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Nuts and their bioactive constituents: effects on serum lipids and other factors that affect disease risk^1,2

¹ From the Graduate Program in Nutrition and the Department of Dairy and Animal Science, The Pennsylvania State University, University Park, and the Department of Nutrition, School of Public Health, Loma Linda University, CA.

² Address reprint requests to PM Kris-Etherton, Nutrition Department, S-126 Henderson Building, Pennsylvania State University, University Park, PA 16802. E-mail: pmk3{at}psu.edu.

	ABSTRACT

TOP ABSTRACT INTRODUCTION PREDICTIVE EQUATIONS FOR BLOOD... FAT, FATTY ACID, AND... FEEDING STUDIES THAT USED... EVIDENCE OF NONFAT... BEYOND LIPIDS: OTHER NUTRIENTS... PLANNING HEART-HEALTHY DIETS... SUMMARY AND CONCLUSIONS REFERENCES

 
Because nuts have favorable fatty acid and nutrient profiles, there is growing interest in evaluating their role in a heart-healthy diet. Nuts are low in saturated fatty acids and high in monounsaturated and polyunsaturated fatty acids. In addition, emerging evidence indicates that there are other bioactive molecules in nuts that elicit cardioprotective effects. These include plant protein, dietary fiber, micronutrients such as copper and magnesium, plant sterols, and phytochemicals. Few feeding studies have been conducted that have incorporated different nuts into the test diets to determine the effects on plasma lipids and lipoproteins. The total- and lipoprotein-cholesterol responses to these diets are summarized in this article. In addition, the actual cholesterol response was compared with the predicted response derived from the most current predictive equations for blood cholesterol. Results from this comparison showed that when subjects consumed test diets including nuts, there was an 25% greater cholesterol-lowering response than that predicted by the equations. These results suggest that there are non–fatty acid constituents in nuts that have additional cholesterol-lowering effects. Further studies are needed to identify these constituents and establish their relative cholesterol-lowering potency. 1999(suppl);70:504S–11S.

Key Words: Nuts • plant foods • dietary fat • saturated fatty acids • monounsaturated fatty acids • polyunsaturated fatty acids • predictive equations • coronary heart disease risk reduction • cardiovascular disease prevention • blood cholesterol • LDL cholesterol • phytochemicals • plant sterols • dietary fiber • copper • magnesium

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PREDICTIVE EQUATIONS FOR BLOOD... FAT, FATTY ACID, AND... FEEDING STUDIES THAT USED... EVIDENCE OF NONFAT... BEYOND LIPIDS: OTHER NUTRIENTS... PLANNING HEART-HEALTHY DIETS... SUMMARY AND CONCLUSIONS REFERENCES

 
In nutrition, a new era is emerging that is characterized by the search for dietary constituents that have benefits beyond those ascribed to the macro- and micronutrients. Historically, in the area of cardiovascular disease (CVD), efforts have been directed toward identifying the type and, to some extent, amount of dietary fat that can achieve maximal risk reduction. It is now clear that although a fat-modified diet can significantly affect CVD risk, other components in the diet, such as dietary fiber, plant protein, and soy protein appear to confer additional protective effects that extend beyond the lipid-lowering effects of the recommended diets. Identification of additional dietary constituents that elicit favorable effects will facilitate the development of diets that are even more effective for both the prevention and treatment of CVD and other chronic diseases.

In the search for bioactive components in foods that favorably affect CVD risk, nuts have begun to attract attention. Nuts are complex plant foods that are not only rich sources of unsaturated fat but also contain several nonfat constituents such as plant protein, fiber, micronutrients (eg, copper and magnesium), plant sterols, and phytochemicals (1). Because nuts have a favorable fatty acid profile and contain several bioactive compounds that may confer additional protective effects, there is interest in evaluating the role of nuts in cholesterol-lowering diets. Thus, the purpose of this article is to summarize the results of studies that have examined the effects of diets containing nuts on blood lipids and lipoproteins. Interestingly, when these data were compared with results predicted from regression equations using changes in dietary fatty acid profiles, nuts appeared to elicit a more potent lipid-lowering effect than would be expected. This provocative evidence suggests that there are other bioactive components in nuts that have cholesterol-lowering effects. In addition, other putative beneficial effects of constituents in nuts, beyond those associated with lowering blood cholesterol, are discussed briefly in this article.

