Trends in Food Science & Technology 19 (2008) 31e39

In the search of new

functional food

ingredients from

algae

Merichel Plaza, AlejandroCifuentes and Elena Ibanez*

Institute of Industrial Fermentations (CSIC), Juan de la

Cierva 3, 28006 Madrid, Spain; (Tel.: D34 91

5622900x388; fax: D34 91 5644853; e-mail: elena@ifi.csic.es)

The well-known correlation between diet and health demon-

strates the great possibilities of food to maintain or even improve

our health. This fact has brought about a great interest for seeking

new products that can contribute to improve our health and

well-being. This type of foods able to promote our health has ge-

nerically been defined as functional foods. Nowadays, one of

the main areas of research in Food Science and Technology is

the extraction and characterization of new natural ingredients

with biological activity (e.g., antioxidant, antiviral, antihyperten-

sive, etc.) that can contribute to consumer’s well-being as part of

new functional foods. The present work shows the results of a bib-

liographic revision done on the chemical composition of different

macroalgae togetherwithacriticaldiscussionabout theirpotential

as natural sources of new functional ingredients.

IntroductionThe economic, cultural and scientific development of

our society has given rise to important changes in ourfood habits and life-style. For example, diets in developedcountries are highly caloric, rich in saturated fats andsugars, while the consumption of complex carbohydratesand dietetic fiber is low. This fact, together with a decreasein physical activity, has given rise to an increase of obesityproblems, and along with it, a raise in the incidence of heartdiseases, diabetes and hypertension in the population(Geslain-Laneelle, 2006).

* Corresponding author.

0924-2244/$ - see front matter � 2007 Published by Elsevier Ltd.doi:10.1016/j.tifs.2007.07.012

Review

The increasing number of scientific papers published forthe last two decades correlating diet and some chronic dis-eases has shown the extraordinary possibilities of foods tosupport, or even to improve, our health (Palanca, Rodri-guez, Senorans, & Reglero, 2006; Roche, 2006). As a con-sequence, nowadays, there is a huge interest amongconsumers and food industry on products that can promotehealth and well-being (Sloan, 1999). These foods have beengenerically named functional foods.

The concept of functional food as a mean to protect con-sumer’s health was developed at the beginning of the 1980sin Japan, as a way to reduce the high health costs derivedfrom a population with high life expectations (Arai,1996). In Europe, in the second half of the 1990s, a workinggroup coordinated by the European Section of the Interna-tional Life Science Institute (ILSI) and supported by theEuropean Commission, was created to promote inside theIV Framework Program the action FUFOSE (FunctionalFood Science in Europe) to stimulate the scientific studyon functional foods. From this project a definition for func-tional food was generated. Namely, a food can be consid-ered ‘‘functional’’ if, besides its nutritious effects, it hasa demonstrated benefit for one or more functions of the hu-man organism, improving the state of health or well-beingor reducing the risk of disease (Diplock et al., 1999). In thisdefinition it is necessary to emphasize three important andnew aspects: (a) the functional effect is different that thenutritious one; (b) the functional effect must be demon-strated satisfactorily; and (c) the benefit can consist in animprovement of a physiological function or in a reductionof risk of developing a pathological process. Besides, thefunctional foods must have a series of additional character-istics as, for instance, the need of effectiveness in theirbeneficial action at the normal consumed doses.

In the future, functional foods will be regulated by thenew guideline approved in December 2006, by the Euro-pean Union (Regulation (CE) 1924/2006 of the EuropeanParliament and of the Council, December 20, 2006: nutri-tion and health claims made on foods). In this regulationthe nutritional allegations and/or healthy properties of thenew products are regulated, including their presentation,labeling and promotion.

The beneficial action exercised by functional foods (seeTable 1 for some examples) is due to a component or a seriesof ingredients that either are not present in the analogousconventional food or are present at lower concentrations.

32 M. Plaza et al. / Trends in Food Science & Technology 19 (2008) 31e39

These ingredients are called functional ingredients. Thus,foods were initially enriched with vitamins and/or minerals,such as vitamin C, vitamin E, folic acid, zinc, iron, and cal-cium (Sloan, 2000). Later, the approach changed to enrichfoods with several micronutrients such as u3 fatty acids,linoleic acids, phytosterols, soluble fiber (inulin and fructoo-ligosaccharides, called prebiotics), etc., trying to promoteconsumers health or to prevent different diseases (Hasler,1998; Sloan, 2002; Unnevehr & Hasler, 2000). Also, foodscan be changed to contain or enriched with viable microor-ganisms that can benefit human health; these products arecalled probiotics and are able to improve the activity inthe intestinal tract and the immune system, among otherfunctions. Usually the microorganisms added to the foodare lactic acid bacteria including Lactobacillus acidophilus,Lactobacillus johnsonii, Lactobacillus reuteri, Lactobacilluscasei shirota, etc. (Sanders, 1999).

Algae are photosynthetic organisms, which possess re-productive simple structures. These organisms constitutea total of 25e30,000 species, with a great diversity of formsand sizes, and that can exist from unicellular microscopicorganisms (microalgae) to multicellular of great size (mac-roalgae). Algae can be a very interesting natural source ofnew compounds with biological activity that could be usedas functional ingredients. In fact, some algae are organismsthat live in complex habitats submitted to extreme conditions

Table 1. Some examples of functional foods and functional ingredi-ents together with their possible effect on human health (accordingto Hasler, 2002)

Functional food Functionalingredients

Possible health effect

Chocolate Flavonoids(procyanidins)

Reduce LDL cholesterol

Green tea Catechins Reduce risk of certaintypes of cancer

Tomatoes andprocessed tomatoproducts

Lycopene Reduce risk of certaintypes of cancer

Red wine Polyphenoliccompounds

Reduce risk of certainheart diseases

Fatty fish (n-3) Fatty acids Reduce risk of certainheart diseases

Fermented dairyproducts

Probiotics Support intestinal tracthealth, boost immunity

Cruciferous Glucosinolates,indoles

Reduce risk of certaintypes of cancer

Lamb, turkey, beef,dairy

Conjugatedlinoleic acids(CLA)

Reduce breast cancer

Cranberry juice Proanthocyanidins Reduce urinary tractinfections

Fortified margarines Plant sterol andstanol esters

Reduce total and LDLcholesterol

Fortified juice Soluble fiber Reduce total and LDLcholesterol

Garlic Organosulfurcompounds

Reduce total and LDLcholesterol

(for example, changes of salinity, temperature, nutrients,UVevis irradiation), therefore, they must adapt rapidly tothe new environmental conditions to survive, producinga great variety of secondary (biologically active) metabo-lites, which cannot be found in other organisms (Carlucci,Scolaro, & Damonte, 1999). Also, considering their greattaxonomic diversity, investigations related to the search ofnew biologically active compounds from algae can be seenas an almost unlimited field.

