A provegetarian food pattern and reduction in total mortality in the Prevención con Dieta Mediterránea (PREDIMED) study PDF

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AJCN. First published ahead of print May 28, 2014 as doi: /ajcn A provegetarian food pattern and reduction in total mortality in the Prevención con Dieta Mediterránea (PREDIMED) study

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AJCN. First published ahead of print May 28, 2014 as doi: /ajcn A provegetarian food pattern and reduction in total mortality in the Prevención con Dieta Mediterránea (PREDIMED) study 1 4 Miguel A Martínez-González, Ana Sánchez-Tainta, Dolores Corella, Jordi Salas-Salvadó, Emilio Ros, Fernando Arós, Enrique Gómez-Gracia, Miquel Fiol, Rosa M Lamuela-Raventós, Helmut Schröder, Jose Lapetra, Lluis Serra-Majem, Xavier Pinto, Valentina Ruiz-Gutierrez, and Ramon Estruch for the PREDIMED Group ABSTRACT Background: Vegetarian diets have been associated with reduced mortality. Because a pure vegetarian diet might not easily be embraced by many individuals, consuming preferentially plant-derived foods would be a more easily understood message. A provegetarian food pattern (FP) emphasizing preference for plant-derived foods might reduce all-cause mortality. Objective: The objective was to identify the association between an a priori defined provegetarian FP and all-cause mortality. Design: We followed 7216 participants (57% women; mean age: 67 y) at high cardiovascular risk for a median of 4.8 y. A validated 137-item semiquantitative food-frequency questionnaire was administered at baseline and yearly thereafter. Fruit, vegetables, nuts, cereals, legumes, olive oil, and potatoes were positively weighted. Added animal fats, eggs, fish, dairy products, and meats or meat products were negatively weighted. Energy-adjusted quintiles were used to assign points to build the provegetarian FP (range: points). Deaths were confirmed by review of medical records and the National Death Index. Results: There were 323 deaths during the follow-up period (76 from cardiovascular causes, 130 from cancer, 117 for noncancer, noncardiovascular causes). Higher baseline conformity with the provegetarian FP was associated with lower mortality (multivariableadjusted HR for $40 compared with,30 points: 0.59; 95% CI: 0.40, 0.88). Similar results were found with the use of updated information on diet (RR: 0.59; 95% CI: 0.39, 0.89). Conclusions: Among omnivorous subjects at high cardiovascular risk, better conformity with an FP that emphasized plant-derived foods was associated with a reduced risk of all-cause mortality. This trial was registered at as ISRCTN Am J Clin Nutr doi: /ajcn INTRODUCTION Food patterns (FPs) 5 that are based on plant-derived foods are purportedly healthier than those in which meat, especially red and processed meat, are the main sources of macronutrients (1 6). Specifically, an FP characterized by very low intakes of meat and processed meat (7, 8) appears to be associated with greater longevity and lower cardiometabolic risk (9). When most foods are derived from vegetable sources (ie, a vegetarian diet is adopted), health benefits are apparent. Thus, coronary artery disease (CAD) mortality was reported to be significantly lower by 24% among vegetarians compared with nonvegetarians in a collaborative reanalysis of 5 prospective studies (10). Subsequently, a meta-analysis of 7 cohort studies confirmed a lower cardiovascular mortality in vegetarians, but inconsistent results for the association between vegetarian diets and death from any cause were found (11). More recently, a 5-y follow-up of the Adventist Health Study 2 cohort showed an overall association of vegetarian dietary patterns with lower mortality (12). Most available comparisons between vegetarians and nonvegetarians relied on a single measurement of diet at baseline, but dietary patterns may change over time and the length of exposure to vegetarianism may account for heterogeneity between results from different cohorts (10, 13, 14). In a pooled analysis of 5 cohort studies, vegetarian diets were inversely associated with CAD mortality, but when vegetarians were subdivided according to whether or not they had followed their current diet for $5 y, the cardiovascular benefits were confined only to those who had been vegetarian for.5 y (15). Given that in most cultures the proportion of true vegetarians is low, it would be interesting to examine whether moderate or intermediate approaches to a predominantly plant-based FP relate 1 From the Department of Preventive Medicine and Public Health, University of Navarra, Pamplona, Spain (MAM-G and AS-T); the CIBER Fisiopatologia de la Obesidad y Nutricion (DC, JS-S, ER, MF, RML-R, HS, JL, and RE), CIBER Epidemiologia y Salud Pública (HS), and the PREDIMED Network, Instituto de Salud Carlos III) (RE, JS-S, FA, EG-G, VR-G, RML-R, LlS-M, XP, and MAM-G), Spain; the Department of Internal Medicine (RE) and the Lipid Clinic, Department of Endocrinology and Nutrition (ER), Institut d Investigacions Biomediques August Pi