumours of the stomach (n = 8). In addition, individuals who were in the top or bottom 1% of energy intake (seven cases) or with missing data on diet or educational attainment (75 cases) were excluded from the analysis. The Lauren classification was used to define histological subtypes, considering the two main subtypes (diffuse and intestinal) in further analyses.24 For a number of reasons, some gastric cancer cases could not be classified by anatomical subsite or histological subtype. The analysis of cardia cancers included the 17 GEJ tumours in addition to the 68 cardia gastric cancer cases.
Nested case-control study
Design details of the nested case-control study, including the laboratory work, have been described extensively elsewhere.25 In brief, for each newly diagnosed gastric cancer case with available blood sample for laboratory analysis (n = 215), four controls individually matched by centre, gender, age (±2.5 years) and blood donation date (±45 days) were randomly selected. Serum samples values above 100 arbitrary enzyme-linked immunosorbent assay units (EU) were considered as positive for anti-H. pylori immunoglobulin G (IgG) antibodies (84.2% of cases and 66.9% controls were positive).
Socioeconomic position
Educational level was used to characterize the participants for socioeconomic position. Four categories were used in the analyses defined as (i) primary school or less, (ii) vocational secondary education, (iii) other secondary education and (iv) college or university. Subjects without school attendance were assigned to the lowest educational level. In addition, the RII26 was calculated. Comparisons of measures between socioeconomic indicators suffer from unequal group sizes. The RII was constructed to avoid the problem of large ratios of risk due to small groups at the edges. The classification is based on a hierarchical order of education. Assignment was performed by ranking the distribution of the educational level according to the proportion of participants within strata for study centres, 10-year age groups and sex. The midpoint of each class of the cumulative proportional distribution of educational level was used to calculate the score of the RII. For example, if within a stratum (centre, age group, sex) 40% of subjects have a low education level, the midpoint of this group was chosen and each cohort member in that stratum would be assigned a score of 20, corresponding to the proportion of population above this midpoint. If the proportion of subjects in the next educational group with a medium education level was 30%, the score would be 55 (40 plus 30/2). Accordingly, the remaining 30% of subjects in this stratum with high educational level would receive a score of 85 (40 + 30 + 30/2). Participants were assigned to a RII score of 1 (low), 2 (middle) or 3 (high) based on tertiles of the values.
Statistical methods
Cox proportional hazard regression models (SAS PHREG procedure) were used for the analyses of the cohort data. The analyses were stratified by sex, age and centre to control for potential confounding due to differences in follow-up procedures, questionnaire design and other centre-specific characteristics. Age was used as the time scale variable in all models. Time at entry into the study was defined as age at recruitment, and time at exit was defined as age of diagnosis (for cases) or age at censoring (for at-risk subjects). Crude and multivariate models were calculated. The following variables were considered for adjustment: height (m, continuous), weight (kg, continuous), smoking habits [never smoked, former smoker (ceased smoking 
10 years, ceased <10 years, unknown), current smoker (<15, 15–25, 25, unknown cigarette/day), and unknown smoking status], lifelong average cigarette smoking (cigarette/day), duration of smoking (years), alcohol intake (g/day, quintiles), lifelong alcohol drinking (g/day quintiles, unknown), overall physical activity [metabolic equivalent of energy expenditure score (METs)], total energy intake (kcal/day, quintiles) consumption of meat and processed meat (g/day, quintiles), fruits (g/day, quintiles), and vegetables (g/day, quintiles). Initially, analyses were done for men and women separately, but because no substantial gender differences emerged, results are presented for both sexes combined. Analyses of gastric cancer using anatomical subsites and histological subtypes were performed.
We tested for heterogeneity of effect between different variables using Wald statistics.27 Conditional logistic regression analysis (SAS PHREG procedure) was used to calculate the odds ratios (OR) and 95% confidence intervals (95% CI) in the nested case-control study, controlling for the variables as in the full cohort study as well as H. pylori seroprevalence. SAS statistical software 9.13 (SAS institute Inc, Cary, NC) was used for all statistical analyses.