Besides its natural character, other important aspects re-lated to the algae are their easy cultivation, their rapidgrowing (for many of the species) and the possibility ofcontrolling the production of some bioactive compoundsby manipulating the cultivation conditions. In this way, al-gae and microalgae can be considered as genuine naturalreactors being, in some cases, a good alternative to chemi-cal synthesis for certain compounds. Moreover, one of theleast studied aspects, which is one of the research lines ofour group, is the development of more appropriate, fast,cost-effective and environmental-friendly extraction proce-dures able to isolate the compounds or compounds of inter-est from these natural sources.

ObjectiveAt present, one of the principal research lines in Food

Science and Technology is the extraction and characteriza-tion of new functional ingredients of natural origin. In ourlaboratory, we have studied for years different natural sour-ces of functional ingredients including plants, spices, etc.(Cifuentes, Bartolome, & Gomez-Cordoves, 2001; Ibanezet al., 1999, 2001; Senorans et al., 2001). Recently, wehave started a new line of investigation in which differentalgae and microalgae are being studied as possible naturalsources of functional ingredients (Herrero, Ibanez, Senor-ans, & Cifuentes, 2004; Herrero, Simo, Ibanez, & Cifuentes,2005), combining their use with clean extraction technolo-gies based on sub- and supercritical fluids (Jaime et al.,2005; Mendiola et al., 2005).

The objectives of this review paper are first to presentthe results obtained of a detailed bibliographical searchabout the composition of different algae and, secondly, todiscuss their possibilities as new sources of functional in-gredients. The information provided on the different algaedoes not refer in many cases to the same constituents sinceit has been taken from different research papers with differ-ent objectives. Nevertheless, we believe the informationprovided can be useful to many research groups consideringthe huge interest in the search for new natural sources offunctional ingredients.

Chemical composition of different algaeThe species of algae described in this work are macro-

algae (namely, Sargassum vulgare, Undaria pinnatifida,Himanthalia elongata, Chondrus crispus, Porphyra sp.,

33M. Plaza et al. / Trends in Food Science & Technology 19 (2008) 31e39

Cystoseira spp. and Ulva spp.) and have been selected con-sidering their potential as natural sources of new functionalingredients. Also, an important factor to consider here wasthe low toxicity of the selected varieties, assuming that anyhypothetical new functional ingredient obtained from themcould be used for the future development of new functionalfoods.

S. vulgareS. vulgare belongs to the group of brown algae that have

been traditionally consumed in the East countries. The dif-ferent species present good nutritional values as sources ofproteins, carbohydrates, minerals and vitamins. Accordingto the study done by Marinho-Soriano, Fonseca, Carneiro,and Moreira (2006) on the chemical composition ofS. vulgare, the major components of this type of algaewere carbohydrates (67.80%); according to the abovementioned study, the synthesis of carbohydrates seemedto be favored by both, intensity of light and temperaturewhile decreasing the nitrogen and proteins content. Thepercentage of lipids in this type of macroalgae was verylow (0.45%); on the other hand, S. vulgare had a high per-centage of fiber (7.73%) and proteins (15.76%). In a studydeveloped by Dietrich et al. (1995), it was demonstratedthat S. vulgare contained also polysaccharides withpotential antiviral action formed principally by alginicacid, xylofucans and two species of fucans.

According to Barbarino and Lourenco (2005), proteinsof S. vulgare had a high nutritional value since they con-tained all the essential amino acids in significant amounts.Although in general, algae do not contain valuable quanti-ties of the essential amino acid methionine, S. vulgare pre-sented high levels of this amino acid (1.7%). Also, althoughpractically all the species of algae are rich in phenylalanine,tyrosine and treonine, S. vulgare presented as main aminoacids leucine (8.2%), alanine (6.8%), glutamic (17.4%)and aspartic acid (10.6%).

H. elongata, U. pinnatifida, Porphyra sp. andC. crispus

Porphyra sp. and C. crispus belong to the group of redalgae while H. elongata and U. pinnatifida are brown algae.Nowadays, these macroalgae are very interesting to con-sumers and food industry due to their low content in calo-ries and high content in vitamins, minerals and dieteticfiber.

The algae, H. elongata (dehydrated and canned),U. pinnatifida and Porphyra sp. (dehydrated), have beenstudied by Sanchez-Machado, Lopez-Cervantes, Lopez-Hernandez, and Paseiro-Losada (2004). These authorsshowed the valuable protein content of these algae (ashigh as 24%, given as gram of protein per 100 g of alga)and the low percentage of lipids (about 1% in all cases). In-terestingly, although these algae showed a low lipid content,they possessed a high level of polyunsaturated fatty acids

(PUFAs) as can be seen in Table 2 (Sanchez-Machado,Lopez-Cervantes, Lopez-Hernandez, & Paseiro-Losada,2004). Thus, these algae seemed to be an interesting sourceof some polyunsaturated u3-fatty acids, as for example, theeicosapentaenoic acid (EPA), given as C20:5 u3. Theseu3-fatty acids have demonstrated their effect on the reduc-tion of coronary diseases (Simopoulos, 2004). Besides,Kamat et al. (1992) have demonstrated that some fatty acidsfrom algae can have certain antiviral activity. According toLe Tutour et al. (1998), the use of an extract containingsoluble lipids from H. elongata increased synergicallythe antioxidant effect of vitamin E, in a percentage ashigh as 45%.

