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The evolution of omega-3 fatty acids in the human diet
Abstract
The evolution of the human diet over the past 10,000 years has lead to considerable changes in dietary fatty acid composition, predominately omega-3 polyunsaturated fatty acids (n-3 PUFA). The diets of our Paleolithic ancestors consisted of wild plant and animal foods abundant in alpha-linolenic acid (ALA), eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA). With the domestication of animals and plants during the Agricultural Revolution, shifts in the macro and micro-nutrient composition of formerly wild foods initiated the elimination of n-3 PUFA from the diet. Over the past 100 years the Industrial Revolution resulted in a manufactured diet that the human genome was not adapted to, abundant in refined grains, as well as fats and oils rich in n-6 PUFA while deficient in n-3 PUFA. The current fatty acid imbalance of Western diets hinders the conversion of ALA to n-3 long-chain (LC)PUFA, an already inefficient pathway utilizing non-evolved enzymatic machinery. Recently, several professional health organizations have outlined recommendations for n-3 PUFA, with the latest dietary guidelines targeting a minimum intake of 250 mg/day of EPA+DHA for adults. Despite these recommendations, current intakes of n-3 PUFA in Western diets are low and challenges regarding availability, safety and sustainability of fish resources exist. Taken together, a new era of n-3 PUFA enriched functional foods and dietary supplements is emerging to enhance n-3 PUFA intakes. This review explores the evolution of n-3 PUFA in the human diet and emphasizes recent recommendations and novel dietary options to realign our modern fatty acid intake with our Paleolithic genome.
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With increasing interest in the potential effects of n-6 and n-3 fatty acids in early life, there is a need for data on the dietary intake of polyunsaturated fatty acids (PUFA) in low-income countries. This review compiles information on the content in breast milk and in foods that are important in the diets of low-income countries from the few studies available. We also estimate the availability of fat and fatty acids in 13 low-income and middle-income countries based on national food balance sheets from the United Nations' Food and Agriculture Organization Statistical Database (FOASTAT). Breast milk docosahexaenoic acid content is very low in populations living mainly on a plant-based diet, but higher in fish-eating countries. Per capita supply of fat and n-3 fatty acids increases markedly with increasing gross domestic product (GDP). In most of the 13 countries, 70-80% of the supply of PUFA comes from cereals and vegetable oils, some of which have very low α-linolenic acid (ALA) content. The total n-3 fatty acid supply is below or close to the lower end of the recommended intake range [0.4%E (percentage of energy supply)] for infants and young children, and below the minimum recommended level (0.5%E) for pregnant and lactating women in the nine countries with the lowest GDP. Fish is important as a source of long-chain n-3 fatty acids, but intake is low in many countries. The supply of n-3 fatty acids can be increased by using vegetable oils with higher ALA content (e.g. soybean or rapeseed oil) and by increasing fish production (e.g. through fish farming).
Despite progress made in post-myocardial infarction (MI) revascularization and background therapy for the failing heart, the prevention of adverse cardiac remodeling associated with severe rhythm disorders remains an important drug target. Part of the remodeling can be counteracted by modulating the activity of ion channels and exchangers by omega-3 acids eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA). In the GISSI-Prevenzione and GISSI-HF trials, omega-3 fatty acids were administered as ethyl esters (Omacor Solvay Pharmaceuticals) and not as triglycerides present in fish oil. Ethyl esters result in a sustained intestinal absorption of EPA and DHA and require various purification steps during production, thereby minimizing the content of environmental toxins. Also the rather high (38%) DHA content of Omacor should not be ignored since in rats with low dose intake of omega-3 acids, DHA but not EPA inhibited ischemia-induced arrhythmias. In patients on multiple tablets, 840 mg EPA+DHA in one capsule is preferred to increase compliance. It is not justified to refer to Omacor as "n-3 polyunsaturated fatty acid supplementation" or even "fish oil" and, based on controlled clinical trials, there is no evidence that fish oil could be a substitute of Omacor. To avoid further confusion, guidelines should be precise and refer to the medication, eg, as in NICE guideline CG48: "Omega-3-acid ethyl esters treatment licensed for secondary prevention post-MI." The anti-arrhythmogenic action of Omacor should be seen in the context of implantable cardioverter-defibrillator trials (DINAMIT, IRIS) where non-sudden death was increased and total mortality unaltered. However, Omacor administered in the GISSI-HF trial reduced the incidence of severe arrhythmic events and mortality. Also in the GISSI-Prevenzione trial, arrhythmic death and mortality were reduced. At higher dosages (daily, 3-4 g) Omacor exhibits more pronounced cardiovascular benefits and, as a licensed indication, improves hypertriglyceridemia and related lipid parameters.
