Globe artichoke A functional food and source of nutraceutical 2009.pdf

8/11/2019 Globe artichoke A functional food and source of nutraceutical 2009.pdf

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Globe artichoke: A functional food and source of nutraceutical

ingredients

Vincenzo Lattanzioa,*, Paul A. Kroonb, Vito Linsalatac, Angela Cardinalic

aDipartimento di Scienze Agro-Ambientali, Chimica e Difesa Vegetale, Facoltadi Agraria, Universitadegli Studi di Foggia,

Via Napoli, 25, 71100 Foggia, ItalybPlant Natural Products Programme, Institute of Food Research, Norwich Research Park, Norwich NR4 7UA, UKcIstituto di Scienze delle Produzioni Alimentari CNR, Via Amendola 122/O, 70126 Bari, Italy

A R T I C L E I N F O

Article history:

Received 13 October 2008

Accepted 23 December 2008

Available online 28 February 2009

Keywords:

Cynara

Caffeoylquinic acids

Cynarin

Flavonoids

Anthocyanin pigmentsInulin

By-products

A B S T R A C T

Globe artichoke (Cynara cardunculusL. subsp.scolymus(L.) Hayek, (formerlyCynara scolymus

L.) represents an important component of the Mediterranean diet, and is a rich source of

bioactive phenolic compounds, and also inulin, fibre and minerals. In addition, artichoke

leaf extracts have long been used in folk medicine, particularly for liver complaints. These

therapeutic properties have been often been ascribed to the cynarin (1,3-O-dicaffeoylquinic

acid) content of these extracts. In various pharmacological test systems, artichoke leaf

extracts have exhibited hepatoprotective, anticarcinogenic, antioxidative, antibacterial,

anti-HIV, bile-expelling, and urinative activities as well as the ability to inhibit cholesterol

biosynthesis and LDL oxidation. These broad therapeutic indications cannot be ascribed to

a single, but to several active compounds that together generate additive or synergistic

pharmacologic effects; these include mono- and dicaffeoylquinic acids, and flavonoidssuch as luteolin and its 7-O-glucoside. Artichoke by-products such as leaves, external

bracts and stems that are produced by the artichoke processing industry, represent a huge

amount of discarded material (about 8085% of the total biomass of the plant), which could

be used as a source of inulin but also of phenolics, and should be considered as a raw mate-

rial for the production of food additives and nutraceuticals.

2009 Elsevier Ltd. All rights reserved.

1. Introduction

Over the last few years a renewed and growing interest in theartichoke, an old plant with new uses in functional foods, has

been observed. Artichoke, Cynara cardunculus L. subsp. scoly-

mus(L.) Hayek, (formerlyCynara scolymusL.) is an ancient her-

baceous perennial plant, originating from the Mediterranean

area, which today is widely cultivated all over the world. The

botanical name is derived in part from the tradition of fertil-

izing the plant with ashes (Latin: cinis,cineris), and partly from

the Greek skolymos, meaning thistle from the spines found

on the bracts (they are not leaves) that enclose the flower

heads forming the edible portion of the plant (Oliaro, 1969).

Artichoke is widely cultivated for its large immature inflores-cences, called capitula or heads, with edible fleshy leaves

(bracts) and receptacle, which represent an important

component of the Mediterranean diet and is a rich source of

bioactive phenolic compounds, and also inulin, fibres and

minerals (Lattanzio, 1982; Orlovskaya et al., 2007). In addition,

the leaves, also rich in phenolic compounds (Lattanzio & Mor-

one, 1979; Lattanzio & Van Sumere, 1987; Lattanzio et al.,

1989, 1994; Fratianni et al., 2007), are used as a herbal medi-

1756-4646/$ - see front matter

2009 Elsevier Ltd. All rights reserved.doi:10.1016/j.jff.2009.01.002

* Corresponding author: Tel.: +39 320 4394738; fax: +39 0881 740211.E-mail address:[email protected](V. Lattanzio).

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cine and have been recognised since ancient times for their

beneficial and therapeutic effects: extracts from artichoke

have been used for hepatoprotection (Adzet et al., 1987) as a

choleretic (Preziosi et al., 1959; Preziosi, 1962), diuretic (Prezi-

osi, 1969), liver-protective, and lipid-lowering agents (Geb-

hardt, 1997).