H. elongata also presented high levels of a-tocopherol,as demonstrated by Sanchez-Machado, Lopez-Hernandez,and Paseiro-Losada (2002); for example, the content ofa-tocopherol in H. elongata dehydrated (33.3 mg/g dryweight) was considerably higher than in H. elongatacanned (12.0 mg/g dry weight), which clearly indicatesthe important effect of the processing on this compound.Other compounds that could be found in these algae weresterols (Sanchez-Machado, Lopez-Hernandez, Paseiro-Losada, & Lopez-Cervantes, 2004). Thus, the algaeH. elongata, U. pinnatifida and Porphyra sp., containedethylenecholesterol, with relative small variations in theircontent, what seems to indicate a much lower effect ofthe conditions of conservation on this compound (dehy-drated or canned for H. elongata). The predominant sterolfor the brown algae (H. elongata and U. pinnatifida) was fu-costerol (1706 mg/g of dry weight and 1136 mg/g of dryweight, respectively), and for the red alga (Porphyra sp.)was demosterol (337 mg/g of dry weight). Cholesterol, ingeneral, was present at very low quantities, except inPorphyra sp. that can contain up to 8.6% of the totalcontent of sterols as cholesterol.

Algae present in general high fiber contents (seeTable 3). Thus, in red algae the soluble fraction wasprincipally composed of sulphated galactans such as agaror carrageenans, while in brown algae, the soluble fractionwas principally composed of alginates, fucans and lami-narin; in both cases, the insoluble fraction was basicallyformed of cellulose (Sanchez-Machado, Lopez-Cervantes,Lopez-Hernandez, Paseiro-Losada, & Simal-Lozano,2004).

Folates act as vitamins cofactors and are essential for thesynthesis of purines and pyrimidines, as well as for the pro-duction of methionine from homocysteine. They also playan important role in neural tube defects. It has been demon-strated in animal studies that low levels of folic acid canincrease the risk of suffering cancer. Interestingly, redand brown algae can also contain high levels of folic acidand folate derivatives including 5-metil-tetrahydro-folate,5-formyl-tetrahydro-folate and tetrahydro-folate. Thus,amounts as high as 150 mg of total folic acid per 100 g ofdry algae had been detected in U. pinnatifida (Rodriguez-Bernaldo de Quiros, Castro de Ron, Lopez-Hernandez, &

34 M. Plaza et al. / Trends in Food Science & Technology 19 (2008) 31e39

Table 2. Fatty acids profile of different algae canned and dehydrated according to Sanchez-Machado, Lopez-Cervantes, Lopez-Hernandez, andPaseiro-Losada (2004)

Fatty acids Canned Dehydrated

Himanthalia elongata Himanthalia elongata Undaria pinnatifida Porphyra sp.

C14:0 9.57� 0.81 5.85� 0.35 3.17� 0.31 0.53� 0.21C16:0 36.73� 2.16 32.53� 1.61 16.51� 1.35 63.19� 1.93C16:1 u7 3.00� 0.38 2.79� 0.25 3.70� 0.88 6.22� 0.70C16:2 u4 Tr Tr Tr TrC16:3 u4 0.06� 0.01 4.38� 1.33 2.31� 1.94 1.56� 0.51C18:0 0.59� 0.07 0.68� 0.15 0.69� 0.08 1.23� 0.10C18:1 u9 22.64� 1.80 19.96� 2.01 6.79� 0.90 6.70� 1.16C18:1 u7 e e e 1.29� 0.68C18:2 u6 5.80� 0.21 4.39� 0.34 6.23� 0.32 1.17� 0.13C18:3 u3 6.77� 0.79 8.79� 0.71 11.97� 1.75 0.23� 0.16C18:4 u3 1.94� 0.43 3.53� 0.56 22.60� 2.48 0.24� 0.35C20:1 u9 e e e 4.70� 0.26C20:4 u6 9.78� 2.27 10.69� 1.30 15.87� 1.68 6.80� 1.18C20:4 u3 0.35� 0.19 0.88� 1.80 0.70� 0.14 0.07� 0.02C20:5 u3 2.77� 0.80 5.50� 1.78 9.43� 0.69 6.03� 0.95Saturated fatty acid 46.89� 3.03 30.06� 2.11 20.39� 1.73 64.95� 2.24Monounsaturated 25.64� 2.18 22.75� 2.26 10.50� 1.78 18.91� 2.81PUFAs 27.47� 4.73 38.16� 7.84 69.11� 9.01 16.10� 3.31PUFAs u6 15.58� 2.48 15.08� 1.64 22.10� 2.00 7.97� 1.31PUFAs u3 11.83� 2.21 18.70� 4.84 44.70� 5.05 7.20� 1.48Ratio u6/u3 1.32 0.81 0.49 1.21

Lage-Yusty, 2004). U. pinnatifida is a brown alga that isconsumed preferably in some regions of the coast ofAustralia and New Zealand. This alga also contained highlevels of sulphated polysaccharides (sulphated fucansor fucoidans) that present potential antiviral activity(Hemmingson, Falshaw, Furneaux, & Thompson, 2006).

Volatile compounds have also been identified in samplesof U. pinnatifida cultured in different conditions (Shin,2003). Namely, a total of 127 volatile compounds were iden-tified including 4 organic acids, 34 aldehydes, 19 alcohols,34 ketones, 8 esters, 12 hydrocarbons, 5 sulfur-containingcompounds, and 11 more of different nature.

The brown alga U. pinnatifida and the red algaC. crispus could be used as a food supplement to help meet-ing the recommended daily intake of some minerals, macroelements (Na, K, Ca, Mg, ranging from 8.1 to 17.9 mg/100 g), and trace elements (Fe, Zn, Mn, Cu ranging from5.1 to 15.2 mg/100 g) according to Ruperez (2002). In

this regard, some studies have been directed to demonstratethe effect of the consumption of U. pinnatifida on the bonescalcification in rats (Yamaguchi, Hachiya, Hiratuka, &Suzuki, 2001); however, the results obtained were not con-clusive in favor of the consumption of this alga. Anotherstudy investigated the effect of fiber from U. pinnatifidaon the cardiovascular diseases (hypertension and hypercho-lesterolemia) (Ikeda et al., 2003). In the same study (Ikedaet al., 2003), authors discuss that the possible preventiveeffect of this alga on cerebrovascular diseases could be par-tially due to its content in fucoxanthin, which could protectof ischemic neuronal cells death. Other authors claimedthat fucoxanthin from algae could increase the metabolism,helping to control the weight and reducing the obesity inanimal studies (Maeda, Hosokawa, Sashima, Funayama,& Miyashita, 2005).

