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Groupe d’Epidémiologie Métabolique, Centre de Recherche en Cancérologie, INSERM-CRLC, Montpellier, France
3To whom correspondence should be addressed. E-mail: marietger{at}valdorel.fuclcc.fr
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONComponents of the comprehensive...Introduction to the...LITERATURE CITED |
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KEY WORDS: • cancer prevention • diet quality index • dietary pattern • Mediterranean diet
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONComponents of the comprehensive...Introduction to the...LITERATURE CITED |
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–6
). It is time to reconsider what we know about the multistep process of cancer, complexity of the diet and limits of nutritional epidemiology, interpret these recent findings, and introduce a comprehensive approach to the relationship between diet and cancer. |
Components of the comprehensive approach |
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TOPABSTRACTINTRODUCTIONComponents of the comprehensive...Introduction to the...LITERATURE CITED |
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A mutation in normal cells resulting in transformed or initiated cells is the first step of carcinogenesis. This mutation is either present in the cells (hereditary cancer) or, more often, induced by an environmental factor (e.g., chemical carcinogens, ionizing radiation). Food may provide carcinogenic contaminants (xenobiotics) or be a mutagen itself after some nutrient is transformed (e.g., heterocyclic aromatic amines in meat overcooked at a high temperature). Genetic polymorphisms render some subjects more or less susceptible than others to environmental carcinogens. Oxidative stress is one of the main ways DNA is altered and results from either an exogenous or an endogenous source (inflammation). Antioxidant micronutrients oppose this effect. Thus, food interacts in different ways with the initiation phase, and the protective effect of food is likely to be more important than food’s contribution as a mutagen.
The promotion step is the clonal proliferation of mutated cells that occurs as the result of genetic alterations and epigenetic modulations and will achieve tumor growth. Reactive oxygen species are necessary to intracell signaling for the synthesis of growth factor, and antioxidants may interfere in this pathway. They may also oppose apoptosis at high doses, as shown by Cognault et al. (7
). One of the strongest hypotheses involving food at this step is the effect of food on growth factors through metabolic pathways. Insulin resistance is accompanied by increased synthesis, altered regulation or both of insulin-like growth factor 1, a growth factor involved in several cancers such as colon, prostate, breast and endometrium. Extraovary synthesis of estrogens, which are growth factors for breast and endometrium cancers, can occur in adipose tissue.
Less is known about the effect of food at the invasion step. Food can interfere with the genetic and epigenetic alterations at work in this phase; for example, some experimental work suggests that phenolic compounds can modify angiogenesis (A. Scalbert, INRA, Theix, personal communication, 2001), an important component of the invasion phase.
Diet.
The effect of diet does not occur through the addition of single nutrients; rather, each food combines many nutrients that allow for a synergistic action when present in a certain balance. Moreover, several foods constitute a meal and may reinforce a protective effect or be antagonistic. Variety in daily food intake will avoid the repetitious intake of unfavorable food and provide the largest array of protective nutrients. Thus, dietary pattern, i.e., the comprehensive study of food intake, should be introduced into the study of the relationship between diet and cancer.
Nutritional epidemiology.
Descriptive epidemiology unraveled the discrepancy of cancer incidences among various countries of the world. Migrant studies generated the hypothesis that a change in the environment from one country to another and from one food culture to another also changed cancer incidence. Ecological studies were interesting in that they considered the relationship between cancer and the whole environment of a country; error was introduced when the environment was reduced to a single nutrient (e.g., fat). Statistical validity imposed a necessary progression, which was accomplished by analytical methods in nutritional epidemiology. This useful step in understanding disease etiology has led to the confusion of a methodological approach with a preventive approach. Failure of single-nutrient–based intervention assays (1
, 2
) illustrates this error. Statistical methods derived from those used in social sciences may lead to a better understanding of the complex relationship between diet and cancer.
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Introduction to the comprehensive approach of the relationship between diet and cancer |
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TOPABSTRACTINTRODUCTIONComponents of the comprehensive...Introduction to the...LITERATURE CITED |
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Synergy of micronutrients.
The synergy of micronutrients was suggested by the Linxian intervention study (8
) and also by combining single nutrients identified by the analytic method in a statistical model (9
).
