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Nut consumption, weight gain and obesity: Epidemiological evidence
Nutrition, Metabolism & Cardiovascular Diseases (2011) 21, S40eS45 available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/nmcd
Nut consumption, weight gain and obesity: Epidemiological evidence ´lez *, M. Bes-Rastrollo M.A. Martı´nez-Gonza Department of Preventive Medicine and Public Health, University of Navarra, Spain Received 12 August 2010; received in revised form 8 November 2010; accepted 18 November 2010
KEYWORDS Walnut; Hazelnut; Overweight; Fiber; Mediterranean diet; Monounsaturated fat; Poly-unsaturated fat; Satiety
Abstract Background and aims: Short-term trials support that adding tree nuts or peanuts to usual diets does not induce weight gain. We reviewed the available epidemiological evidence on long-term nut consumption and body weight changes. We also report new results from the SUN (“Seguimiento Universidad de Navarra”) cohort. Methods and results: Published epidemiologic studies with 1-yr follow-up were located. Two published reports from large cohorts (SUN and Nurses Health Study-2) showed inverse associations between frequency of nut consumption and long-term weight changes. A beneficial effect of a Mediterranean diet supplemented with tree nuts on waist circumference was reported after 1-yr follow-up in the first 1224 high-risk participants in the PREDIMED (“PREvencion DIeta MEDiterranea”) trial. After assessing 11,895 participants of the SUN cohort, a borderline significant (p value for trend Z 0.09) inverse association between baseline nut consumption and average yearly weight gain (multivariate-adjusted means Z 0.32 kg/yr (95% confidence interval: 0.22e0.42) and 0.24 (0.11e0.37) kg/yr for participants with no consumption and >4 servings/week, respectively) was found after a 6-yr follow-up. Conclusions: Consumption of nuts was not associated with a higher risk of weight gain in longterm epidemiologic studies and clinical trials. ª 2010 Elsevier B.V. All rights reserved.
Introduction Overweight, obesity and age-related weight gain are major health problems in developed countries and are strongly related to dietary habits [1]. Rapidly increasing rates of overweight and obesity in most countries highlight that the
primary determinant of obesity development comes from behavioral and dietary changes rather than from genetic factors [2,3]. Increasing trends of overweight/obesity with potentially devastating long-term consequences underline the importance of understanding the role of key food items in the prevention of age-related weight gain. Tree nuts or
* Corresponding author. Universidad de Navarra, Ed. Investigacio ´n. C/Irunlarrea 1, 31008 Pamplona, Navarra, Spain. Tel.: þ34 948 425600x6463; fax: þ34 948 455649. E-mail address: [email protected] (M.A. Martı´nez-Gonza ´lez). 0939-4753/$ - see front matter ª 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.numecd.2010.11.005
Nuts and weight gain peanuts (which actually are legumes) can be a good candidate to prevent obesity and obesity-related metabolic and cardiovascular diseases. Several epidemiological studies have reported that frequent nut consumption is inversely associated with fatal and nonfatal coronary heart disease [4e7]. A recently published pooled analysis of 25 feeding studies with different nuts supported also a consistent cholesterol-lowering effect of nut consumption [8]. Epidemiological studies suggest that nut consumption protects against the development of diabetes in women [9] and against hypertension in men [10]. In a cross-sectional assessment of 847 participants in one of the centers of the PREDIMED study, nut consumption was inversely associated with adiposity measures (BMI and waist circumference) independently of other factors. The adjusted models predicted that BMI and waist circumference decreased by 0.78 kg/m2 and 2.1 cm, respectively, for each daily serving of 30 g of nuts [11]. Despite these findings, since nuts are energy-dense foods with a high-fat content, there is still a fear that their consumption may lead to unwanted increases in body weight and to a higher long-term risk of developing overweight or obesity. However, available metabolic studies and short-term controlled feeding trials support that adding nuts to usual diets does not induce weight gain, despite an expected increase in total caloric intake. Some small trials have also suggested that isocaloric replacement of other food items by nuts may reduce body weight and fat mass [12]. However, these studies only assessed the short-term effects of nuts in small groups of volunteers and did not assess the association of nut consumption with long-term (1 yr) weight changes or with the risk of developing overweight/obesity in the subsequent years. Therefore, the aim of our study was to prospectively evaluate the long-term association between nut consumption and weight gain or incidence of overweight/obesity in epidemiologic studies. We did a literature search and also analysed new data of a Mediterranean cohort, the SUN (Seguimiento Universidad de Navarra) project.
Methods Literature search We initially conducted a Medline search using the following search strategy: (nut OR nuts OR walnuts OR almonds OR hazelnuts OR *nuts) & (weight OR overweight OR obesity OR adiposity OR waist) & (follow-up OR cohort). This search retrieved 49 articles. Our selection criteria were a sample size larger than 500 participants and that, after a minimum follow-up period of 1 year, there was an assessment of the relationship between the consumption of nuts and at least one of the following outcomes (a) weight change, (b) change in waist circumference, (c) incidence of overweight, or (d) incidence of obesity. Only 2 of the initially selected studies met one of these criteria [13,14]. Additional contact with experts provided another study [15].