Artichoke is a species belonging to the Asteraceae family,

which has been known since the 4th century B.C. as a food

and remedy. This plant has been appreciated by the ancient

Egyptians, Greeks, and Romans, who used it both as a food

and as a medicine (for their beneficial effects against hep-

ato-biliary diseases and as a digestive aid) (Marzi et al.,

1975; Sonnante et al., 2002). Globe artichoke still plays an

important role in human nutrition, especially in the Mediter-

ranean region. Globe artichoke contributes significantly to the

Mediterranean agricultural economy, with an annual produc-

tion of about 770,000 tonnes (t) (>60% of total global produc-

tion) from over 80 kha of cultivated land. Italy is the leading

world producer (about 474,000 t), followed by Spain

(215,000 t), France (55,000 t) and Greece (25,000 t). Globe arti-

choke is also cultivated in the Near East (Turkey and Iran),

North Africa (Egypt, Morocco, Algeria, Tunisia), South Amer-

ica (Argentina, Chile and Peru), and the United States (mainly

in California), and its cultivation is spreading in China

(65,000 t in 2007) (FAO, 2007; Bianco, 2005). The edible parts

of the artichoke plants are the large immature flowers (more

formally referred to as capitula), harvested in the early stages

of their development, which represent about the 3040% of its

fresh weight, depending on the variety and the harvesting

time. Since only the central portion of the capitula is con-

sumed, the ratio of edible fraction/total biomass produced

by the plant is very low, being less than 1520% of total plant

biomass. This ratio decreases further if the contribution to

the total biomass represented by offshoots, removed from

the field by common cultural procedures, is also considered

(Marzi & Lattanzio, 1981; Lattanzio, 1982).

Nutritional and pharmaceutical properties of both arti-

choke heads and leaves are linked to their special chemical

composition, which includes high levels of polyphenolic com-

pounds and inulin. Caffeic acid derivatives are the main phe-

nolic compounds in artichoke heads and leaves, with a wide

range of caffeoylquinic acid derivatives with chlorogenic acid

(5-O-caffeoylquinic acid) as the most important of these

derivatives. Other phenolics such as the flavonoids apigenin

and luteolin (both present as glucosides and rutinosides) as

well as different cyanidin caffeoylglucoside derivatives have

been identified in artichoke tissues (Aubert & Foury, 1981;

Lattanzio, 1981; Lattanzio & Van Sumere, 1987; Lattanzio

et al., 1989, 1994).

In addition, artichoke, like other members of the Astera-

ceae, synthesizes and accumulates inulin as a major carbohy-

drate reserve in their storage organs. Inulin molecules with a

chain length of up to 200, which is the highest degree of poly-

merization (DP) of inulin molecules known in plants, are pres-

ent in artichoke. Inulin belongs to a group of fructose-based

polysaccharides called fructans, which are not digested in

the small intestine because humans lack the enzymes re-

quired for hydrolysis of fructans. A further reason for the re-

cent interest in inulins has been due to the publication of data

showing that they positively influence the composition of the

gut microflora, and there are indications of beneficial effects

on mineral absorption, blood lipid composition, and preven-

tion of colon cancer. In addition, inulin is a low-calorie fibre

that has potential for use in the production of fat-reduced

foods (Frehner et al., 1984; Pollock, 1986; Darwen & John,

1989; Pontis, 1990; Carpita et al., 1991; Rapaille et al., 1995;

Hellwege et al., 1998; Roberfroid & Delzenne, 1998; Van Loo

et al., 1999; Hellwege et al., 2000).

2. Caffeoylquinic derivatives

The chemical components of artichoke have been studied

extensively and this plant has been found to be a rich source

of polyphenolic compounds, with mono- and dicaffeoylquinic

acids as the major chemical components (Lattanzio, 1981).

Artichoke accumulates various caffeic acid (3,4-dihydroxycin-

namic acid) depsides, positional isomers of caffeic acid esters

of quinic acid. Two mechanisms for the formation of such

esters have been described; one involving the hydroxycinna-

moyl-CoA thioester and the other one the 1-O-(hydroxycin-

namic acid)-acyl glucoside (Barz et al., 1985; Strack et al.,1987). The former mechanism was first shown to operate in

the formation of chlorogenic acid inNicotianacell-suspension

cultures (Stockigt & Zenk, 1974). However, it is now known

that both pathways can lead to the same product, depending

on the source of enzyme used, since recently it was shown

that Ipomoea root tissue catalyzes the formation of

chlorogenic acid from 1-O-caffeoylglucose (Villegas & Kojima,

1985; Villegas & Kojima, 1986). Moreover, alternative

esterification (transacylations) may also be possible. For

example, chlorogenic acid, which is common in Asteraceae,

may act as an acyl donor molecule for caffeoyltransferase

(Kojima & Kondo, 1985; Villegas et al., 1987; Strack & Gross,

1990).

