Olive oil and walnut breakfasts reduce the postprandial inflammatory response in mononuclear cells compared with a butter breakfast in healthy men

Abstract

Background

Inflammation is crucial in all stages of atherosclerosis, and few studies have investigated the effect of dietary fat on markers of inflammation related to this disease during the postprandial period.

Objective

To evaluate the chronic effects of dietary fat on the postprandial expression of proinflammatory genes in peripheral blood mononuclear cells (PBMCs) in healthy subjects.

Design

20 healthy men followed three different diets for 4 weeks each, according to a randomized crossover design: Western diet: 15% protein, 47% carbohydrates (CHO), 38% fat (22% saturated fatty acid (SFA)); Mediterranean diet: 15% protein, 47% CHO, 38% fat (24% monounsaturated fatty acid (MUFA)); CHO-rich and n-3 diet: 15% protein, 55% CHO, <30% fat (8% polyunsaturated fatty acid (PUFA)). After 12-h fast, volunteers were given a breakfast with a fat composition similar to that consumed in each of the diets—butter breakfast: 35% SFA; olive oil breakfast: 36% MUFA; walnut breakfast: 16% PUFA, 4% α-linolenic acid (LNA).

Results

The butter breakfast induced a higher increase in tumor necrosis factor (TNF)-α messenger RNA (mRNA) expression than the olive oil or walnut breakfasts (P = 0.014) in PBMCs. Moreover, we found a higher postprandial response in the mRNA of interleukin (IL)-6 with the intake of butter and olive oil breakfasts than with the walnut breakfast (P = 0.025) in these cells. However, the effects of the three fatty breakfasts on the plasma concentrations of these proinflammatory parameters showed no significant differences (P = N.S.).

Conclusion

Consumption of a butter-enriched meal elicits greater postprandial expression of proinflammatory cytokine mRNA in PBMCs, compared to the olive oil and walnut breakfasts.

Introduction

Atherosclerosis is the major cause of death in western societies [1] and there is evidence that inflammation plays a central role in all phases of the atherosclerotic process [2]. A first step in this condition is the adhesion of circulating monocytes to the endothelium and its migration to the intima layer [3]. A crucial chemokine responsible for the recruitment of monocytes to inflammatory lesions in the vasculature is monocyte chemoattractant protein-1 (MCP-1) [4], [5]. This chemokine is highly expressed in the macrophage-rich area of the atherosclerotic lesions in human [6] and its expression and secretion from vascular cells have been proved to account for the increased monocyte chemotatic activity [7]. Once monocytes have reached the subendothelial space, the modified LDL and various molecules produced by the T lymphocytes, endothelial cells and smooth muscle cells stimulate the transformation of the monocytes into macrophages, which are important mediators of inflammation. In the final stage, the plaque is ruptured in the shoulder [8], area more vulnerable, which is enriched in T lymphocytes and macrophages.

The diet, and particularly its fat content, can modulate the cardiovascular risk factors and the mechanisms related to the formation and development of the atheroma plaques [9], [10]. However, the influence of the diet on atherosclerosis goes beyond its known effects on the classic cardiovascular risk factors [9]. Fatty acids and other components of the diet modulate the expression of several genes involved in the inflammatory and immune response, such as proinflammatory cytokines, adhesion molecules, chemokines and inflammatory enzymes [11], [12], [13].

Changes in postprandial metabolism take place every time we eat a meal and alterations in this state may play an important role in the development of cardiovascular and associated diseases [14], [15], [16]. During postprandial lipemia, there is an increase in circulating triacylglycerol-rich lipoproteins (TRL), which may be deposited into the arterial wall and accumulated in atheromatous plaques [16], formation of highly oxidisable small, dense LDL and a reduction in the concentration of HDL [17]. Furthermore, it has been found that during this phase, when triacylglycerols (TG) and glucose rise, the neutrophil count increases with the subsequent production of proinflammatory cytokines and oxidative stress, with these changes possibly contributing to endothelial dysfunction [18], [19]. Moreover, van Oostrom et al. [20] provided evidence that postprandial triglyceridemia is related to the proinflammatory state due to the high expression of the activation markers in neutrophils and monocytes. Our group has also shown that butter and walnuts, but not olive oil, elicit postprandial activation of nuclear factor-κB (NF-κB) in PBMCs in healthy men [21]. Since human beings spend much of the day in the postprandial state it is important to understand the inflammatory changes that take place during this period in terms of the type of fat consumed. Our aim was therefore to evaluate the chronic effect of the type of fat on the postprandial expression of proinflammatory genes in PBMCs from healthy men. Because apolipoprotein (apo)E is an important mediator of the clearance of circulating TRL by receptor [22] and the apoE E2/E3/E4 polymorphism is implicated in a variable lipid postprandial response [23], we realized the study in subjects with the apoE3/E3 genotype, the most common allele in the population.