	PREDICTIVE EQUATIONS FOR BLOOD CHOLESTEROL

TOP ABSTRACT INTRODUCTION PREDICTIVE EQUATIONS FOR BLOOD... FAT, FATTY ACID, AND... FEEDING STUDIES THAT USED... EVIDENCE OF NONFAT... BEYOND LIPIDS: OTHER NUTRIENTS... PLANNING HEART-HEALTHY DIETS... SUMMARY AND CONCLUSIONS REFERENCES

 
Data from well-controlled feeding studies conducted during the past 40 y were used for regression analyses that resulted in development of predictive equations for plasma cholesterol. These equations provided important information about the qualitative and quantitative effects of fatty acid classes on blood cholesterol concentrations. The first predictive equations for cholesterol were developed by Keys et al (2) and Hegsted et al (3) (Table 1). These equations were subsequently modified by Mensink and Katan (4), Hegsted et al (5), and Yu et al (6) to predict the effects of fatty acid classes on LDL- and HDL-cholesterol responses (Table 1).

A recent meta-analysis of 395 metabolic-ward studies (7) confirmed the results of the regression analyses conducted to date and extended these findings to show that the results are not affected by experimental design, age, sex, body weight, energy intake, baseline cholesterol intake, or study duration. Thus, the predictive equations are useful for estimating the effects of dietary change on lipids and lipoproteins in any population group. Moreover, these equations can provide important clues about the presence of additional dietary components that exert a cholesterol-lowering effect that is greater than predicted. Any physiologically important deviation from what would be predicted based on the fatty acid profile of the diet provides evidence suggesting the presence of additional bioactive substances that regulate blood cholesterol concentrations.

	FAT, FATTY ACID, AND NUTRIENT COMPOSITION OF NUTS

TOP ABSTRACT INTRODUCTION PREDICTIVE EQUATIONS FOR BLOOD... FAT, FATTY ACID, AND... FEEDING STUDIES THAT USED... EVIDENCE OF NONFAT... BEYOND LIPIDS: OTHER NUTRIENTS... PLANNING HEART-HEALTHY DIETS... SUMMARY AND CONCLUSIONS REFERENCES

 
The energy content of nuts ranges from 23.7 to 29.3 kJ/g (161 to 199 kcal/oz) and the fat content is 0.51 to 0.73 g/g. Nuts that are higher in energy are higher in fat. Thus, 79% of the energy in nuts comes from fat. Nuts are low in SFA and high in unsaturated fatty acids. The predominant type of unsaturated fatty acid in most nuts is MUFA, contributing on average 62% of the energy from fat. MUFA and PUFA together contribute 91% of the energy from fat. Of the tree nuts, walnuts are unique because they are a rich source of -linolenic acid. Compared with vegetable oils that are commonly used in the United States, nuts have less SFA than olive oil and slightly more SFA than canola and high-oleic-acid safflower oils, on average. The oleic-acid content of nuts is similar to that of canola oil, but less than that of olive oil and high-oleic-acid safflower oil. Canola oil and nuts contain similar amounts of linoleic acid, and these amounts are appreciably greater than those present in olive oil and high–oleic acid safflower oil. The fatty acid profiles of selected nuts and vegetable oils are shown in Table 2.

	FEEDING STUDIES THAT USED DIETS CONTAINING NUTS

TOP ABSTRACT INTRODUCTION PREDICTIVE EQUATIONS FOR BLOOD... FAT, FATTY ACID, AND... FEEDING STUDIES THAT USED... EVIDENCE OF NONFAT... BEYOND LIPIDS: OTHER NUTRIENTS... PLANNING HEART-HEALTHY DIETS... SUMMARY AND CONCLUSIONS REFERENCES

 
To date, 9 studies have evaluated the effects of diets containing nuts on blood lipids and lipoproteins (10–18). The experimental designs of these studies were variable and subject characteristics differed, as did the degree of dietary control (Table 3). Six studies (10–15) were designed to specifically evaluate the effects of nuts on plasma lipids and lipoproteins; the nuts studied were almonds, walnuts, and macadamia nuts. Three studies (16–18) used nuts and other fat sources to achieve the fatty acid profile of the experimental diets tested (ie, high-MUFA and high-PUFA test diets). The total-fat and fatty acid profiles of the experimental diets varied, as shown in Table 4. In general, the experimental diets containing nuts were low in cholesterol (300 mg/d) and saturated fat, although the macadamia nut diet in the study conducted by Colquhoun et al (13) provided 11% of energy from SFA. Total fat content varied, ranging from 26% (14) to 42% (13) of energy. The studies compared the effects of high-MUFA diets on plasma lipids, lipoproteins, or both with those of baseline, reference, or high-SFA diets; high-PUFA diets; or low-fat, high-carbohydrate diets. Spiller et al (10) and Abbey et al (18) also compared high-PUFA diets with high-SFA or reference diets. The study conducted by Sabaté et al (12) was unique because it compared two Step I diets, one of which was high in walnuts and, as a result, was high in PUFAs.

