Annals of Oncology Advance Access published online on July 31, 2008
Annals of Oncology, doi:10.1093/annonc/mdn536
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Dietary intake of selected micronutrients and gastric cancer risk: an Italian case-control study
1 Istituto di Ricerche Farmacologiche "Mario Negri", Milan, Italy
2 Istituto di Statistica Medica e Biometria "G. A. Maccacaro", Università degli Studi di Milano, Milan, Italy
* Correspondence to: Dr C. Pelucchi, ScD, Istituto di Ricerche Farmacologiche "Mario Negri", Via Giuseppe La Masa 19, 20156 Milan, Italy. Tel: +39-02-39014577; Fax: +39-02-33200231; E-mail: pelucchi{at}marionegri.it
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Abstract |
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Background: A high consumption of non-starchy vegetables and fruits likely decreases the risk of gastric cancer, but no specific constituent of plant foods has been consistently identified to explain this association.
Patients and methods: We considered several micronutrients and minerals in an Italian case–control study conducted between 1997 and 2007, including 230 patients with incident, histologically confirmed gastric cancer and 547 matched controls, admitted with acute conditions. Micronutrients computation was based on a validated and reproducible food frequency questionnaire, through an Italian food composition database. We estimated odds ratios (ORs) using conditional logistic regression, adjusted for energy intake and selected covariates.
Results: We found decreased ORs for the highest versus lowest quartile of vitamin E (OR = 0.50), alpha-carotene (OR = 0.52) and beta-carotene (OR = 0.42) intake. Gastric cancer was directly associated with sodium, with ORs of 2.22 for the second, 2.56 for the third and 2.46 for the fourth quartile of intake. No significant relation emerged with iron, calcium, potassium, zinc, vitamin C, thiamin, riboflavin, niacin, vitamin B6, folate, vitamin D, retinol, beta-cryptoxanthin, lycopene and lutein plus zeaxanthin.
Conclusions: Our data support a favourable effect on gastric cancer of vitamin E and selected carotenoids and a detrimental effect of sodium even at intermediate levels of intake.
case–control study, diet, epidemiologic studies, micronutrients, stomach neoplasms, vitamins
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Dietary habits and intake of nutrients play an important role in the prevention and causation of gastric cancer [1]. According to a recent report from the World Cancer Research Fund and American Institute for Cancer Research (WCRF/AICR), there is ‘probable evidence’ that high consumption of non-starchy vegetables and fruits might decrease the risk of gastric cancer, while salt and salted foods might be directly associated with risk. There is also ‘limited evidence’ for a role of a number of other foods. This notwithstanding, no specific constituent of these foods has been yet identified to explain the reported associations.
Various micronutrients have been analysed in epidemiological studies considering both dietary and plasma levels. Vitamin C, retinol and selected carotenoids are among the dietary components identified to explain the protective effect of fruit and vegetables against gastric carcinogenesis, but the issue is still open to discussion [2–9]. Vitamin C has elicited widespread interest in studies of gastric cancer because of its properties that include antioxidant effects and inhibition of both Helicobacter pylori infection and production of N-nitroso compounds [10–12]. Several plausible explanations for an anticancer role of carotenoids have been proposed, including their antioxidant effects, a modulation of immunologic functions and, for carotenes, the regulation of cell differentiation via their conversion to vitamin A [13]. Similar protective mechanisms of action have been suggested for retinol, i.e. preformed vitamin A [14]. Furthermore, a role of folate has been hypothesized after the finding of an association between methylenetetrahydrofolate reductase (MTHFR) C677T polymorphism, which is involved in folate metabolism, and gastric cancer [15, 16]. Studies that examined dietary intake and plasma levels of folate and gastric cancer, however, reported inconsistent results [16, 17].
With reference to minerals, sodium intake has been linked to an increased risk of gastric cancer in several epidemiological studies, and the mechanistic evidence for a role of salt is strong [1, 18]. Information on other minerals, including dietary iron, zinc and calcium, is more limited and generally inconclusive [5, 9, 19].
Thus, we considered the relation between intake of these and several other micronutrients and minerals and the risk of gastric cancer in a case–control study conducted in northern Italy, based on a detailed and validated food frequency questionnaire (FFQ).