The SUN cohort The SUN project is a prospective cohort study with a dynamic design (enrollment is continually open). It was designed in
S41 collaboration with the Harvard School of Public Health, following a similar methodology to that of large American cohorts such as the Nurses’ Health Study or the Health Professionals Follow-up Study. Details on the objectives, design and methods of this cohort have been published elsewhere [16,17]. Briefly, beginning on December 1999, all Spanish alumni of the University of Navarra and several other professional collectives with a university degree received a letter of invitation to participate in the study, a questionnaire to respond and a postage-prepaid envelope to return the questionnaire. This baseline questionnaire gathered information about sociodemographic variables, lifestyle factors, as well as information on health and diet through a validated 136item semiquantitative food frequency questionnaire (FFQ) [18e20]. All participants who completed a baseline assessment (Q_0) up to October 2006 (n Z 16,593) were assessed. Among them we excluded 1653 who reported total energy intake out of predefined values (<800 kcal/d for men, <500 kcal/d for women or >4000 kcal/d for men, >3500 kcal/d for women), 753 who reported chronic disease at baseline (cancer or cardiovascular disease), 54 deceased participants, 1727 subjects with no follow-up data (retention rate Z 88%), and 556 participants with missing data in some variable of interest, leaving a total of 11,895 participants available for the analyses. The study was approved by the Institutional Review Board at the University of Navarra. Informed consent was implied by the voluntary completion of the baseline questionnaire. The FFQ was collected only at baseline and was based on typical portion sizes and had nine options for the average frequency of intake in the previous year of each food item (ranging from never/almost never to at least six times per day). Questions on nut consumption included walnuts, almonds, hazelnuts, and peanuts. These four types represent >95% of total nut consumption in the Spanish general population [13]. Information on body weight of each participant was recorded at baseline and at follow-up questionnaires, which were completed every two years. The reliability and validity of self-reported weight was assessed in a subsample of the cohort. The mean relative error in self-reported weight was 1.45%, and the correlation coefficient between measured and self-reported weight was 0.99 (95% CI: 0.98e0.99) [21]. The outcomes were (1) the change in body weight during follow-up, defined as average change in body weight per year of follow-up [the last weight reported minus the baseline weight divided by the years of follow-up]. (2) Weight gain 3 kg/yr during follow-up. Physical activity during leisure time was assessed with a previously validated questionnaire [22]. The Spearman correlation coefficient between energy expenditure assessed with this questionnaire and with a triaxial accelerometer was 0.51, 95% confidence interval (CI) 0.23, 0.71. An activity metabolic equivalent (MET) index was computed by assigning a multiple of resting metabolic rate (MET score) to each activity (17 activities). Time spend in each of the activities was multiplied by the MET score specific to each activity, and then summed over all activities obtaining a value of overall weekly MET-hours [23]. Generalized linear models were used to assess the association between total nut consumption, based on the frequency of servings (50 g) categorized as never/almost
S42 never, 1e3/month, 1/week, 2e4/week and 4/week, and average yearly weight change during follow-up. Logistic regression models were fitted to assess the association between 3 categories of baseline consumption of a serving of nuts (1e3/month, 1/week, 2/week) and the risk of gaining on average 3 kg/yr. Odds ratios were calculated using the lowest category (never/almost never) as the reference. All models were adjusted for age, sex, baseline body mass index, previous weight gain (during the 5 years before recruitment), physical activity at baseline and baseline prevalence of hypertension, dyslipidemia or diabetes. We evaluated the interaction between the exposure and sex and between age and sex through interaction terms included in the multivariate model. The PREDIMED (PREvencion Dieta MEDiterranea) study is a large, parallel-group, multicenter, randomized trial aimed to assess the effects of the MeDiet on the primary prevention of cardiovascular disease. The objectives, design, methods and other aspects of this trial have been published elsewhere [24,25]. Participants are men aged 55e80 years and women aged 60e80 years without any previous cardiovascular event, but with high cardiovascular risk (either type 2 diabetes or at least three of the following major risk factors, including smoking, hypertension, hyperlipidemia, low HDL-cholesterol, overweight or obesity or family history of cardiovascular disease). Participants were assigned to receive one of three different dietary interventions: control (low-fat) diet, MeDiet supplemented with extra virgin olive oil (MeDiet þ VOO) or MeDiet supplemented with tree nuts (MeDiet þ nuts). Participants allocated to the control group were advised to reduce all types of fat and were given written recommendations according to the American Heart Association guidelines. The groups assigned to MeDiet were advised to use extra virgin olive oil for cooking and dressing, to increase vegetable, nuts and fish consumption, to consume white meat instead of red or processed meat and for alcohol drinkers to follow a pattern of moderate red wine consumption. Each participant received a personal interview with a trained dietitian and a group session conducted by the same dietitian every 3 months during these four years. The two MeDiet groups received either free olive oil (1 L/week) or mixed nuts (30 g/day, as 15 g of walnuts and 15 g of almonds). No energy restrictions were prescribed for any intervention group. The dietary intervention procedures have been shown to be able to obtain significantly different between-group changes in nutrient intake and in the overall dietary pattern [25].
Results Review of published studies Table 1 shows the results of previously published epidemiological studies. The SUN cohort found inverse associations between baseline consumption of nuts and average weight gain or the risk of gaining 5 kg during 28-month follow-up [13]. No association was found between nut consumption and the risk of developing overweight or obesity during the same period for participants who initially had a body mass index <25 kg/m2.