As far as the sub-cellular localization of caffeoylquinic

derivatives is concerned, biochemical and ultrastructural evi-

dence suggests a strict compartmentalization in the synthe-

sis and transport of phenolic compounds in the cell. Such

compartmentalization may be considered as pathways con-

sisting of complexes composed of consecutively assembled,

membrane-associated enzymes, where end products of syn-

thesis are accumulated in a membrane enclosure. These ves-

icles could then be transported to the central vacuole for

internal sequestration or to the plasma membrane for secre-

tion. According to this mechanism, chloroplasts are involved

in some steps of phenolic biosynthesis leading to the forma-

tion of cinnamic acid derivatives. It is likely that cinnamic

units, formed at the level of phenylalanine-ammonia lyase

(PAL, EC 4.1.3.5) (associated with the endoplasmic reticulum),

are converted to quinic esters in the chloroplasts since the en-

zymes that catalyze the final steps in their biosynthesis are

described as chloroplastic: the association with chloroplasts

suggests that caffeoylquinic acids have a role in protecting

against light damage (Alibert et al., 1977; Alibert & Boudet,

1982; Boudet et al., 1985; Hrazdina & Wagner, 1985; Mondolot

et al., 2006).

Caffeic acid esters of quinic acid in artichoke extracts

have been well characterized, especially by the Panizzi group

starting from the 1950s (Panizzi & Scarpati, 1954, 1965;

Panizzi et al., 1954, 1955; Scarpati et al., 1957, 1964; Scarpati

132 J O U R N A L O F F U N C T I O N A L F O O D S 1 ( 2 0 0 9 ) 1 3 11 4 4


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& Esposito, 1963). The most well-known caffeoylquinic acid

derivative identified in artichoke extracts (heads and leaves),

even though it is not the most abundant, is cynarin. This

compound was isolated from artichoke leaf extracts and char-

acterized for the first time by Panizzi and Scarpati (1954).

Within the framework of a multidisciplinary research effort

to identify artichoke components that stimulate biliary secre-

tion and cholesterinic metabolism, they isolated a crystalline

substance showing these physiological activities. The sub-

stance exhibited left-handed rotatory power and a weak acid

reaction; i.e. a deep yellow and slightly stable in air alkaline

solution, and a green colour in the presence of ferric chloride.

In order to prevent confusion here, it must be pointed out

that in the 1950s and 1960s a pre-IUPAC nomenclature for

cyclitols (where the positional number of carbon atoms in

the quinic acid ring were assigned in an anticlockwise man-

ner; seeTable 1) was utilized. The effect of this was that cyn-

arin structure, initially described as 1,4-O-dicaffeoylquinic

acid (Panizzi et al., 1954), was identified as 1,5-O-dicaffeoyl-

quinic acid (Panizzi & Scarpati, 1965).

Other caffeoylquinic derivatives identified in artichoke

extracts are: 1-O-caffeoylquinic acid; 3-O-caffeoylquinic acid

(chlorogenic acid), 4-O-caffeoylquinic acid (cryptochlorogenic

acid), 5-O-caffeoylquinic acid (neochlorogenic acid), 1,3-O-

dicaffeoylquinic acid, 1,4-O-dicaffeoylquinic acid, and 3,5-O-

dicaffeoylquinic acid. All these compounds can be found in

both leaves and heads of artichoke: their relative abundance

is dependent on the solvent, the pH, and the temperature

used for their extraction (Panizzi et al., 1954, 1955; Scarpati

et al., 1957, 1964; Scarpati & Esposito, 1963; Dranik et al.,

1964; Panizzi & Scarpati, 1965; Michaud, 1967; Nichiforesco,

1970). In the 1970s and 1980s, following the advent of HPLC

(high performance liquid chromatography) techniques for

the separation and identification of plant phenolics, further

caffeoylquinic derivatives, namely 3,4-O-dicaffeoylquinic acid

and 4,5-O-dicaffeoylquinic acid, were identified (Fig. 1)

(Lattanzio et al., 1989, 1994).

At this point, it is paramount that the reader understands

that there were changes to the way caffeoylquinic acids were

classified in 1973, and according to the new IUPAC nomencla-

ture of cyclitols (positional number assigned to the carbon

atoms of the quinic acid ring in clockwise sense) (IUPAC,

1976), the structures of both mono- and dicaffeoylquinic acids

were renamed (Table 1). As a result, chlorogenic acid (for-

merly 3-O-caffeoylquinic acid), the most abundant phenolic

compound in artichoke tissues, is now called 5- O-caffeoylqui-

nic acid, while cynarin (formerly 1,5-O-dicaffeoylquinic acid)

became 1,3-O-dicaffeoylquinic acid. For the purposes of this

review, all subsequent references to caffeoylquinic acid struc-

tures will use the post-IUPAC nomenclature system.