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Results |
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The cohort of 425 613 participants was followed for an average of 6.5 (SD = 1.8) years with a total of 2 765 038 person-years. Table 1 shows the number of incident cancer cases and person-years at risk in each participating country. In total, 268 cases of gastric adenocarcinoma, 56 cases of oesophageal adenocarcinoma, and 17 cases of cancers at the GEJ were identified. Cases were more likely to be smokers and to be older than non-cases (data not shown). The mean age of the subjects with gastric cancer was 58.8 years in men and 58.2 years in women.
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Table 2 shows the distribution of baseline characteristics stratified by educational level in men and women separately. Subjects in the highest education category were leaner (only in women), had a higher lifelong intake of alcohol in women but a lower in men, higher vegetable intake (in women) and a lower intake of meat, lower duration of smoking and lower prevalence of high cigarette smokers than those in the lowest education category. Subjects in the highest education category also had a lower prevalence of H. pylori infections than those in the lowest education category. With regarding to fruit consumption, no clear educational gradient was found.
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Overall,a higher educational level was significantly inversely associated with risk of gastric adenocarcinoma [highest vs lowest level of education: HR 0.64, 95% CI: 0.43–0.98] (Table 3). No statistically significant heterogeneity between countries was observed (data not shown). In the analysis by subsite of gastric cancer, a significant and strong negative association between education and cancer risk was observed for cases in the cardia subsite (highest vs lowest level of education HR 0.42, 95% CI: 0.20–0.89), while a non-significant negative association was observed for non-cardia gastric cancer (P for heterogeneity = 0.16). With histological subtype, a strong negative association was also observed for the intestinal type (highest vs lowest level of education HR 0.13, 95% CI: 0.04–0.44), while a non-significant negative association was observed for the diffuse type (P for heterogeneity = 0.42). Due to the low number of cases, further analysis by both subsite and subtype of gastric cancer was not possible.
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In the nested case-control study (Table 4), an inverse but statistically non-significant association was found after additional adjustment for H. pylori infection (highest vs lowest level of education: OR 0.53, 95% CI: 0.24–1.18). A non-significant inverse association was also found for educational level and risk of adenocarcinoma of the oesophagus (highest vs lowest level of education: HR 0.67: 95% CI: 0.30–1.52).
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Table 5 shows the results of the association between RII and gastric cancer risk in the cohort and nested case-control study. Overall, RII score was associated with an inverse, but statistical non-significant risk of gastric adenocarcinoma (highest vs lowest RII score: HR 0.74, 95% CI: 0.53–1.05). Similar to the results obtained for educational level, the association between RII and gastric cancer risk was strongest for cardia (highest vs lowest RII score: HR 0.49, 95% CI: 0.27–0.90, P for heterogeneity = 0.22) and intestinal-type gastric cancers (highest vs lowest score: HR 0.33, 95% CI: 0.16–0.68, P for heterogeneity = 0.13).
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In the nested case-control study, additional adjustment for H. pylori slightly attenuated the risk estimates. The OR between the RII-score and risk of gastric adenocarcinoma was 0.81 (95% CI: 0.43–1.51) with adjustment for H. pylori seroprevalence.
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Discussion |
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A higher educational level was associated with a reduced risk of gastric adenocarcinoma, an effect that seems to be stronger for cardia and particularly for intestinal-type gastric cancers. No statistically significant heterogeneity between countries was observed. Differences in the distribution of known or potential risk factors for gastric cancer, such as smoking, alcohol consumption, obesity, physical activity or some dietary factors which are correlated with socioeconomic position, did not explain a considerable part of this effect. However, after adjustment for H. pylori seroprevalence, this association was attenuated and was no longer statistically significant. Consistent with other results, an inverse association between educational level and oesophageal adenocarcinoma was observed,28 although it was not statistically significant and there were too few cases for reasonable interpretation.
