Proximate nutrient comparison of 200 calories servings of nuts, grains and dry beans.
Abstract
In the last several years research has been accumulating that demonstrates that nuts and seeds are beneficial for all people. While some plant-based diet programs have embraced the inclusion of nuts and seeds, other programs have eschewed nuts and seeds, remaining firmly committed to a starch-based dietary pattern. This chapter assembles the scientific evidence regarding the benefits of nuts and seeds into three issues: (1) The nutrient density of nuts and seeds compared to grains and legumes of the same caloric content, (2) The improvement of health outcomes and extra benefits when nuts and seeds are included in plant-based diets, (3) The safety of nuts and seeds when a person is dealing with cancer. As a result of examining these issues with the known scientific evidence it will become apparent that one to two ounces of nuts and seeds daily is a very beneficial part of a plant-based diet.
Keywords
- nuts
- seeds
- cardiovascular disease
- cancer
- plant based diet
1. Introduction
The scientific evidence for the benefits of a plant-based diet is enumerated in the various chapters of this book. Much of the evidence comes from programs and clinical trials that avoided any added fats or fatty foods, even from plant sources. So a title containing “nuts” and “benefits” in the same sentence may seem like an oxymoron, a contradiction in terms at the least. The inclusion of fatty foods like nuts and seeds has been and continues to be a controversial topic within the plant-based research community. While newer publications from the last several years relate to benefits of nuts and seeds, the older plant-based diet literature largely found positive results without the inclusion of nuts or seeds. Dr. Dean Ornish and Dr. Caldwell Esselstyn established the benefits of a low-fat plant-based diet for reversing heart disease. Dr. Ornish was one of the first doctors to prove that a plant-based diet could reverse heart disease, using the best testing methods available to provide the evidence to sway beliefs [1]. Dr. Esselstyn also reversed heart disease using this very low-fat diet, having about a 99% success rate [2]. Both Dr. Ornish and Dr. Esselstyn were able to get their great clinical success purposefully avoiding nuts and seeds and any added fats in the diet. Their success has been continued by others as well [3].
On the other hand, the position paper of the American Dietetic Association states “A well-planned vegetarian diet containing vegetables, fruits, whole grains, legumes, nuts, and seeds can provide adequate nutrition.” [4]. The use of enhanced intake of beans, greens, seeds, nuts, whole grains, and other colorful plant products is recommended for athletes by Fuhrman and Ferreri [5]. In examining protein intakes on plant-based diets Mariotti and Gardner warn, “An insufficient protein intake from vegetarian diets may occur if the diet does not include protein-rich foods such as legumes (the most traditional source) and nuts and seeds, or any protein analogs of animal foods” [6].
In view of the lingering scientific controversy of the inclusion of nuts and seeds into a healthy plant-based diet this chapter is written so that the information is clearly available in one place for people to understand how nuts and seeds can be beneficial. There are 3 main issues to be addressed in this article. They are:
The nutrient density of nuts and seeds compared to grains and legumes.
The improvement of health outcomes and extra benefits when nuts and seeds are included in vegetarian or vegan diets.
The safety of nuts and seeds when a person is dealing with cancer.
As a result of examining these issues, it will become apparent that 1 to 2 ounces of nuts and seeds on a daily basis is a very beneficial part of a healthy plant-based diet.
2. Nutrient density of nuts versus grains and legumes
The first issue is to examine the nutrient density of nuts and seeds compared to grains and legumes. To examine this issue, four common nuts and five common seeds were compared with five grains and six types of beans and lentils. A 200-calorie serving of each food was compared for nutrients, as this is just slightly more than a 1 ounce serving of nuts or seeds. Nutrient amounts were taken from USDA standard reference nutrient tables incorporated into the software program NutriBase (Version 11.71, Phoenix, AZ).
As shown in Table 1, equal caloric amounts of nuts, cooked grains and cooked beans vary in serving sizes, measured in grams. About 1 ounce of seeds or nuts yields 200 calories, while it takes about one cup of cooked grains or about ¾ cup of cooked beans to get the same amount of calories. The main difference is the amount of water that is not in nuts and seeds and the fact that fats pack more calories into a smaller space than carbohydrates and proteins.
Ingredient | Grams | Protein (g) | %Cal, Protein | Carbs (g) | Fiber (g) | Net Carb (g) | %Cal, Carb | Fat (g) | %Cal, Fat |
---|---|---|---|---|---|---|---|---|---|
Almond, Raw | 35.0 | 7.3 | 14.8 | 7.5 | 4.3 | 3.1 | 6.4 | 17.3 | 78.8 |
Walnut, Raw | 30.6 | 4.7 | 9.0 | 4.2 | 2.1 | 2.2 | 4.2 | 20.0 | 86.8 |
Pecan, Raw | 29.0 | 2.7 | 5.2 | 4.0 | 2.8 | 1.2 | 2.4 | 20.9 | 92.3 |
Pistachio, Rstd | 35.3 | 7.4 | 14.8 | 10.4 | 3.5 | 6.9 | 13.8 | 15.8 | 71.4 |
Sunflower Seed | 34.3 | 7.1 | 14.0 | 6.9 | 3.0 | 3.9 | 7.7 | 17.7 | 78.3 |
Sesame Seed | 34.9 | 6.2 | 12.6 | 8.2 | 4.1 | 4.1 | 8.3 | 17.3 | 79.2 |
Flax Seed | 37.5 | 6.9 | 15.9 | 10.8 | 10.2 | 0.6 | 1.4 | 15.8 | 82.7 |
Chia Seed | 41.2 | 6.8 | 17.7 | 17.4 | 14.2 | 3.2 | 8.3 | 12.7 | 74.0 |
Pumpkin Seed | 35.8 | 10.8 | 20.8 | 3.8 | 2.2 | 1.7 | 3.2 | 17.6 | 76.0 |
Quinoa, ckd | 166.7 | 7.3 | 16.2 | 35.5 | 4.7 | 30.8 | 68.0 | 3.2 | 15.9 |
Wild Rice, ckd | 198 | 7.9 | 16.4 | 42.3 | 3.6 | 38.7 | 80.4 | 0.7 | 3.2 |
Brown Rice, ckd | 180.2 | 4.7 | 10.0 | 41.4 | 3.2 | 38.1 | 82.1 | 1.6 | 7.9 |
WW Bread | 72.0 | 6.0 | 12.7 | 37.0 | 4.3 | 32.7 | 68.8 | 3.9 | 18.4 |
Oatmeal, wtr | 281.7 | 7.2 | 15.6 | 33.8 | 4.8 | 29.0 | 63.3 | 4.3 | 21.0 |
Pinto Bean, bld | 139.9 | 12.6 | 32.5 | 36.7 | 12.6 | 24.1 | 62.2 | 0.9 | 5.3 |
Black Bean, bld | 151.5 | 13.4 | 35.3 | 35.9 | 13.2 | 22.7 | 59.8 | 0.8 | 4.8 |
Chickpea, cnd | 227.3 | 11.2 | 26.7 | 30.7 | 10.0 | 20.7 | 49.4 | 4.4 | 23.9 |
GN Bean, bld | 169.5 | 14.1 | 35.6 | 35.8 | 11.9 | 23.9 | 60.1 | 0.8 | 4.3 |
Navy Bean, bld | 142.9 | 11.8 | 32.7 | 37.2 | 15.0 | 22.2 | 61.8 | 0.9 | 5.5 |
Pink Bean, bld | 134.2 | 12.2 | 27.6 | 37.5 | 7.1 | 30.3 | 69.0 | 0.7 | 3.4 |
Lentil, bld | 172.4 | 15.6 | 40.8 | 34.7 | 13.6 | 21.1 | 55.3 | 0.7 | 3.9 |
2.1 Macronutrient content in nuts versus grains and legumes
Nuts and seeds and grains have about 6.5 grams of protein per 200-calorie serving, while cooked dry beans have about double this amount, at 13 grams of protein per 200-calorie serving. So for protein, beans are a better source of protein than nuts and seeds. Beans average 35% of the calories as protein, ranging from 26 percent (pink beans and chickpeas) to 40 percent (lentils). Nuts and seeds are about 14% protein, ranging from about 5 percent (pecans) to 20 percent (pumpkin seed kernels). Grains are similar to nuts in protein content ranging from 10 percent (brown rice) to 16 percent (quinoa).
