Seaweed Lipids as Nutraceuticals

Ladislava MiSurcova,*'1 Jarmila Ambrozovâ/ and DuSan Samek*






Health Importance of PUFA


A. Significance of PUFAs in human diet


B. The o-6/o-3 ratio as health-promoting factor



Lipids and PUFAs in Seaweed


A. The variability of seaweed lipid composition


B. The lipid composition of seaweeds


C. Distribution of PUFAs in seaweed lipids



The Lipid Composition of Marine Microalgae







Abstract Seaweeds are known as low-energy food. Despite low lipid con tent, o-3 and o-6 polyunsaturated fatty acids (PUFAs) introduce a significant part of seaweed lipids. PUFAs are the important components of all cell membranes and precursors of eicosanoids that are essential bioregulators of many cellular processes. PUFAs effectively reduce the risk of cardiovascular diseases, cancer, ostheo-porosis, anddiabetes. Because ofthe frequent usage of seaweeds in Asia and their increasing utilization as food also in other parts of the world, seaweeds could contribute to the improvement of a low level of o-3 PUFAs, especially in the Western diet. The major

* Department of Food Technology and Microbiology, Faculty of Technology, Tomas Bata University in Zlin, Zlin, Czech Republic

{ Department of Food Analysis and Chemistry, Faculty of Technology, Tomas Bata University in Zlin, Zlin, Czech Republic

1 Corresponding author: Ladislava Misurcova, E-mail address: [email protected]

Advances in Food and Nutrition Research, Volume 64 © 2011 Elsevier Inc.

ISSN 1043-4526, DOI: 10.1016/B978-0-12-387669-0.00027-2 All rights reserved.

commercial sources of o-3 PUFAs are fish, but their wide usage as food additives is limited for the typical fishy smell, unpleasant taste, and oxidative nonstability. Nevertheless, growing requirements of healthy functional foods have led to produce PUFAs as nutraceuticals in controlled batch culture of marine microalgae, especially Thraustochytrium and Schizochytrium strains.


Lipids belong to fundamental nutrients for human. Their components are fatty acids (FAs), which could be classified to saturated (SFAs—without double bonds), monosaturated (MUFAs—with one double bond), and polyunsaturated FAs (PUFAs—with two or up to six double bonds). Humans are able to synthesize both SFAs and MUFAs. Nevertheless, PUFAs with the first bond on the third or sixth carbon atom are essential because of the inability to be synthesized by the human body. Thus, they have to be obtained from the diet. Their main sources are chloroplasts of higher plants and fat of water organisms.

Nowadays, essential FAs (EFAs) are considered to be functional food and nutraceuticals with many health benefits including the potential of reducing the risk of cardiovascular diseases (CVD), cancer, ostheoporosis, and diabetes. CVD have been believed to be the main cause of death in most Western countries. Coronary heart disease (CHD) is closely connected with a progress of atherosclerosis evoked by interactions between plasma lipids, lipoproteins, monocytes, platelets, endothelium, and smooth muscle of arterial walls, which results in narrowing of coronary arteries. Thus, the composition of dietary lipids is an important factor of genesis of hearth diseases together with the quality and alluviation of arterial walls. This could lead to thrombosis and finally to coronary infarctions.

Dietary pattern has been modified throughout the human evolution. The origin composition of a hunter-gathered diet with a lower intake of total fats has been altered by a higher intake of total lipids with a high representation of saturated and trans-FAs, which are detrimental for health. Contemporary Western human diet is noted for a low content of o-3 EFAs that results in an imbalance of o-3 and o-6 EFAs and in a progress of various pathophysiologies.