Our findings are consistent with the results of other case-control studies11,13–15,29–31 and cohort studies.10,12 Only few risk factors, including smoking, obesity and low consumption of fruit and vegetables, are known to affect the risk of gastric and oesophageal cancers.4 It is well established that differences in socioeconomic position are associated with inequalities in health32 that may be mediated by differences in health-related behaviour.33–35 This is in agreement with our observations that participants with a higher educational level were leaner, ate more vegetables and were less likely to be smokers at recruitment. Also in men, lifelong alcohol intake was lower in the highest educational categories. The correlation of these risk factors with socioeconomic position might help to explain the inverse association of the latter with gastric cancer incidence, but in previous cohort studies10,12 a complete set of covariates was not always available.
H. pylori infection has been shown to be associated with lower social class.36 Education may reflect childhood socioeconomic circumstances, such as family size and hygiene conditions of life, which correlate with the H. pylori infection rate.35,37,38 This is in line with our observation, that educational attainment is correlated with the H. pylori seroprevalence, and as expected, further adjustment for H. pylori infections attenuated the risk estimates for non-cardia and gastric cancer overall. However, the findings from the present study suggest that these covariates, even the consideration of H. pylori infection, cannot fully explain the inverse association between socioeconomic factors and gastric cancer risk.
Few studies analysed the association between socioeconomic position and anatomical subsites or histological subtypes of gastric cancer.12,14,39,40 Powell and McConkey39 observed increasing incidence of cardia and decreasing incidence of pyloric gastric cancer cases in groups with high social position between 1961 and 1981 in the UK. In another registry based study, lower socioeconomic position was related to higher incidence of non-cardia gastric cancer, but no clear relationship was found with respect to cardia gastric cancer during 1987 to 1996 in Scotland.41 In contrast, Wu-Williams et al.40 found no association between socioeconomic position and risk of cardia cancer, although educational level was associated with distal gastric cancer in men aged 55 years and older. However, in their study neighbourhood controls were chosen, therefore direct comparability of their results with our data is limited. Another case-control study found higher socioeconomic position to be associated with decreased risk of both cardia and non-cardia cancer cases.14 Consistent with our observations, van Loon et al.12 found a higher educational level to be associated with a lower risk of cardia cancer, although this association was attenuated after adjustment for lifestyle variables. Conflicting results between socioeconomic position and gastric cancer may be attributed to the changes in temporal pattern of site and type of gastric cancer.39,41,42
Since educational attainment may vary substantially across Europe, we additionally examined the association between the RII score and gastric cancer risk, a marker commonly used in social epidemiology, and which takes into account the age and sex distribution of the population in each centre.26,43 However, both education level and the RII score showed similar inverse associations with gastric adenocarcinoma risk overall, and with anatomical and histological subtypes.
Some potential limitations of this study should be considered. Our study findings might have been affected by residual confounding and measurement error in the variables included in the models.44 Dietary data are prone to measurement error.45 In our data, however, the adjustment for known risk factors did not substantially change the association between educational level and gastric cancer risk. In the nested case-control study, a possible attenuation of risk may have occurred when H. pylori infection was close to the time of cancer diagnosis.46 However, in our study the length of follow-up is still relatively short. Another source of error to be considered is residual confounding of other factors related to socioeconomic position that may determine gastric cancer risk. We did not take into account other measures for adulthood socioeconomic position such as occupation or income; however, measures of economic distress have been shown to be in good correlation with each other.35 Rather than single indicators of socioeconomic position, multiple indicators covering life course may be necessary to create indicators which can better discriminate between social groups and identify risk factors.35,47 Regarding socioeconomic position misclassification is unlikely to be a matter of concern. Since educational attainment applies for every person and is easily recordable, measurement error of the exposure variable is unlikely to have seriously biased our results. Period effects regarding the educational levels were considered by age-group stratified analyses. The participants of our cohort study are likely to be more educated than the general population, which may result in attenuated risk estimates and limit the generalizability of the results.
The strength of this study is the prospective study design, the consideration of relevant confounding variables including H. pylori infection, and the stratification by anatomical subsites and histological subtypes, for which the subclassification and verification for which was done by a panel of experienced pathologists, although these results by subtypes of gastric cancer should be confirmed in a larger study with more cases.