It is becoming clear that an adequate level of long-chain highly unsaturated fatty acids in the nervous system is required for optimal function and development; however, the ability of infants to biosynthesize long-chain fatty acids is unknown. This study explores the capacity of human infants to convert 18-carbon essential fatty acids to their elongated and desaturated forms, in vivo. A newly developed gas chromatography/negative chemical ionization/mass spectrometry method employing 2H-labeled essential fatty acids allowed assessment of this in vivo conversion with very high sensitivity and selectivity. Our results demonstrate that human infants have the capacity to convert dietary essential fatty acids administered enterally as 2H-labeled ethyl esters to their longer-chain derivatives, transport them to plasma, and incorporate them into membrane lipids. The in vivo conversion of linoleic acid (18:2n6) to arachidonic acid (20:4n6) is demonstrated in human beings. All elongases/desaturases necessary for the conversion of linolenic acid (18:3n3) to docosahexaenoic acid (22:6n3) are also active in the first week after birth. Although the absolute amounts of n-3 fatty acid metabolites accumulated in plasma are greater than those of the n-6 family, estimates of the endogenous pools of 18:2n6 and 18:3n3 indicate that n-6 fatty acid conversion rates are greater than those of the n-3 family. While these data clearly demonstrate the capability of infants to biosynthesize 22:6n3, a lipid that is required for optimal neural development, the amounts produced in vivo from 18:3n3 may be inadequate to support the 22:6n3 level observed in breast-fed infants.
We examined the effect of altering the linoleic acid (LA, 18:2n-6) to α-linolenic acid (ALA, 18:3n-3) ratio in the dietary fats of 3 day old piglets fed formula for 3 weeks. The LA-ALA ratios of the experimental formulas were 0.5:1, 1:1, 2:1, 4:1, and 10:1. The level of LA was held constant at 13% of total fats while the level of ALA varied from 1.3% (10:1 group) to 26.8% (0.5:1 group). Incorporation of the n-3 long chain PUFA EPA and 22:5n-3 into erythrocytes, plasma, liver, and brain tissues was linearly related to dietary ALA. Conversely, incorporation of DHA into all tissues was related to dietary ALA in a curvilinear manner, with the maximum incorporation of DHA appearing to be between the LA-ALA ratios of 4:1 and 2:1. Feeding LA-ALA ratios of 10:1 and 0.5:1 resulted in lower and similar proportions of DHA in tissues despite the very different levels of dietary ALA (1.3 vs. 26.8% of total fats, respectively).
These results are relevant to term infant studies in that they confirm our earlier findings of the positive effect on DHA status by lowering the LA-ALA ratio from 10:1 to 3:1 or 4:1, and they predict that ratios of LA-ALA below 4:1 would have little further beneficial effect on DHA status.
This editorial refers to ‘The effect of micronutrient supplementation on quality-of-life and left ventricular function in elderly patients with chronic heart failure’† by K.K.A. Witte et al., on page 2238
The incidence of chronic heart failure (CHF), the common end-result of most cardiac diseases, is increasing steadily in most countries.1 In recent years, most of the research efforts on CHF have focused on drug therapies and devices (implantable defibrillators and resynchronization), and little attention has been paid to non-pharmacological approaches, and particularly to nutrition. Only recently, it has been recognized that increased oxidative stress, for instance, may be involved in the pathogenesis of CHF.2 The intimate link between diet and oxidative stress is obvious, knowing that our body derives its main antioxidant defences from essential nutrients (meaning that they are necessarily obtained from foods).
Although it is generally considered that a diet high in sodium is harmful (and may result in acute decompensation of CHF through a volume overload mechanism), little is known about the other aspects of diet in CHF, in terms of both general nutrition and micronutrients, such as vitamins and minerals. In CHF patients, it is important not only to properly screen for and aggressively treat the traditional risk factors of coronary heart disease (CHD) (the main cause of CHF), such as high blood pressure and cholesterol (because they can aggravate the syndrome), but also to recognize and correct malnutrition and deficiencies in specific micronutrients. Some macronutrients such as essential fatty acids (discussed subsequently) may even be critical.
Witte et al .3 report the results of a double-blind trial testing the effects of micronutrient supplementation in patients with overt CHF. In spite of some obvious limitations (small sample size, no biological measurements to evaluate the degree of malnutrition in these patients, and no evaluation of …
*Corresponding author: Laboratoire NVMCV, UFR de Medecine et Pharmacie, Domaine de la Merci, 38706 La Tronche, Grenoble, France. E-mail address : michel.delorgeril{at}ujf-grenoble.fr
Prevention of cardiovascular diseases by paleolithic or hunter-gatherer diets has been discussed during recent years.