In a recent study (Amano, Kakinuma, Coury, Ohno, &Hara, 2005), the usefulness of a mixture of several

Table 3. Uronic acid contents in the total dietary fiber fractions from some algae according to Sanchez-Machado, Lopez-Cervantes, Lopez-Hernandez, Paseiro-Losada, et al. (2004)

Fatty acids Canned Dehydrated

Himanthalia elongata Himanthalia elongata Undaria pinnatifida Porphyra sp.

Total dietaryfiber (g/100 g dry weight)

53.3� 3.5 32.6� 0.4 42.7� 1.8 40.5� 2.8

b-D-mannuronic acid (%) 78.2� 1.4 75.6� 1.8 78.3� 2.7 Not determineda-L-guluronic acid (%) 21.8� 1.4 24.4� 1.8 21.7� 2.7 Not determined

35M. Plaza et al. / Trends in Food Science & Technology 19 (2008) 31e39

brown algae (Eisenia bicyclis (‘Arame’), Hizikia fusifor-mis (‘Hijiki’), and U. pinnatifida sporophylls (‘Mekabu’))and the red alga Porphyra yezoensis (‘Susabinori’) wasinvestigated for the reduction of lipid levels in bloodand thrombosis prevention. This effect was associatedto the presence of polysaccharides in all the algae. Inthis study, a group of rats were fed using a choles-terol-rich diet containing this mixture of algae (9e10%w/w) for 28 days. Serum total cholesterol, LDLcholesterol, free cholesterol, and triglyceride levelswere significantly reduced to 49.7%, 48.1%, 49.0% and74.8%, respectively, of those of the control. Nevertheless,HDL cholesterol did not present significant changes,while platelet aggregation also decreased significantly(Amano et al., 2005).

Fatty acids and sterols content determined in red alga C.crispus showed that the main fatty acids were palmitic,palmitoleic, oleic, arachidonic and eicosapentanoic acids(Tasende, 2000). These five fatty acids represent morethan 78% of the total fatty acids content, showing that un-saturated fatty acids are present in a much greater quantity(>80%) than saturated fatty acids. The major sterol wascholesterol (>94%), containing smaller amounts of 7-dehydrocholesterol and stigmasterol and minimum amountsof campesterol, sitosterol and 22-dehydrocholesterol(Tasende, 2000).

The red alga Porphyra sp., contained sulphated polysac-charides (porphyrans) that have been shown to presentpotential apoptotic activities (Kwon & Nam, 2006).

Cystoseira spp. and Ulva spp.Cystoseira spp. belongs to the group of brown algae,

while Ulva spp. belongs to the group of green algae. Thesetwo macroalgae are good natural sources of proteins, carbo-hydrates, minerals and vitamins, while containing lowlevels of lipids.

Cystoseira spp. possesses, among their more significantcompounds, different types of terpenes. Terpenes contain-ing aryl groups have been attracting more and moreattention because they present a broad spectra of pharmaco-logical activities, and combine valuable curative propertieswith practically no harmful side effects. A very comprehen-sive review on arylterpenes in algae was carried out by

Kukovinets and Kislitsyn (2006). The existing informationabout terpenes contents in algae can be summarized asfollows.

The more representative diterpenes are of types 1e3(see Fig. 1), which exhibit antimicrobial activity, andwere isolated from the marine alga Cystoseira spinosavar. Squarrosa. On the other hand, brown algae Cystoseirausneoides, which contained usneoidone E, exhibited anti-viral and antitumor activity (Kukovinets & Kislitsyn, 2006).The marine algae Cystoseira josteroides and Sargassummacrocarpum are good sources of zosterdiol A, zosterdiolB, zosteronol and zosteronediol and of a new toluquinolderivative with antibacterial properties. Prenyldiketones(see Fig. 2) were found in important amounts in the marinealga Cystoseira spp. (Kukovinets & Kislitsyn, 2006). How-ever, no biological activity of these compounds has beenreported so far.

Antimicrobial activity of several extracts of the algaCystoseira barbata has also been investigated (Ozdemir,Horzum, Sukatar, & Karabay-Yavasoglu, 2006). Namely,hexane, methanol, dichloromethane and chloroform ex-tracts were tested for their antimicrobial activities againstfour Gram-positive bacteria, four Gram-negative bacteriaand Candida albicans ATCC 10239 yeast (Ozdemir et al.,2006). Hexane extracts showed higher antimicrobial activ-ity than methanol, dichloromethane and chloroform ex-tracts. The volatile oils of these algae did not remarkablyinhibit the growth of tested microorganisms. In these vola-tile oils authors identified hydrocarbon compounds such as

1a,bOR1

OMe

O

R

OR1

R

OMe O

2a,b

1, 2: R = CH2CH2CH2(Me) CHCOCH2(Me)2 C(OH);1a, 2a: R1 = Me; 1b, 2b: R1 = H

Fig. 2. Diterpenes from alga Cystoseira spp. Modified from Kukovinetsand Kislitsyn (2006).

1 2 3

OH

OH

OR=

OR

OH

OH

O

ROH

OH

OHR

Fig. 1. Diterpenes of alga Cystoseira spinosa var. Squarrosa. Modified from Kukovinets and Kislitsyn (2006).

36 M. Plaza et al. / Trends in Food Science & Technology 19 (2008) 31e39

docosane (7.61%) and tetratriacontane (7.47%), amongothers.

According to the investigation carried out by Kapeta-novic et al. (2005), the main sterols in the green algaUlva lactuca were cholesterol and isofucosterol, while inthe brown alga Cystoseira adriatica, the principal sterolswere cholesterol and stigmast-5-en-3 beta-ol, containingthe latter a very low concentration of fucosterol (Kapeta-novic et al., 2005).

Sulphated polysaccharides have been identified in thebrown alga Cystoseira canariensis (Ramazanov, Jimenezdel Rio, & Ziegenfuss, 2003). These sulphated polysaccha-rides comprise a complex group of macromolecules witha wide range of important physiological properties able to reg-ulate the bioactivity of growth factors and cytokines such asthe basic fibroblast growth factor, interferon, various enzymesand transforming growth factor (Ramazanov et al., 2003).