In this large prospective study, high educational level was associated with a reduced risk of gastric adenocarcinoma, which was strongest for cardia cancer and intestinal histological subtype. This gives support to the hypothesis that socioeconomic factors are diversely related to site and types of gastric cancer, a relationship that is not completely explained by differences in established risk factors for gastric cancer. Our observations emphasize the need of adjustment for socioeconomic position in studies evaluating risk factors for stomach cancer. Future investigations of the socioeconomic determinants of gastric adenocarcinoma should consider differential effects by subsites and subtypes. Emphasis should be put on studying correlates of socioeconomic position which can help explain the association with stomach cancer risk.
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We thank the members of the pathologist panel for their valuable work: Dr Roger Stenling, Umea, Sweden; Dr Johan Offerhaus, Amsterdam The Netherland; Dr Vicki Save, Cambridge, United Kingdom, Dr Julio Torrado, San Sebastian, Spain; Dr Gabriella Nesi, Firenze, Italy; Dr U Mahlke, Postdam, Germany; Dr Hendrik Bläker, Heildelberg; Germany; Dr Claus Fenger, Denmark and Dr Dimitrious Roukos, Ioannina, Greece. We thank Catia Moutinho, Porto, Portugal, for her technical work in the preparation of pathological material.
Specific study results of the nested case-control study within EPIC (EUR-GAST) were obtained with financial support from the FP5 of European Commission (QLG1-CT-2001-01049).
The EPIC study was funded by ‘Europe Against Cancer’ Programme of the European Commission (SANCO); Ligue contre le Cancer (France); Société 3M (France); Mutuelle Générale de l’Education Nationale; Institut National de la Santé et de la Recherche Médicale (INSERM); German Cancer Aid; German Cancer Research Center; German Federal Ministry of Education and Research; Danish Cancer Society; Health Research Fund (FIS) of the Spanish Ministry of Health (RCESP-C03/09); the participating regional governments and institutions of Spain; Cancer Research UK; Medical Research Council, UK; the Stroke Association, UK; British Heart Foundation; Department of Health, UK; Food Standards Agency, UK; the Wellcome Trust, UK; Greek Ministry of Health; Greek Ministry of Education; Italian Association for Research on Cancer; Italian National Research Council; Dutch Ministry of Public Health, Welfare and Sports; Dutch Ministry of Health; Dutch Prevention Funds; LK Research Funds; Dutch ZON (Zorg Onderzoek Nederland); World Cancer Research Fund (WCRF); Swedish Cancer Society; Swedish Scientific Council; Regional Government of Skane, Sweden; Norwegian Cancer Society.
Conflict of interest: None declared.
KEY MESSAGES
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1 Parkin DM, Bray F, Ferlay J, Pisani P. (2005) Global cancer statistics, 2002. CA Cancer J Clin 55:74–108.
2 Plummer M, Franceschi S, Munoz N. (2004) Epidemiology of gastric cancer. IARC Sci Publ 157:311–26 Review.
3 Crew KD. (2004) Neugut AI. Epidemiology of upper gastrointestinal malignancies. Semin Oncol 31:450–64.[CrossRef][Web of Science][Medline]
4 Engel LS, Chow WH, Vaughan TL, et al. (2003) Population attributable risks of esophageal and gastric cancers. J Natl Cancer Inst 95:1404–13.
5 Gammon MD, Schoenberg JB, Ahsan H, et al. (1997) Tobacco, alcohol, and socioeconomic status and adenocarcinomas of the esophagus and gastric cardia. J Natl Cancer Inst 89:1277–84.
6 Wong MD, Shapiro MF, Boscardin WJ, Ettner SL. (2002) Contribution of major diseases to disparities in mortality. N Engl J Med 347:1585–92.
7 Huisman M, Kunst AE, Bopp M, et al. (2005) Educational inequalities in cause-specific mortality in middle-aged and older men and women in eight western European populations. Lancet 365:493–500.[Web of Science][Medline]
8 Dalstra JA, Kunst AE, Borrell C, et al. (2005) Socioeconomic differences in the prevalence of common chronic diseases: an overview of eight European countries. Int J Epidemiol 34:316–26 [Epub 2005 Feb 28].