Within the caffeoylquinic derivatives, chlorogenic acid

(5-O-caffeoylquinic acid) is the most abundant single compo-

nent (39%), followed by 1,5-O-dicaffeoylquinic acid (21%) and

3,4-O-dicaffeoylquinic acid (11%), based on total caffeoylqui-

nic acid contents (see Table 2). Cynarin (1,3-O-dicaffeoylqui-

nic acid) content in methanolic extracts of artichoke are

very low (about 1.5%). It should be remembered that the caf-

feoylquinic derivative content of artichoke tissues is highly

dependent on the physiological stage of the tissues: the total

caffeoylquinic acid content ranges from about 8% on dry mat-

ter basis in young tissues to less of 1% in senescent tissues)

(Lattanzio & Morone, 1979; Lattanzio & Van Sumere, 1987;

Lattanzio, 1981; Lattanzio et al., 1978, 2005; Adzet & Puigma-

cia, 1985).

Artichoke dry extracts are currently commercialized as

drugs mainly for treatment of liver diseases: these include

Cynara (200 mg of artichoke extract; Vesta Pharmaceuticals,

Inc.), Artichoke 500 mg (artichoke leaf extract; Jarrow For-

mula, Inc.), Artichoke (artichoke leaf extract containing 0.3%

flavonoids expressed as luteolin-7-O-glucoside and 2.5% caf-

feoylquinic acid expressed as chlorogenic acid, Indena

S.p.A.), CINARAN (artichoke flowering head extracts contain-

ing 1318% of caffeoylquinic acids, Indena S.p.A.) among oth-

ers (Llorach et al., 2002). This growing commercial utilization

of artichoke active principle as choleretic, hypocholestero-

lemic, and antidyspeptic compounds, and the need to de-

scribe the active principals, requires that there is great care

in use of the nomenclature of caffeoylquinic derivatives. As

previously stated, 1,5-O-dicaffeoylquinic acid is one of the

most abundant phenolic compounds in artichoke tissues,

while the content of 1,3-O-dicaffeoylquinic acid in methanolic

extracts of artichoke is very low. Therefore, to establish the

right nomenclature of cynarin (1,3-O-dicaffeoylquinic acid or

1,5-O-dicaffeoylquinic acid, depending on the IUPAC rules uti-

lized), is of fundamental importance not only from a system-

atic viewpoint but also from an economic point of view.

Table 1 Nomenclature of artichoke mono- and dicaffeoylquinic esters.

IUPAC recommendations, 1973a Pre-IUPAC numbering

1-O-Caffeoylquinic acid 1-O-Caffeoylquinic acid

3-O-Caffeoylquinic acid (Neochlorogenic acid) 5-O-Caffeoylquinic acid

4-O-Caffeoylquinic acid (Cryptochlorogenic acid) 4-O-Caffeoylquinic acid

5-O-Caffeoylquinic acid (Chlorogenic acid) 3-O-Caffeoylquinic acid

1,3-O-Dicaffeoylquinic acid (Cynarin) 1,5-O-Dicaffeoylquinic acid

1,4-O-Dicaffeoylquinic acid 1,4-O-Dicaffeoylquinic acid





a IUPAC (1976).

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Fig. 1 Artichoke mono- and dicaffeoylquinic acids (according to IUPAC, 1976).

Table 2 Mono- and dicaffeoylquinic acids in artichoke heads of marketable quality (adapted from Lattanzio et al., 1994).

Caffeoylquinic acid derivative mg/100 g dry weight

1-O-Caffeoylquinic acid 38.14




1,3-O-Dicaffeoylquinic acid 61.24








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The presence of caffeoylquinic esters in artichoke tissues

is responsible for the appearance of browning phenomena

which occur through enzymatic oxidation of orthodihydroxy-

phenolic substrates by polyphenol oxidase (PPO, EC 1.14.18.1)

or to formation of iron-chlorogenic acid complexes (Lattanzio,

2003). Browning of raw fruit and vegetables during handling

and storage is a significant problem for the food industry

and is believed to be one of the main causes of quality loss

during storage of plant commodities. While enzymatic oxida-

tions of phenolics generally promote brown discoloration in

plant tissues, mechanically damaged ironphenol complexes

are relevant during processing of some fruits and vegetables

such as potatoes, cauliflowers, asparagus and olives. This lat-

ter mechanism of darkening has been observed in stored

plant commodities, in good agreement with the fact that in

healthy, non-mechanically damaged plant tissues, the ripen-

ing process induces changes in cell membrane permeability,

in phenolic metabolism, and in PPO properties: as the fruit

ages more enzyme becomes soluble. Non-enzymatic brown-

ing reactions, caused by iron-polyphenol complexing, may oc-

cur in cold-stored non-mechanically damaged artichoke

heads. During storage of artichoke heads at 4 C low-temper-

ature induction of PAL activity causes a biosynthetic increase

of phenolics, especially chlorogenic acid. On the other hand,

PPO activity does not change significantly during the storage

period. Therefore, the increased content of phenolics is suffi-

cient to provide an adequate substrate for the browning phe-

nomena. These reactions start from the chloroplasts, the site

of chlorogenic acid biosynthesis where the iron is stored as

ferritin. The release of ferritin iron, as Fe2+, is induced by

chlorogenic acid, producing a colourless complex with an ex-

cess of chlorogenic acid. Subsequently, oxidizing conditions

occurring during the senescence process and/or low temper-

ature-induced formation of toxic oxygen products forms lead

to the formation of a grey-blue chlorogenic acid/Fe3+ complex

and subsequently the browning phenomena (Lattanzio et al.,

1994).