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Data were derived from a case–control study of stomach cancer, conducted between 1997 and 2007 in the greater Milan area, northern Italy [20]. Cases were 230 patients (143 males and 87 females) aged 22–80 years (median age 63 years) admitted to major teaching and general hospitals in the study area with incident, histologically confirmed stomach cancer (Ninth Revision of the International Classification of Diseases, ICD-IX: 151.0-151.9), diagnosed no longer than 3 months before the interview, and with no previous diagnosis of any cancer. Controls were 547 patients (286 males and 261 females) aged 22–80 years (median age 63 years) frequency matched to cases by age and sex (with a ratio of 2 : 1 for men and 3 : 1 for women), admitted to the same hospitals as cases for a wide spectrum of acute, non-neoplastic conditions, unrelated to known or potential risk factors for stomach cancer and long-term diet modification. Twenty per cent of controls were admitted for traumas, 23% for other orthopaedic disorders, 22% for acute surgical conditions and 35% for miscellaneous other illnesses, including eye, nose, ear or skin disorders. Less than 5% of cases and controls approached refused to be interviewed.
For both cases and controls, data were collected during their hospital stay by trained interviewers using a structured questionnaire. This included information on socio-demographic characteristics, such as marital status, education and occupation, anthropometric measures, selected lifestyle habits, including tobacco smoking and alcohol consumption, physical activity, a personal medical history and family history of cancer.
Information on diet was based on an FFQ, tested for reproducibility [21] and validity [22]. The FFQ included questions on 78 foods and beverages, including a range of the most common recipes in the Italian diet, grouped into six sections: milk and hot beverages, bread and cereal dishes (first courses), meat and other main dishes (second courses), vegetables, fruit, sweets, desserts and soft drinks. A separate section dealt with consumption of alcoholic beverages. Subjects were asked to indicate the average weekly frequency of consumption for each dietary item; intakes lower than once a week but at least once a month were coded as 0.5 per week. For a few vegetables and fruits, seasonal consumption and the corresponding duration was elicited. At the end of each section, one or two open questions were used to include other foods that were not in the questionnaire but were eaten at least once per week. Several questions aimed at assessing fat intake pattern were also included in the questionnaire. Dietary supplements were not considered, given their low frequency of consumption in this population. Energy and nutrient intakes were computed from the FFQ using an Italian food composition database, integrated with other sources when needed [23, 24].
Odds ratios (ORs) of stomach cancer and the corresponding 95% confidence intervals (CIs) were estimated using conditional multiple logistic regression models [25]. All models were conditioned on age (5-year groups) and sex, and adjusted for education, period of interview, body mass index (BMI), tobacco smoking, family history of stomach cancer in first-degree relatives and total energy intake. Tests for trend were based on the likelihood-ratio test between models with and without a linear term for each micronutrient. To test for interaction, the difference in –2 x log(likelihood) of the models with and without interaction terms were compared with the 
2 distribution with the same number of degrees of freedom as the interaction terms.
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Table 1 gives the distribution of 230 cases of gastric cancer and 547 controls according to sex, age and selected characteristics. By design, the proportion of women was higher in controls than in cases, and cases and controls had similar age distributions. Compared with controls, cases were more frequently ex- and current smokers, had a higher calorie intake and reported more often a family history of gastric cancer. The distribution of cases and controls was similar according to education and BMI.