M.A. Martı´nez-Gonza ´lez, M. Bes-Rastrollo Inverse associations between nut consumption and baseline and average weight gain during the subsequent 8 years were also reported by the Nurses Health Study-2 [14]. Moreover, among women who were not obese at baseline, the risk of developing obesity during the 8-yr period of follow-up was lower (hazard ratio Z 0.62, 95% CI: 0.32e0.99) for women consuming at baseline 2 or more servings of nuts per week than among those with rare or null consumption [14]. The report of the PREDIMED randomized trial about Mediterranean diet (MeDiet) and the metabolic syndrome [15] found that a MeDiet enriched with nuts was inversely associated with the incidence of the metabolic syndrome after 1-yr of intervention. The group allocated to MeDiet þ nuts also exhibited a significant reduction after 1-yr in the prevalence of abdominal obesity in comparison with the control group.
The SUN cohort: 6-yr follow-up Table 2 shows that an inverse association between baseline consumption of nuts and average yearly weight change was apparent in the univariate analysis during a 6-yr period of follow-up of this Mediterranean cohort. However, further adjustment for some potential confounders attenuated this association and the statistical significance for the linear trend test (p Z 0.09) did not reach the conventional five percent cut-off point. A similar pattern was observed for the risk of gaining 3 or more kg/yr, with a significant inverse association that was attenuated after multivariate adjustment. In any case none of these results suggested any association between nut consumption and a higher risk of weight gain. On the contrary all the point estimates in the SUN cohort suggested that the lower weight gains were always observed among participants consuming 2 servings of nuts/week. Table 3.
Discussion The available epidemiological evidence together with the new results hereby reported does not suggest that nut consumption in the usual amounts (up to 4 servings/week) leads to any appreciable weight gain in the long-term. Even when total energy intake was slightly increased because of the addition of nuts to the usual dietary pattern, no significant weight gain was observed. Ideally, nuts should be used within an isocaloric diet to replace other food items with high energy density or unhealthy snacks. Our results are consistent with the previously observed null or beneficial effect of nuts in smaller, short-term feeding trials showing a protection against adiposity [12,26]. Beyond cross-sectional studies which have found that nut consumers usually have a lower body mass index than non-consumers, available data from prospective studies provide an adequate temporal sequence and a sufficiently long follow-up. They consistently support the notion that the addition of nuts to the usual diet leads to less than predicted increases in body weight or adiposity. Several biological mechanisms may explain this lack of weight gain observed in association with nut consumption. Nuts are known to induce satiation (reduction in the total amount of food eaten in a single meal) and satiety (reduction in the frequency of meals). A sizable amount of the energy
Nuts and weight gain Table 1 obesity.
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Published epidemiological studies on nut consumption and weight gain, risk of overweight, obesity or abdominal
Study
n
Follow-up
Outcome
Exposure (comparison)
Results
SUN cohort [12]
8865
28 months
average weight gain
SUN cohort [12]
8865
28 months
Odds Ratio (OR) for gaining 5 kg
Weight gain difference between both groups Z 410g (95% CI: 740 to 80)a OR Z 0.71 (95% CI: 0.54e0.93)a OR Z 1 (ref.)
SUN cohort [12]
6630
28 months
NHS2 cohort [13]
51,188
8 years
Odds Ratio (OR) for overweight or obesity average weight gain
2/servings/wk vs. never or almost never (ref.) 2/servings/wk vs. never or almost never 2/servings/wk vs. never or almost never
NHS2 cohort [13]
408,664 personyears 1224 1-year
PREDIMED trial [14]
Hazard Ratio (HR) for obesity Prevalence (%) of abdominal obesity (1-year changes)
OR Z 0.73 (95% CI: 0.48e1.11)a OR Z 1 (ref.)
2/servings/wk vs. rare consumption 2/servings/wk vs. rare consumption
4.43 kg vs. 5.53 kg (p < 0.001)b
MeDiet þ nuts: vs. control: (low-fat diet)
64.5% (baseline) to 59.6% (1-year) vs. 65.3% (baseline) to 68.0% (1-year)c
HR Z 0.62 (0.32e0.99)b HR Z 1 (ref.)
MeDiet Z Mediterranean-type diet; SUN: “Seguimiento Universidad de Navarra” (Follow-up Navarra University); PREDIMED: “Prevencio ´n con Dieta Mediterra ´nea” (Prevention with Mediterranean Diet). OR Z Odds Ratio; HR Z Hazard Ratio; CI Z Confidence Interval; NHS2 Z Nurses’ Health Study-2; ref. Z reference group. a Adjusted for age, baseline BMI, leisure-time physical activity, smoking status, snacking (no, yes), television watching time and total energy intake. b Adjusted for age, alcohol intake, physical activity, smoking, postmenopausal hormone use (no, current or past, missing), oral contraceptive use, baseline BMI, glycemic load, and intakes of total fiber, trans fat, fruit, vegetables, red meat, processed meat, refined grain, whole grain, snacks, sugar-sweetened beverages, diet beverages, low-fat dairy products, and high-fat dairy products. c p < 0.05.
provided by nuts (55e75%) can be compensated by lower energy intake in future meals [27]. The satiation/satiety properties of nuts are attributed to their macronutrient profile (rich in fiber and protein) and also to their physical characteristics and the need of increased mastication [26]. The macronutrient profile of nuts is also associated with increased release of glucagon-like protein 1 (GLP-1) and cholecystokinin (CCK), gastrointestinal hormones with satiety effects [28]. Preliminary data also suggest that usual consumption of tree nuts or peanuts might be associated with a slight increase in resting energy expenditure [26,29] or thermogenesis [30]. The high fiber content of nuts [31] is also related to delayed gastric emptying and reduced Table 2
absorption. An incomplete mastication of nuts is common and leads to increased fecal losses of energy-providing macronutrients [11]. On the other hand, mono- and polyunsaturated fatty acids present in nuts are more readily oxidized than saturated or trans fatty acids, leading to reduced fat accumulation [12]. The reviewed studies and the new results presented here might have some methodological limitations. The most important limitation is related to the well-known measurement error inherent in nutritional epidemiology and the potential misclassification bias derived from using food frequency questionnaires to appraise the consumption of nuts or estimate for total energy intake. However, the
Mean yearly weight change according to nut consumption in the SUN cohort (6-yr follow-up).