Cancer multistep process and synergy of micronutrients.
Van’t Veer et al. (10
) worked out two hypotheses; one, which was based on the effect of foods, was concerned with providing or avoiding oxidative stress at the initiation phase, namely, a high intake of antioxidants and a low intake of lipoperoxidable substrate, polyunsaturated fatty acids (PUFA).4
The second hypothesis was based on the metabolism of estrogens with a high intake of fat capable to increased adipose store and on the action of fiber and fermented milk in facilitating the excretion of conjugated estrogens. The authors showed that combining a low intake of fat and a high intake of fermented milk and fiber decreased breast cancer risk (Table 1
). This finding demonstrated that several types of foods could act synergistically toward a single effect, the decrease of estrogen in blood, and that the effect of fiber depended on the colon flora, which itself depended on some types of foods. It also suggested that in a case-control study at the clinical tumor phase, a mechanism related to tumor promotion and growth is more easily shown than one possibly related to initiation.
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A leap onward was accomplished by Slattery et al. (11
) when they introduced principal component analysis in a case-control study of food-related colon cancer risk. With this type of analysis, they identified several dietary patterns, among them the Western diet (high intake of processed and red meats, fast food, refined grain, added sugar and high fat dairy food and a low intake of yogurt), a prudent diet (high intake of fish, fresh fruit, legumes, cruciferous, carrots, tomatoes and other vegetables) and a "drinker" diet (high intake of fish, liquor and wine). In Table 2
the Western diet is shown to increase colon cancer risk whereas the prudent diet appears to be protective. Note that the drinker diet also increases colon cancer risk although it contains fish, which is also part of the prudent diet. This illustrates how results based on a single food can be misinterpreted, because a high fish intake belongs to both a favorable and an unfavorable dietary pattern.
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). Nutritional assessment was obtained by a validated food-frequency questionnaire (FFQ) (13
, 14
) for 922 subjects in five subregions characterized by socioeconomic variables such as income, population density, employment, number of shopping centers, fast food restaurants and women’s activity. We included food and cancer incidences as quantitative variables and the five socioeconomic subregions as individuals in a principal component analysis to reveal the association between quantitative variables (food intake and cancer incidences, columns of the matrix) and between individuals (the five subregions, line of the matrix) and to interpret simultaneously the contributions of variables and individuals. Because incidences are aggregated values for each of the five subregions, individual nutrition data were reaggregated for each of the five subregions and introduced as the median value of the individuals’ data. This analysis is illustrated in Figure 1
for 454 men.
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, the radius of the circle represent the values of the contributions of the variables to the plane defined by axes 1 and 2 (the closer to the circle, the higher the coefficient; threshold: 0.52). The individuals are represented along the two axes that define the plane of the circle. Three different dietary patterns can be seen, i.e., a Mediterranean type, with typical foods such as olive oil, fish and sea-food, olives and herbs; a rich diet characteristic of the French southwest region with a high intake of processed meat, foie gras and wine but also fruits and vegetables; and a fast food diet characterized by a high intake of fast foods (various sandwiches, hamburgers and pizzas), cheeses, meat and dried fruit. A Mediterranean diet and a fast food diet are the opposite of each other, i.e., all sites of cancer and prostate and lung cancer incidences are associated with the fast food dietary pattern and hence not associated with the Mediterranean diet pattern. High intakes of fruits and vegetables are opposite stomach cancer, whereas colon rectum cancer incidence appears associated with the rich diet, especially wine and alcohol intake, despite the association with a high intake of fruits and vegetables. Subregions 1, 2, 4 and 5 are clearly dissociated along the two axes. When they are projected on this representation, regions 1 (rural area in keeping with traditional dietary pattern) and 2 (seashore area in keeping with traditional dietary pattern) are clearly projected onto the Mediterranean diet pattern. Region 5 (the southwest subregion) is related to its typical dietary pattern. Bladder cancer shows a weak association with the dietary pattern of region 5, but this risk may be confounded by occupational risk in this region (use of solvents in leather industry). Region 1 (the city of Montpellier and the suburbs) is projected on the fast food pattern. Region 3, which contains a medium-sized city in a vine-growing area with an intermediary diet pattern (loss of Mediterranean or traditional pattern, influence of urbanization), shows a high incidence of kidney, head and neck cancers without any clear association with an identified food pattern. Thus, considering dietary patterns may help in the interpretation of results in the context of the whole dietary pattern, whereas the analysis based on single nutrients or foods could have led to unexpected or uninterpretable results [fish and colon cancer in Slattery et al. (11
), fruits and vegetables and colon cancer in MEDHEA]. Dietary patterns may also be considered within the complexity of an ecological framework that accounts for socioeconomic variables that are useful for delivering an effective prevention message. Predetermined dietary patterns.