Dispensability of PUFAs for human has already been known for many decades. Oversized dietary intake of most SFAs and trans-FAs is harmful for health due to increasing the risk of CVD. The human body cannot synthesize PUFAs with the first double bond on the C3 and C6 from the methyl-end. These FAs are EFAs, and their level in the human body depends on their intake from the diet. EFAs form two biologically important groups which are o-3 and o-6 EFAs according to the location of their first double bond from the methyl-end of FAs. They are also called long chains o-3 and o-6 PUFAs (LCPUFAs). However, some recent studies have concluded that humans of every age could transform a-linolenic acid (ALA, 18:3, o-3) to docosahexaenoic acid (DHA, 22:6, o-3) but only in the insufficient concentration (Brenna, 2002; Brenna et al., 2009; Burdge and Calder, 2005; Burdge and Wootton, 2002).

In Fig. 27.1, there are shown the metabolic transformations of o-3 and o-6 PUFAs and their important derivates such as prostaglandins (PG), thromboxanes (TX), and leukotrienes (LK).

It is generally known that primary precursors of o-3 and o-6 EFAs are ALA and linoleic acid (LA), respectively. Both are formed by the gradual desaturation of oleic acid in the endoplasmic reticulum and chloroplasts of plantae. Because of the absence of A12 and A15 desaturases required for the synthesis of ALA from stearic acid (18:0), humans cannot synthesize ALA. It has to be obtained from the diet.

LCPUFAs are formed by series of reactions that are catalyzed by desaturases and elongases. Further, conversion of dietary ALA (18:3, o-3) into EPA (20:5, o-3) is limited because ALA and LA (18:2, o-6) compete for common desaturation and elongation enzymes. The affinity of A desaturase for ALA is greater than for LA (Burdge and Calder, 2005). It was proved that the relationship between ALA and LA is very important for the maintenance of their homeostasis. But the amount of ALA and LA in the diet is significant for ALA conversion to EPA (20:5, o-3) and DHA and not for their ratio (Goyens et al., 2006).

Polyunsaturated o-3 LCPUFAs have significant roles in many biochemical pathways which result in different health promotion activities. Generally, LCPUFAs show cardioprotective effect that results from their considerable anthiatherogenic, antithrombotic, anti-inflammatory, antiar-rhythmic, hypolipidemic effect and other health benefits, which are based on complex influence of concentrations of lipoproteins, fluidity of biological membranes, function of membraned enzymes and receptors, modulation of eicosanoids production, blood pressure regulation, and finally on the metabolism of minerals (Flachs et al., 2005; Hu et al., 2001; Kinsella et al., 1990; Tvrzicka et al., 2009; Weiss et al., 2005).

PUFAs of o-3 series have many pleiothropic metabolic effects as ligands of peroxisome proliferator-activated receptors (PPAR-a). It is assumed that the activation of PPAR-a results in decrease of lipogenesis and secretion of a very low density lipoprotein (VLDL), further in growth of lipoprotein lipase activity and decrease of apolipoprotein C-III concentration, and on increased reverse transport of cholesterol (Corton and Anderson, 2000; Olivieri et al., 2003; Tvrzicka et al., 2009).

Stearidonic acid (SDA; 18:4, ra-3)

- A6- Desaturase -(competition)


PG, TXA — Series 3 PGE3, PGH3, PGI3, TXA3 Leukotrienes — Series 5

Eicosatetraenoic acid Dihomo y-linolenic acid (ETA; 20:4, ra-3) (DGLA; 20:3, ra-6) r*-A5- Desaturase -H


— Series 1


, PGE1,



Docosapentaenoic acid (DPA; 22:5, ra-3)

Tetracosapentaenoic acid (24:5, ra-3)



PG, TX — Series 2 pgd2, pge2, PGF2B' pgh2, pgl2, txa2

Leukotrienes — Series 4

Docosatetraenoic acid (AA; 20:4, ra-6)

A6- Desaturase

Tetracosatetraenoic acid (24:4, ra-6)

Tetracosahexaenoic acid (24:6, ra-3)

Peroxisomal b-oxidation

Tetracosapentaenoic acid (24:5, ra-6)

Docosahexaenoic acid (DHA; 22:6, ra-3)

Docosapentaenoic acid (22:5, ra-6)

FIGURE 27.1 The metabolic transformation of o-3 and o-6 PUFAs and their derivates.