Nut consumption (servings)
n Weight change (kg) Age-, sexadjusted Multivariateadjusteda a
Never/almost never
1e3/month
1/week
2e4/week
>4/week
2512 0.30 (0.26e0.35)
5420 0.29 (0.26e0.32)
2369 0.32 (0.28e0.37)
1083 0.25 (0.18e0.31)
511 0.20 (0.12e0.29)
0.03
0.29 (0.24e0.33)
0.28 (0.25e0.31)
0.32 (0.28e0.37)
0.27 (0.20e0.34)
0.25 (0.15e0.35)
0.34
0.32 (0.22e0.42)
0.31 (0.21e0.40)
0.34 (0.24e0.44)
0.28 (0.18e0.39)
0.24 (0.11e0.37)
0.09
Statistical significance (p value for linear trend)
All weight changes after 6-yr follow-up were positive. They were adjusted for age, baseline BMI, leisure-time physical activity, weight gain during the 5 years previous to entering the cohort, prevalence of hypertension, hyperlipidemia and diabetes.
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M.A. Martı´nez-Gonza ´lez, M. Bes-Rastrollo
Table 3 Risk of gaining 3 kg/yr according to nut consumption in the SUN cohort (6-yr follow-up). Odds ratios (95% Confidence intervals). Nut consumption
n Crude OR Age-, sex-adjusted Multivariate-adjusteda
Never/almost never
1e3/month
1/week
2/week
Linear trend
2512 1 (ref.) 1 (ref.) 1 (ref.)
5420 0.94 (0.67e1.32) 0.96 (0.68e1.35) 1.02 (0.72e1.44)
2369 1.00 (0.67e1.49) 1.03 (0.69e1.53) 1.16 (0.77e1.74)
1594 0.46 (0.26e0.82) 0.51 (0.28e0.91) 0.61 (0.34e1.10)
0.009 0.021 0.093
ref. Z reference group. a Adjusted for age, baseline BMI, leisure-time physical activity, weight gain during the 5 years previous to entering the cohort, prevalence of hypertension, hyperlipidemia and diabetes.
questionnaires used in both cohorts have been repeatedly assessed and validated [18e20]. More importantly, the consistency of findings between observational cohorts using a self-reported food assessment tool and randomized intervention studies, such as the PREDIMED trial, is reassuring and speaks against a misclassification bias. Another potential criticism might be related to selection bias, specially in the context of highly educated-cohorts (such as the Nurses Health Study or the SUN Project). These cohorts are in no way representative of the general population. It is plausible that these highly-educated participants might be more motivated to adhere to healthier diets. This feature may have affected the generalizability of some of the reported findings, but it could also have actually reinforced the validity of the reported results because the high level of education and homogeneity of the cohorts is likely to reduce the potential confounding related to socioeconomic status. In addition, these motivated and highly-educated participants usually provide high-quality information in their selfreported questionnaires. In conclusion, the available evidence strongly support that adding nuts to the usual diet does not adversely affect body weight.
Role of the funding source The sources of funding for the SUN study are the Official Spanish Agencies for funding biomedical research. The SUN study receives no funding from any food industry. The agencies funding our study had no role in the study design, collection, analysis or interpretation of data; in the writing of the manuscript; or in the decision to submit the manuscript for publication.
Conflict of interest We have no conflict of interest. The authors do not have any financial or personal relationships with other people or organisations that could inappropriately influence (bias) their work.
Acknowledgements RTIC 06/0045 is an initiative of the Instituto de Salud Carlos III, Spanish Government. We thank to all participants in the
PREDIMED trial and the SUN study and other investigators of the PREDIMED group (Estruch R, Ros E, Salas-Salvado ´ J, Corella D, Covas MI, Fiol M, Aros F, Go ´mez-Gracia E, RuizGutierrez V, Warnberg J, Lamuela-Raventos RM, Saez G, Lapetra J, Serra-Majem L, Pinto X, Tur JA, Mitjavila MT, and Portillo MP) and the SUN Project (Alonso A, Benito S, BasterraGortari FJ, Beunza JJ, de Irala J, de la Fuente-Arrillaga C, Delgado-Rodriguez M, Guillen-Grima F, Krafka J, Llorca J, Lo ´pez del Burgo C, Marti A, Martı´nez JA, Martı´nez-Gonza ´lez MA, Nun ˜ez-Cordoba JM, Pimenta AM, Sa ´nchez D, Sa ´nchezVillegas A, Segui-Go ´mez M, Serrano-Martı´nez M, Toledo E, Va ´zquez Z). We thank all the sources of support, including the Department of Health of the Navarra Government (Spain) (grants PI45/2005, PI36/2008), and the Instituto de Salud Carlos III (FIS, PI042241, PI040233, PI050976, PI070240, and PI0801943).