Our aim was to assess the effect of a paleolithic diet in a pilot study on healthy volunteers during 3 weeks. The intention was to include 20 subjects, of whom 14 fulfilled the study. Complete dietary assessment was available for six subjects.
Mean weight decreased by 2.3 kg (P<0.001), body mass index by 0.8 (P<0.001), waist circumference by 0.5 cm (P=0.001), systolic blood pressure by 3 mm Hg (P=0.03) and plasminogen activator inhibitor-1 by 72% (P=0.020). Regarding nutrient intake, intake of energy decreased by 36%, and other effects were also observed, both favourable (fat composition, antioxidants, potassium-sodium rate) and unfavourable (calcium).
This short-term intervention showed some favourable effects by the diet, but further studies, including control group, are needed.
This report addresses the current controversy about possible health hazards of dietary trans fatty acid isomers, which are created during hydrogenation of unsaturated fats to change their textural properties and melting points. Estimates of intakes are approximations based on limited data and problematic analytic techniques. Major contributors in the diet are fried and baked foods and margarine, in which partially hydrogenated vegetable oils may replace fat sources richer in saturated fatty acids and cholesterol. Consumption of trans fatty acids in the United States has been relatively constant, and new food technologies are yielding decreases in the trans fatty acid content of commercially prepared foods. When intake of trans fatty acids (as hydrogenated fat) is compared with that of saturated fat, total and low- density-lipoprotein (LDL)-cholesterol concentrations in blood are lower, but both trans fats and saturated fats increase total and LDL concentrations when compared with cis fatty acids or native unhydrogenated fat. Epidemiologic data are conflicting with respect to cardiovascular disease outcomes. We cannot conclude that the intake of trans fatty acids is a risk factor for coronary heart disease nor can we expect that substituting trans- for cis- containing fats will reduce the risk of coronary heart disease. Few rigorous studies have dealt with biomedical effects of trans fatty acids and possible mechanisms relevant to human health and diseases. The nutrition labeling issue is unresolved. The options, recommendations, and research suggestions in this report should outline for nutrition scientists the database needed before any new dietary recommendations or changes in nutrition policy concerning trans fatty acids can be made. The debate about trans fatty acids should not detract from dietary recommendations to limit the intake of saturated fat and total fat.
The purpose of this study was to investigate the effects of consuming a novel docosahexaenoic acid (DHA)-enriched shell egg on the serum lipid levels and ω−3 polyunsaturated fatty acids (n−3 PUFA) of serum phospholipid in statin-treated hypercholesterolemic patients. Fifteen subjects were randomly divided into two treatment groups and consumed either two control or two novel DHA-enriched eggs during two organized breakfast periods of 21 consecutive days each using a double-blinded, cross-over design. The novel enriched eggs from feeding the specialty ration provided 217mg of DHA and 629mg of total n−3 PUFA per day. Total serum cholesterol levels were unchanged with either egg consumption and no significant alterations in lipid levels were found due to a treatment effect. The novel egg group exhibited a significant rise in eicosapentaenoic acid (EPA) plus DHA levels in serum phospholipid (by 23%) which can be related to a reduced risk for fatal ischemic heart disease. Consumption of this novel egg offers an alternative food option for more than doubling current sub-optimal DHA intakes in North America.
Following the comprehensive systematic review of domestic and overseas scientific evidence, the "Dietary Reference Intakes for Japanese, 2005 (DRI-J)" was published in April, 2005. The DRIs-J were prepared for health individuals and groups and designed to present a reference for intake values of energy and 34 nutrients to maintain and promote health and to prevent lifestyle-related diseases and illness due to excessive consumption of either energy or nutrients. The DRI-J also includes a special chapter for basic knowledge of DRIs. The energy recommendation is provided as an estimated energy requirement (EER), while five indices were used for nutrients: Estimated average requirement (EAR), recommended dietary allowance (RDA), adequate intake (AI), tolerable upper intake level (UL), and tentative dietary goal for preventing lifestyle-related [chronic non-communicable] diseases (DG). Whilst the first four indices are same as the ones used in other countries, DG is unique index in Japan, which was set as a reference value for preventing non-communicable diseases such as cardiovascular (including hypertension), major types of cancer and osteoporosis. This report (DRI-J) is the first dietary guidance in Japan, which applied evidence-based approach utilizing a systematic review process. Only a few articles from within Japan and other Asian countries could be used for its establishment. The project to establish the DRI-J revealed a severe lack of researchers and publications focused upon establishing DRIs for Japanese. Further review is therefore required in preparation for the next revision scheduled in 2010.