The antifungal and anti-aflatoxinogenic activity of thebrown alga Cystoseira tamariscifolia has also been studiedagainst pathogenic and toxigenic strains of yeasts andmoulds (Zinedine, Elakhdari, Faid, & Benlemlih, 2004).Namely, antimicrobial effect of different alga extracts (us-ing methanol, ethanol, diethyl ether, hexane, chloroformand water) was investigated. Results from inhibitory testsshowed that only ethanolic extracts present antimicrobialactivity against moulds and yeasts. The growth of two typesof yeasts, C. albicans HSZ02 and C. albicans IP4872, wascompletely inhibited by a concentration of 50 and 100 ppmof ethanolic extract of this alga. The growth of the speciesSacharomyces cerevisiae S326 was affected by 25 ppm ofethanol extract. For moulds, the growth of Penicillium cy-clopium strain IP1231-80 was inhibited by 50 ppm whilethe growth of all Aspergillus strains used was inhibited by100 ppm of the same extract. The ethanolic extract ofC. tamariscifolia showed also aptitude to reduce theproduction of aflatoxin B1 by Aspergillus parasiticusNRRL2999. Results showed that the reduction on aflatoxinB1 biosynthesis was, respectively, about 25.4%, 37.6%,75.8%, and 96.3% by 10, 25, 50, and 100 ppm of the etha-nolic extract.

Contents of proteins, ashes, humidity and carbohydrateswere determined for different macroalgae (De Padua,Fontoura, & Mathias, 2004). It was observed thatUlva oxysperma and Ulva spp showed high mineral levelsand low calories, while U. oxysperma presented lower pro-tein levels than Ulva spp. (De Padua et al., 2004). As anexample, composition of U. oxysperma was determinedto be the following: humidity (16e20%), ash (17e31%dry base), proteins (6e10% dry base), lipids (0.5e3.2%dry base), fibers (3e12% dry base), and carbohydrates(46e72% dry base); which corresponded to 192e270 kcal/100 g (wet base). On the other hand, U. lactuca(15e18% dry base) and Ulva fasciata (13e16% drybase) revealed a content slightly higher of proteins, buta similar energetic content (250e272 and 225e239 kcal/100 g, respectively) (De Padua et al., 2004).

Discussion on the potential of some algae as naturalsources of functional ingredients

One of the main objectives of the functional food sci-ence is to identify the beneficial interactions amonga food, or specific ingredient, and one or more functionsof the organism, obtaining, if possible, definitive proofsabout the mechanisms involved in the interaction. This pri-mary objective must be based on investigations in vitro orex vivo in cellular lines or culture tissues, later in animalmodels and finally they must be corroborated in studiesof observation or intervention in human (clinical trials).

The rigorous design of a functional food needs to knowthe biological activity at molecular level of their compo-nents and the bases of the disease (or diseases) consideredas target. The recent branch of science that studies inter-actions between genes and food ingredients is calledNutritional Genomic or Nutrigenomic (Palanca et al.,2006; Roche, 2006). Theoretically, we might manage toselect a diet according to our genome with the objectiveto reduce the genetic risk of suffering certain diseasesor to find on the market products designed specificallyfor ‘‘difficult days’’, for some sports competitions, etc.(Marriott, 2000).

The principal guideline to follow in the design of a newfunctional food is to increase as much as possible the ben-efit/risk ratio, acting simultaneously on both: trying to in-crease to the maximum the benefit and to reduce to theminimum the risk. Increasing the benefit implies to lookfor a physiological wide effect, assuring that existing bio-availability and that the mentioned bioavailability are goingto be kept along all the useful life of the food. In order toreduce the risk it is necessary to carry out toxicity studies,to use the functional ingredient in a minimal effective dosesand to use as functional ingredients products naturallyfound in foods or natural sources.

The composition of the different algae described aboveshows that these organisms can be an interesting naturalsource of functional ingredients (see Table 4). Thus, in gen-eral all of them present good nutritional values that makethem good candidates as source of proteins, carbohydrates,fiber, minerals, vitamins and, besides, they present a lowcontent in lipids. Although, logically, the toxicological as-pects associated with some of their components must betaken into account here. It is interesting to mention thattheir content in proteins, carbohydrates, lipids, fiber, metab-olites, etc. can be influenced by the growing parameters(water temperature, salinity, light and nutrients), conclud-ing that algae can be considered as a magnificent bioreactorable to provide different types of compounds at differentquantities.

Algae have mainly been used in west countries as rawmaterial to extract alginates (from brown algae) and agarand carragenates (from red algae). However, from thedescription given above it is concluded that algae alsocontain multitude of bioactive compounds that mighthave antioxidant, antibacterial, antiviral, anticarcinogenic,

37M. Plaza et al. / Trends in Food Science & Technology 19 (2008) 31e39

Table 4. Some examples of algae together with their functional ingredients and possible effect on human health

Algae Functional ingredients Possible health effect

Sargassum vulgare Alginic acid, xylofucans Antiviral activityHimanthalia elongate PUFAs Reduce risk of certain heart diseases

a-Tocoferol Antioxidant activitySterols Reduce total and LDL cholesterolSoluble fiber Reduce total and LDL cholesterol

Undaria pinnatifida PUFAs Reduce risk of certain heart diseasesSterols Reduce total and LDL cholesterolSoluble fiber Reduce total and LDL cholesterolFolates Reduce risk of certain types of cancerSulphated polysaccharides Antiviral activityFucoxanthin Preventive effect on cerebrovascular diseases

Increase the metabolismPhorphira spp. PUFAs Reduce risk of certain heart diseases

Sterols Reduce total and LDL cholesterolSoluble fiber Reduce total and LDL cholesterol

Chondrus crispus PUFAs (n-3) fatty acids Reduce risk of certain heart diseasesSterols Reduce total and LDL cholesterolSoluble fiber Reduce total and LDL cholesterolSulphated polysaccharides (porphyrans) Apoptotic activities

Cystoseira spp. Terpenes Valuable curative propertiesSterols Reduce total and LDL cholesterolSulphated polysaccharides Regulate the bioactivity of growth factors and cytokines

Ulva spp. Sterols Reduce total and LDL cholesterol

etc. properties. Some of them are outlined later due to theirspecial interest as possible functional ingredients.