Although these proposed studies should provide useful information about any health effects associated with the nonfat components of nuts, it is evident from the existing data that nuts can be included in, and even used to design, cholesterol-lowering diets that have desirable fat contents and fatty acid profiles. Because of their distinguishing macronutrient and fatty acid characteristics, nuts can be used to reduce the SFA content of the diet by replacing SFA energy with energy from unsaturated fatty acids while maintaining the amount of dietary fat. This is an effective strategy for not only achieving reductions in total- and LDL-cholesterol concentrations but also preventing the HDL-cholesterol–lowering and triacylglycerol-raising effects of low-fat, high-carbohydrate diets.

	EVIDENCE OF NONFAT HYPOCHOLESTEROLEMIC FACTORS IN NUTS

TOP ABSTRACT INTRODUCTION PREDICTIVE EQUATIONS FOR BLOOD... FAT, FATTY ACID, AND... FEEDING STUDIES THAT USED... EVIDENCE OF NONFAT... BEYOND LIPIDS: OTHER NUTRIENTS... PLANNING HEART-HEALTHY DIETS... SUMMARY AND CONCLUSIONS REFERENCES

 
There is convincing evidence that the fatty acid profiles of nuts have favorable effects on blood lipids, but a related and as of yet unanswered question is, Are there other constituents in nuts that also affect blood cholesterol concentrations? This is a most intriguing question because there are several potentially bioactive components in nuts. Studies conducted with soy products have shown beneficial effects of both soy protein and phytoestrogens (20, 21). Given that nuts contain plant protein and many different phytochemicals, it is not unreasonable to speculate that the nonfat fraction of nuts could exert beneficial biological effects.

We reasoned that to determine whether there is any basis for this theory, any discrepancies between changes in total- and LDL-cholesterol concentrations estimated from the predictive equations and the actual values observed as a result of changes in dietary fatty acid consumption would be revealing. Specifically, if the observed change exceeded the predicted change in plasma lipids, this might indicate the presence of bioactive, nonfat, cholesterol-lowering compounds.

We conducted an analysis to compare the observed changes to the predicted changes in total-, LDL-, and HDL-cholesterol concentrations. To accomplish this, we first calculated the change in dietary fatty acid composition when subjects were switched from an experimental diet not containing nuts, or a baseline diet, to an experimental diet containing nuts. These values were used to calculate the predicted total-, LDL-, and HDL-cholesterol responses to the change in dietary fatty acids using the Hegsted et al (5) and Mensink and Katan (4) regression equations. One of the original equations developed for total cholesterol (3) was also used. The observed changes were simply determined by calculating the mean changes in total-, LDL-, and HDL-cholesterol concentrations (12–15, 18). The Student's t test was then used to compare the predicted with the observed lipid and lipoprotein changes.

The evidence shown in Figure 1 suggests that components in nuts further reduce total- and LDL-cholesterol concentrations beyond the effects predicted by equations based on the fatty acid profiles of nuts (P < 0.05) (3, 4, 5). The magnitude of the cholesterol-lowering effect is 25% greater than would be predicted based on the fatty acid profiles of the test diets studied. Similarly, a recent study (22) that investigated the effect of a diet high in vegetables, fruit, and nuts found that total serum cholesterol was reduced 34% and 49% more than was predicted by the Keys et al (2) and Hegsted et al (3) equations, respectively. The interpretation we favor is that there seem to be other constituents in nuts that account for this response. We hasten to add, however, that this conclusion is based on limited data and there is no direct experimental evidence to support this conclusion. Thus, it will be important to conduct the necessary studies to clarify this potentially important nutrition question. This question could be readily addressed by conducting controlled feeding studies in which one experimental diet includes nuts and is compared with another test diet that has the same fat content and fatty acid profile but does not contain nuts.

View larger version (29K): [in this window] [in a new window]   FIGURE 1. Comparison of observed changes (mean ± SE) in total-, LDL-, and HDL-cholesterol concentrations (12–15, 18) with those calculated by using the predictive equations for plasma cholesterol of Hegsted et al (5) and Mensink and Katan (4) (see Table 1; data are means of the results from both equations). *Observed change was significantly different from the predicted change, P < 0.05 (t test).

	BEYOND LIPIDS: OTHER NUTRIENTS IN NUTS THAT ARE THOUGHT TO CONFER HEALTH BENEFITS

TOP ABSTRACT INTRODUCTION PREDICTIVE EQUATIONS FOR BLOOD... FAT, FATTY ACID, AND... FEEDING STUDIES THAT USED... EVIDENCE OF NONFAT... BEYOND LIPIDS: OTHER NUTRIENTS... PLANNING HEART-HEALTHY DIETS... SUMMARY AND CONCLUSIONS REFERENCES

Nuts are a source of dietary fiber (7 g/100g), of which 25% is soluble fiber. Soluble fiber has been shown to reduce total- and LDL-cholesterol concentrations and improve glycemic control (34). Thus, in the context of a high-MUFA diet in which nuts are the primary source of MUFA, nuts (ie, 100 g) can contribute appreciably to the recommended fiber intake (ie, 20–35 g/d) (9).

