Article pubs.acs.org/JAFC
Lipid Peroxidation in a Stomach Medium Is Affected by Dietary Oils (Olive/Fish) and Antioxidants: The Mediterranean versus Western Diet Oren Tirosh, Adi Shpaizer, and Joseph Kanner* Institute of Biochemistry, Food Science and Nutrition, Faculty of Agriculture, Food and Environment, The Hebrew University, Rehovot 76100, Israel ABSTRACT: Red meat is an integral part of the Western diet, and high consumption is associated with an increased risk of chronic diseases. Using a system that simulated the human stomach, red meat was interacted with different oils (olive/fish) and lipid peroxidation was determined by measuring accumulation of malondialdehyde (MDA) and lipid peroxides (LOOH). Olive oil decreased meat lipid peroxidation from 121.7 ± 3.1 to 48.2 ± 1.3 μM and from 327.1 ± 9.5 to 77.3 ± 6.0 μM as assessed by MDA and ROOH, respectively. The inhibitory effect of olive oil was attributed to oleic acid rather than its polyphenol content. In contrast, fish oils from tuna or an ω-3 supplement dramatically increased meat lipid peroxidation from 96.2 ± 3.6 to 514.2 ± 6.7 μM MDA. Vitamin E inhibited meat lipid peroxidation in the presence of olive oil but paradoxically increased peroxidation in the presence of fish oil. The inhibitory properties of oleic acid may play a key role in the health benefits of the Mediterranean diet. KEYWORDS: stomach medium, lipid peroxidation, olive oil, fish oil, antioxidants
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INTRODUCTION
Other sources of oil have also been studied with regard to their cardioprotective attributes. There is increasing interest in ω-3 PUFA due to their potential health benefits, commonly known as the “Eskimo factor”. Eskimos traditionally have a low prevalence of certain diseases including cardiovascular diseases27,28 and neurological disorders.29 However, recent evidence has raised the concern that transition toward a more Western dietary pattern in the Eskimo and Japanese populations may overcome the cardioprotective effects of ω-3 PUFA.27 In addition, these highly unsaturated fatty acids are readily oxidized and may be more dangerous than beneficial.30,31 Red-meat consumption is an integral part of the Western diet and is associated with an increased risk of chronic diseases. In recent years ω-3-rich oils have also been recommended and may be consumed together with red meat. We chose to determine the effect of fish oil and concentrated ω-3 fatty acids because it simulates the Western diet, which contains abundant quantities of oxidized fried oils32,33 but differs from the traditional “Eskimo diet” (100 years ago), which was based on fresh fish most likely lacking oxidized oils. This is in contrast to the “modern trend” of supplementation, where the population uses pills of ω-3 fatty acids extracted from fish stored for extended periods and shown to contain 1−10 mM hydroperoxides and 44−120 μM alkenals (and more other reactive carbonyls).30,34,35 The aim of this study was to better understand the interrelationship of red meat, a typical Western food rich in ω6 fatty acids such as arachidonic acid (20:4), with different dietary oils, in a model system that simulates food lipid peroxidation in the human stomach.