Thus, the main part of the described algae presentsa high fiber content in which the soluble fraction is com-posed principally of sulphated galactans as agar or carra-genates (in red algae) and of alginates, fucans andlaminarin (in brown algae). Consumption of dietetic fiberhas a positive influence on several aspects related to health,reducing the risk of suffering colon cancer, constipation,hypercholesterolemia, obesity and diabetes. Besides,many constituents of the dietetic fiber show antioxidant ac-tivity as well as immunological activity (Suzuki et al.,2004). In this sense, U. pinnatifida (wakame) showedsome positive effect on several cardiovascular diseases (hy-pertension and hypercholesterolemia) (Ikeda et al., 2003);this alga contains basically dietetic fiber, being its principalcomponent alginate. This alginic acid has demonstrated toreduce hypertension in hypertensive rates (Ikeda et al.,2003).

Another family of compounds of great interest, and thatare common to many of the algae described in this work,are polysaccharides with potential antiviral action. For ex-ample, S. vulgare contains alginic acid, xylofucans and twospecies of fucans (Dietrich et al., 1995), whereas U. pinna-tifida (brown alga) contains high levels of sulphated poly-saccharides, specifically, sulphated fucans (fucoidans)(Hemmingson et al., 2006) and sulphate of galactofucan(Thompson & Dragar, 2004). These compounds have dem-onstrated a powerful antiviral activity against herpes type 1virus (HSV-1), HSV-2, and cytomegalovirus in humans

(HCMV). The fucoidans, moreover, might be used also asanticoagulant and antithrombotics agents (Lee, Hayashi,Hashimoto, Nakano, & Hayashi, 2004), and they have dem-onstrated, in studies in vivo, to have an antitumoral effect inrats with mammary carcinogenesis (Maruyama, Tamauchi,Hashimoto, & Nakano, 2003). On the other hand, the redalga Porphyra sp. contains a sulphated polysaccharidecalled porphyran that has demonstrated some potential ap-optotic activity (evaluated using AGS cells from a humangastric cancer) inducing the death of the carcinogenic cells(Kwon & Nam, 2006).

Among the most relevant compounds found in the algae,antioxidants are probably the substances that have attractedmajor interest. Algae, as photosynthetic organisms, are ex-posed to a combination of light and high oxygen concentra-tions what induces the formation of free radicals and otheroxidative reagents. The absence of structural damage in thealgae leads to consider that these organisms are able to gen-erate the necessary compounds to protect themselvesagainst oxidation. In this respect, algae can be consideredas an important source of antioxidant compounds that couldbe suitable also for protecting our bodies against the reac-tive oxygen species formed e.g., by our metabolism or in-duced by external factors (as pollution, stress, UVradiation, etc.). In algae there are antioxidant substancesof very different nature, among which vitamin E (or a-tocopherol) and carotenoids can be highlighted within thefat-soluble fraction, whereas the most powerful water-soluble antioxidants found in algae are polyphenols, phyco-biliproteins and vitamins (vitamin C).

38 M. Plaza et al. / Trends in Food Science & Technology 19 (2008) 31e39

In brown algae the principal tocopherol is a-tocopherol(0.052 mg/g in H. elongata), this compound is highly stableto heat and acids, and unstable to alkali, UV radiation andoxygen. a-Tocopherol has antioxidant activity because itfixes free radicals, thanks to the presence of a phenol groupin its structure. Carotenoids are a family of compounds ofimportance also due to their high antioxidant activity andits great structural diversity. There are numerous studiesthat associate the antioxidant activity of different algaewith the carotenoids contents. In this regard, a type of ca-rotenoids called xantophylls obtained from U. pinnatifidahave demonstrated some activity against cerebrovasculardiseases (Ikeda et al., 2003).

Algae are also a magnificent source of polyunsaturatedfatty acids, as the eicosapentanoic acid (EPA) describedin H. elongata, U. pinnatifida and Porphyra sp. These u3fatty acids have demonstrated their effect on the reductionof coronary diseases, thrombosis and arteriosclerosis(Simopoulos, 2004).

Other compounds of great importance that can be foundin most of the algae described in this work are sterols. Di-verse clinical studies have demonstrated that diets withsterols (from plants) might help to reduce cholesterollevels in blood. Additionally, they have antiinflammatory,antibacterial, antifungicidal, antiulcerative and antitumoralactivity (Dunford & King, 2000; Kamal-Eldin, Maatta,Toivo, Lampi, & Piironen, 1998; Sanchez-Machado,Lopez-Hernandez, Paseiro-Losada, & Lopez-Cervantes,2004).

In summary, in this work a bibliographical revision hasbeen carried out on the composition and biological activityof some algae discussing their possibilities as natural sour-ces of functional ingredients. Thus, it is possible to con-clude that these organisms show a high potential asnatural sources of ingredients with many different biologi-cal activities. However, once their usefulness is demon-strated, it will be necessary to approach other new aspectsrelated to e.g., production of ingredients at industrial scale,algae growing, ingredients extraction, purification, etc. Inthis regard, the development of environment-friendly ex-traction processes to isolate the compound (or compounds)of interest in a fast, cost-effective and non-aggressive waywill be one of the main topics for new developments. Itis foreseeable that this line of investigation (i.e., the searchof new functional ingredients from natural sources) will beone of the hot challenges in Food Science and Technologythat, basically, tries to give response to the social demand ofnew functional foods with scientifically demonstratedhealth properties.

AcknowledgementsThis work has been financed by Ministerio de Educacion

y Ciencia (Project AGL2005-06726-C04-02) and by Comu-nidad de Madrid (Project ALIBIRD, S-505/AGR-0153).MP would like to thank CSIC for a I3P grant.

References

Amano, H., Kakinuma, M., Coury, D. A., Ohno, H., & Hara, T.(2005). Effect of a seaweed mixture on serum lipid level and

platelet aggregation in rats. Fisheries Science, 71, 1160e

1166.Arai, S. (1996). Studies of functional foods in Japan e state of the art.

Bioscience, Biotechnology, Biochemistry, 60, 9e15.Barbarino, E., & Lourenco, S. O. (2005). An evaluation of methods

for extraction and quantification of protein from marinemacro- and microalgae. Journal of Applied Phycology, 17(5),447e460.