Carbohydrate content is again a big difference between nuts and seeds and grains/beans. The carbohydrate content of nuts and seeds is very low, especially considering their fiber content. Nuts and seeds averaged about 3 grams of net carbohydrate per 200-calorie serving. Only pistachios were above 5 grams. Grains averaged about 34 grams of net carbs, while beans averaged 24 grams. About 72% of the calories in grains come from carbohydrates; 60% of calories in beans are from carbohydrates.
Fiber is another category where the beans are about double the amount in nuts and seeds and grains, with about 12 grams of fiber per serving of beans compared to about 4 grams for grains and 5 grams for nuts and seeds. Flax seeds and chia seeds are much higher in fiber than other seeds or nuts. The average fiber content without these two seeds is 3.1 grams per serving.
Nuts and seeds are rich in fat, with about 80 percent of the calories coming from fats. Pecans and walnuts are particularly high in fat, with 87 and 92 percent of their calories, respectively, coming from fat. Beans on average have about 4.5 percent of the calories as fat, except for chickpeas which are at about 24 percent. Grains are also naturally low in fat.
So, nuts and seeds are a modest source of protein, very low in carbohydrates and a rich source of fats. Grains are a modest source of protein, low in fat and have a large amount of starch in them. Dry beans and lentils are an excellent source of protein, very low in fat, and a very good source of fiber as well.
One of the benefits of nuts and seeds here is the lack of glycemic response from their consumption. A recent randomized trial compared glucose and insulin levels after consuming a 253-calorie serving of mixed nuts or unsalted pretzels after an overnight fast. In the pretzel group glucose and insulin levels 60 minutes after eating were elevated, while in the mixed nuts group neither glucose nor insulin levels were significantly different from baseline levels [7]. In addition to nuts, flax seeds and chia seeds are very rich in dietary fiber. When 15 volunteers took, in random order, a 50-gram glucose challenge by itself or along with 25 g chia seeds or 31.5 g flax seeds the blood glucose response during 2 hours was blunted significantly by 39 and 28% by chia seeds and flax seeds, respectively [8]. These seeds, especially chia seeds, were able to turn glucose into a slow-release carbohydrate with their high-viscosity fiber.
A comparison of the classes of fats in nuts and seeds is given in Figure 1 for a 200-calorie serving of four kinds of nuts and five kinds of seeds. As seen in Figure 1, there is very little saturated fat in nuts and seeds. Almonds, pecans, and pistachio nuts are high in monounsaturated fatty acids (MUFAs) with over 50 percent of their fat as MUFA. Only walnuts, flax seeds, and chia seeds have significant amounts of omega 3 polyunsaturated fatty acids (PUFAs) as alpha linolenic acid (ALA), a short-chain omega 3 fatty acid. Walnuts, sunflower, sesame, and pumpkin seeds have a large amount of the omega 6 fatty acid linoleic acid (LA). In their unprocessed, raw form both LA and ALA are very valuable fats and are essential nutrients, not found in grains and legumes in appreciable amounts. This is another benefit of nuts and seeds. So, these raw nuts and seeds are a good source of LA and ALA, which can be damaged by roasting, especially for long times over the temperature of 300°F (150°C) [9]. Though only trace amounts are transformed into the long-chain omega 3 fatty acid DHA [10], there are many health benefits from ALA and EPA generated from ALA [11]. Overall, the fatty acid profiles of nuts and seeds are very favorable to cardiovascular health as MUFAs and especially PUFAs tend to lower cholesterol and the incidence of cardiovascular disease compared to saturated fats [12]. And whatever is protective of the heart is likely to be beneficial for the brain, bones, joints, and muscles of the body.
2.2 Vitamin content
A comparison of the vitamin content of 200-calorie servings of common nuts and seeds, grains and dry beans is given in Table 2. The Recommended Daily Intake (RDI) is given for each nutrient, as it is much easier to compare percentages rather than actual amounts. The nutrient amount for a particular food is in bold case for amounts greater than 20 percent of the RDI. As you can see, these foods are not a rich source of several of these vitamins, such as vitamin A, vitamin C, and vitamin K. These vitamins are found in higher amounts in fruits and vegetables. The vitamins which contents are high in nuts and seeds are mentioned in the text below.
Ingredient | Vit-A μg RAE | B1 mg | B2 mg | B3 mg | B5 mg | B6 mg | Chol mg | Folate μg DFE | Vit C mg | Vit E mg | K1 μg |
---|---|---|---|---|---|---|---|---|---|---|---|
RDI, absolute amounts | 900 | 1.2 | 1.3 | 16 | 5 | 1.7 | 550 | 400 | 90 | 15 | 120 |
Almond, Raw | 0% | 6% | 8% | 3% | 3% | 3% | 4% | 0% | 0% | ||
Walnut, Raw | 0% | 8% | 4% | 2% | 3% | 9% | 2% | 7% | 0% | 1% | 1% |
Pecan, Raw | 0.1% | 16% | 3% | 2% | 5% | 4% | 2% | 2% | 0% | 3% | 1% |
Pistachio, Rstd | 0.5% | 6% | 3% | 4% | 5% | 5% | 1% | 6% | 4% | ||
Sunflower Seed | 0.1% | 9% | 18% | 8% | 3% | 19% | 1% | 0% | |||
Sesame Seed | 0% | 7% | 10% | 0% | 16% | 2% | 8% | 0% | 1% | 0% | |
Flax Seed | 0% | 5% | 7% | 7% | 11% | 5% | 8% | 0% | 1% | 1% | |
Chia Seed | 0% | 5% | 1% | 1% | |||||||
Pumpkin Seed | 0% | 8% | 4% | 11% | 5% | 3% | 4% | 5% | 1% | 5% | 2% |
0.1% | 8% | 9% | 5% | 12% | 3% | 7% | 0% | 17% | 1% | ||
Quinoa, ckd | 0% | 15% | 14% | 4% | 12% | 7% | 18% | 0% | 7% | 0% | |
Wild Rice, ckd | 0% | 8% | 13% | 16% | 6% | 16% | 4% | 13% | 0% | 3% | 1% |
Brown Rice, ckd | 0% | 14% | 4% | 17% | 10% | 15% | 3% | 2% | 0% | 0% | 1% |
WW Bread | 0% | 18% | 12% | 18% | 7% | 8% | 3% | 14% | 0% | 4% | 6% |
Oatmeal, wtr | 0% | 18% | 3% | 4% | 18% | 1% | 4% | 4% | 0% | 2% | 1% |
0% | 15% | 9% | 12% | 10% | 10% | 4% | 10% | 0% | 3% | 2% | |
Pinto Bean, bld | 0% | 7% | 3% | 6% | 19% | 1% | 9% | 4% | |||
Black Bean, bld | 0% | 7% | 5% | 7% | 6% | 0% | 0% | 0% | |||
Chickpea, cnd | 0.2% | 6% | 2% | 2% | 14% | 10% | 14% | 0% | 3% | 4% | |
GN Bean, bld | 0% | 8% | 7% | 9% | 12% | 2% | |||||
Navy Bean, bld | 0% | 7% | 6% | 8% | 12% | 12% | 0% | 1% | |||
Pink Bean, bld | 0% | 6% | 5% | 8% | 14% | 9% | 0% | 9% | 4% | ||
Lentil, bld | 0.1% | 10% | 11% | 18% | 10% | 3% | 1% | 2% | |||
7% | 6% | 10% | 10 | 1% | 4% | 3% |
A serving of sunflower seeds provides over 40 percent of the RDI for thiamin (vitamin B1). A 200-calorie serving of flax seeds provides over 50 percent of the RDI. Most seeds are generally an excellent source of thiamin, with pumpkin seeds being the exception. Grains on average provide 15 percent of the RDI. Beans are also an excellent source of vitamin B1, providing between 20 and 30 percent of the RDI for thiamin, similar to the average for seeds.