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journal homepage: www.elsevier.com/locate/nmcd
Nut consumption, weight gain and obesity: Epidemiological evidence ´lez *, M. Bes-Rastrollo M.A. Martı´nez-Gonza Department of Preventive Medicine and Public Health, University of Navarra, Spain Received 12 August 2010; received in revised form 8 November 2010; accepted 18 November 2010
KEYWORDS Walnut; Hazelnut; Overweight; Fiber; Mediterranean diet; Monounsaturated fat; Poly-unsaturated fat; Satiety
Abstract Background and aims: Short-term trials support that adding tree nuts or peanuts to usual diets does not induce weight gain. We reviewed the available epidemiological evidence on long-term nut consumption and body weight changes. We also report new results from the SUN (“Seguimiento Universidad de Navarra”) cohort. Methods and results: Published epidemiologic studies with 1-yr follow-up were located. Two published reports from large cohorts (SUN and Nurses Health Study-2) showed inverse associations between frequency of nut consumption and long-term weight changes. A beneficial effect of a Mediterranean diet supplemented with tree nuts on waist circumference was reported after 1-yr follow-up in the first 1224 high-risk participants in the PREDIMED (“PREvencion DIeta MEDiterranea”) trial. After assessing 11,895 participants of the SUN cohort, a borderline significant (p value for trend Z 0.09) inverse association between baseline nut consumption and average yearly weight gain (multivariate-adjusted means Z 0.32 kg/yr (95% confidence interval: 0.22e0.42) and 0.24 (0.11e0.37) kg/yr for participants with no consumption and >4 servings/week, respectively) was found after a 6-yr follow-up. Conclusions: Consumption of nuts was not associated with a higher risk of weight gain in longterm epidemiologic studies and clinical trials. ª 2010 Elsevier B.V. All rights reserved.
Introduction Overweight, obesity and age-related weight gain are major health problems in developed countries and are strongly related to dietary habits [1]. Rapidly increasing rates of overweight and obesity in most countries highlight that the
primary determinant of obesity development comes from behavioral and dietary changes rather than from genetic factors [2,3]. Increasing trends of overweight/obesity with potentially devastating long-term consequences underline the importance of understanding the role of key food items in the prevention of age-related weight gain. Tree nuts or
* Corresponding author. Universidad de Navarra, Ed. Investigacio ´n. C/Irunlarrea 1, 31008 Pamplona, Navarra, Spain. Tel.: þ34 948 425600x6463; fax: þ34 948 455649. E-mail address: [email protected] (M.A. Martı´nez-Gonza ´lez). 0939-4753/$ - see front matter ª 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.numecd.2010.11.005
Nuts and weight gain peanuts (which actually are legumes) can be a good candidate to prevent obesity and obesity-related metabolic and cardiovascular diseases. Several epidemiological studies have reported that frequent nut consumption is inversely associated with fatal and nonfatal coronary heart disease [4e7]. A recently published pooled analysis of 25 feeding studies with different nuts supported also a consistent cholesterol-lowering effect of nut consumption [8]. Epidemiological studies suggest that nut consumption protects against the development of diabetes in women [9] and against hypertension in men [10]. In a cross-sectional assessment of 847 participants in one of the centers of the PREDIMED study, nut consumption was inversely associated with adiposity measures (BMI and waist circumference) independently of other factors. The adjusted models predicted that BMI and waist circumference decreased by 0.78 kg/m2 and 2.1 cm, respectively, for each daily serving of 30 g of nuts [11]. Despite these findings, since nuts are energy-dense foods with a high-fat content, there is still a fear that their consumption may lead to unwanted increases in body weight and to a higher long-term risk of developing overweight or obesity. However, available metabolic studies and short-term controlled feeding trials support that adding nuts to usual diets does not induce weight gain, despite an expected increase in total caloric intake. Some small trials have also suggested that isocaloric replacement of other food items by nuts may reduce body weight and fat mass [12]. However, these studies only assessed the short-term effects of nuts in small groups of volunteers and did not assess the association of nut consumption with long-term (1 yr) weight changes or with the risk of developing overweight/obesity in the subsequent years. Therefore, the aim of our study was to prospectively evaluate the long-term association between nut consumption and weight gain or incidence of overweight/obesity in epidemiologic studies. We did a literature search and also analysed new data of a Mediterranean cohort, the SUN (Seguimiento Universidad de Navarra) project.
Methods Literature search We initially conducted a Medline search using the following search strategy: (nut OR nuts OR walnuts OR almonds OR hazelnuts OR *nuts) & (weight OR overweight OR obesity OR adiposity OR waist) & (follow-up OR cohort). This search retrieved 49 articles. Our selection criteria were a sample size larger than 500 participants and that, after a minimum follow-up period of 1 year, there was an assessment of the relationship between the consumption of nuts and at least one of the following outcomes (a) weight change, (b) change in waist circumference, (c) incidence of overweight, or (d) incidence of obesity. Only 2 of the initially selected studies met one of these criteria [13,14]. Additional contact with experts provided another study [15].