9 Isaacs SL and Schroeder SA. (2004) Class - the ignored determinant of the nation's health. N Engl J Med 351:1137–42.
10 Pukkala E and Teppo L. (1986) Socioeconomic status and education as risk determinants of gastrointestinal cancer. Prev Med 15:127–38.[CrossRef][Web of Science][Medline]
11 Ferraroni M, Negri E, La Vecchia C, D’Avanzo B, Franceschi S. (1989) Socioeconomic indicators, tobacco and alcohol in the aetiology of digestive tract neoplasms. Int J Epidemiol 18:556–62.
12 van Loon AJ, Goldbohm RA, van den Brandt PA. (1998) Socioeconomic status and stomach cancer incidence in men: results from The Netherlands Cohort Study. J Epidemiol Community Health 52:166–71.[Abstract]
13 Faggiano F, Zanetti R, Costa G. (1994) Cancer risk and social inequalities in Italy. J Epidemiol Community Health 48:447–52.
14 Palli D, Bianchi S, Decarli A, et al. (1992) A case-control study of cancers of the gastric cardia in Italy. Br J Cancer 65:263–66.[Web of Science][Medline]
15 Brown LM, Silverman DT, Pottern LM, et al. (1994) Adenocarcinoma of the esophagus and esophagogastric junction in white men in the United States: alcohol, tobacco, and socioeconomic factors. Cancer Causes Control 5:333–40.[CrossRef][Web of Science][Medline]
16 Malaty HM and Nyren O. (2003) Epidemiology of Helicobacter pylori infection. Helicobacter 8:suppl 1, 8–12.
17 Hansson LE, Baron J, Nyren O, Bergstrom R, Wolk A, Adami HO. (1994) Tobacco, alcohol and the risk of gastric cancer. A population-based case-control study in Sweden. Int J Cancer 57:26–31.[Web of Science][Medline]
18 Gonzalez CA, Pera G, Agudo A, et al. (2006) Fruit and vegetables intake and the risk of stomach and oesophagus adenocarcinoma in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST). Int J Cancer 118:2559–66.[CrossRef][Web of Science][Medline]
19 Blaser MJ, Perez Perez GI, Kleanthous H, et al. (1995) Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 55:2111–15.
20 Catalano V, Labianca R, Beretta GD, Gatta G, de Braud F, Van Cutsem E. (2005) Gastric cancer. Crit Rev Oncol Hematol 54:209–41.[Web of Science][Medline]
21 Kelley JR and Duggan JM. (2003) Gastric cancer epidemiology and risk factors. J Clin Epidemiol 56:1–9 Review.[CrossRef][Web of Science][Medline]
22 Riboli E and Kaaks R. (1997) The EPIC Project: rationale and study design. European Prospective Investigation into Cancer and Nutrition. Int J Epidemiol 26:suppl 1, S6–14.
23 Riboli E, Hunt KJ, Slimani N, et al. (2002) European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr 5:1113–24.[CrossRef][Web of Science][Medline]
24 Lauren PA. (1965) The two main histologic types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. Acta Pathol Microbiol Scand 64:31–49.[Web of Science][Medline]
25 Palli D, Masala G, Del Giudice G, et al. ( Nov 27, 2006) CagA, Helicobacter pylori infection and gastric cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST) study. Int J Cancer [Epub ahead of print].
26 Mackenbach JP and Kunst AE. (1997) Measuring the magnitude of socio-economic inequalities in health: an overview of available measures illustrated with two examples from Europe. Soc Sci Med 44:757–71.[CrossRef][Web of Science][Medline]
27 Greenland S and Rothman KJ. (1998) Introduction to stratified analysis. In Rothman KJ and Greenland S (Eds.). Modern epidemiology 2nd (Lippincott-Raven, Philadelphia (PA)) pp. 53–79.