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Table 2 shows the relation between intake of selected micronutrients and minerals and the risk of gastric cancer. Comparing the highest to the lowest quartile of intake, significantly reduced ORs were found for vitamin E (OR = 0.50, 95% CI = 0.27–0.93), alpha-carotene (OR = 0.52, 95% CI = 0.32–0.87) and beta-carotene (OR = 0.42, 95% CI = 0.25–0.71). For lutein plus zeaxanthin intake, the ORs were significantly below unity in the second (OR = 0.61, 95% CI = 0.39–0.98) and third quartile (OR = 0.58, 95% CI = 0.36–0.93), but not in the highest quartile of intake (OR = 0.69, 95% CI = 0.43–1.10). Gastric cancer was directly associated with sodium, with ORs of 2.22 (95% CI = 1.27–3.88) for the second, 2.56 (95% CI = 1.41–4.63) for the third and 2.46 (95% CI = 1.22–4.95) for the fourth quartile, as compared to the lowest level of intake, and phosphorus, with an OR of 2.09 (95% CI = 1.00–4.34) for the highest versus lowest quartile of intake. Corresponding values were 0.67 (95% CI = 0.39–1.14) for vitamin C, 1.65 (95% CI = 0.88–3.11) for folate and 1.50 (95% CI = 0.90–2.50) for retinol intake. Significant inverse trends in risk emerged for vitamin E (P = 0.01), alpha-carotene (P = 0.01) and beta-carotene (P = 0.001). The test for trend for phosphorus intake was not significant (P = 0.15).
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Table 3 gives the ORs of gastric cancer for the highest versus the lowest quartile of intake of selected micronutrients and minerals, in strata of sex, age and education. No significant difference between ORs was found in strata of sex and education. Associations were systematically stronger in subjects younger than 60 years, although risks were significantly heterogeneous only for vitamin E (P = 0.026, OR = 0.30 in <60 years and OR = 0.64 in
60 years) and beta-carotene intake (P = 0.009, OR = 0.18 in <60 years and OR = 0.85 in 60 years).
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The WCRF/AICR Report on Food, Nutrition, Physical Activity, and the Prevention of Cancer re-evaluated in 2007 the role of dietary factors in the aetiology of cancer, including stomach cancer [1]. With reference to intake of micronutrients and minerals, the evaluation Panel judged that no conclusion could be drawn for a role of carotenoids, thiamin, riboflavin, vitamin C, vitamin D, iron and calcium, nor for use of multivitamin or mineral supplements, on gastric cancer. For vitamin C, the evaluation was changed from ‘Probable evidence of decreases in risk’ in the 1997 Report [26] to ‘No conclusion’ in 2007. The issues are therefore still unsettled.
The most convincing finding of our study was the increase in risk observed in subjects with moderate to high intakes of sodium. Our results are in agreement with most studies that examined salt use, measured through consumption of salted foods (e.g. processed meats and salted fish), addition of salt at the table or sodium intake. At least 3 cohort, 21 case–control and 12 ecological studies have been conducted on the issue, and a meta-analysis of case–control studies reported a 18% elevated risk for an increase of 1 g/day of sodium intake [1, 18, 27–29]. In this study, the corresponding continuous OR yielded a 32% increase in risk. However, no clear increase in risk was seen when we analysed sodium intake in quartiles and the risk was lower only for subjects in the first quartile (i.e. <1.57 g/day). This notwithstanding, the role of salt in gastric cancer aetiology is not yet definitely assessed. Some inconsistencies across studies might be explained by different methods used to measure salt intake and relevant differences in salt use levels in various populations. The relation between salt intake and gastric cancer has been explained through an increased endogenous N-nitroso compound formation, enhancement of the action of carcinogens and increased risk of H. pylori infection that might be provoked by high salt use [1].
With regard to carotenoids and retinol, we found an inverse association between alpha- and beta-carotene intake and gastric cancer. A protective effect of lutein plus zeaxanthin, carotenoids with no provitamin A activity, was also suggested, though there was no evidence of a dose–response relation. The apparently stronger relation observed for beta-carotene and other micronutrients in subjects below age 60 further supports the existence of real associations, since recall of diet tends to be less accurate and valid in the elderly, when cancer causes become often less easy to identify. The heterogeneity between age groups, however, was significant for beta-carotene and vitamin E only. Our results are in substantial agreement with a recent Japanese nested case–control study of gastric cancer, based on plasma levels of carotenoids and retinol, that found inverse associations with alpha- and beta-carotene, but not with other carotenoids [30]. Alpha- and beta-carotene intakes are usually highly correlated and, in fact, in this population, the Pearson correlation coefficient was 0.75. In any case, their dietary sources are not totally overlapping, and companion studies that examined other cancer sites were able to differentiate the results for these micronutrients [31]. Possible mechanisms of action of carotenoids on cancer risk include their antioxidant functions against oxidative DNA damage [13], capability to induce gap junctional intercellular communication, independently from the antioxidant capacities [32], induction of apoptosis in transformed cells [33] and regulation of immune response [34]. Recent data from the European Prospective Investigation into Cancer and Nutrition cohort [3] and a Swedish prospective study [6] are suggestive of a favourable role of retinol, while our study reported no significant relation. Lycopene has been found to protect from gastric cancer in a few previous investigations [4, 35], but not in others [6, 8, 30]. No association with lycopene emerged in this population characterized by a relatively frequent use of tomatoes and tomato sauces, i.e. the primary sources of lycopene in the diet.
