Omega-3 fatty acids

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SIMOPOULOS Biol Res 37, 2004, 263-277 Biol Res 37: 263-277, 2004 263 BR Omega-3 Fatty Acids and Antioxidants in Edible Wild Plants ARTEMIS P SIMOPOULOS The Center for Genetics, Nutrition and Health, Washington, DC, USA ABSTRACT Human beings evolved on a diet that was balanced in the omega-6 and omega-3 polyunsaturated fatty acids (PUFA), and was high in antioxidants. Edible wild plants provide alpha-linolenic acid (ALA) and higher amounts of vitamin E and vitamin C than cultivated plants. I
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  263 SIMOPOULOS  Biol Res 37, 2004, 263-277     Biol Res 37: 263-277, 2004 B R Omega-3 Fatty Acids and Antioxidants in Edible WildPlants ARTEMIS P SIMOPOULOS The Center for Genetics, Nutrition and Health, Washington, DC, USA ABSTRACT Human beings evolved on a diet that was balanced in the omega-6 and omega-3 polyunsaturated fatty acids(PUFA), and was high in antioxidants. Edible wild plants provide alpha-linolenic acid (ALA) and higheramounts of vitamin E and vitamin C than cultivated plants. In addition to the antioxidant vitamins, edible wildplants are rich in phenols and other compounds that increase their antioxidant capacity. It is thereforeimportant to systematically analyze the total antioxidant capacity of wild plants and promote theircommercialization in both developed and developing countries. The diets of Western countries have containedincreasingly larger amounts of linoleic acid (LA), which has been promoted for its cholesterol-loweringeffect. It is now recognized that dietary LA favors oxidative modification of low density lipoprotein (LDL)cholesterol and increases platelet response to aggregation. In contrast, ALA intake is associated withinhibitory effects on the clotting activity of platelets, on their response to thrombin, and on the regulation of arachidonic acid (AA) metabolism. In clinical studies, ALA contributed to lowering of blood pressure, and aprospective epidemiological study showed that ALA is inversely related to the risk of coronary heart diseasein men. Dietary amounts of LA as well as the ratio of LA to ALA appear to be important for the metabolismof ALA to longer-chain omega-3 PUFAs. Relatively large reserves of LA in body fat, as are found in vegansor in the diet of omnivores in Western societies, would tend to slow down the formation of long-chain omega-3 fatty acids from ALA. Therefore, the role of ALA in human nutrition becomes important in terms of long-term dietary intake. One advantage of the consumption of ALA over omega-3 fatty acids from fish is that theproblem of insufficient vitamin E intake does not exist with high intake of ALA from plant sources. Key words : Alpha-linolenic acid, antioxidants, chronic diseases, edible wild plants, evolutionary aspects of diet, omega-3 fatty acids. Abbreviations: AA: arachidonic acid; AI: Adequate Intake; ALA: alpha-linolenic acid; ARP: antiradicalpower; DHA: docosahexaenoic acid; DPPH ã : 2,2-diphenyl-1-picrylhydrazyl; FRAP: ferric-reducing ability of plasma; LA: linoleic acid; LDL: low density lipoprotein; EPA: eicosapentaenoic acid; ORAC: oxygen radicalabsorbance assay; PUFA: polyunsaturated fatty acids. Corresponding author: Dr Artemis P Simopoulos. The Center for Genetics, Nutrition and Health 2001 S Street, NW, Suite530, Washington, DC 20009, USA. Phone: (202) 462-5062. Fax: (202) 462-5241. E-mail: cgnh@bellatlantic.netReceived: November 18, 2002. Accepted: December 3, 2002INTRODUCTION In nutritional terms, human physiologyevolved in the context of wild plants andanimals in the wild. Most likely, humanbeings made use of both aquatic andterrestrial foods. Over the past 20 years, manystudies and clinical investigations have beencarried out on the metabolism of polyunsaturated fatty acids (PUFAs) ingeneral and on omega-3 fatty acids inparticular. Today we know that omega-3 fattyacids are essential for normal growth anddevelopment and may play an important rolein the prevention and treatment of coronaryartery disease, hypertension, diabetes,arthritis, other inflammatory and autoimmunedisorders, and cancer (1-10). Research hasbeen carried out in animal models, tissuecultures, and human beings. The srcinalobservational studies have given way tocontrolled clinical trials. Great progress hastaken place in our knowledge of thephysiologic and molecular mechanisms of thevarious fatty acids in health and disease.Specifically, their beneficial effects have been  SIMOPOULOS  