28 Jansson C, Johansson AL, Nyren O, Lagergren J. (2005) Socioeconomic factors and risk of esophageal adenocarcinoma: a nationwide Swedish case-control study. Cancer Epidemiol Biomarkers Prev 14:1754–61.
29 Ferraroni M, Negri E, La Vecchia C, D’Avanzo B, Franceschi S. (1989) Socioeconomic indicators, tobacco and alcohol in the aetiology of digestive tract neoplasms. Int J Epidemiol 18:556–62.
30 Choi SY and Kahyo H. (1991) Effect of cigarette smoking and alcohol consumption in the etiology of cancers of the digestive tract. Int J Cancer 49:381–86.[Web of Science][Medline]
31 Jedrychowski W, Wahrendorf J, Popiela T, Rachtan J. (1986) A case-control study of dietary factors and stomach cancer risk in Poland. Int J Cancer 37:837–42.[Web of Science][Medline]
32 Smith GD and Brunner E. (1997) Socio-economic differentials in health: the role of nutrition. Proc Nutr Soc 56:75–90 Review.[Web of Science][Medline]
33 Irala-Estevez JD, Groth M, Johansson L, Oltersdorf U, Prattala R, Martinez-Gonzalez MA. (2000) A systematic review of socio-economic differences in food habits in Europe: consumption of fruit and vegetables. Eur J Clin Nutr 54:706–14.[CrossRef][Web of Science][Medline]
34 Shahar D, Shai I, Vardi H, Shahar A, Fraser D. (2005) Diet and eating habits in high and low socioeconomic groups. Nutrition 21:559–66.[CrossRef][Web of Science][Medline]
35 Krieger N, Williams DR, Moss NE. (1997) Measuring social class in US public health research: concepts, methodologies, and guidelines. Annu Rev Public Health 18:341–78.[CrossRef][Web of Science][Medline]
36 Boffetta P. (1997) Infection with Helicobacter pylori and parasites, social class and cancer. IARC Sci Publ 138:325–29.
37 Ueda M, Kikuchi S, Kasugai T, Shunichi T, Miyake C. (2003) Helicobacter pylori risk associated with childhood home environment. Cancer Sci 94:914–18.[CrossRef][Medline]
38 Malaty HM and Nyren O. (2003) Epidemiology of Helicobacter pylori infection Helicobacter. 8:(suppl 1), 8–12.
39 Powell J and McConkey CC. (1990) Increasing incidence of adenocarcinoma of the gastric cardia and adjacent sites. Br J Cancer 62:440–43.[Web of Science][Medline]
40 Wu-Williams AH, Yu MC, Mack TM. (1990) Life-style, workplace, and stomach cancer by subsite in young men of Los Angeles County. Cancer Res 50:2569–76.
41 Brewster DH, Fraser LA, McKinney PA, Black RJ. (2000) Socioeconomic status and risk of adenocarcinoma of the oesophagus and cancer of the gastric cardia in Scotland. Br J Cancer 83:387–90.[CrossRef][Web of Science][Medline]
42 Ekstrom AM, Hansson LE, Signorello LB, Lindgren A, Bergstrom R, Nyren O. (2000) Decreasing incidence of both major histologic subtypes of gastricadenocarcinoma—a population-based study in Sweden. Br J Cancer 83:391–96.[CrossRef][Web of Science][Medline]
43 Hayes LJ and Berry G. (2002) Sampling variability of the Kunst-Mackenbach relative index of Inequality. J Epidemiol Community Health 56:762–65.
44 Greenland S and Robins JM. (1985) Confounding and misclassification. Am J Epidemiol 122:495–506.
45 Day NE, Wong MY, Bingham S, et al. (2004) Correlated measurement error—implications for nutritional epidemiology. Int J Epidemiol 33:1373–81.
46 Helicobacter and Cancer Collaborative Group. (2001) Gastric cancer and Helicobactyer pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut 49:347–53.
47 Lahelma E, Martikainen P, Laaksonen M, Aittomaki A. (2004) Pathways between socioeconomic determinants of health. J Epidemiol Community Health 58:327–32.
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