EPA and DHA are fundamental EPAs from o-3 series of LCPUFAs. DHA is the main structural component of cell membranes, at high level in brain tissue and retina. DHA is formed from EPA by peroxisomal p-oxidation (Burdge and Calder, 2005). EPA and DPA (22:5, o-3) can also be synthesized from DHA via p-oxidation in peroxisomes by catalytic activity of probably A-4 enoyl CoA reductase and A-2 enoyl CoA isomerase (Gr0nn et al., 1991).

The principal LCPUFA of o-6 series is arachidonic acid (AA; 20:4) acting as a precursor for eicosanoids synthesized from LA. LCPUFAs of o-6 series have been considered as activators of PPAR-g. Their metabolic effects include increased synthesis of cholesterol, increased activity of LDL receptors, increased activity of cholesterol 7 a-hydroxylase (Cyp 7A1), and decreased conversion of VLDL to LDL. As ligands of PPAR-g, o-6 PUFAs may improve insulin sensitivity, change fat distribution, and affect adipo-cyte differentiation (Chiang et al., 2001; Corton and Anderson, 2000).

Biological activities of individual EFAs might be derived from the course of their interactions. Their major derivates are eicosanoids, signaling molecules having important functions in many regulation systems and performing as messengers in the central nervous systems (Hertting and Seregi, 1989; Leslie and Watkins, 1985).

Eicosanoids are divided into four following classes: PG, TX, prostacy-clins, and LK. Further within each class, there are two or three series of eicosanoids. Eicosanoids derived from o-3 and o-6 FAs have antagonistic effects. Their amount depends on the composition of dietary FAs influenced by the competition with AA and EPA FAs as substrates for cycloox-ygenases and 5-lipoxygenases (Kinsella et al., 1990; Simopoulos, 2002a,b).

PG are oxygenated, unsaturated cyclic FAs responsible for the processes of many hormone-like actions. Arachidonic acid o-6 PUFA is converted to an unstable intermediate hydroxyl-endoperoxide prostaglandin H2 which is subsequently converted to PGE2 by the enzymatic activity of cyclooxygen-ase-2 (COX-2). PGE2 as proinflammatory eicosanoids have been related to carcinogenesis of breast and prostate, as well as cancer initiation (Kobayashi et al., 2006; Terry et al, 2003). EPA and DHA from marine oils inhibit COX-2 and suppress the production of PGE2. It has been proved that EPA and DHA also inhibit lipoxygenases contributing to synthesis of hydroxyeicosa-tetraenoic acids and LK. 12-Hydroxyeicosatetraenoic acid has been connected with the suppression of apoptosis, stimulation of angiogenesis, and further with stimulation of tumor cell adhesion (Rose, 1996).

A. Significance of PUFAs in human diet

Lipids represent one of the main sources of energy for human metabolic processes. Lipid consumption in most Western countries is relatively high with the contribution of approximately 40% of total calories (Narayan et al., 2006), despite the nutritious recommendation that 25% of energy should be covered by lipids (Sugano and Hirahara, 2000). Qualities of lipids are derived from their FAs composition which is various according to their sources. In general, vegetable oils from terrestrial plants are composed from SFAs and unsaturated FAs (UNFAs) with the chains formed by 16- and 18-carbon molecules, whereas the representation of individual FAs depends on plant species. Nevertheless, oils origined from marine organisms consist typically of UNFAs with the abundant amount of EPA and DHA, especially (Hu et al., 2001).

The absolute amount of lipids in the diet is not the main promoter of CVD. The important factor is relative concentration and distribution of dietary FAs with proved effects on lowering a risk of CVD (Cordain et al., 2002). Relative concentrations and distribution of dietary EFAs are different among various nationalities because of diverse dietary patterns. In Fig. 27.2, there are demonstrated trends of the total male and female mortality (CHD, CVD) in different countries in comparison with the distinct dietary intake of LCPUFAs. There is an evident dependency of the highest mortality in the countries with the lowest intakes of dietary n-3 LCPUFAs. The graphs have been constructed from data of several studies (Astorg et al., 2004; Hibbeln et al., 2006; Kris-Etherton et al., 2000; Meyer et al., 2003; Miyake et al., 2010).