Biol Res 37, 2004, 263-277  264shown in the prevention and management of coronary heart disease (11-14), hypertension(15-17), type 2 diabetes (18,19), renal disease(20, 21), rheumatoid arthritis (22), ulcerativecolitis (23), Crohn’s disease (24), and chronicobstructive pulmonary disease (25).Epidemiologic studies indicate that fruits andvegetables decrease the risk of chronicdiseases, including cancer, cardiovascular andcerebrovascular disease. This protection hasbeen attributed to the various antioxidantscontained in them (26-29).Oxidative damage, as a result of normalmetabolism or secondary to environmentalpollutants, leads to free radical formationwhich has been considered to play a centralrole in cancer and atherosclerosis.Therefore, antioxidants, which canneutralize free radicals, may be importantin the prevention of these diseases.However, results from intervention trialswith single compounds such as vitamins Eand C or beta-carotene have not supportedany protective effect (30-36). In fact,supplementation with beta-carotene resultedin adverse disease outcomes in clinicaltrials (37-40). One reason for theineffective clinical trials may be the factthat the protective effects of fruits andvegetables most likely result from theaction of lesser known antioxidantcompounds, or from a mixture of antioxidants present in foods. Thus, anumber of dietary antioxidants, such asflavonoids, carotenoids, polyphenols andsulfides, etc., are bioactive and work synergistically as do vitamin C and vitaminE. This hypothesis led to the thinking thatthe total amount of electron-donatingantioxidants in the diet, derived from acombination of various antioxidantsoccurring naturally in foods, need to bedetermined. A number of methods havebeen used to assess the total antioxidantcapacity of dietary plants (41-43). Thispaper focuses on omega-3 fatty acids andantioxidants in edible wild plants. EVOLUTIONARY ASPECTS OF DIET On the basis of estimates from studies inPaleolithic nutrition and modern-dayhunter-gatherer populations, it appears thathuman beings evolved consuming a dietthat was much lower in saturated fatty acidsthan is today’s diet (44). Furthermore, thediet contained small and roughly equalamounts of omega-6 and omega-3 PUFAs(ratio of 1-2:1) and much lower amounts of  trans fatty acids than does today’s diet (Fig.1) (45, 46). Wild plants contributed higheramounts of vitamin E and vitamin C, andother antioxidants than cultivated plants,providing additional protection againstcancer and atherosclerosis (7).The current Western diet is very high inomega-6 fatty acids (the ratio of omega-6 toomega-3 fatty acids is 10 - 20:1) because of the indiscriminate recommendation tosubstitute omega-6 fatty acids for saturatedfats to lower serum cholesterol concentrations(48). Table I compares the omega-6: omega-3intake of various populations (49-53). Thepopulation of Crete obtained a higher intakeof alpha-linolenic acid (ALA) from purslaneand other wild plants, walnuts and figs,whereas the Japanese obtained it from canolaoil and soybean oil (49).Intake of omega-3 fatty acids is muchlower today because of the decrease in fishconsumption and the industrial productionof animal feeds rich in grains containingomega-6 fatty acids, leading to productionof meat rich in omega-6 and poor in omega-3 fatty acids (54). The same is true forcultured fish (55) and eggs (56). Evencultivated vegetables contain fewer omega-3 fatty acids than do plants in the wild (57,58). In summary, modern agriculture, withits emphasis on production, has decreasedthe omega-3 fatty acid content in manyfoods: green leafy vegetables, animalmeats, eggs, and even fish. Although RDAsdo not officially exist, the Adequate Intake(AI) of essential fatty acids has beenestablished (59) as well as the ratio of 18:2 ω  6 to 18:3 ω  3 (60). EFFECTS OF DIETARY ALA COMPARED WITHLONG-CHAIN OMEGA-3 FATTY ACID DERIVATIVESON PHYSIOLOGIC INDEXES Several clinical and epidemiologic studieshave been conducted to determine the effects  265 SIMOPOULOS  Biol Res 37, 2004, 263-277  Figure 1. Hypothetical scheme of fat, fatty acid ( ω  -6, ω  -3, trans and total) intake (as percent of calories from fat) and intake of vitamins E and C (mg/d).Data were extrapolated from cross-sectional analyses of contemporary hunter-gatherer populationsand from longitudinal observations and their putative changes during the preceding 100 years.Trans fatty acids, the result of the hydrogenation process, have increased dramatically in the foodsupply during this century (46). TABLE I Omega-6:omega-3 ratios in various populations Populationomega-6:omega-3ReferencePaleolithic0.7950Greece prior to 19601.00 – 2.051Current US16.7450Current UK and Northern Europe15.0052Current Japan4.0053 Hunter Gatherer Agricultura IndustrialYears % calories from fat 40302010060010030100-4 x 106-10,0001,8001,9002,000 mg/day Vitamin CTotal fatVitamin ESaturatedTrans ω  -6 ω  -3  SIMOPOULOS  Biol Res 37, 2004, 263-277  266of long-chain omega-3 PUFAs on variousphysiologic indexes (7). Whereas the earlierstudies were conducted with large doses of fishor fish-oil concentrates, more recent studieshave used lower doses (14). ALA, theprecursor of omega-3 fatty acids, can beconverted to long-chain omega-3 PUFAs andcan therefore be substituted for fish oils. Theminimum intake of long-chain omega-3PUFAs needed for beneficial effects dependson the intake of other fatty acids. Dietaryamounts of linoleic acid (LA) as well as theratio of LA to ALA appear to be important forthe metabolism of ALA to long-chain omega-3PUFAs. Indu and Ghafoorunissa (61) showedthat while keeping the amount of dietary LAconstant, 3.7 g ALA appears to have biologicaleffects similar to those of 0.3 g long-chainomega-3 PUFA with conversion of 11 g ALAto 1 g long-chain omega-3 PUFA. Thus, a ratioof 4 (15 g LA: 3.7 g ALA) is appropriate forconversion. This ratio is also consistent withthe Lyon Heart Study (12). In human studies,Emken et al. (62) showed that the conversionof deuterated ALA to longer-chain metaboliteswas reduced by ~50 % when dietary intake of LA was increased from 4.7 % to 9.3 % of energy as a result of the known competitionbetween omega-6 and omega-3 fatty acids fordesaturation.Indu and Ghafoorunissa (61) furtherindicated that increasing dietary ALAincreases eicosapentaenoic acid (EPA)concentrations in plasma phospholipids afterboth 3 and 6 wk of intervention. Dihomo- γ  -linolenic acid (20:3 ω  6) concentrations werereduced but arachidonic acid (AA)concentrations were not altered. Thereduction in the ratio of long-chain omega-6PUFAs to long-chain omega-3 PUFAs wasgreater after 6 wk than after 3 wk. Indu andGhafoorunissa were able to showantithrombotic effects by reducing the ratioof omega-6 to omega-3 fatty acids withALA-rich vegetable oil. After ALAsupplementation there was an increase inlong-chain omega-3 PUFA in plasma andplatelet phospholipids and a decrease inplatelet aggregation. ALA supplementationdid not alter triacylglycerol concentrations.As shown by others, only omega-3 long-chain PUFAs have triacylglycerol-loweringeffects (63).In Australian studies, ventricularfibrillation in rats was reduced with canolaoil as much or even more efficiently thanwith fish oil, an effect attributable to ALA(64). Further studies should be able to showwhether this result is a direct effect of ALAper se or occurs as a result of itsdesaturation and elongation to EPA anddocosahexaenoic acid (DHA).The diets of Western countries havecontained increasingly larger amounts of LA, whish has been promoted for itscholesterol-lowering effect. It is nowrecognized that dietary LA favors oxidativemodification of LDL cholesterol (65, 66),and increases platelet response toaggregation (67). In contrast, ALA intake isassociated with inhibitory effects on theclotting activity of platelets, on theirresponse to thrombin (68, 69), and on theregulation of AA metabolism (70). Inclinical studies, ALA contributed tolowering of blood pressure (71). In aprospective epidemiological study, Ascherioet al. (72) showed that ALA is inverselyrelated to the risk of coronary heart diseasein men.ALA is not equivalent in its biologicaleffects to the long-chain omega-3 fattyacids found in marine oils. EPA and DHAare more rapidly incorporated into plasmaand membrane lipids and produce morerapid effects than does ALA. Relativelylarge reserves of LA in body fat, as arefound in vegans or in the diet of omnivoresin Western societies, would tend to slowdown the formation of long-chain omega-3fatty acids from ALA. Therefore, the role of ALA in human nutrition becomes importantin terms of long-term dietary intake. Oneadvantage of the consumption of ALA overomega-3 fatty acids from fish is that theproblem of insufficient vitamin E intakedoes not exist with high intake of ALAfrom plant sources. EDIBLE WILD PLANTS AS A SOURCE OF ALPHA-LINOLENIC ACID In view of the fact that a number of studiesindicate that 18:3 ω  3 (ALA) is converted toEPA and DHA in human beings, it is
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