A serving of almonds provides over 30 percent of the RDI for riboflavin (vitamin B2). But most nuts and seeds are not this rich a source of riboflavin, averaging about 5 percent of the RDI. Grains and beans are not much better, with less than 10 percent of the RDI per serving.
Sunflowers are a notable source of niacin (vitamin B3), with 18 percent of the RDI per serving. But chia seeds are even better at 23 percent. Rice and whole wheat bread are good sources with 16–18 percent of the RDI of niacin per serving. Beans are not a rich source of niacin with only lentils providing more than 10 percent of the RDI.
Pistachio nuts and sunflower seeds are excellent sources of vitamin B6, with sesame and flax seeds also being good sources. Grains are good sources, except for oatmeal. Beans are also good sources, with chickpeas delivering over 60% of the RDI per serving.
Almonds and sunflower seeds are very rich sources of vitamin E. Most other nuts and seeds, grains and beans provide little vitamin E, but these two foods are two of the richest food sources of vitamin E. In a South Korean trial using 56 g/day of almonds or a control cookie in a 4-week cross-over pattern, volunteers doubled their intake of vitamin E, which resulted in an 8.5% increase in plasma α-tocopherol levels while simultaneously reducing total cholesterol 5.5% and non-HDL cholesterol by 6.4% [13].
From this analysis of vitamins, we can deduce a few points. First, different foods have different strengths as sources of nutrients, so it is helpful to encourage people to eat a variety of plant foods to take advantage of different nutrient profiles to even out overall intake. Second, when averaging the percent of the RDI for each vitamin, sunflower seeds are, on average, the best source of micronutrients (19%) of all of these foods listed in Table 3. Almonds are also a good source of vitamins with an average of 11% RDI. Beans average is 12% RDI, with lentils coming in highest at 16%. This vitamin analysis shows that sunflower seeds, almonds, and lentils are great foods for at least weekly consumption, if not more frequently.
Ingredient | Calc (mg) | Mag (mg) | Phos (mg) | Pot (mg) | Cop (mg) | Iron (mg) | Mng (mg) | Sel (μg) | Zn (mg) |
---|---|---|---|---|---|---|---|---|---|
RDI, absolute amounts | 1300 | 420 | 1250 | 4700 | 0.9 | 18 | 2.3 | 55 | 11 |
Almond, Raw | 7% | 13% | 5% | 7% | 3% | 10% | |||
Walnut, Raw | 2% | 12% | 8% | 3% | 5% | 3% | 9% | ||
Pecan, Raw | 2% | 8% | 6% | 3% | 4% | 2% | 12% | ||
Pistachio, Rstd | 3% | 9% | 13% | 8% | 8% | 19% | 6% | 8% | |
Sunflower Seed | 2% | 18% | 5% | 10% | 33% | 16% | |||
Sesame Seed | 18% | 3% | 28% | 22% | |||||
Flax Seed | 7% | 19% | 6% | 12% | 17% | 15% | |||
Chia Seed | 4% | 18% | 41% | 17% | |||||
Pumpkin Seed | 1% | 6% | 18% | 6% | |||||
8% | 18% | 5% | 12% | 15% | 15% | ||||
Quinoa, ckd | 2% | 6% | 14% | 8% | 17% | ||||
Wild Rice, ckd | 0% | 15% | 13% | 4% | 7% | 3% | |||
Brown Rice, ckd | 1% | 18% | 12% | 2% | 4% | 10% | |||
WW Bread | 2% | 14% | 11% | 5% | 12% | 10% | |||
Oatmeal, wtr | 2% | 18% | 17% | 4% | 14% | ||||
2% | 18% | 15% | 4% | 10% | 17% | ||||
Pinto Bean, bld | 5% | 17% | 16% | 13% | 16% | 16% | 12% | ||
Black Bean, bld | 3% | 25% | 17% | 11% | 18% | 3% | 15% | ||
Chickpea, cnd | 6% | 15% | 15% | 7% | 16% | 8% | 14% | ||
GN Bean, bld | 9% | 20% | 14% | 20% | 13% | 14% | |||
Navy Bean, bld | 8% | 18% | 16% | 12% | 19% | 8% | 13% | ||
Pink Bean, bld | 5% | 21% | 18% | 15% | 17% | 3% | 12% | ||
Lentil, bld | 3% | 15% | 14% | 32% | 9% | ||||
6% | 19% | 18% | 12% | 20% | 9% | 14% |
2.3 Mineral content
As can be seen from Table 3, nuts and seeds, whole grains and dry beans all provide a much higher amount of the essential minerals than of the vitamins. The RDI amount in milligrams or micrograms (for selenium) are given in the first row of the table.
Sesame seeds and chia seeds are both excellent sources of calcium, providing 26 and 20 percent of the RDI, respectively. Almonds and flax seeds are also decent sources, with about 95 mg of calcium per serving. Great Northern beans and navy beans are also decent sources of calcium, around 100 mg per serving, but the other beans are not so high. Calcium has long been a nutrient of concern for people following plant-based diets, so the inclusion of nuts and seeds rich in calcium will boost intakes of calcium compared to eating isocaloric amounts of grains.
Magnesium is a shortfall nutrient for the US population. About 50 percent of all American consume less than the Estimated Average Requirement (EAR) for magnesium [14]. Among the elderly it is worse, with 75% of men age 71+ and 63% of women age 71+ under the EAR for magnesium. Adolescents do not fare well, either, with 78 and 89 percent of males and females, respectively, 14–18 years of age consuming less than the EAR. Magnesium is very important for cardiovascular health, bone health, prevention of diabetes, cognitive function [15], and prevention of eclampsia during pregnancy [16].