3. Flavonoids

Besides caffeoylquinic acid derivatives, other phenolics

belonging to the flavonoid class such as the flavones apigenin

and luteolin, and the anthocyanidins cyanidin, peonidin, and

delphinidin have been identified in artichoke tissues. Apige-

nin and luteolin glycosides have been detected in both leaves

and artichoke heads, while anthocyanin pigments are presentonly in capitula. From a quantitative viewpoint these com-

pounds are considered minor constituents of the total phen-

olics content (about 10% or less) of artichoke tissues.

Nevertheless, luteolin is a strong antioxidant that protects

low density lipoproteins from oxidation while anthocyanin

pigments, besides their health-promoting properties, play

an important role in the appearance of food plants and there-

fore in food acceptance by consumers (Aubert & Foury, 1981;

Lattanzio, 1981; Lattanzio & Van Sumere, 1987; Lattanzio

et al., 1994; Brown & Rice-Evans, 1998).

Fig. 2shows the most representatives flavone glycosides

identified in artichoke tissues: luteolin-7-O-b-D-glucopyrano-

side (luteolin-7-O-glucoside = cynaroside) (I), luteolin-7-O-a-

L-rhamnosyl(1 !6)-b-D-glucopyranoside (luteolin-7-O-ruti-

noside = scolymoside) (II), apigenin-7-O-b-D-glucopyranoside

(apigenin-7-O-glucoside) (III), apigenin-7-O-a-L-rhamno-

syl(1 !6)-b-D-glucopyranoside (apigenin-7-O-rutinoside) (IV)

(Lattanzio, 1981; Lattanzio & Van Sumere, 1987; Lattanzio

et al., 1994; Fritsche et al., 2002; Schutz et al., 2004; Zhu

et al., 2004). More recently, two flavanone glycosides (naringe-

nin-7-O-glucoside and naringenin-7-O-rutinoside) have been

identified as minor phenolic compounds in artichoke (San-

chez-Rabaneda et al., 2003; Schutz et al., 2004). However,

these observations require verification.

Anthocyanin pigments are responsible for most of the

blue, purple, red and intermediate hues of plant tissues: gen-

erally an increase in anthocyanin pigmentation is considered

a positive attribute of plant foods. The anthocyanin pattern of

artichoke heads, whose colour ranges from green to violet,

has been investigated initially byFoury and Aubert (1977), Pif-

feri and Vaccari (1978), and byAubert and Foury (1981), who

tentatively identified some cyanidin glycosides: cyanidin

3-O-b-glucoside (V), cyanidin 3-O-b-sophoroside (VI), cyanidin

3-caffeoylglucoside, cyanidin 3-caffeoylsophoroside, cyanidin

3-dicaffeoylsophoroside, and cyanidin 3,5-diglucoside (VII).

More recentlySchutz et al. (2006a)found that the main antho-

cyanins in artichoke heads were cyanidin 3,5-diglucoside,

cyanidin 3-O-b-glucoside, cyanidin 3,5-malonyldiglucoside,

cyanidin 3-(300-malonyl)glucoside (VIII), and cyanidin 3-(600-

malonyl)glucoside (IX). Besides the main anthocyanins, sev-

eral minor compounds, consisting of aglycones other than

those of cyanidin, have been found. Among these, two peoni-

din derivatives and one delphinidin derivative have been

characterized by high performance liquid chromatography

electrospray ionization mass spectrometry: the two peonidin

derivatives were identified as peonidin 3-O-b-glucoside (X)

and peonidin 3-(600-malonyl)glycoside (XI)(Fig. 3).

4. Inulin

Fructans are a diverse group of linear or branched fructose

(oligo)polymers that contain one or more b-linked fructose

units. In the most prominent structural types, inulin and le-

van, the fructose chain emerges from the fructose part of a

sucrose molecule, proceeding via b-2,1- and b-2,6-linkages,

respectively. Besides inulin and levan, the so-called neo-kes-

tose series has been described where chain elongation occurs

at the glucose portion of sucrose or in both directions (Rober-

froid & Delzenne, 1998; Heyer et al., 1999). Fructans are ofgrowing interest as functional food ingredients because of

their potential benefits for human health. As human enzymes

cannot digest fructans, they reach the colon and serve as a

substrate for enterobacterial growth. Fructan containing diets

selectively stimulate bifidobacteria and make them the pre-

dominant species (Roberfroid et al., 1998). Consequently, an

increased fecal content of short-chain fatty acids and a de-

creased concentration of tumour-promoting substances, such

as ammonia, is observed (Gallaher et al., 1996; Heyer et al.,

1999).