Sunyer, Hospital Clinic de Barcelona, University of Barcelona, Barcelona, Spain; the Human Nutrition Department, Institut d Investigacions Sanitaries Pere i Virgili, Universitat Rovira i Virgili, Reus (JS-S); the Cardiovascular and Nutrition Research Group, Institut de Recerca Hospital del Mar, Barcelona, Spain (HS); the Department of Preventive Medicine, University of Valencia, Valencia, Spain (DC); the Department of Cardiology, University Hospital of Alava, Vitoria, Spain (FA); the Department of Preventive Medicine, University of Malaga, Malaga, Spain (EG-G); the Instituto de la Grasa, Consejo Superior de Investigaciones Cientificas, Seville, Spain (VR-G); the Institute of Health Sciences IUNICS, University of Balearic Islands, and Hospital Son Espases, Palma de Mallorca, Spain (MF); the Department of Family Medicine, Primary Care Division of Sevilla, San Pablo Health Center, Seville, Spain (JL); the Department of Nutrition and Food Science, School of Pharmacy, Xarxa de Referència en Tecnologia d Aliments, University of Barcelona, Barcelona, Spain (RML-R); the Research Institute of Biomedical and Health Sciences University of Las Palmas de Gran Canaria, Las Palmas, Spain (LS-M.); and the Lipids and Vascular Risk Unit, Internal Medicine, Hospital Universitario de Bellvitge, Hospitalet de Llobregat, Barcelona, Spain (XP). 2 Presented at the symposium Sixth International Congress on Vegetarian Nutrition held in Loma Linda, CA, February Am J Clin Nutr doi: /ajcn Printed in USA. Ó 2014 American Society for Nutrition 1S of 9S Copyright (C) 2014 by the American Society for Nutrition 2S of 9S MARTÍNEZ-GONZÁLEZ ET AL to lower mortality. To our knowledge, previous investigations on the relation between a priori defined FPs and mortality have included both vegetable- and animal-derived foods as positive items in the score used to build the hypothesized healthy FP (16). In this context, an FP that positively weighs vegetable-derived foods and negatively weighs animal-derived foods can be conceptualized as a progressive and gentle approach to vegetarianism (ie, a provegetarian FP) that incorporates a range of progressively increasing proportions of plant-derived foods and concomitant reductions in animal-derived foods. We hypothesized that such a provegetarian FP would relate to improved survival. Confirmation of this hypothesis might have a good translational impact, because the recommendation to preferentially consume foods from plant sources instead of foods from animal sources would be an easily understandable message for health promotion. We assessed this association between an a priori, hypothesis-oriented provegetarian FP and all-cause mortality in a Mediterranean cohort of elderly subjects at high cardiovascular risk. SUBJECTS AND METHODS Design The design, objectives, and methods of the Prevención con Dieta Mediterránea (PREDIMED) study have been reported elsewhere (17, 18). Briefly, the PREDIMED study is a parallelgroup, multicenter, randomized clinical trial designed to test the effects of 2 Mediterranean-type diets (MedDiets) on cardiovascular disease compared with a control (low-fat) diet (www. predimed.es). PREDIMED investigators are listed in the Supplemental Appendix under Supplemental data in the online issue. Participants were drawn from primary care health centers and centrally randomly assigned in a 1:1:1 ratio to 1 of 3 different dietary patterns: a MedDiet supplemented with extra-virgin olive oil, a MedDiet supplemented with nuts, or a control diet. Primary 3 The PREDIMED trial was supported by the official funding agency for Biomedical Research of the Spanish Government, Instituto de Salud Carlos III (ISCIII), through CIBER-obn and grants provided to research networks specifically developed for the PREDIMED trial: RTIC G03/140 (years ; coordinator: R Estruch) and RTIC RD 06/0045 (years ; coordinator: MA Martinez-Gonzalez); other additional research grants also funded by the ISCIII (Spanish equivalent to the NIH): PI , PI05/2584, PI07/0240, PI07/1138, PI07/0954, PI07/0473, PI08/1259, PI10/01407, PI10/ 02658, PI11/01647, PI11/02505, AGL C03-03, and PI11/01791 (all from ISCIII, Fondo de Investigación Sanitaria Fondo Europeo de Desarrollo Regional); and by the Generalitat Valenciana, Spain (ACOMP/2013/ 165 and ACOMP/2013/159). CIBERobn and RTIC RD 06/0045 are initiatives of ISCIII, Spain. The supplemental foods used in the study were generously donated by Patrimonio Comunal Olivarero and Hojiblanca from Spain (extra-virgin olive oil), the California Walnut Commission (Sacramento, CA) (walnuts), and Borges SA (almonds) and La Morella Nuts (hazelnuts) (both from Reus, Spain). The funding sources played no role in the design, collection, analysis, or interpretation of the data or in the decision to submit the manuscript for publication. 4 Address correspondence and reprint requests to MA Martínez-González, Department of Preventive Medicine and Public Health, Facultad de Medicina- Clínica Universidad de Navarra, Universidad de Navarra, Irunlarrea 1, Pamplona, Navarra, Spain. 