The SUN cohort The SUN project is a prospective cohort study with a dynamic design (enrollment is continually open). It was designed in
S41 collaboration with the Harvard School of Public Health, following a similar methodology to that of large American cohorts such as the Nurses’ Health Study or the Health Professionals Follow-up Study. Details on the objectives, design and methods of this cohort have been published elsewhere [16,17]. Briefly, beginning on December 1999, all Spanish alumni of the University of Navarra and several other professional collectives with a university degree received a letter of invitation to participate in the study, a questionnaire to respond and a postage-prepaid envelope to return the questionnaire. This baseline questionnaire gathered information about sociodemographic variables, lifestyle factors, as well as information on health and diet through a validated 136item semiquantitative food frequency questionnaire (FFQ) [18e20]. All participants who completed a baseline assessment (Q_0) up to October 2006 (n Z 16,593) were assessed. Among them we excluded 1653 who reported total energy intake out of predefined values (<800 kcal/d for men, <500 kcal/d for women or >4000 kcal/d for men, >3500 kcal/d for women), 753 who reported chronic disease at baseline (cancer or cardiovascular disease), 54 deceased participants, 1727 subjects with no follow-up data (retention rate Z 88%), and 556 participants with missing data in some variable of interest, leaving a total of 11,895 participants available for the analyses. The study was approved by the Institutional Review Board at the University of Navarra. Informed consent was implied by the voluntary completion of the baseline questionnaire. The FFQ was collected only at baseline and was based on typical portion sizes and had nine options for the average frequency of intake in the previous year of each food item (ranging from never/almost never to at least six times per day). Questions on nut consumption included walnuts, almonds, hazelnuts, and peanuts. These four types represent >95% of total nut consumption in the Spanish general population [13]. Information on body weight of each participant was recorded at baseline and at follow-up questionnaires, which were completed every two years. The reliability and validity of self-reported weight was assessed in a subsample of the cohort. The mean relative error in self-reported weight was 1.45%, and the correlation coefficient between measured and self-reported weight was 0.99 (95% CI: 0.98e0.99) [21]. The outcomes were (1) the change in body weight during follow-up, defined as average change in body weight per year of follow-up [the last weight reported minus the baseline weight divided by the years of follow-up]. (2) Weight gain 3 kg/yr during follow-up. Physical activity during leisure time was assessed with a previously validated questionnaire [22]. The Spearman correlation coefficient between energy expenditure assessed with this questionnaire and with a triaxial accelerometer was 0.51, 95% confidence interval (CI) 0.23, 0.71. An activity metabolic equivalent (MET) index was computed by assigning a multiple of resting metabolic rate (MET score) to each activity (17 activities). Time spend in each of the activities was multiplied by the MET score specific to each activity, and then summed over all activities obtaining a value of overall weekly MET-hours [23]. Generalized linear models were used to assess the association between total nut consumption, based on the frequency of servings (50 g) categorized as never/almost
S42 never, 1e3/month, 1/week, 2e4/week and 4/week, and average yearly weight change during follow-up. Logistic regression models were fitted to assess the association between 3 categories of baseline consumption of a serving of nuts (1e3/month, 1/week, 2/week) and the risk of gaining on average 3 kg/yr. Odds ratios were calculated using the lowest category (never/almost never) as the reference. All models were adjusted for age, sex, baseline body mass index, previous weight gain (during the 5 years before recruitment), physical activity at baseline and baseline prevalence of hypertension, dyslipidemia or diabetes. We evaluated the interaction between the exposure and sex and between age and sex through interaction terms included in the multivariate model. The PREDIMED (PREvencion Dieta MEDiterranea) study is a large, parallel-group, multicenter, randomized trial aimed to assess the effects of the MeDiet on the primary prevention of cardiovascular disease. The objectives, design, methods and other aspects of this trial have been published elsewhere [24,25]. Participants are men aged 55e80 years and women aged 60e80 years without any previous cardiovascular event, but with high cardiovascular risk (either type 2 diabetes or at least three of the following major risk factors, including smoking, hypertension, hyperlipidemia, low HDL-cholesterol, overweight or obesity or family history of cardiovascular disease). Participants were assigned to receive one of three different dietary interventions: control (low-fat) diet, MeDiet supplemented with extra virgin olive oil (MeDiet þ VOO) or MeDiet supplemented with tree nuts (MeDiet þ nuts). Participants allocated to the control group were advised to reduce all types of fat and were given written recommendations according to the American Heart Association guidelines. The groups assigned to MeDiet were advised to use extra virgin olive oil for cooking and dressing, to increase vegetable, nuts and fish consumption, to consume white meat instead of red or processed meat and for alcohol drinkers to follow a pattern of moderate red wine consumption. Each participant received a personal interview with a trained dietitian and a group session conducted by the same dietitian every 3 months during these four years. The two MeDiet groups received either free olive oil (1 L/week) or mixed nuts (30 g/day, as 15 g of walnuts and 15 g of almonds). No energy restrictions were prescribed for any intervention group. The dietary intervention procedures have been shown to be able to obtain significantly different between-group changes in nutrient intake and in the overall dietary pattern [25].
Results Review of published studies Table 1 shows the results of previously published epidemiological studies. The SUN cohort found inverse associations between baseline consumption of nuts and average weight gain or the risk of gaining 5 kg during 28-month follow-up [13]. No association was found between nut consumption and the risk of developing overweight or obesity during the same period for participants who initially had a body mass index <25 kg/m2.