Consuming more nuts and seeds can improve intake of magnesium. On average nuts and seeds are better sources of magnesium than grains or beans, though there is some variation. A 200-calorie serving of seeds averages 35% of the RDI for magnesium, making them a superfood for magnesium. Almonds are the only nut that is an excellent source (≥20% of RDI) of magnesium. Grains are good sources, with quinoa excelling at 25% of RDI for magnesium. Some beans are excellent sources of magnesium (black beans, Great Northern beans, pink beans) and the average for beans comes out to 18% of RDI for magnesium. Generally, grains and beans have only half of the amount of magnesium found in seeds, so substituting a serving of seeds for a serving of whole grains will improve a persons’ magnesium status.
Though high intake of potassium is a strength of plant-based diets and contributes to normal blood pressure [17], strong bones [18], and cardiovascular and overall survival [19], nuts and seeds and grains are low sources of potassium, while beans are generally good sources. Potassium is found in abundance in fruit and vegetables, so this is where most of the requirements are met. Beans win this mineral by a two-fold margin.
Copper is easily obtained in a plant-based diet. It is easy to get half of the RDI for copper with a 200-calorie serving of nuts or seeds. Sesame seeds provide 1.4 mg of copper, almost 160% of the RDI. Beans are also an excellent source of copper, but not as good as nuts and seeds.
Plant-based diets need good sources of iron. Women of reproductive age following plant-based diets especially need iron to replace iron lost in their monthly reproductive cycle to prevent anemia. While some whole grains are good sources of iron, seeds are an even better source of iron, and sesame seeds are an excellent source. Nuts and rice are not rich in iron. Beans are a good source, with lentils and Great Northern beans being excellent sources. Beans, on average, are a better source of iron than even the seeds.
Selenium is important as an antioxidant mineral, contributing to the synthesis of the intracellular antioxidant glutathione and selenoproteins. Good selenium status has been found to improve a body’s defenses against viral diseases such as HIV and COVID [20]. Brazil nuts are well known for their selenium content, a listing of over 580 μg per 200 calories (30.5 grams, about 6 nuts). Other nuts are generally low in selenium along with beans, but most seeds are an excellent source of selenium. Pinto beans and Great Northern beans are good sources of selenium.
Zinc is an essential mineral with many roles in the body. Zinc plays a role in immune defense, showing effectiveness against respiratory viruses [21]. Higher dietary intake of zinc from non-red meat sources was associated with lower risk of progression of coronary artery calcification scores [22]. Nuts and seeds are generally good sources of zinc, with sesame seeds and pumpkin seeds being excellent sources. Wild rice and oatmeal, but not whole wheat, are also excellent sources of zinc from the grain category. Dry beans are good sources, with lentils being an excellent source of zinc.
In conclusion, when averaging the RDIs for all minerals, nuts have 15%, seeds have 28%, grains 19% and beans 20% of the RDIs. So, nuts are not as mineral dense as seeds, but seeds are a really good way of increasing essential mineral intake. Overall mineral intake is important, as indicated in a study of the Iowa Women’s Health Study. Quintiles of mineral intake were used to create an overall mineral score, with positive scores for calcium, magnesium, manganese, zinc, selenium, potassium and iodine, and negative scores for iron, copper, phosphorus and sodium. Higher ranks of the mineral score were associated with lower risk of colorectal cancer in these 55- to 69-year-old women, up to 25% decreased risk comparing highest to lowest rank of mineral score [23]. So, increasing mineral intake by substituting a serving of grains out for a serving of seeds will likely reduce risk of disease.
2.4 Summary of nutrient comparison
To summarize this section nuts and seeds are the category of food that is the best way to get an extra 200 calories. When comparing just nuts and seeds versus grains one can see that nuts and seeds are more nutrient dense and deliver more nutrients per 200 calories. The average percentage of RDI for vitamins and minerals are 14.4 percent for nuts and seeds and 12.3 percent for grains (see Table 4). However, if we remove walnuts, pecans and pistachio nuts from the equation and just look at almonds and the seeds, the average RDI is now 17.6 percent. This is 43 percent more nutrition than what you get from grains, on average. So, seeds and almonds are more nutrient dense than grains.
Food Group | Average % of RDI | Nutrient Density |
---|---|---|
Grains | 12.3% | 1.0 |
All nuts and seeds | 14.4% | +17% |
Beans | 15.6% | +27% |
Almonds and seeds | 17.6% | +43% |
Seeds | 18.5% | +50% |
Lentils | 19.1% | +55% |
When comparing nuts and seeds versus beans it can be seen that almonds and seeds have a slightly higher average RDI compared to the beans (17.6 versus 15.6 percent). So, even though they are lower in protein (about 7.5 versus 13 g of protein per serving) almonds and seeds are still overall more nutritionally dense than the average dry bean. For some nutrients beans, especially lentils, are actually more nutrient dense, so it would be wise to still be include beans in the diet as well, but not in the place of a serving of nuts and/or seeds.
So, it can be concluded that nuts, particularly almonds, and seeds are nutritionally more dense than grains, about 43 percent more. Seeds are also about 19 percent more nutritionally dense than dry beans in general. Should almonds and seeds replace grains in this 200-calorie serving? From a nutrient standpoint the answer is a clear yes.
3. Health outcomes of eating nuts and seeds
As mentioned in the introduction, Drs. Esselstyn and Ornish obtained excellent results in reversing heart disease without the inclusion of nuts and seeds. However, since the publication of their results there have been many investigations in the area of nuts and seeds. There have been short-term studies on the effects of various nuts on cholesterol and blood lipids. There have been short-term studies on satiety and weight loss and/or weight gain. There have been prospective cohort studies that have reported observations of groups of people over long periods of time. And there have been some randomized controlled clinical trials using nuts and seeds as well. Now we have more evidence about the benefits of nuts and seeds.
The issue to be examined here is whether health outcomes are better or worse when nuts and seeds are included in vegetarian or vegan diets.
This issue will be examined from four lines of evidence: (1) short-term studies on weight gain and obesity, (2) short-term studies on blood lipids, (3) health outcomes in population studies, and (4) vegetarian population studies in particular.
3.1 Short-term body weight studies
Since nuts are energy-dense foods, it is important to know if they caused weight gain, or if they were associated with obesity. In a review and meta-analysis of 33 controlled clinical trials, it was found there was no difference in body weight, body mass index (BMI) or waist circumference between the nut or control diet groups [24]. Population studies have also found that nut consumption did not affect body weight. People who regularly ate nuts actually tended to not gain weight or become obese over time [25, 26]. It appears that people compensate for eating nuts by eating less of other foods. Nuts’ fat and protein content tend to make them a satisfying, filling food, whether eaten as snacks or with meals [27].
3.2 Short-term blood lipid studies
Since population studies have indicated that nuts reduced risk of cardiovascular disease, short-term studies have been conducted to attempt to deduce the mechanism for this health outcome. Many controlled clinical trials have examined different nuts and blood lipid levels, but there are few reports including inflammatory markers and endothelial function. A review and meta-analysis of 61 blood lipid studies found that for a 1-ounce (28 gram) serving of nuts per day, there was a decrease in total cholesterol (−4.7 mg/dL), low-density lipoprotein (LDL) cholesterol (−4.8 mg/dL), ApoB lipoprotein (−3.7 mg/dL) and triglycerides (−2.2 mg/dL) [28]. The results were better for 2 ounces a day than for just 1 daily ounce. This significant, but small decrease in cholesterol levels is probably not the only reason that nuts are beneficial, but these results do point in the right direction. A recent review of 26 walnut controlled interventions found similar results, with no negative effects on body weight or blood pressure [29]. Almonds have been examined separately as well, with 27 almond-control datasets yielding very similar results [30]. So, the amount of nuts rather than the type of nut contributes to the lipid-lowering effect.