Growing evidence suggests that omega-3 long chain polyunsaturated fatty acids (VLC-PUFAs), especially eicosapentaenoic acid (EPA; 20:5Δ5,8,11,14,17) and docosahexaenoic acid (DHA; 22:6Δ4,7,10,13,16,19) play critical roles in human health and development. VLC-PUFAs are mainly found in fish, some fungi, marine bacteria and microalgae. Currently, the predominant dietary sources of VLC-PUFAs are marine fish and seafood. However, the increasing demand for fish and fish oils is putting enormous pressure on marine ecosystems leading to a depletion of fish stocks while commercial cultivation of marine microorganisms and aquaculture are not sustainable and cannot compensate for the shortage in fish supply. Therefore, there is an obvious requirement for an alternative and sustainable source for VLC-PUFAs. Over the last decade, many genes encoding the primary VLC-PUFAs biosynthetic activities became available providing a toolkit for the "reverse-engineering" of transgenic plants to produce fish oils. In this review, we will describe the recent advances in this field and the insights they give us into the complexities of metabolic engineering of oil-seed crops producing VLC-PUFAs.
High intakes of linoleic acid (LA,18:2n-6) have raised concern due to possible increase in arachidonic acid (ARA, 20:4n-6) synthesis, and inhibition of alpha linolenic acid (ALA, 18:3n-3) desaturation to eicosapentaenoic (EPA, 20:5n-3) and docosahexaenoic acid (DHA, 22:6n-3). In healthy men, 10.5% energy compared to 3.8% energy LA with 1% energy ALA increased plasma phospholipid LA and 20:2n-6, the elongation product of LA, and decreased EPA, with no change in ARA. However, LA was inversely related to ARA at both 10.5% energy and 3.8% energy LA, (r=-0.761, r=-0.817, p<0.001, respectively). A two-fold variability in ARA among individuals was not explained by the dietary LA, ARA, ALA, or fish intake. Our results confirm LA requirements for ARA synthesis is low, <3.8% energy, and they suggest current LA intakes saturate Delta-6 desaturation and adversely affect n-3 fatty acid metabolism. Factors other than n-6 fatty acid intake are important modifiers of plasma ARA.
A clinical case of linoleic acid deficiency has been investigated because of the unknown effect in an adult man. The patient had had all but 60 cm of his small intestine removed and was maintained solely by intravenous therapy for 100 days, without fat. At this stage there was no clinical evidence of malnutrition, but his serum phospholipids were found to contain 10% 5,8,11 eicosatrienoic acid and he developed a skin rash. A soybean fat emulsion containing 86 g/l of linoleic acid was given intravenously for 12 days, discontinued for 43 days and then resumed. During each period of fat administration (linoleic acid intake 22.8 g/day) the serum phospholipid content of eicosatrienoic acid fell and arachidonic acid rose. Simultaneously the serum triglycerides fell to normal, the proportions of the triglycerides carried by the lipoproteins (d < 1.006) rose to normal and the rash disappeared. A second case of linoleic acid deficiency, in this instance associated with severe malnutrition, was investigated and here also a high level of plasma triglycerides was mostly associated with lipoproteins with d < 1.006. In an attempt to estimate his minimal daily requirements, feeding 7.5 g/day of linoleic acid in this form did not eliminate the eicosatrienoic acid, but instead allowed a small increase. It is concluded that adult man requires at least 7.5 g/day of linoleic acid and that the proportion of the triglycerides carried by the very low density lipoproteins is lowered in the absence of linoleic acid.Copyright © 1971 S. Karger AG, Basel
Samples of crude fish oil have been refined, and the crude fish oil together with samples taken out after each step of the refining process have been analysed for organochlorine pesticides and PCB (quantified both as CB congeners and total PCB). The levels of organochlorine contaminants in fish oils remain almost constant during the neutralisation and bleaching steps of the refining process. The deodorisation step seems to cause a decrease in the amount of contaminants, especially for the most volatile compounds (alpha-HCH, lindane, HCB) where the levels were reduced to below the detection level. Concentrations of the less volatile organochlorine pesticides (dieldrin, p,p'-DDE and p,p'-DDD) and PCB are reduced to about half the concentration in the crude fish oil.