Findings based on dietary patterns that depend on the consumption characteristics of the sample under study cannot be generalized. Kant et al. (15
) used recommended food scores calculated from the sum of 23 foods (fruits, vegetables, whole grains, low fat dairy, poultry and fish) given by the FFQ in a prospective study on breast cancer. They showed that the risk for all cancer sites was decreased by 40% (odds ratio = 0.60; confidence interval = 0.49–0.74) for the highest recommended food scores.
Mc Cullough et al. (16
, 1417
) devised a healthy eating index (HEI) based on current guidelines for the consumption of 10 components. The best quality score, 100, is obtained with an intake of total fat <30% of energy intake, an intake of saturated fatty acids <10% of energy intake, cholesterol <300 mg, sodium <2.4 g and at least 16 different foods consumed over 3 d. The 0 score is >45% of energy intake from fat, >15% energy intake from saturated fatty acids, >450 mg cholesterol, >4.8 g sodium and six or fewer different foods consumed over 3 d. For other foods, HEI varies with age and sex. Briefly, the HEI for women 19–50 y is the same as that for men 
51 y; men 19–50 y should have a slightly higher intake and women 51 y should have a slightly lower intake. The score of 100 is given by 9 servings per day of grains, 3 of fruits, 4 of vegetables, 2 of milk and 2.4 of meats. Quantities were extrapolated from the recommended servings in the USDA pyramid (18
). This HEI was applied to the Nurses Health Study (16
) and to the Health Professionals Follow-Up Study (17
). The subjects presenting the highest scores in both studies did not show a reduced risk of cancer. However, the grouping of the foods requires some comment, i.e., vegetables include potatoes (including French fries) and green or orange-yellow vegetables, which do not have the same nutritional qualities; meats includes all meats, poultry, fish, dry beans, eggs and nuts. Lipids present as total lipids and saturated fat may have an excessive influence on the score.
To evaluate food patterns in our region, we first constructed a diet quality index (DQI) based on the American Heart Association (19
), which also selected two variables to characterize lipid intake and recommended a moderate amount of protein without any distinction of the source. Such a DQI did not enable a regular progressive classification of the subjects. Therefore, another construction, the Mediterranean DQI (Med-DQI), had to be created (Table 3
). The major differences from other such indices is the presence of two different sources of fat (saturated fat and olive oil) and two different sources of protein (meat and fish) with opposite scores, one on the poor side, the other on the good side, respectively. The findings of this study have been published (20
, 21
) and will be summarized only briefly.
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-carotenes, vitamin E, eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA); EPA and DHA are long-chain (n-3) PUFA, markers of fish intake. Each biomarker was correlated with the Med-DQI. A higher correlation coefficient between the Med-DQI and a composite index using the highest tertiles of each biomarker was observed (0.58 instead of 0.32 for DHA, the highest coefficient correlation with a single biomarker), indicating that this composite index reflected the whole dietary pattern. These findings may be summarized as follows: subjects with a level of DHA >4.2% and EPA >0.7% in erythrocyte membranes and levels of - and ß-carotene >1.3 µmol/L and vitamin E >30.5 µmol/L in plasma are likely to have a good diet, whereas subjects with a level of DHA <2.7%and of EPA <0.4% in erythrocytes membranes and levels of - and ß-carotene <0.66 µmol/L and vitamin E <24.2 µmol/L in plasma are likely to have a poor diet. This Med-DQI is going to be used in case-control and prospective studies on breast cancer. Nutritional approach in intervention assays.