Carlucci, M. J., Scolaro, L. A., & Damonte, E. B. (1999). Inhibitoryaction of natural carrageenans on Herpes simplex virus infection ofmouse astrocytes. Chemotherapy, 45(6), 429e436.

Cifuentes, A., Bartolome, B., & Gomez-Cordoves, C. (2001). Fastdetermination of procyanidins and other phenolic compoundsin food samples by micellar electrokinetic chromatographyusing acidic buffers. Electrophoresis, 22, 1561e1567.

De Padua, M., Fontoura, P. S. G., & Mathias, A. L. (2004). Chemicalcomposition of Ulvaria oxysperma (Kutzing) bliding, Ulva lactuca(Linnaeus) and Ulva fascita (Delile). Brazilian Archives of Biologyand Technology, 47(1), 49e55.

Dietrich, C. P., Farias, G. G. M., Deabreu, L. R. D., Leite, E. L., DaSilva, L. F., & Nader, H. B. (1995). A new approach for the char-acterization of polysaccharides from algae: presence of four mainacidic polysaccharides in three species of the class Phaeophycea.Plant Science, 108, 143e153.

Diplock, A. T., Aggett, P. J., Ashwell, M., Bornet, F., Fern, E. B., &Roberfroid, M. B. (1999). Scientific concepts of functional foods inEurope: consensus document. British Journal of Nutrition, 81,S1eS27.

Dunford, N. T., & King, J. W. (2000). Phytosterol enrichment of ricebran oil by a supercritical carbon dioxide fractionation technique.Journal of Food Science, 65(8), 1395e1399.

European Parliament and of the Council relative to the nutritionaldeclarations and of healthy properties in the food. (2006). PE-CONS 3616/06 of September 1.

Geslain-Laneelle, C. (2006). Conference on nutrition and healthclaims. Bologna: Noviembre.

Hasler, C. M. (1998). Functional foods: their role in disease preventionand health promotion. Food Technology, 52, 63e70.

Hasler, C. M. (2002). Functional foods: benefits, concerns and chal-lenges e a position paper from the American Council on Scienceand Health. Journal of Nutrition, 132, 3772e3781.

Hemmingson, J. A., Falshaw, R., Furneaux, R. H., & Thompson, K.(2006). Structure and antiviral activity of the galactofucan sulfatesextracted from Undaria pinnatifida (Phaeophyta). Journal ofApplied Phycology, 18, 185e193.

Herrero, M., Ibanez, E., Senorans, J., & Cifuentes, A. (2004). Pressur-ized liquid extracts from Spirulina platensis microalga: determi-nation of their antioxidant activity and analysis by micellarelectrokinetic chromatography. Journal of Chromatography A,1047, 195e203.

Herrero, M., Simo, C., Ibanez, E., & Cifuentes, A. (2005). Capillaryelectrophoresis-mass spectrometry of Spirulina platensis proteinsobtained by pressurized liquid extraction. Electrophoresis, 26,4215e4224.

Ibanez, E., Lopez-Sebastian, S., Tabera, J., Bueno, J. M., Ballester, L., &Reglero, G. (2001). Influence of the CO2 quality in the antioxidantactivity of rosemary extracts de aromatized by SFE and used for oilstabilization. Food Science and Technology International, 7(2),177e182.

Ibanez, E., Oca, A., De Murga, G., Lopez-Sebastian, S., Tabera, J., &Reglero, G. (1999). Supercritical fluid extraction and fractionationof different pre-processed rosemary plants. Journal of Agriculturaland Food Chemistry, 47(4), 1400e1404.

39M. Plaza et al. / Trends in Food Science & Technology 19 (2008) 31e39

Ikeda, K., Kitamura, A., Machida, H., Watanabe, M., Negishi, H.,Hiraoka, J., et al. (2003). Effect of Undaria pinnatifida (Wakame) onthe development of cerebrovascular diseases in stroke-pronespontaneously hypertensive rats. Clinical and Experimental Phar-macology and Physiology, 30, 44e48.

Jaime, L., Mendiola, J. A., Herrero, M., Soler, C., Santoyo, S.,Senorans, F. J., Cifuentes, A., & Ibanez, E. (2005). Separation andcharacterization of antioxidants from Spirulina platensis microalgacombining pressurized liquid extraction, TLC and HPLC-DAD.Journal of Separation Science, 28, 2111e2119.

Kamal-Eldin, A., Maatta, K., Toivo, J., Lampi, A. M., & Piironen, V.(1998). Acid-catalyzed isomerization of fucosterol and D5-avenasterol. Lipids, 33(11), 1073e1077.

Kamat, S. Y., Wahıdulla, S., Dsouza, L., Naik, C. G., Ambiye, V.,Bhakuni, D. S., et al. (1992). Bioactivity of marine organisms, VI.Antiviral evaluation of marine algal extracts from the Indian coast.Botanica Marina, 35, 161e164.

Kapetanovic, R., Sladic, D., Popov, S., Zlatovic, M., Kljajic, Z., &Gasic, M. J. (2005). Sterol composition of the Adriatic sea algaeUlva lactuca, Codium dichotonium, Cystoseira adriatica and Fucusvirsoides. Journal of the Serbian Chemical Society, 70(12),1395e1400.

Kukovinets, O. S., & Kislitsyn, M. I. (2006). Natural Arylterpenes andtheir biological activity. Chemistry of Natural Compounds, 42(1).

Kwon, M. J., & Nam, T. J. (2006). Porphyran induces apoptosis relatedsignal pathway in AGS gastric cancer cell lines. Life Sciences, 79,1956e1962.

Lee, J. B., Hayashi, K., Hashimoto, M., Nakano, T., & Hayashi, T.(2004). Novel antiviral fucoidan from sporophyll of Undaria pin-natifida (Mekabu). Chemical and Pharmaceutical Bulletin, 52(9),1091e1094.

Le Tutour, B., Benslimane, F., Gouleau, M. P., Gouygou, J. P.,Saadan, B., & Quemeneur, F. (1998). Antioxidant an pro-oxidantactivities of the brown algae, Lalminaria digitata, Himanthaliaelongata, Fucus vesiculosus, Fucus serratus and Ascophyllumnodosum. Journal of Applied Phycology, 10, 121e129.