Cohort and case–control investigations suggested inverse associations between vitamin C, another micronutrient supplied by fruit and vegetables, and gastric cancer, though results were heterogeneous [2, 4, 5, 7, 8]. For example, in a prospective study of Finnish male smokers, a moderate to high dietary intake of vitamin C decreased the risk of gastric noncardia cancer by 40%, while it was unrelated to gastric cardia cancer [4]. On the other hand, another prospective investigation from 10 European countries including 215 cases of gastric cancer showed no significant association with dietary vitamin C, but an inverse relation with plasma vitamin C (OR = 0.55 for the highest versus lowest quartile), particularly for gastric cardia cancer [2]. Our findings of an about 30% decreased risk in the highest category of vitamin C intake is in broad agreement with previous results.
In this study, there was a protective effect of vitamin E on gastric cancer. Again, epidemiological information on the issue is not consistent [3–5, 36, 37]. Even in the Italian context, two separate investigations showed different results. A decreased risk emerged with increasing intake of alpha-tocopherol in a case–control study conducted in high- and low-risk areas of Italy [37], whereas in a previous study, conducted in the same areas of this study during the late 1980s, no association was found with vitamin E intake [5].
Vitamins C and E are among the micronutrients more frequently investigated in intervention trials based on supplement use. In contrast with the majority of observational studies, most of these found a lack of effect of the use of nutritional supplements on gastric cancer or precancerous lesions [38–40]. This may be, at least in part, due to the limited duration of intervention trials. Some inconsistent results—possibly explained by large differences in gastric cancer rates and/or nutritional status of the populations analysed—were observed in intervention studies, too. The potential effect of dietary supplements and micronutrients naturally present in foods might also be different. The complex mixture of vitamins and other micronutrients deriving from diet might be more effective than large supplemental doses of a limited number of micronutrients if several of these compounds interact or work together, but have limited effect individually, or if other dietary components are effectors of micronutrient action [41].
Among the limitations of our investigation, we had no information on H. pylori infection. Case–control studies, in any case, have limited ability to measure H. pylori because blood samples obtained at stomach cancer diagnosis are of low value [42]. Some of the micronutrients investigated, e.g. some carotenoids, were highly correlated with each other, and it is difficult to disentangle their effects on risk. With regard to selection bias, the catchment area of cases and controls was comparable, and participation was almost complete. All control patients with diagnoses linked to long-term changes in diet or admitted for chronic conditions were excluded. Furthermore, case–control studies are susceptible to information bias [25]. However, the questionnaire was administered to cases and controls by the same interviewers under similar conditions. A major strength of our study was the use of a satisfactorily reproducible and valid FFQ [21, 22] that allowed us to estimate the intake of several macro- and micronutrients—including various carotenoids for which data are relatively scanty—and to adjust for total energy intake [43].
In conclusion, this Italian study found an approximately halved risk of gastric cancer for high intakes of selected carotenoids and vitamin E, and a direct association with sodium even at intermediate levels of intake. We found no significant effect of vitamin C, retinol and folate intake on the risk of gastric cancer in this population.
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Italian Association for Cancer Research and the Italian League against Cancer. Fellowship from the Italian Foundation for Cancer Research (to P.B.).
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The work in this paper was undertaken while C.L.V. was a Senior Fellow at the International Agency for Research on Cancer. The authors thank Ms I. Garimoldi for editorial assistance.
Received for publication April 8, 2008. Revision received June 30, 2008. Accepted for publication July 1, 2008.
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