Intervention assays (or ethically approved human experimentation) appear the best for establishing a causal relationship between diet and cancer. However, this method also faces difficulty. The nutritional intervention will last for a long period and compliance might be difficult to maintain. If an intermediate endpoint is used, whenever it exists, the dietary factors assayed after results of observational studies might be related to a different step of the carcinogenic process from the one related to the intermediate endpoint.
The study by Shatzkin et al. (4
) on colorectal adenoma recurrence is a good illustration of these difficulties. Compliance could not be ascertained because the change in the only nutritional marker used (ß-carotene) was modest (22
). Fiber intake and low fat may not be dietary factors of importance at the colorectal adenoma stage, whereas tobacco and alcohol may adversely and calcium protectively influence this stage (23
, 24
). Thus one major protective dietary component was possibly missing.
The study by Berrino et al. (25
) was successful with regard to results but failed to provide clear-cut information on the mechanism by which the nutritional approach affected the endpoint. Postmenopausal women (n = 354) with high testosterone levels were enrolled and followed a diet rich in phytoestrogens from soy, flaxseed, and various grains and legumes and low in simple sugars. The endpoint was the measurement of hormones as intermediary markers because hormones act as tumor growth factors for breast cancer. An increase in sex hormone–binding globulin and a decrease in testosterone as well as a decrease in insulin peak and waist-to-hip ratio were observed. It is difficult to determine whether the effect on the hormones resulted from the dietary change per se (namely, the high intake of phytoestrogens) or the weight loss or the reversal of the signs of an insulin-resistance syndrome.
The ultimate goal is prevention, and successful results of this nutritional approach together with the findings of most of the observational studies either with dietary patterns or the DQI suggest the necessity to propose a comprehensive diet pattern introducing both variety and specificity with respect to the selected foods along a weekly rhythm. A model that uses the main characteristics of the Mediterranean diet is currently proposed in a nutritional intervention assay with subjects at risk for cardiovascular disease (26
), i.e., the RIVAGE study (Risques Cardio-Vasculaires, Alimentation Méditerranéenne et Génétique). Recommendations are given together with a complete set of menus and recipes.
To guide subjects with certain precision toward consuming a variety of foods over several days, we proposed a schematic representation. There are seven sections, each for a day of the week, organized in the shape of a circle, with common features at the center. The common features are bread, to be eaten at each meal of the day, olive oil, for cooking and seasoning and one glass of wine for each day. Surrounding the center circle are concentric circles grouped by meals as follows: 1) three circles for breakfast, i.e., one for fruit, the second for cereals or bread and the third for dairy products; 2) four circles for lunch, the first for raw or cooked vegetable as an hors d’oeuvres, the second for fish (four times per week), poultry (once or twice per week), meat (once per week) or an egg-based dish (once per week or never); for the third, to accompany the high protein source, we propose either vegetables (twice per week), legumes (twice per week), cereals (twice per week) or potatoes (once per week) and for the fourth, a fruit everyday but pastry or ice cream on Sunday or another special day; and 3) three circles for dinner, the first a vegetable dish (raw or cooked vegetables, legumes, cereals), the second a dairy product, preferably yogurt or goat or sheep cheese, and the third a fresh or dried fruit.
The choices are calculated to cover the necessary variety and amount of nutrients over a week. The food portions are calculated according to the age, sex and body mass index of the subjects, who receive a set of copies of the scheme that indicate the portion to select. Lunch and dinner can be inverted to suit the subjects’ daily routine. This model was shown to be practical and helpful when the principle of daily menus and of weekly rhythm is understood. Our purpose was not to reduce the complexity of the comprehensive approach because simple principles appear difficult to implement in everyday food habits, and thorough counseling and advice are necessary to reach the goal of satisfactory compliance in nutritional intervention assays.
A critical review of past or current studies that have taken a comprehensive approach to diet has been presented. It helped to explain some unexpected results or failures and open the way to a better understanding of the relationship between diet and cancer.
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FOOTNOTES |
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2 Supported by Ligue contre le cancer-34; Conseil Regional Languedoc-Roussillon.