M.A. Martı´nez-Gonza ´lez, M. Bes-Rastrollo Inverse associations between nut consumption and baseline and average weight gain during the subsequent 8 years were also reported by the Nurses Health Study-2 [14]. Moreover, among women who were not obese at baseline, the risk of developing obesity during the 8-yr period of follow-up was lower (hazard ratio Z 0.62, 95% CI: 0.32e0.99) for women consuming at baseline 2 or more servings of nuts per week than among those with rare or null consumption [14]. The report of the PREDIMED randomized trial about Mediterranean diet (MeDiet) and the metabolic syndrome [15] found that a MeDiet enriched with nuts was inversely associated with the incidence of the metabolic syndrome after 1-yr of intervention. The group allocated to MeDiet þ nuts also exhibited a significant reduction after 1-yr in the prevalence of abdominal obesity in comparison with the control group.
The SUN cohort: 6-yr follow-up Table 2 shows that an inverse association between baseline consumption of nuts and average yearly weight change was apparent in the univariate analysis during a 6-yr period of follow-up of this Mediterranean cohort. However, further adjustment for some potential confounders attenuated this association and the statistical significance for the linear trend test (p Z 0.09) did not reach the conventional five percent cut-off point. A similar pattern was observed for the risk of gaining 3 or more kg/yr, with a significant inverse association that was attenuated after multivariate adjustment. In any case none of these results suggested any association between nut consumption and a higher risk of weight gain. On the contrary all the point estimates in the SUN cohort suggested that the lower weight gains were always observed among participants consuming 2 servings of nuts/week. Table 3.
Discussion The available epidemiological evidence together with the new results hereby reported does not suggest that nut consumption in the usual amounts (up to 4 servings/week) leads to any appreciable weight gain in the long-term. Even when total energy intake was slightly increased because of the addition of nuts to the usual dietary pattern, no significant weight gain was observed. Ideally, nuts should be used within an isocaloric diet to replace other food items with high energy density or unhealthy snacks. Our results are consistent with the previously observed null or beneficial effect of nuts in smaller, short-term feeding trials showing a protection against adiposity [12,26]. Beyond cross-sectional studies which have found that nut consumers usually have a lower body mass index than non-consumers, available data from prospective studies provide an adequate temporal sequence and a sufficiently long follow-up. They consistently support the notion that the addition of nuts to the usual diet leads to less than predicted increases in body weight or adiposity. Several biological mechanisms may explain this lack of weight gain observed in association with nut consumption. Nuts are known to induce satiation (reduction in the total amount of food eaten in a single meal) and satiety (reduction in the frequency of meals). A sizable amount of the energy
Nuts and weight gain Table 1 obesity.
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Published epidemiological studies on nut consumption and weight gain, risk of overweight, obesity or abdominal
Study
n
Follow-up
Outcome
Exposure (comparison)
Results
SUN cohort [12]
8865
28 months
average weight gain
SUN cohort [12]
8865
28 months
Odds Ratio (OR) for gaining 5 kg
Weight gain difference between both groups Z 410g (95% CI: 740 to 80)a OR Z 0.71 (95% CI: 0.54e0.93)a OR Z 1 (ref.)
SUN cohort [12]
6630
28 months
NHS2 cohort [13]
51,188
8 years
Odds Ratio (OR) for overweight or obesity average weight gain
2/servings/wk vs. never or almost never (ref.) 2/servings/wk vs. never or almost never 2/servings/wk vs. never or almost never
NHS2 cohort [13]
408,664 personyears 1224 1-year
PREDIMED trial [14]
Hazard Ratio (HR) for obesity Prevalence (%) of abdominal obesity (1-year changes)
OR Z 0.73 (95% CI: 0.48e1.11)a OR Z 1 (ref.)
2/servings/wk vs. rare consumption 2/servings/wk vs. rare consumption
4.43 kg vs. 5.53 kg (p < 0.001)b
MeDiet þ nuts: vs. control: (low-fat diet)
64.5% (baseline) to 59.6% (1-year) vs. 65.3% (baseline) to 68.0% (1-year)c
HR Z 0.62 (0.32e0.99)b HR Z 1 (ref.)
MeDiet Z Mediterranean-type diet; SUN: “Seguimiento Universidad de Navarra” (Follow-up Navarra University); PREDIMED: “Prevencio ´n con Dieta Mediterra ´nea” (Prevention with Mediterranean Diet). OR Z Odds Ratio; HR Z Hazard Ratio; CI Z Confidence Interval; NHS2 Z Nurses’ Health Study-2; ref. Z reference group. a Adjusted for age, baseline BMI, leisure-time physical activity, smoking status, snacking (no, yes), television watching time and total energy intake. b Adjusted for age, alcohol intake, physical activity, smoking, postmenopausal hormone use (no, current or past, missing), oral contraceptive use, baseline BMI, glycemic load, and intakes of total fiber, trans fat, fruit, vegetables, red meat, processed meat, refined grain, whole grain, snacks, sugar-sweetened beverages, diet beverages, low-fat dairy products, and high-fat dairy products. c p < 0.05.
provided by nuts (55e75%) can be compensated by lower energy intake in future meals [27]. The satiation/satiety properties of nuts are attributed to their macronutrient profile (rich in fiber and protein) and also to their physical characteristics and the need of increased mastication [26]. The macronutrient profile of nuts is also associated with increased release of glucagon-like protein 1 (GLP-1) and cholecystokinin (CCK), gastrointestinal hormones with satiety effects [28]. Preliminary data also suggest that usual consumption of tree nuts or peanuts might be associated with a slight increase in resting energy expenditure [26,29] or thermogenesis [30]. The high fiber content of nuts [31] is also related to delayed gastric emptying and reduced Table 2
absorption. An incomplete mastication of nuts is common and leads to increased fecal losses of energy-providing macronutrients [11]. On the other hand, mono- and polyunsaturated fatty acids present in nuts are more readily oxidized than saturated or trans fatty acids, leading to reduced fat accumulation [12]. The reviewed studies and the new results presented here might have some methodological limitations. The most important limitation is related to the well-known measurement error inherent in nutritional epidemiology and the potential misclassification bias derived from using food frequency questionnaires to appraise the consumption of nuts or estimate for total energy intake. However, the
Mean yearly weight change according to nut consumption in the SUN cohort (6-yr follow-up).