Inulin is a highly water-soluble carbohydrate, which serves

as an alternative storage carbohydrate in the vacuole of

approximately 15% of all flowering plant species. Inulin-type



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fructans are mainly found in dicot species belonging to the

Asteraceae, including well-investigated species such as chic-

ory (Cichorium intybus L.), Jerusalem artichoke (Helianthus

tuberosusL.), artichoke (C. scolymus), dandelion (Taraxacum offi-

cinale), dahlia (Dahlia variabilis) and yacon (Polymnia sonchifolia)

(Hellwege et al., 1998, 2000). Unlike dietary carbohydrates that

are absorbed as hexose sugars (glucose, fructose) and which

have a caloric value of 3.9 kcal/g (16.3 kJ/g), and whose cellular

metabolism produces about 38 mol ATP/mol, inulin and oligo-

fructose resist digestion and they are not absorbed in the

upper part of the gastrointestinal tract [=non-digestible oligo-

saccharides (NDO)]. After oral ingestion, they reach the colon

intact where they are hydrolyzed and extensively fermented

by saccharolytic bacteria. Depending on both the degree of

their colonic fermentation and the assumptions of the model

used, the caloric value of such non-digested but fermented

carbohydrates varies between 0 and 2.5 kcal/g (Roberfroid,

1999a). As far as the functional food properties of NDO is con-

cerned: (i) there is strong evidence for a prebiotic effect of

NDO in human subjects (a prebiotic effect was defined as a

food-induced increase in numbers and/or activity predomi-

nantly of bifidobacteria and lactic acid bacteria in the human

large intestine); (ii) there is strong evidence for a positive ef-

fect of NDO on bowel habit; (iii) there is emerging evidence

that consumption of inulin-type fructans may result in in-

creased Ca absorption in man; (iv) there are preliminary indi-

cations that inulin-type fructans interact with the

functioning of lipid metabolism (Van Loo et al., 1999). Re-

search in experimental animal models has revealed that inu-

lin-type fructans have anticarcinogenic properties. A number

of studies report the effects of inulin-type fructans on chem-

ically induced pre-neoplastic lesions or tumours in the colon

HO

O

HOOH

HO

O

O

OH

OH

OH

O

HO

O

HOOH

CH2 O

O

OH

OH

OH

O

O

H3CHO

HO

HO

O

HO

O

HOOH

HO

O

O

OH

OH

O

HO

O

HOOH

CH2 O

O

OH

OH

O

O

H3CHO

HO

HO

O

I

II

III

IV

Fig. 2 Flavone glycosides identified in artichoke tissues.



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of rats and mice. The effects have been reported to be associ-

ated with gut flora-mediated fermentation and production of

butyrate. In human cells, inulin-derived fermentation prod-

ucts inhibited cell growth, modulated differentiation and re-

duced metastasis activities. Evidence that shows that

inulin-type fructans and corresponding fermentation prod-

ucts reduced the risks for colon cancer has been accumulat-

ing. The proposed mechanisms include reducing the

exposure to mutagens and carcinogens, and suppression of

tumour cell survival (Pool-Zobel, 2005).

As previously stated, globe artichoke synthesizes inulin

molecules with a chain length of up to 200 (Hellwege et al.,

2000). A high molecular weight inulin has also been extracted

from artichoke agro-industrial wastes where the source was

the external bracts and the average degree of polymerization

was 46, higher than found in Jerusalem artichoke, chicory,

and dahlia inulins. The differences in the average degree of

polymerization (DPn) between different inulins account for

their distinctly different functional attributes. Long chain

length inulins are less soluble, and they have the ability to

form inulin microcrystals when sheared in water or milk.

These crystals are not discretely perceptible in the mouth,

but they interact to form a smooth creamy texture and pro-

vide a fat-like mouth sensation. Inulin has been used success-

fully to replace fat in table spreads, baked goods, fillings, dairy

products, frozen desserts and dressings. Artichoke inulin is

Fig. 3 Anthocyanins identified in artichoke heads.



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moderately soluble in water (maximum 5% at room tempera-

ture), it has a bland neutral taste, without any off-flavour or

aftertaste, and is not sweet. Therefore, it combines easily with

other ingredients without modifying delicate flavours (Lopez-

Molina et al., 2005).

The edible part of artichoke heads is characterized by a

high reducing sugar content and a high percentage of

water-soluble polysaccharides (inulin) (Table 3), mainly lo-

cated in the receptacle: the inulin content may represent still

75% of the total glucidic content. In addition, the inulin con-

tent of the edible portion is relatively higher (about 30% more)

in artichoke heads of marketable quality compared to those

at earlier stages of development (Lattanzio et al., 2002).