4 Abbreviations used: DHA, docosahexaenoic acid; DQI, diet quality index; EPA, eicosapentaenoic acid; FFQ, food-frequency questionnaire; HEI, healthy eating index; Med-DQI, Mediterranean DQI; PUFA, polyunsaturated fatty acids.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONComponents of the comprehensive...Introduction to the...LITERATURE CITED |
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1. The Alpha-Tocopherol, Beta-Carotene, Cancer Prevention, Study Group (1994) The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. N. Engl. J. Med. 330:1029-1035.
2. Omenn, G. S., Goodman, G. E., Thornquist, M. D., Balmes, J., Cullen, M. R., Glass, A., Keogh, J. P., Meyskens, F. L., Valanis, B., Williams, J. H., Barnhart, S. & Hamma, S. (1996) Effects of a combination of beta carotene and vitamin A on lung cancer and cardiovascular disease. N. Engl. J. Med. 334:1150-1155.
3. Alberts, D. S., Martinez, M. E., Roe, D. J., Guillén-Rodriguez, J. M., Marshall, J. R., Van Leeuwen, B., Reid, M. E., Ritenbaugh, C., Vargas, P. A., Bhattacharyya, A. B., Earnest, D. L. & Sampline, R. E. (2000) The Phoenix Colon Cancer Prevention Physicians’ Network. Lack of effect of a high-fiber cereal supplement on the recurrence of colorectal adenomas. N. Engl. J. Med. 342:1156-1162.
4. Shatzkin, A., Lanza, E., Corle, D., Lance, P., Iber, F., Caan, B., Shike, M., Weissfeld, J., Burt, R., Cooper, M. R., Kikendall, J. W. & Cahill, J., The Polyp Prevention Trial Study Group (2000) Lack of effect of a low-fat, high-fiber diet on the recurrence of colorectal adenomas. N. Engl. J. Med. 342:1149-1155.
5. Feskanich, D., Ziegler, R. G., Michaud, D. S., Giovannucci, E. L., Speizer, F. E., Willett, W.C. & Colditz, G. A. (2000) Prospective study of fruit and vegetable consumption and risk of lung cancer among men and women, J. Natl. Cancer Inst. 92:1812-1823.
6. Fuchs, C. S., Giovannucci, E. L., Colditz, G. A., Hunter, D. J., Stampfer, M. J., Rosner, B., Speizer, F. E. & Willett, W. C. (1999) Dietary fiber and the risk of colorectal cancer and adenoma in women, N. Engl. J. Med. 340:169-176.
7. Cognault, S., Jourdan, M. L., Germain, E., Pitavy, R., Morel, E. & Durand, G. (2000) Effect of an alpha-linolenic acid-rich diet on rat mammary tumor growth depends on the dietary oxidative status. Nutr. Cancer 36:33-41.[Medline]
8. Blot, W. J., Li, H. Y., Taylor, P. R., Guo, W., Dawsey, S., Wang, G. Q., Yang, C. S., Zheng, S. F., Gail, M. & Li, G.Y. (1993) Nutrition intervention trials in Linxian, China: supplementation with specific vitamin/mineral combinations, cancer incidence, and disease-specific mortality in the general population. J. Natl. Cancer Inst. 85:1483-1492.
9. Yong, L. C., Brown, C. C., Schatzkin, A., Dresser, C. M., Slesinski, M. J., Cox, C. S. & Taylor, P. R. (1997) Intake of vitamins E, C, and A and risk of lung cancer. The NHANES I epidemiologic follow up study. Am. J. Epidemiol. 146:231-243.
10. Van’T Veer, P., Van Leer, E. M., Rietdijk, A., Kok, F. J., Schouten, E. G., Hermus, R. J. & Sturmans, F. (1991) Combination of dietary factors in relation to breast-cancer occurrence. Int. J. Cancer 47:649-653.[Medline]
11. Slattery, L. M., Boucher, K. M., Caan, B. J., Potter, J. D. & Ma, K. N. (1998) Eating patterns and risk of colon cancer. Am. J. Epidemiol. 148:4-16.
12. Siari, S., Scali, J., Richard, A., Tretarre, B., Daurès, J. P., Padilla, M., Grosclaude, P. & Gerber, M. (2001) Infra-regional variations of dietary consumption and cancer incidences in Southern France 2001 Proc. Nutrition and Cancer International Meeting Lyon, France (in press). .