Vegetarians have lower platelet and plasma concentrations of n-3 polyunsaturated fatty acids (PUFAs) than do omnivores. We recently showed that male vegetarians have higher platelet aggregability than do omnivores.
We investigated whether male vegetarians (n = 17) who consumed an increased amount of dietary alpha-linolenic acid (ALA) showed any changes in their tissue profile of PUFAs, plasma thromboxane concentrations, platelet aggregability, or hemostatic factors.
During the study, all subjects maintained their habitual vegetarian diets except that a proportion of dietary fat was replaced with vegetable oils and margarines that were provided. Initially, all subjects consumed a low-ALA diet (containing safflower oil and safflower oil-based margarine) for 14 d; they then consumed either a moderate-ALA diet (containing canola oil and canola oil-based margarine) or a high-ALA diet (containing linseed oil and linseed oil-based margarine) for 28 d. Blood samples were collected at day 0 (baseline), day 14, and day 42.
Eicosapentaenoic acid, docosapentaenoic acid, total n-3 PUFAs, and the ratio of n-3 to n-6 PUFAs were significantly increased (P < 0.05), whereas the ratio of arachidonic acid to eicosapentaenoic acid was decreased (P < 0.05), in platelet phospholipids, plasma phospholipids, and triacylglycerols after either the moderate-ALA or high-ALA diet compared with the low-ALA diet. No significant differences were observed in thrombotic risk factors.
ALA from vegetable oils (canola and linseed) has a beneficial effect on n-3 PUFA concentrations of platelet phospholipids and plasma lipids in vegetarian males.
Vegans do not consume meat and fish and have therefore low intakes of long chain polyunsaturated fatty acids (LCP). They may consequently have little negative feedback inhibition from dietary LCP on conversion of alpha -linolenic acid (ALA) to the LCP omega 3 eicosapentaenoic (EPA) and docosahexaenoic (DHA) acids. We investigated whether supplementation of nine apparently healthy vegans with 2.01 g ALA (4 ml linseed oil), 1.17 g gamma-linolenic acid (GLA) (6 ml borage oil) or their combination increases the LCP omega 3 contents of erythrocytes (RBC) and platelets (PLT), and of plasma phospholipids (PL), cholesterol esters (CE) and triglycerides (TG). The supplements changed the dietary LA/ALA ratio (in g/g) from about 13.7 (baseline) to 6.8 (linseed oil), 14.3 (borage oil) and 6.4 (linseed + borage oil), respectively. ALA or GLA given as single supplements did not increase LCP omega 3 status, but their combination augmented LCP omega 3 (in CE) and EPA (in fasting TG) to a statistically significant, but nevertheless negligible, extent. We conclude that negative feedback inhibition by dietary LCP, if any, does not play an important role in the inability to augment notably DHA status by dietary ALA. The reach of a DHA plateau already at low dietary ALA intakes suggests that dietary DHA causes a non-functional DHA surplus, or is, alternatively, important for maintaining DHA status at a functionally relevant level.
Concentrations of 160 polychlorinated biphenyl (PCB) congeners or congener groups were determined in approximately 600 farmed Atlantic salmon from around the world and wild (ocean-caught) Pacific salmon from the Northeast Pacific. Concentrations and PCB congener profiles were analyzed to provide insight into the sources and uptake of PCBs in salmon as well as regional differences. Although total PCB concentrations in wild salmon appeared to be correlated to total lipid content, the increased proportion of total lipids in the farmed salmon could not account for the much greater PCB concentrations. We investigated the PCB congener patterns of hundreds of salmon samples using principal component analysis to further illuminate regional and species differences. Three major PCB patterns were observed, in most wild fish (except British Columbia and Oregon chinook), in farmed fish from the Atlantic, and in most farmed fish from the Pacific. The PCB congener profiles of farmed salmon often closely corresponded to a sample of commercial feed purchased in the same region, indicating that the feed is likely to be the major source of PCBs for farmed salmon. In such cases where PCB profiles in fish and feed were similar, a comparison of congener concentrations in fish and the feed showed that the majority of congeners, with some notable exceptions, were bioaccumulative to the same extent, irrespective of physical properties.
The US Food and Drug Administration's final ruling on trans-fatty acid labeling issued in 2003 has caused a rapid transformation in the fat and oil industries. Novel ingredients and improved technologies are emerging to replace partially hydrogenated fats in foods. We present an overview of the structure and formation of trans fatty acids in foods, and a comprehensive review of the newly formulated products and current procedures practiced by the edible oil industry to reduce or eliminate trans fatty acids in response to the Food and Drug Administration's regulations mandating trans fat labeling of foods.