Vitamin E in high doses (>100 IU/d) has been shown to reduce the risk of coronary heart disease (35). This cardioprotective effect appears to be due to vitamin E-induced inhibition of LDL oxidation [vitamin E is transported in the LDL particle (36)], a key step in the atherogenic process. Nuts are a rich source of vitamin E, although the quantities obtained from typical nut consumption are far less than the amounts shown to have beneficial effects on coronary heart disease. Nonetheless, nut consumption is still an effective means of increasing vitamin E intake.

Folic acid is also found in nuts. Consumption of 100 g nuts provides 16% of the daily reference intake (DRI) for folic acid, which is 400 µg/d (9). Adequate consumption of folic acid is important for preventing elevated homocysteine concentrations, which have been shown to correlate with the severity of carotid-artery stenosis (37).

On average, 1 ounce of nuts contains 18% of the DRI for copper (2 mg) (9) and therefore nuts can be a significant source of this essential mineral (38). Copper plays a key role in hematopoiesis and diets low in copper have been associated with adverse changes in lipids, glucose tolerance, blood pressure, and electrocardiograms (39).

Almost all nuts are good sources of magnesium, providing 8–20% of the DRI (400 mg) (9) for this essential mineral in a 28.4-g (1-oz) serving (1, 40). Magnesium is important in maintaining the proper balance of calcium to potassium; low magnesium status can contribute to dysrhythmias, myocardial infarction, and possibly hypertension. Magnesium is also critical to enzyme function, healthy tooth enamel, muscle relaxation, and nerve transmission.

A meta-analysis of 38 controlled clinical studies showed that consumption of soy protein (ie, 47 g/d) reduced total- and LDL-cholesterol concentrations by 10% (20). The biological mechanisms responsible for this hypocholesterolemic effect are not clear. There is some evidence suggesting that arginine, the second most abundant amino acid found in nut proteins, may account for the hypocholesterolemic effect observed (41, 42). In addition, there is evidence that the phytoestrogens in soy protein have cardioprotective effects (43). Little is known about phytoestrogens in nuts.

Plant sterols inhibit cholesterol absorption. Sitosterol, the most abundant plant sterol in vegetable oils, has been shown to elicit a marked hypocholesterolemic effect (44). Little is known about the plant-sterol content of nuts and the effects, if any, on cholesterol absorption and blood-cholesterol concentrations.

It is clear that nuts contain many nutrients and dietary factors that may confer protective health effects. Some of the components in nuts that are thought to be beneficial are listed in Table 7. A great deal of research will be needed to clarify the effects of these constituents found in nuts on the risk of coronary heart disease and other chronic diseases.

	PLANNING HEART-HEALTHY DIETS CONTAINING NUTS

TOP ABSTRACT INTRODUCTION PREDICTIVE EQUATIONS FOR BLOOD... FAT, FATTY ACID, AND... FEEDING STUDIES THAT USED... EVIDENCE OF NONFAT... BEYOND LIPIDS: OTHER NUTRIENTS... PLANNING HEART-HEALTHY DIETS... SUMMARY AND CONCLUSIONS REFERENCES

	SUMMARY AND CONCLUSIONS

TOP ABSTRACT INTRODUCTION PREDICTIVE EQUATIONS FOR BLOOD... FAT, FATTY ACID, AND... FEEDING STUDIES THAT USED... EVIDENCE OF NONFAT... BEYOND LIPIDS: OTHER NUTRIENTS... PLANNING HEART-HEALTHY DIETS... SUMMARY AND CONCLUSIONS REFERENCES

 
Nuts have many beneficial attributes. The foremost at this time, simply because of the extensive data available, is the favorable fatty acid profile, which can be exploited in planning blood cholesterol-lowering diets. There may be a number of other bioactive compounds in nuts that potentiate cholesterol-lowering effects and independently affect risk factors for various chronic diseases. However, the data on this topic are limited and much research is needed to define the roles that these compounds may play in reducing the risk of chronic diseases, as well as the biological mechanisms involved. Irrespective of this, there are sufficient data to justify the recommendation to include nuts in the diet. As discussed, nuts can be readily incorporated into the diet. Efforts are needed to educate the public about the health benefits of nuts and ways to use them in planning a healthy diet.

	REFERENCES

TOP ABSTRACT INTRODUCTION PREDICTIVE EQUATIONS FOR BLOOD... FAT, FATTY ACID, AND... FEEDING STUDIES THAT USED... EVIDENCE OF NONFAT... BEYOND LIPIDS: OTHER NUTRIENTS... PLANNING HEART-HEALTHY DIETS... SUMMARY AND CONCLUSIONS REFERENCES

 

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