13. Bonifacj, C., Gerber, M., Scali, J. & Daurès, J. P. (1997) Comparison of dietary assessment methods in a Southern French population. Use of weighed records estimated-diet records and a food-frequency questionnaire. Eur. J. Clin. Nutr. 51:217-231.[Medline]
14. Daurès, J. P., Gerber, M., Scali, J., Astre, C., Bonifacj, C. & Kaaks, R. (2000) Validation of a food frequency questionnaire using multiple day records and biochemical markers: application of the methods of triads. J. Epidemiol. Biostat. 5:109-115.[Medline]
15. Kant, A. K., Schatzkin, A., Graubard, B. I. & Schairer, C. (2000) A prospective study of diet quality and mortality in women. J. Am. Med. Assoc. 283:2109-2115.
16. McCullough, M. L., Feskanich, D., Stampfer, M. J., Rosner, B. A., Hu, F. B., Hunter, D. J., Varyam, J. N., Colditz, G. A. & Willett, W. C. (2000) Adherence to Dietary Guidelines for Americans and risk of major chronic disease in women. Am. J. Clin. Nutr. 72:1214-1222.
17. McCullough, M. L., Feskanich, D., Rimm, E. B., Giovanucci, E. L., Ascherio, A., Varyam, J. N., Spiegelman, D., Stampfer, M. J. & Willett, W. C. (2000) Adherence to Dietary Guidelines for Americans and risk of major chronic disease in men. Am. J. Clin. Nutr. 72:1223-1231.
18. U.S. Department of Agriculture & Human Nutrition Information Service (1992) The Food Guide Pyramid: Home and Garden Bulletin no 1992:252 Human Nutrition Information Service Hyattsville, MD. .
19. Krauss, R. M., Deckelbaum, R. J., Ernst, E., Fisher, E, Howard, B. V., Knopp, R. H., Kotchen, T., Lichenstein, A. H., McGill, H. C., Pearson, T. A., Prewitt, T. E., Stone, N. J., Horn, L. V. & Weinberg, R. (1996) Dietary guidelines for healthy American adults. A statement for health professionals from the Nutrition Committee. American Heart Association. Circulation 94:1795-1800.
20. Gerber, M., Scali, J., Michaud, A., Durand, M., Astre, C., Dallongeville, J. & Romon, M. (2000) Profiles of a healthy diet and its relationship with biomarkers in a population sample from Mediterranean Southern France. J. Am. Diet Assoc. 100:1164-1171.[Medline]
21. Scali, J., Richard, A. & Gerber, M. (2001) Diet profiles in a population sample from Mediterranean Southern France. Public Health Nutr 4:255-264.[Medline]
22. Gerber, M. (2000) Diet, colorectal adenomas and colorectal cancers (Correspondence). N. Engl. J. Med. 343:737.[Medline]
23. for the Polyp Prevention Study GroupBaron, J. A., Beach, M., Mandel, J. S., van Stoclk, R. U., Haile, R. W., Sandler, R. S., Rothstein, R., Summers, R. W., Snover, D. C., Beck, G. J., Bond, J. H. & Greenberg, E. R. (1999) Calcium supplements for the prevention of colo-rectal adenomas N. Engl. J. Med. 340:101-107.
24. Bonithon-Kopp, C., Kronborg, O., Giacosa, A., Rath, U. & Faivre, J., European Cancer Prevention Organization Study Group (2000) Calcium and fiber supplementation of colo-rectal adenoma recurrence: a randomised intervention trial. Lancet 356:1286-1287.[Medline]
25. Berrino, F., Bellati, C., Secreto, G., Camerini, E., Pala, V., Panico, S., Allegro, G. & Kaaks, R. (2001) Reducing bioavailable sex hormones through a comprehensive change in diet: the diet and androgens (DIANA) randomised trial. Cancer Epidemiol. Biomark. Prev. 10:26-33.[Medline]
26. Vincent, S., Defoort, C., Gerber, M, Bernard, M. C., Renucci, J. F., Vague, P. & Lairon, D. (2001) Micronutrients, Mediterranean diet and cardiovascular risk: the RIVAGE study. Proc Cost 916, Roma 2000 (in press) .
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