Fig. 4shows the variability of inulin content in the edible

portion of different cultivars of globe artichoke. Inulin con-

tents range between 18.9% and 36.2% on a dry matter basis:

the highest content of inulin has been found in cv. Romane-

sco and the lowest inulin content in cv. Violet Margot. The ob-

served variability in inulin content could be due to the

samples use for analysis being at different physiological

stages, since it virtually impossible to establish in an accurate

way the morphological age of different artichoke heads. Sim-

ilarly, morphological differences are the main factor deter-

mining the inulin content in different cultivars: e.g. cv.

Romanesco, whose receptacle contributes more to the total

weight of the capitula than cv. Violet of Provenza, has an inu-

lin content of 36.2% of dry weight (d.w.) compared to only

21.5% of d.w. for that of Violet of Provence (Lattanzio et al.,

2002). Although the inulin content in by-products originating

from artichoke processing (leaves, external bracts of heads) is

more than 30% lower than that of the edible part, these by-

products could be considered a promising and cheap source

of inulin and fructose.

5. Therapeutic properties

Long known as an herbal medicine, the dried leaves of arti-

choke have long been used in folk medicine for their choleret-

ic and hepatoprotective activities, that are often related to the

cynarin content (Cairella & Vecchi, 1969; Preziosi, 1969). In

various pharmacological test systems, artichoke leaf extracts

have shown hepatoprotective (Eberhardt, 1973; Adzet et al.,

1987), anticarcinogenic (Clifford, 2000), antioxidative (Geb-

hardt, 1997; Gebhardt & Fausel 1997; Brown & Rice-Evans,

1998; Jimenez-Escrig et al., 2003), antibacterial, anti-HIV,

bile-expelling, and urinative activities (Cairella & Vecchi,

1969; Preziosi, 1969) as well as the ability to inhibit cholesterol

biosynthesis and LDL oxidation (Clifford & Walker, 1987; Eng-

lisch et al., 2000). These broad therapeutic indications cannot

be ascribed to a single compound, but to several active com-

pounds providing additive or synergistic pharmacologic ef-

fects, including mono-caffeoylquinic and dicaffeoylquinic

acids, and flavonoids such as luteolin and its 7-O-glucoside

(Brown & Rice-Evans, 1998; Speroni et al., 2003; Wang et al.,

2003; Schutz et al., 2004, 2006b).

The hepatoprotective activity against CCl4 toxicity in iso-

lated rat hepatocytes (an experimental model widely used

to mimic several aspects related to liver pathology character-

ized by increased lipid peroxidation and cytotoxicity due to

oxidative stress) of some polyphenolic compounds, such as

cynarin, isochlorogenic acid, chlorogenic acid, luteolin-7-O-

glucoside, and two organic acids (caffeic and quinic) from C.

scolymus has been reported (Preziosi, 1969; Adzet et al.,

1987). The toxic manifestations of CCl4in isolated rat hepato-

cytes is typically detected by glutamate oxaloacetate trans-

aminase and glutamate pyruvate transaminase leakage. In

these experiments only cynarin and, to a lesser extent, caffeic

acid showed cytoprotective action, and this demonstrates

that the activity of cynarin is attributable only to the caffeoyl

moiety. The observed effects of cynarin and caffeic acid have

been assigned to the antioxidant activity of these compounds,

which prevents the CCl4-induced oxidation of the phospho-

lipids that are constituents of the hepatocyte membranes.

Gebhardt and Fausel (1997)show that aqueous artichoke ex-

tracts reduce lipid peroxidation (measured as production of

malondialdehyde) and cytotoxicity (measured as lactate

dehydrogenase leakage) in cultures of rat primary hepato-

cytes exposed to tert-butyl hydroperoxide (t-BHP). Further-

more, artichoke extracts prevented the corresponding loss

of intracellular glutathione caused byt-BHP, which in turn in-

duces lipid peroxidation. In contrast to the findings ofAdzet

et al. (1987), thet-BHP assay shows that a variety of artichoke

specific compounds, like cynarin and luteolin 7-O-glucoside,

as well as other phenolic compounds such as caffeic and

chlorogenic acids, all of which are present in artichoke, may

contribute to the hepatoprotective potential of these extracts.

In addition, it has been observed that extracts are resistant to

tryptic digestion, boiling, acidification, and other treatments,

but are slightly sensitive to alkalinisation (Gebhardt, 1997).

A traditional use of artichoke leaf extract in gastroenterol-

ogy is mainly based upon its strong antidyspeptic actions

which are mediated through its choleretic activity. Saenz

Rodriguez et al. (2002) investigated the effects of artichoke

leaf extracts on bile flow and the formation of bile com-

pounds in anaesthetised Wistar rats after acute and repeated

oral administration. A significant increase in bile flow was ob-

served after acute treatment with artichoke extract as well as

after repeated administration. The choleretic effects of arti-

choke extract were similar to those of the reference com-

pound dehydrocholic acid. A strong artichoke extract-

Table 3 Glucidic content in the edible portion of artichoke heads cv. Romanesco (adapted fromLattanzio et al., 2002).