Studies have also examined the effect of nuts on blood pressure. No consistent significant results have been obtained [31]. Nor have there been significant reductions in markers of inflammation. Serum C-reactive protein has been measured in multiple studies with little change due to eating nuts [32].
However, there has been a consistent improvement in endothelial cell function, measured by flow-mediated dilation (FMD). Endothelial cells allow more blood flow through the release of nitric oxide. Flow-mediated dilation is a strong predictor of future cardiovascular disease [33]. A review of 10 trials found that nut consumption significantly improved FMD, but walnuts were the only nut that had a significant effect [34].
In summary, short-term studies have found significant effects on cholesterol levels, and walnuts for endothelial function, but no significant effects for blood pressure or inflammation. Nuts also contain phytosterols and other antioxidants that may be beneficial. Whatever the mechanism, long-term studies of populations of people have clearly demonstrated an advantage of eating nuts and seeds.
3.3 Long-term studies of populations
A recent review of reviews and meta-analyses on nuts and cardiovascular disease was published. There have been so many studies and meta-analyses of studies, which synthesize the information from individual studies into a coherent conclusive statement, that they could actually do an overview of all of the reviews and meta-analyses that have been done on population studies of eating nuts. There are 234 references to reviews, meta-analyses and large individual study reports in this article by Kim et al. [35]. Here is what these authors found about nuts and cardiometabolic disease. Consumption of nuts was associated with a 19–20 percent decrease in all-cause mortality. Coronary heart disease (CHD) incidence was reduced by 20–34 percent and CHD death was reduced by 27–30 percent. Cardiovascular disease (CVD) incidence (includes strokes as well as heart disease) was reduced by 19 percent and CVD death was reduced by 25 percent. Stroke incidence was reduced by 10–11 percent and stroke death was reduced by 18 percent.
In addition to this review, Aune et al. [36] have found a 15 percent reduction in total cancer death and a 39 percent decrease in diabetes deaths, and a 75 percent decrease in infectious disease deaths. For specific cancers, Wu et al. [37] reviewed 36 observational studies with a total of over 30,000 people. They found significant associations between eating nuts and a 15 percent overall reduction in cancer. Specific cancers with reductions were colorectal cancer (24% reduction), endometrial cancer (42% reduction), and pancreatic cancer (32% reduction). A recent meta-analysis by Naghshi et al. [38], which included 43 articles on cancer risk and 9 articles on cancer mortality, found a 14% reduction in cancer risk associated with total nut intake, and a 13% reduction in overall cancer mortality from eating nuts, in close agreement with the work of Aune et al. [36]. A 5 g/d increase in nut intake was found to be associated with a 3, 6 and 25% lower risk of overall, pancreatic and colon cancer, respectively.
It is possible that the people eating nuts are just healthier overall because of other dietary choices and lifestyle habits. Even though population studies control for other dietary and lifestyle factors, there is a small question still. Direct evidence against the healthy nut eater hypothesis comes from a population study from Iran. In the 50,000-person Golestan Cohort nut eating was not associated with other healthy lifestyle habits. People who ate more nuts were also more likely to smoke, drink alcohol, be obese, less likely to exercise, but also were younger, of higher social economic status and had more education. In this cohort the nuts were still protective, leading to less coronary heart disease death and cancer death, especially among women. All-cause mortality was 29 percent less among people consuming three or more servings of nuts per week [39]. So, it appears that the benefits of nuts can be attributed to the nuts consumption and not to other lifestyle behaviors.
3.4 Long-term studies of vegetarian populations
The benefits of nuts have been seen among vegetarians and vegans who have healthy lifestyles as well. In a publication from the Adventist Health Study 2, there was a factor analysis looking at the sources of protein and risk of death [40]. For animal protein, there was a 61 percent increased risk of cardiovascular death, but for the nut protein factor there was a 40 percent decrease in risk of cardiovascular death. There were no significant associations with the factors for protein from grains, processed foods, or legumes, fruits, and vegetables. Among younger adults, aged 25–44 the meat protein factor risk was associated with 2-fold higher risk of cardiovascular death and the nut factor was associated with 3-fold lower risk. Nuts seemed to be protective and meat protein specifically seemed to increase risk of death. The protective effect of nuts was seen across different levels of plant-based dietary patterns in this population, suggesting that focusing on more specific plant protein-based diets may improve the ability of dietary recommendations to prevent CVD.
In the first Adventist Health Study this protective effect of nuts was first reported. When people who ate nuts at least 4 times per week were compared to those who ate nuts less than 1 time per week there was a 48 percent decrease in fatal CHD events and a 55 percent decrease in definite non-fatal heart attacks in the nut-eating group [41]. This protective effect was seen regardless of sex, age, smoking status, hypertensive status, vegetarian or nonvegetarian, exercise level, or whether or not people ate white bread. Nuts were protective despite all these other factors.
3.5 Summary of health benefits of nuts and seeds
The health benefits of nuts and seeds are summarized in Table 5. The evidence is robust. The benefits of nuts have been seen in at least 20 different cohorts, including populations at least from the USA, Europe, Iran, and China over a period of more than 26 years. The benefits from one or two ounces of nuts per day are substantial —20% reduction in all-cause mortality, 30% reduction in death by heart disease, 18% reduction in stroke death, 39% reduction in type 2 diabetes death and a 13–15% reduction in cancer death. Optimal results will be realized by optimizing all aspects of dietary and lifestyle choices, but the inclusion of a serving of nuts per day appears to be a wise choice.
Description of Study | Amount of Nuts | Study Length | Health Outcomes | Ref. |
---|---|---|---|---|
n = 1888, 33 clinical trials | Varied | Varied | No significant difference in body weight, BMI, waist circumference | Flores-Mateo [24] |
n = 51,188 women, Nurses’ Health Study II | ≥2 X /wk. vs. rare | 8 years | Slightly less weight gain over time, non-significant lower risk of obesity | Bes-Rastrollo [25] |
n = 373,293, EPIC-PANACEA | 12.4 g/d median vs. none | 5 years | ↓5% becoming overweight or obese | Freisling 2018 [26] |
Meta-analysis of 61 controlled clinical studies, n = 2852 | 1 serving = 28 g/d Median dose 56 g/d | 3 to 26 weeks | Nut intake (per serving/d) lowered total cholesterol −4.7 mg/dL, LDL cholesterol −4.8 mg/dL, ApoB -3.7 mg/dL, and triglycerides −2.2 mg/dL. Stronger effects were observed for ≥60 g nuts/d. | Del Gobbo [28] |
Review of 10 trials, n = 374 | 37 to 128 g/d | 8 to 24 weeks | nut consumption significantly improved flow mediated dilation | Xiao [34] |
Review of meta-analyses of prospective studies | Varied | Varied | ↓19–20% overall mortality ↓20–34% CHD incidence ↓27–30% CHD mortality ↓19% all CVD incidence ↓25% all CVD mortality ↓10–11% stroke incidence ↓18% stroke mortality | Kim [35] |
Meta-analysis of prospective studies | Results per 28 g/d | Varied | ↓15% total cancer mortality ↓39% diabetes mortality ↓52% respiratory disease mortality ↓75% infectious disease mortality | Aune [36] |
Meta-analysis, 36 studies, n = 30,708 Prospective and case–control studies | Varied | Varied | ↓15% total cancer mortality ↓24% colorectal, ↓42% endometrial, ↓32 pancreatic | Wu [37] |
Review and meta-analysis, n = 819,851 | Highest vs. lowest intake compared | Varied | ↓14% cancer risk ↓13% cancer mortality | Naghshi [38] |
Golestan Cohort Study, Iran, n = 50,045 | 3 serving/ wk. vs. none | 7 years | ↓29% all-cause mortality, nut consumption not associated with healthy lifestyle | Eslamparast [39] |
Adventist Health Study, n = 31,208 | 4x/wk. vs. <1x/wk | 6 years | ↓48% CHD mortality, ↓55% definite non-fatal CHD events | Fraser [41] |
Adventist Health Study 2, n = 81,337 | Median 9.9 years | ↓40% risk of CVD death; 3-fold lower for age 25–44 | Tharrey [40] |
4. The safety of nuts and seeds when dealing with cancer
There is one remaining issue to address here. The evidence above indicates that nuts help prevent some cancers, but what is the role of nuts and seeds after diagnosis, or during treatment or remission of cancer?