Nut consumption (servings)
n Weight change (kg) Age-, sexadjusted Multivariateadjusteda a
Never/almost never
1e3/month
1/week
2e4/week
>4/week
2512 0.30 (0.26e0.35)
5420 0.29 (0.26e0.32)
2369 0.32 (0.28e0.37)
1083 0.25 (0.18e0.31)
511 0.20 (0.12e0.29)
0.03
0.29 (0.24e0.33)
0.28 (0.25e0.31)
0.32 (0.28e0.37)
0.27 (0.20e0.34)
0.25 (0.15e0.35)
0.34
0.32 (0.22e0.42)
0.31 (0.21e0.40)
0.34 (0.24e0.44)
0.28 (0.18e0.39)
0.24 (0.11e0.37)
0.09
Statistical significance (p value for linear trend)
All weight changes after 6-yr follow-up were positive. They were adjusted for age, baseline BMI, leisure-time physical activity, weight gain during the 5 years previous to entering the cohort, prevalence of hypertension, hyperlipidemia and diabetes.
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M.A. Martı´nez-Gonza ´lez, M. Bes-Rastrollo
Table 3 Risk of gaining 3 kg/yr according to nut consumption in the SUN cohort (6-yr follow-up). Odds ratios (95% Confidence intervals). Nut consumption
n Crude OR Age-, sex-adjusted Multivariate-adjusteda
Never/almost never
1e3/month
1/week
2/week
Linear trend
2512 1 (ref.) 1 (ref.) 1 (ref.)
5420 0.94 (0.67e1.32) 0.96 (0.68e1.35) 1.02 (0.72e1.44)
2369 1.00 (0.67e1.49) 1.03 (0.69e1.53) 1.16 (0.77e1.74)
1594 0.46 (0.26e0.82) 0.51 (0.28e0.91) 0.61 (0.34e1.10)
0.009 0.021 0.093
ref. Z reference group. a Adjusted for age, baseline BMI, leisure-time physical activity, weight gain during the 5 years previous to entering the cohort, prevalence of hypertension, hyperlipidemia and diabetes.
questionnaires used in both cohorts have been repeatedly assessed and validated [18e20]. More importantly, the consistency of findings between observational cohorts using a self-reported food assessment tool and randomized intervention studies, such as the PREDIMED trial, is reassuring and speaks against a misclassification bias. Another potential criticism might be related to selection bias, specially in the context of highly educated-cohorts (such as the Nurses Health Study or the SUN Project). These cohorts are in no way representative of the general population. It is plausible that these highly-educated participants might be more motivated to adhere to healthier diets. This feature may have affected the generalizability of some of the reported findings, but it could also have actually reinforced the validity of the reported results because the high level of education and homogeneity of the cohorts is likely to reduce the potential confounding related to socioeconomic status. In addition, these motivated and highly-educated participants usually provide high-quality information in their selfreported questionnaires. In conclusion, the available evidence strongly support that adding nuts to the usual diet does not adversely affect body weight.
Role of the funding source The sources of funding for the SUN study are the Official Spanish Agencies for funding biomedical research. The SUN study receives no funding from any food industry. The agencies funding our study had no role in the study design, collection, analysis or interpretation of data; in the writing of the manuscript; or in the decision to submit the manuscript for publication.
Conflict of interest We have no conflict of interest. The authors do not have any financial or personal relationships with other people or organisations that could inappropriately influence (bias) their work.
Acknowledgements RTIC 06/0045 is an initiative of the Instituto de Salud Carlos III, Spanish Government. We thank to all participants in the
PREDIMED trial and the SUN study and other investigators of the PREDIMED group (Estruch R, Ros E, Salas-Salvado ´ J, Corella D, Covas MI, Fiol M, Aros F, Go ´mez-Gracia E, RuizGutierrez V, Warnberg J, Lamuela-Raventos RM, Saez G, Lapetra J, Serra-Majem L, Pinto X, Tur JA, Mitjavila MT, and Portillo MP) and the SUN Project (Alonso A, Benito S, BasterraGortari FJ, Beunza JJ, de Irala J, de la Fuente-Arrillaga C, Delgado-Rodriguez M, Guillen-Grima F, Krafka J, Llorca J, Lo ´pez del Burgo C, Marti A, Martı´nez JA, Martı´nez-Gonza ´lez MA, Nun ˜ez-Cordoba JM, Pimenta AM, Sa ´nchez D, Sa ´nchezVillegas A, Segui-Go ´mez M, Serrano-Martı´nez M, Toledo E, Va ´zquez Z). We thank all the sources of support, including the Department of Health of the Navarra Government (Spain) (grants PI45/2005, PI36/2008), and the Instituto de Salud Carlos III (FIS, PI042241, PI040233, PI050976, PI070240, and PI0801943).
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