The stomach, which acts as a bioreactor, is an important junction in human digestion and is the site of many chemical and biochemical reactions. It also provides an excellent medium for lipid peroxidation and co-oxidation of dietary constituents and vitamins and generation of advanced lipid oxidation endproducts (ALEs).1 Several studies have been published by our research group1−4 and others5,6 demonstrating that red meat in the stomach generates free radicals, lipid peroxidation, cooxidation of vitamins, and production of ALEs. The ALEs that are classified as reactive carbonyls (RCs) can be absorbed from the gut into the bloodstream2,3 and modify LDL to MDA-LDL.7 Red-meat consumption has been associated with an increased risk of chronic diseases such as coronary heart disease,8,9 atherosclerosis,8,10 diabetes,11−14 prostate cancer,15 breast cancer,16 colon cancer,17−20 and overall mortality.20 The rate of lipid peroxidation and production of RCs in the stomach medium depends on many conditions including fattyacid composition, degree of saturation, and the amount of hydroperoxides previously present in foods.21−23 The relative rates of autoxidation of oleic (18:1), linoleic (18:2), linolenic (18:3), arachidonic (20:4), and docosahexaenoic acid (22:6) have been compared in the past on the basis of oxygen absorption without catalyzers and found to be relatively 1- to ∼40-, 100-, 200-, and 400-fold higher than that of oleic acid, respectively.21 The Mediterranean diet, containing meaningful amounts of olive oil rich in ω-9 fatty acids, has been ranked as the most likely dietary pattern to prevent coronary heart diseases.24 To evaluate primary cardiovascular prevention, a randomized trial was carried out to test the efficacy of the Mediterranean diet supplemented with high levels of olive oil in comparison to a control low-fat diet. An adjusted hazard ratio of 0.70 for the Mediterranean diet versus the control group was reported.25 Clinical intervention trials have provided evidence that olive oil contributes to protection against LDL lipid peroxidation damage in humans.26 © 2015 American Chemical Society
Received: Revised: Accepted: Published: 7016
April 29, 2015 July 5, 2015 July 13, 2015 July 13, 2015 DOI: 10.1021/acs.jafc.5b02149 J. Agric. Food Chem. 2015, 63, 7016−7023
Article
Journal of Agricultural and Food Chemistry Table 1. Fatty Acid Composition of Oilsa fatty acid myristic acid palmitic acid palmitoleic acid margaric acid heptadecenoic acid stearic acid oleic acid vaccenic acid linoleic acid α-linolenic acid stearidonic acid arachidic acid gondoic acid eicosadienoic acid dihomo-γ-linolenic acid eicosatrienoic acid arachidonic acid eicosapentaenoic acid (EPA) heneicosylic acid behenic acid erucic acid docosadienoic acid docosatrienoic acid adrenic acid docosapentaenoic acid (DPA) osbond acid docosahexaenoic acid (DHA) tricosylic acid lignoceric acid nervonic acid a
C14:0 C16:0 C16:1 C17:0 C17:1 C18:0 C18:1 C18:1 C18:2 C18:3 C18:4 C20:0 C20:1 C20:2 C20:3 C20:3 C20:4 C20:5 C21:0 C22:0 C22:1 C22:2 C22:3 C22:4 C22:5 C22:5 C22:6 C23:0 C24:0 C24:1
cis-9 cis-10 cis-9 trans-11 cis-9,12 cis-9,12,15 cis-6,9,12,15 cis-11 cis-11,14 cis-8,11,14 cis-11,14,17 cis-5,8,11,14 cis-5,8,11,14,17
cis-13 cis-13,16 cis-13,16,19 cis-7,10,13,16 cis-7,10,13,16,19 cis-4,7,10,13,16 cis-4,7,10,13,16,19
cis-15
ROO (%)
EVOO (%)
tuna (%)
Alsepa (%)
nd 10.09 0.59 nd nd 3.25 71.54 2.17 7.81 0.49 nd 0.58 0.38 nd nd nd nd nd nd 0.2 nd nd nd nd nd nd nd nd 0.12 nd
nd 12.64 0.71 nd nd 8.63 70.03 1.94 4.05 0.6 nd 0.55 0.24 nd nd nd nd nd nd 0.13 nd nd nd nd nd nd nd nd 0.08 nd
2.24 19.77 4.25 1.4 0.96 8.98 18.68 3.05 1.25 0.58 nd 0.63 1.85 0.38 0.24 0.51 1.59 3.32 nd 0.37 0.55 nd nd nd nd nd 20.66 nd 0.36 1.47
nd 0.35 0.30 nd nd 1.25 3.32 nd 0.29 1.09 1.47 0.46 1.09 0.28 0.17 0.33 0.73 41.13 0.10 0.26 0.54 1.59 1.03 2.21 5.53 1.30 31.75 1.57 0.19 0.43
Standard deviation