A more fundamental issue is whether dietary fats cause growth of tumors.
It is well accepted that sugar feeds cancer directly. The PET scan is done on this principle. A sugar molecule with a radiolabeled tracer on it, typically 18F-fluorodeoxyglucose, is injected into a person. Whatever part of the body is metabolizing sugar the fastest is the biggest tumor. Tumors metabolize sugar at an accelerated rate compared to the rest of the body.
Protein may also be a factor in tumor growth. Tumor cells can grow on the amino acid glutamine nearly as well as with glucose as an energy source, especially under low oxygen conditions [42, 43, 44]. The TCA cycle that produces energy can run on either glucose or glutamine especially in cancer cells.
Protein can also indirectly feed cancer through hormonal effects. High protein, especially animal protein, raises insulin levels and especially raises IGF-1 levels. IGF-1 is a growth hormone that promotes the growth of all cells. Sufficient levels of IGF-1 prevent frailty but excessive levels have been associated in several studies with higher risk of cancer incidence and death [45].
So, sugar and animal protein both contribute to tumor growth. Does dietary fat also cause tumor growth? It is well known that abdominal fat is a risk factor for cancer. Fat cells in your body produce inflammatory substances. Being overweight or obese is a risk factor for cancer. It has already been established that nuts and seeds do not contribute to obesity in populations that habitually consume them daily.
It turns out that the source of dietary fat makes a difference. It always has, even in the Seven Countries Study on fat and international rates of heart disease deaths [46]. When the analysis is separated into plant fats and animal fats the animal fats appear to be associated with disease, but not plant fats. More recent studies have also found this effect.
In recent analysis of data from two large cohorts of the USA population, the Nurses’ Health Study and the Health Professionals Follow-Up Study, the source of MUFAs was separated into plant and animal source. Guasch-Ferré et al. found the MUFAs from plants were associated with lower total mortality and the MUFAs from animals were associated with higher total mortality [47]. Just the opposite effects were seen, depending on the source of the fats. This would indicate that MUFAs from nuts are not in the same category as MUFAs from animal products.
Another recent article also highlighted the difference between MUFAs from plants or animals. The results of analyzing 16 years of follow-up of the NIH-AARP Diet and Health Study with about 520,000 people were that cardiovascular mortality was positively associated with saturated fats, trans fats, arachidonic acid (from animal foods), and animal-sourced MUFAs and was inversely associated with marine omega-3 PUFAs, linoleic acid (omega 6 oil from plants), and plant-sourced MUFAs [48].
So, plant fats are different from animal sourced fats for health outcomes. When looking at the question of whether fat accelerates tumor growth, the source of the fat has to be considered.
A direct answer to our question of the safety of nuts for cancer patients is also available. In a prospective study of colon cancer patients who were enrolled in a randomized adjuvant chemotherapy trial, those that ate two or more servings of tree nuts per week during the 6.5 years of follow-up had a 46 percent improvement in disease-free survival rate and a 53 percent improvement in overall survival [49]. This analysis controlled for other known or suspected risk factors for cancer recurrence, so it appears that the effect is from the nuts themselves. So in this group of cancer patients the ones who ate nuts lived longer without disease and lived longer overall.
Hallelujah Acres and others have advocated the use of flax seeds for cancer patients. The lignans in the fiber of the flax seeds are metabolized into enterodiol and enterolactone, which are well known for reducing cancer risk [50]. Ground flax seeds are considered by many to be a superfood, but while flax seeds are unique, they are a high fat food that has much in common with other nuts and seeds. Sesame seeds also are a precursor source of enterodiol and enterolactone [51]. Other nuts and seeds have phytochemicals in them that appear to be protective to those who eat them as well.
So, the scientific evidence says that nuts and seeds are not only safe, but beneficial in every stage of life, including while battling with cancer. Populations who eat nuts have lower rates of cancer, MUFAs from plants are protective from disease, as opposed to MUFAs from animal sources, there is no clear mechanism for dietary plant fats to accelerate the growth of tumor cells, and a recent clinical trial has shown that intake of nuts by colon cancer patients undergoing chemotherapy had better disease-free survival and overall survival.
5. Conclusion
Let us quickly review the answers to our original queries.
Nuts, particularly almonds, and seeds are nutritionally denser than grains, about 43 percent more. Seeds are also about 19 percent more nutritionally dense than dry beans in general.
The benefits from one or two ounces of nuts per day are substantial—20% reduction in all-cause mortality, 30% reduction in death by heart disease, 18% reduction in stroke death, 39% reduction in type 2 diabetes death and a 13–15% reduction in cancer death.
Nuts are safe to eat when dealing with cancer. Populations who eat nuts have lower rates of cancer and a recent clinical trial has shown that intake of nuts by colon cancer patients undergoing chemotherapy had better disease-free survival and overall survival.
The health benefits of nuts and seeds are clear. Nuts and seeds can be easily integrated into any diet. Plant-based diets are improved with nuts and seeds and omnivorous diets, or even low-carbohydrate diets can be improved by including nuts and seeds. The evidence is sufficient and conclusive. Nuts and seeds are beneficial foods.
Acknowledgments
A special thanks to Olin Idol for constructive conversations and suggestions for improving this manuscript.
References
- 1.
Ornish D, Brown SE, Scherwitz LW, Billings JH, Armstrong WT, Ports TA, et al. Can lifestyle changes reverse coronary heart disease? The lifestyle heart trial. Lancet. 1990; 336 (8708):129-133. DOI: 10.1016/0140-6736(90)91656-U - 2.
Esselstyn CB, Gendy G, Doyle J, Golubic M, Roizen MF. A way to reverse CAD? The Journal of Family Practice. 2014; 63 (7):356-364b - 3.
Campbell EK, Fidahusain M, Campbell TM II. Evaluation of an eight-week whole-food plant-based lifestyle modification program. Nutrients. 2019; 11 (9):2068. DOI: 10.3390/nu11092068 - 4.