5 Abbreviations used: CAD, coronary artery disease; FFQ, food-frequency questionnaire; FP, food pattern; MedDiet, Mediterranean-type diet; PRE- DIMED, Prevención con Dieta Mediterránea. doi: /ajcn care physicians were not informed of the allocation of participants. The methods for the dietary intervention of the PRE- DIMED trial have been described previously (18). Participants received quarterly individual and group sessions, and those allocated to the MedDiets received free provisions of either extravirgin olive oil or tree nuts throughout the study, which lasted a median of 4.8 y. The institutional review board of Hospital Clinic de Barcelona (Barcelona, Spain) approved the study protocol on July In the present study we analyzed the trial as an observational prospective cohort with repeated dietary measurements. The trial was registered at com as ISRCTN Subjects Participants were men aged y or women aged y with no previously documented cardiovascular disease but at high cardiovascular risk. They had either type 2 diabetes or $3 major cardiovascular risk factors at baseline, including current smoking, hypertension ($140/90 mm Hg or treatment with antihypertensive agents), high LDL cholesterol.160 mg/dl, low HDL cholesterol (,40 mg/dl), overweight/obesity [BMI (in kg/m 2 ) $25], or a family history of premature CAD. Exclusion criteria were history of cardiovascular disease (ie, a previous medical diagnosis of CAD, stroke, or peripheral arterial disease), any severe chronic illness, drug or alcohol addiction, history of allergy or intolerance to olive oil or nuts, low predicted likelihood of changing dietary habits according to the stages-of- change model, or illiteracy (17). Primary care physicians reviewed the clinical histories of potential candidates, which were drawn from computer-based records of each participating center, and selected those subjects who apparently met eligibility criteria. They then invited suitable candidates by telephone to attend a screening visit where eligibility criteria were reassessed in a face-to-face interview. We recruited 7447 participants between October 2003 and June All participants provided written informed consent. We excluded 231 subjects who were outside the predefined range for baseline total caloric intake ( kcal/d for women and kcal/d for men), thus leaving 7216 subjects available to be included in the final analyses. The steering committee of the PREDIMED monitored the progress of the trial, which was supervised by an external data and safety monitoring board. Dietary assessment Registered dietitians obtained dietary information on each participant in face-to-face interviews. Food pictures or food models to facilitate the estimation of serving sizes were not used in the interviews. At baseline and yearly thereafter dietitians collected a previously and repeatedly validated 137-item foodfrequency questionnaire (FFQ) (19 21). Spanish food composition tables were used to derive nutrient composition and to estimate total energy intake. The foods included in the provegetarian FP are shown in Table 1. Briefly, to build the provegetarian FP, we adjusted the consumption (g/d) of 7 food groups from plant origin (fruit, vegetables, nuts, cereals, legumes, olive oil, and potatoes) and 5 food groups from animal origin (added animal fats, eggs, fish, dairy products, and meats and meat products) for total energy intake PROVEGETARIAN PATTERN AND MORTALITY 3S of 9S TABLE 1 Scoring criteria for the provegetarian food pattern 1 Component Included foods Vegetable food groups, by quintile 2 1. Vegetables Carrot, Swiss chard, cauliflower, lettuce, tomatoes, green beans, eggplant, peppers, asparagus, spinach, other fresh vegetables 2. Fruit Citrus, banana, apple, pear, strawberry, peach, cherry, fig, melon, watermelon, grapes, kiwi, canned fruit 3. Legumes Lentils, chickpeas, beans, peas 4. Cereals White bread, whole-grain bread, cold breakfast cereal, rice, pasta 5. Potatoes Potato chips, French fries, boiled potatoes 6. Nuts Almonds, peanuts, hazelnuts, pistachios, pine nuts, walnuts 7. Olive oil Common (refined) olive oil, extra-virgin olive oil, olive pomace oil Animal food groups, by reverse quintile 3 8. Meats/meat products Beef, pork, lamb, rabbit, liver, chicken, turkey, cooked ham, Parma ham, mortadella, salami, foie gras, spicy pork sausage, bacon, cured meats, hamburger, hot dog 9. Animal fats for cooking or as a spread Butter, lard 10. Eggs Eggs 11. Fish and other seafood White fish, dark-meat fish, salad or smoked fish, clams, mussels, shrimp, squid 12. Dairy products Whole milk, skim or low-fat milk, condensed milk, cream, milk shake, yogurt, custard, cheese, ice cream 1 The overall provegetarian pattern was built by summing both components with a potential range of The consumption (g/d) of each food group was transformed into energy-adjusted quintiles by using the residuals method (1 = first quintile, 2 = second quintile, 3 = third quintile, 4 = fourth quintile, 5 = fifth quintile). The sum of quintile values across the 7 food groups gave a potential range of Consumption (g/d) was transformed into energy-adjusted quintiles (residuals), and the quintile values were reversed (1 = fifth quintile, 2 = fourth quintile, 3 = third quintile, 4 = second quintile, 5 = first quintile). The sum of reverse quintile values across the 5 food groups had a potential range of by using the residual method separately for men and women. The energy-adjusted estimates (residuals) were ranked according to their sex-specific quintiles. The quintile values for animal products were reversed (assigning a value of 5 for the first quintile, 4 for the second quintile, and successively until the value of 1 was assigned to the fifth quintile). To obtain the provegetarian FP, quintile values of plant foods and reverse quintile values of animal foods were summed; thus, the final scores could range from 12 (lowest adherence) to 60 (highest adherence). We classified adherence to the provegetarian FP in 5 categories (cutoffs): very low (,30), low (30 34), moderate (35 39), high (40 44), and very high (.44) adherence. Because few deaths occurred in the category of very high adherence to the provegetarian diet, we merged the 2 upper categories for the multivariable analyses. We chose to use these specific round cutoffs instead of quantiles because the groups thus built are more meaningful per se and could be more easily used for future comparisons with similar studies. This is in line with current recommendations given in epidemiology about procedures to categorize continuous variables (22). However, we also show the results of an alternative analysis that used quintiles of the provegetarian FP. For the sensitivity analysis, we built a similar FP but used absolute cutoffs for each of the 12 food groups with goals expressed as servings per day or servings per week (ie, normative or absolute cutoffs) instead of using energy-adjusted quintiles of consumption of each food group (23, 24). However, the same food groups as in the quintile-based assessment were considered and the score assigned 1 point for each of the 12 goals that was met (consumption of each item at or above the limit for plant foods and below the limit for animal foods). We set the cutoffs taking into account the number of servings per day or servings per week recommended in a 14-item score of adherence to the MedDiet used in the PREDIMED study (24, 25). The cutoffs for each food group (in servings) were as follows: vegetables ($2/d), fruit ($3/d), cereals ($2/d), potatoes ($1/d), legumes ($3/wk), olive oil ($4 tablespoons/d), nuts ($3/wk), dairy products (#1/d), meat (#3/wk), fish (#3/wk), eggs (#3/wk), and butter or lard (#3/wk). In these analyses, we did not compute residuals from regressions on energy intake; instead, we adjusted only for confounding by total energy intake by introducing it as a covariate in the standard multivariable models. Covariate assessment All measurements were taken at baseline and yearly thereafter by using the same procedures. Information was collected with specific questionnaires and from the subjects medical history. Information on medication use, sociodemographic variables, lifestyle, health conditions, and medical diagnoses was obtained according to standardized protocols and review of medical records. Physical activity was evaluated by using the validated Spanish version of the Minnesota Leisure Time Physical Activity Questionnaire (26, 27). Weight, height, and waist circumference were measured by trained nurses with the use of standardized procedures. The waist-to-height ratio was calculated as waist circumference divided by height, both in centimeters (25). Blood pressure was measured by trained nurses with the use of a validated semiautomatic oscillometer in triplicate (Omron HEM-705CP). The presence of type 2 diabetes at baseline was assessed by American Diabetes Association criteria at the time of the study s inception (2003): namely, fasting plasma glucose $7.0 mmol/l or 2-h plasma glucose $11.1 mmol/l after a 75-g oral-glucose load. A second test that used the same criteria was required for confirmation. Ascertainment of deaths Outcomes were adjudicated by the End-Point Adjudication Committee, chaired by a cardiologist and including 3 general practitioners, 1 endocrinologist, and 1 medical epidemiologist. The panel members were blinded to the intervention group and to the repeated dietary assessments. This committee centrally ascertained 4S of 9S MARTÍNEZ-GONZÁLEZ ET AL deaths from clinical registers on the basis of clinical records and death certificates listing an International Classification of Diseases code corresponding to any fatality. We used the International Classification of Diseases (10th revision) to classify deaths resulting from cancer (codes C00 D48) and cardiovascular disease (codes R00 R09, R55, R57, and R96).The clinical records of all participants were reviewed regardless of their continuation in the trial. Linkage to the National Death Index served to gather additional information on fatal events. Statistical analyses To appraise the degree of overlap between the provegetarian FP and the MedD
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