Typical Western diet with oversized intake of o-6 PUFAs (LA-rich oils from vegetable sources) leads to overproduction of proinflammatory o-6 PG and cytokines, which could be suppressed by higher intake of o-3 PUFAs from fish oils. Simopoulos (2002a,b) reported that high intake of ALA (about 15 g/day) would suppress human protein interleukin (IL-1) and tumor necrosis factor.

Many studies have been conducted on marine fish oil consumption and relation to risk of breast or prostate cancer. The inhibition of eicosa-noids production from o-6 PUFAs by higher consumption of fish oil with high levels of o-3 PUFAs, which is a common feature of lowering a cancer risk, was reported (Bagga et al., 1997; Terry et al., 2004).

Eicosanoids derived from AA are biologically active in small quantities. Their large amounts lead to the formation of thrombi and atheromas, and to the development of allergic and inflammatory disorders (Simopoulos, 2002a,b). In general, o-6 PUFAs have been associated with the enhancement of the promotional phase of mammary carcinogenesis (Rose, 1997).

However, contradictory results of studies on the effect of o-3 and o-6 PUFAs have been reported. It has been shown that AA also inhibits the growth of A549 human lung adenocarcinoma cells, even though DHA has been more effective than AA (Trombetta et al., 2007).

Differences between cis- and trans-configuration of PUFAs and the implication of their dietary intake on the human health have also been

USA Australia France Japan

FIGURE 27.2 Trends of total man and female mortality (CHD, CVD) in some countries with dietary intake of LCPUFAs.

USA Australia France Japan

FIGURE 27.2 Trends of total man and female mortality (CHD, CVD) in some countries with dietary intake of LCPUFAs.

reported. Trans isomers of monounsaturated octadecenoic acid (C18:1) were found as the most common trans-FAs in the diet of many European countries (Hulshof et al., 1999).

Recommended intakes of o-3 LCPUFAs were often discussed in the scientific quarters and varied in different countries because of dissimilar dietary intake of o-3 LCPUFAs. Approximate estimation of the consumption of o-3 LCPUFAs is 0.1-0.5 g/day in Europe, 0.1-0.2 g/day in the United States, while in Japan, it is higher up to 2 g/day (Gomez Candela et al., 2011) due to higher consumption of fish.

B. The m-6/m-3 ratio as health-promoting factor

The significance of the o-6/o-3 ratio has also been discussed many times in research papers within the context of evolutionary aspects of the human diet. The origin ratio of o-6/o-3 was 1. Nowadays, the new lifestyle with the alteration of dietary pattern has caused the change of dietary intake of lipids, especially the distribution of o-3 and o-6 PUFAs in Western countries. At the beginning of the twentieth century, the consumption of vegetable oils and fats has risen. These oils and fats are responsible for an excessive dietary level of o-6 PUFAs and a lowering concentration of o-3 PUFAs in the Western diet (Cordain et al., 2005). Further contributor of altered composition of received FAs is the oversized consumption of margarine and shortening produced from refined vegetable oils by hydrogenation process resulting in the production of trans-isomers of FAs (Hu et al., 2001). The modification of present dietary pattern has led to higher intake of o-6 PUFAs and that has caused an increase of the o-6/o-3 ratio up to 20-30:1 (Gomez Candela et al., 2011). The relationship between low o-6/ffl-3 ratio and rare occurrence of CHD in Inuits has already been described (Bjerregaard et al., 2003). The significance of the balance of the o-6/o-3 ratio is based on the fact that mammalian cells cannot convert o-6 to o-3 FAs due to the absence of the converting enzyme, omega-3 desaturase (Simopoulos, 2006). However, the significance of this ratio has been challenged on behalf of separate recommendations for ALA, marine o-3 PUFAs, and LA (de Deckere et al., 1998).

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