Melina V, Craig W, Levin S. Position of the academy of nutrition and dietetics: Vegetarian diets. Journal of the Academy of Nutrition and Dietetics. 2016; 116 (12):1970-1980. DOI: 10.1016/j.jand.2016.09.025 - 5.
Fuhrman J, Ferreri D. Fueling the vegetarian (vegan) athlete. Current Sports Medicine Reports. 2010; 9 (4):233-241. DOI: 10.1249/JSR.0b013e3181e93a6f - 6.
Mariotti F, Gardner CD. Dietary protein and amino acids in vegetarian diets-a review. Nutrients. 2019; 11 (11):2661. DOI: 10.3390/nu11112661 - 7.
Godwin N, Roberts T, Hooshmand S, Kern M, Hong MY. Mixed nuts may promote satiety while maintaining stable blood glucose and insulin in healthy, obese, and overweight adults in a two-arm randomized controlled trial. Journal of Medicinal Food. 2019; 22 (4):427-432. DOI: 10.1089/jmf.2018.0127 - 8.
Vuksan V, Choleva L, Jovanovski E, Jenkins A, Au-Yeung F, Dias A, et al. Comparison of flax (Linum usitatissimum) and Salba-chia ( Salvia hispanica L.) seeds on postprandial glycemia and satiety in healthy individuals: A randomized, controlled, crossover study. European Journal of Clinical Nutrition. 2017;71 (2):234-238. DOI: 10.1038/ejcn.2016.148 - 9.
Yaacoub R, Saliba R, Nsouli B, Khalaf G, Birlouez-Aragon I. Formation of lipid oxidation and isomerization products during processing of nuts and sesame seeds. Journal of Agricultural and Food Chemistry. 2008; 56 (16):7082-7090. DOI: 10.1021/jf800808d - 10.
Brenna JT, Salem N, Sinclair AJ, Cunnane SC. alpha-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins, Leukotrienes, and Essential Fatty Acids. 2009; 80 (2–3):85-91. DOI: 10.1016/j.plefa.2009.01.004 - 11.
Sala-Vila A, Fleming J, Kris-Etherton P, Ros E. Impact of α-linolenic acid, the vegetable ω-3 fatty acid, on cardiovascular disease and cognition. Advances in Nutrition (Bethesda, Md.). 2022; 13 (5):1584-1602. DOI: 10.1093/advances/nmac016 - 12.
Sacks FM, Lichtenstein AH, Wu JHY, Appel LJ, Creager MA, Kris-Etherton PM, et al. Dietary fats and cardiovascular disease: A presidential advisory from the American heart association. Circulation. 2017; 16 (3):e1-e23. DOI: 10.1161/CIR.0000000000000510 - 13.
Jung H, Chen CYO, Blumberg JB, Kwak HK. The effect of almonds on vitamin E status and cardiovascular risk factors in Korean adults: A randomized clinical trial. European Journal of Nutrition. 2018; 57 (6):2069-2079. DOI: 10.1007/s00394-017-1480-5 - 14.
USDA. Usual nutrient intake from food and beverages, by gender and age. In: What We Eat in America, NHANES 2013–2016. Beltsville, MD: Agricultural Research Service; 2019 - 15.
Barbagallo M, Veronese N, Dominguez LJ. Magnesium in aging, health and diseases. Nutrients. 2021; 13 (2):463. DOI: 10.3390/nu13020463 - 16.
The Magpie Trial Collaborative Group. Do women with pre-eclampsia, and their babies, benefit from magnesium sulphate? The Magpie trial: A randomised placebo-controlled trial. The Lancet. 2002; 359 (9321):1877-1890 - 17.
Zhang Z, Cogswell ME, Gillespie C, Fang J, Loustalot F, Dai S, et al. Association between usual sodium and potassium intake and blood pressure and hypertension among U.S. adults: NHANES 2005–2010. PLoS One. 2013; 8 (10):e75289. DOI: 10.1371/journal.pone.0075289 - 18.
Macdonald HM, New SA, Fraser WD, Campbell MK, Reid DM. Low dietary potassium intakes and high dietary estimates of net endogenous acid production are associated with low bone mineral density in premenopausal women and increased markers of bone resorption in postmenopausal women. The American Journal of Clinical Nutrition. 2005; 81 (4):923-933 - 19.
Narasaki Y, You AS, Malik S, Moore LW, Bross R, Cervantes MK, et al. Dietary potassium intake, kidney function, and survival in a nationally representative cohort. The American Journal of Clinical Nutrition. 2022; 116 (4):1123-1134. DOI: 10.1093/ajcn/nqac215 - 20.
Zhang J, Saad R, Taylor EW, Rayman MP. Selenium and selenoproteins in viral infection with potential relevance to COVID-19. Redox Biology. 2020; 37 :101715. DOI: 10.1016/j.redox.2020.101715 - 21.
Sadeghsoltani F, Mohammadzadeh I, Safari MM, Hassanpour P, Izadpanah M, Qujeq D, et al. Zinc and respiratory viral infections: Important trace element in anti-viral response and immune regulation. Biological Trace Element Research. 2021; 200 :2556-2571. DOI: 10.1007/s12011-021-02859-z - 22.
Gao JW, Zhang SL, Hao QY, Huang FF, Liu ZY, Zhang HF, et al. Association of dietary zinc intake with coronary artery calcium progression: The multi-ethnic study of atherosclerosis (MESA). European Journal of Nutrition. 2021; 60 (5):2759-2767. DOI: 10.1007/s00394-020-02452-5 - 23.
Swaminath S, Um CY, Prizment AE, Lazovich D, Bostick RM. Combined mineral intakes and risk of colorectal cancer in postmenopausal women. Cancer Epidemiology Biomarkers & Prevention. 2019; 28 (2):392-399. DOI: 10.1158/1055-9965.EPI-18-0412 - 24.
Flores-Mateo G, Rojas-Rueda D, Basora J, Ros E, Salas-Salvadó J. Nut intake and adiposity: Meta-analysis of clinical trials. The American Journal of Clinical Nutrition. 2013; 97 (6):1346-1355. DOI: 10.3945/ajcn.111.031484 - 25.
Bes-Rastrollo M, Wedick NM, Martinez-Gonzalez MA, Li TY, Sampson L, Hu FB. Prospective study of nut consumption, long-term weight change, and obesity risk in women. The American Journal of Clinical Nutrition. 2009; 89 (6):1913-1919. DOI: 10.3945/ajcn.2008.27276 - 26.
Freisling H, Noh H, Slimani N, Chajès V, May AM, Peeters PH, et al. Nut intake and 5-year changes in body weight and obesity risk in adults: Results from the EPIC-PANACEA study. European Journal of Nutrition. 2018; 57 (7):2399-2408. DOI: 10.1007/s00394-017-1513-0 - 27.
Tan SY, Mattes RD. Appetitive, dietary and health effects of almonds consumed with meals or as snacks: A randomized, controlled trial. European Journal of Clinical Nutrition. 2013; 67 (11):1205-1214. DOI: 10.1038/ejcn.2013.184 - 28.
Del Gobbo LC, Falk MC, Feldman R, Lewis K, Mozaffarian D. Effects of tree nuts on blood lipids, apolipoproteins, and blood pressure: Systematic review, meta-analysis, and dose-response of 61 controlled intervention trials. The American Journal of Clinical Nutrition. 2015; 102 (6):1347-1356. DOI: 10.3945/ajcn.115.110965 - 29.