Maeda, H., Hosokawa, M., Sashima, T., Funayama, K., & Miyashita, K.(2005). Fucoxanthin from edible seaweed, Undaria pinnatifida,shows antiobesity effect through UCP1 expression in white adiposetissues. Biochemical and Biophysical Research Communications,332(2), 392e397.

Marinho-Soriano, E., Fonseca, P. C., Carneiro, M. A. A., &Moreira, W. S. C. (2006, December). Seasonal variation in thechemical composition of two tropical seaweeds. BioresourceTechnology, 97(18), 2402e2406.

Marriott, B. M. (2000). Functional foods: an ecologic perspective.American Journal of Clinical Nutrition, 71(Suppl.), 1728Se

1734S.Maruyama, H., Tamauchi, H., Hashimoto, M., & Nakano, T. (2003).

Antitumor activity and immune response of Mekabu fucoidanextracted from sporophyll of Undaria pinnatifida. In Vivo, 17(3),245e249.

Mendiola, J. A., Marın, F. R., Hernandez, S. F., Arredondo, B. O.,Senorans, F. J., Ibanez, E., et al. (2005). Characterization via LC-DAD and LC-MS/MS of supercritical fluid antioxidant extracts ofSpirulina platensis microalga. Journal of Separation Science, 28,1031e1038.

Ozdemir, G., Horzum, Z., Sukatar, A., & Karabay-Yavasoglu, N. U.(2006). Antimicrobial activities of volatile components and variousextracts of Dictyopteris membranaceae and Cystoseira barbatafrom the Coast of Izmir, Turkey. Pharmaceutical Biology, 44(3),183e188.

Palanca, V., Rodriguez, E., Senorans, J., & Reglero, G. (2006). Basescientıficas para el desarrollo de productos carnicos funcionalescon actividad biologica combinada. Nutricion Hospitalaria, 21(2),199e202.

Ramazanov, Z., Jimenez del Rio, M., & Ziegenfuss, T. (2003). Sulfatedpolysaccharides of brown seaweed Cystoseira canariensis bind toserum myostatin protein. Acta Physiologica et PharmacologicaBulgarica, 27(2e3), 101e106.

Roche, H. M. (2006). Nutrigenomics e new approaches for humannutrition research. Journal of the Science of Food and Agriculture,86(8), 1156e1163.

Rodriguez-Bernaldo de Quiros, A., Castro de Ron, C., Lopez-Hernandez, J., & Lage-Yusty, M. A. (2004). Determination of folatesin seaweeds by high-performance liquid chromatography. Journalof Chromatography A, 1032(1e2), 135e139.

Ruperez, P. (2002). Mineral content of edible marine seaweeds. FoodChemistry, 79(1), 23e26.

Sanchez-Machado, D. I., Lopez-Cervantes, J., Lopez-Hernandez, J., &Paseiro-Losada, P. (2004). Fatty acids, total lipid, protein and ashcontents of processed edible seaweeds. Food Chemistry, 85(3),439e444.

Sanchez-Machado, D. I., Lopez-Cervantes, J., Lopez-Hernandez, J.,Paseiro-Losada, P., & Simal-Lozano, J. (2004). Determination of theuronic acid composition of seaweed dietary fibre by HPLC.Biomedical Chromatography, 18(2), 90e97.

Sanchez-Machado, D. I., Lopez-Hernandez, J., & Paseiro-Losada, P.(2002). High-performance liquid chromatographic determinationof a-tocoferol in macroalgae. Journal of Chromatography A,976(1e2), 277e284.

Sanchez-Machado, D. I., Lopez-Hernandez, J., Paseiro-Losada, P., &Lopez-Cervantes, J. (2004). An HPLC method for the quantificationof sterols in edible seaweeds. Biomedical Chromatography, 18(3),183e190.

Sanders, M. E. (1999). Probiotics. Food Technology, 53, 67e77.Senorans, F. J., Ruiz-Rodriguez, A., Cavero, S., Cifuentes, A.,

Ibanez, E., & Reglero, G. (2001). Isolation of antioxidant com-pounds from orange juice by using countercurrent supercriticalfluid extraction (CC-SFE). Journal of Agricultural and Food Chem-istry, 49, 6039e6044.

Shin, T. S. (2003). Volatile compounds in sea mustard, Undariapinnatifida. Food Science and Biotechnology, 12(5),570e577.

Simopoulos, A. P. (2004). Omega-3 essential fatty acid ratio andchronic diseases. Food Review International, 20, 77e90.

Sloan, E. (1999). The new market: foods for the not-so-healthy. FoodTechnology, 53, 54e60.

Sloan, A. E. (2000). The top ten functional food trends. Food Tech-nology, 54, 33e62.

Sloan, A. E. (2002). The top ten functional food trends: the next gen-eration. Food Technology, 56, 32e56.

Suzuki, N., Fujimura, A., Nagai, T., Mizumoto, I., Itami, T., Hatate, H.,et al. (2004). Antioxidative activity of animal and vegetable dietaryfibers. Biofactors, 21(1e4), 329e333.

Tasende, M. G. (2000). Fatty acid and sterol composition of gameto-phytes and sporophytes of Chondrus crispus (Gigartinaceae, Rho-dophyta). Scientia Marina, 64(4), 421e426.

Thompson, K. D., & Dragar, C. (2004). Antiviral activity of Undariapinnatifida against herpes simplex virus. Phytotherapy Research,18(7), 551e555.

Unnevehr, L., & Hasler, C. (2000). Health claims and labeling regu-lation: how will consumers learn about functional foods? AgBio-Forum, 3, 10e13.

Yamaguchi, M., Hachiya, S., Hiratuka, S., & Suzuki, T. (2001). Effect ofmarine algae extract on bone calcification in the femoral-methaphyseal tissues of rats: anabolic effect of Sargassumhorneri. Journal of Health Science, 47(6), 533e538.

Zinedine, A., Elakhdari, S., Faid, M., & Benlemlih, M. (2004). Anti-fungal and anti-aflatoxinogenic activity of the brown algaeCystoseira tamarisscifolia. Journal of Mycology Medical, 14(4),201e205.