Guasch-Ferré M, Li J, Hu FB, Salas-Salvadó J, Tobias DK. Effects of walnut consumption on blood lipids and other cardiovascular risk factors: An updated meta-analysis and systematic review of controlled trials. The American Journal of Clinical Nutrition. 2018; 108 (1):174-187. DOI: 10.1093/ajcn/nqy091 - 30.
Musa-Veloso K, Paulionis L, Poon T, Lee HY. The effects of almond consumption on fasting blood lipid levels: A systematic review and meta-analysis of randomised controlled trials. Journal of Nutritional Science. 2016; 5 :e34. DOI: 10.1017/jns.2016.19 - 31.
Mohammadifard N, Salehi-Abargouei A, Salas-Salvadó J, Guasch-Ferré M, Humphries K, Sarrafzadegan N. The effect of tree nut, peanut, and soy nut consumption on blood pressure: A systematic review and meta-analysis of randomized controlled clinical trials. The American Journal of Clinical Nutrition. 2015; 101 (5):966-982. DOI: 10.3945/ajcn.114.091595 - 32.
Neale EP, Tapsell LC, Guan V, Batterham MJ. The effect of nut consumption on markers of inflammation and endothelial function: A systematic review and meta-analysis of randomised controlled trials. BMJ Open. 2017; 7 (11):e016863. DOI: 10.1136/bmjopen-2017-016863 - 33.
Thijssen DHJ, Black MA, Pyke KE, Padilla J, Atkinson G, Harris RA, et al. Assessment of flow-mediated dilation in humans: A methodological and physiological guideline. American Journal of Physiology. Heart and Circulatory Physiology. 2011; 300 (1):H2-H12. DOI: 10.1152/ajpheart.00471.2010 - 34.
Xiao Y, Huang W, Peng C, Zhang J, Wong C, Kim JH, et al. Effect of nut consumption on vascular endothelial function: A systematic review and meta-analysis of randomized controlled trials. Clinical Nutrition. 2018; 37 (3):831-839. DOI: 10.1016/j.clnu.2017.04.011 - 35.
Kim Y, Keogh J, Clifton PM. Nuts and cardio-metabolic disease: A review of meta-analyses. Nutrients. 2018; 10 (12):1935. DOI: 10.3390/nu10121935 - 36.
Aune D, Keum N, Giovannucci E, Fadnes LT, Boffetta P, Greenwood DC, et al. Nut consumption and risk of cardiovascular disease, total cancer, all-cause and cause-specific mortality: A systematic review and dose-response meta-analysis of prospective studies. BMC Medicine. 2016; 14 (1):207. DOI: 10.1186/s12916-016-0730-3 - 37.
Wu L, Wang Z, Zhu J, Murad AL, Prokop LJ, Murad MH. Nut consumption and risk of cancer and type 2 diabetes: A systematic review and meta-analysis. Nutrition Reviews. 2015; 73 (7):409-425. DOI: 10.1093/nutrit/nuv006 - 38.
Naghshi S, Sadeghian M, Nasiri M, Mobarak S, Asadi M, Sadeghi O. Association of total nut, tree nut, peanut, and peanut butter consumption with cancer incidence and mortality: A comprehensive systematic review and dose-response meta-analysis of observational studies. Advances in Nutrition (Bethesda, Md.). 2021; 12 (3):793-808. DOI: 10.1093/advances/nmaa152 - 39.
Eslamparast T, Sharafkhah M, Poustchi H, Hashemian M, Dawsey SM, Freedman ND, et al. Nut consumption and total and cause-specific mortality: Results from the Golestan cohort study. International Journal of Epidemiology. 2017; 46 (1):75-85. DOI: 10.1093/ije/dyv365 - 40.
Tharrey M, Mariotti F, Mashchak A, Barbillon P, Delattre M, Fraser GE. Patterns of plant and animal protein intake are strongly associated with cardiovascular mortality: The adventist health study-2 cohort. International Journal of Epidemiology. 2018; 47 (5):1603-1612. DOI: 10.1093/ije/dyy030 - 41.
Fraser GE, Sabate J, Beeson WL, Strahan TM. A possible protective effect of nut consumption on risk of coronary heart disease: The adventist health study. Archives of Internal Medicine. 1992; 152 (7):1416-1424. DOI: 10.1001/archinte.1992.00400190054010 - 42.
Souba W. Glutamine and cancer. Annals of Surgery. 1993 Dec; 218 :6. DOI: 10.1097/00000658-199312000-00004 - 43.
Li T, Copeland C, Le A. Glutamine metabolism in cancer. Advances in Experimental Medicine and Biology. 2021; 1311 . DOI: 10.1007/978-3-030-65768-0_2 - 44.
Corbet C, Feron O. Cancer cell metabolism and mitochondria: Nutrient plasticity for TCA cycle fueling. Biochimica Et Biophysica Acta. Reviews on Cancer. 2017; 1868 (1):7-15. DOI: 10.1016/j.bbcan.2017.01.002 - 45.
Levine ME, Suarez JA, Brandhorst S, Balasubramanian P, Cheng CW, Madia F, et al. Low protein intake is associated with a major reduction in IGF-1, cancer, and overall mortality in the 65 and younger but not older population. Cell Metabolism. 2014; 19 (3):407-417. DOI: 10.1016/j.cmet.2014.02.006 - 46.
Menotti A, Kromhout D, Blackburn H, Fidanza F, Buzina R, Nissinen A. Food intake patterns and 25-year mortality from coronary heart disease: Cross-cultural correlations in the seven countries study. The seven countries study research group. European Journal of Epidemiology. 1999; 15 (6):507-515. DOI: 10.1023/a:1007529206050 - 47.
Guasch-Ferre M, Zong G, Willett WC, Zock P, Wanders AJ, Hu FB, et al. Associations of monounsaturated fatty acids from plant and animal sources with total and cause-specific mortality in two us prospective cohort studies. Circulation Research. 2019; 124 (8):1266-1275. DOI: 10.1161/CIRCRESAHA.118.313996 - 48.
Zhuang P, Zhang Y, He W, Chen X, Chen J, He L, et al. Dietary fats in relation to total and cause-specific mortality in a prospective cohort of 521,120 individuals with 16 years of follow-up. Circulation Research. 2019; 124 :757-768. DOI: 10.1161/CIRCRESAHA.118.314038 - 49.
Fadelu T, Zhang S, Niedzwiecki D, Ye X, Saltz LB, Mayer RJ, et al. Nut consumption and survival in patients with stage III colon cancer: Results from CALGB 89803 (Alliance). Journal of Clinical Oncology. 2018; 36 (11):1112-1120. DOI: 10.1200/JCO.2017.75.5413 - 50.
Mason JK, Thompson LU. Flaxseed and its lignan and oil components: Can they play a role in reducing the risk of and improving the treatment of breast cancer? Applied Physiology, Nutrition, and Metabolism. 2014; 39 (6):663-678. DOI: 10.1139/apnm-2013-0420 - 51.
Coulman KD, Liu Z, Hum WQ, Michaelides J, Thompson LU. Whole sesame seed is as rich a source of mammalian lignan precursors as whole flaxseed. Nutrition and Cancer. 2005; 52 (2):156-165. DOI: 10.1207/s15327914nc5202_6