% Fresh weight % Dry weight

Glucose 0.44 3.18

Fructose 0.18 1.27

Sucrose 0.98 6.98

Inulin 5.18 37.00



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induced increase in total bile acid concentration over the en-

tire experiment was observed. With the highest dose (400 mg/

kg), a significant increase was obtained after single and re-

peated administration. The bile acids-induced effects of arti-

choke leaf extracts were much more pronounced than those

of the reference compound (dehydrocholic acid). Preziosi

et al. (1959)observed a dose/activity relationship for cynarin

on choleresis: 1530 mg/kg of cynarin caused an increased

secretion of bile similar to that of equimolecular doses of

Na-dehydrocholate. Higher doses of cynarin (75100 mg/kg),

caused a bile secretion 130% higher compared to basal values,and this in turn caused an increased elimination of biliary

cholesterol. This increased biliary flux coincided with an in-

crease in urine secretion. The same authors reported that this

diuretic activity was induced by both cynarin and artichoke

extracts.Gebhardt (2001, 2002a), when studying the effect of

water-soluble extracts of artichoke leaves on choleresis using

primary cultured rat hepatocytes and cholephilic fluorescent

compounds, noticed that the artichoke leaf extracts not only

stimulated biliary secretion, but also re-established it when

secretion was inhibited by addition of taurolithocholate to

the culture medium. Furthermore, taurolithocholate-induced

bizarre bile canalicular membrane distortions, detectable by

electron microscopy, could be prevented by artichoke leaf ex-tracts in a dose-dependent manner when added simulta-

neously with the bile acid. These effects were exerted by

the flavone luteolin and, to a lesser extent, by luteolin-7-O-

glucoside. These results demonstrate that artichoke leaf ex-

tracts exert a potent anticholestatic action at least in the case

of taurolithocholate-induced cholestasis and that luteolin

may contribute significantly to this effect.

Artichoke extract retarded low density lipoprotein (LDL)

oxidation in a dose-dependent manner as measured by a pro-

longation of the lag phase of conjugated diene formation, a

decrease in the rate of propagation, and a sparing effect on

the a-tocopherol within the LDL. The isolated flavone agly-

cone luteolin (1 lM) demonstrated an efficacy similar to that

of 20lg/ml artichoke extract in inhibiting lipid peroxidation.

Luteolin-7-O-glucoside also demonstrated a dose-dependent

inhibition of LDL oxidation but was less effective than luteo-

lin. In addition, studies of the copper-chelating properties of

luteolin-7-O-glucoside and its aglycon luteolin suggest a po-

tential role for chelation in the antioxidant effects of arti-

choke extracts. It is therefore considered that the

antioxidant activity of artichoke extracts relates in part to

its flavonoids, which act as hydrogen donors and metal ion

chelators, and in part to the increased effectiveness imparted

by their portioning between the aqueous and lipophilicphases (Brown & Rice-Evans, 1998).

Artichoke leaf extracts have been used for treating hyper-

cholesterolemia, a metabolic derangement directly associ-

ated with an increased risk for coronary heart disease and

other sequelae of atherosclerosis. In this connection, it has

been shown by Gebhardt (1998) that aqueous extracts from

artichoke leaves applied at high-doses were able to inhibit

cholesterol biosynthesis from 14C-acetate in primary cul-

tured rat hepatocytes in a concentration-dependent biphasic

manner with moderate inhibition (approximately 20%) be-

tween 0.007 and 0.1 mg/ml and strong inhibition at 1 mg/

ml. Cytotoxic effects (evidenced by lactate dehydrogenase

leakage and the 3-[4,5-dimethylthiazol-2-yl]-2,5-dephenyltetrazolium bromide assay) were restricted to higher concen-

trations. Inhibition was observed to occur in a time-depen-

dent manner, to last for several hours even after washing

out the extracts with fresh medium, and to be fully revers-

ible within 20 h of removing the extracts. In addition, the

stimulation of hydroxymethylglutaryl-CoA-reductase (EC

1.1.1.34) activity by insulin was efficiently blocked by the ex-

tracts, although other insulin-dependent phenomena, such

as increased lactate production, were not influenced. These

results suggest an indirect modulation of hydroxymethyl-

glutaryl-CoA-reductase activity as the most likely inhibitory

mechanism of the artichoke extracts. Screening of individual

phenolic constituents of artichoke extracts revealed that

Fig. 4 Inulin content (% d.w.) in artichoke cultivars (adapted fromLattanzio et al., 2002).



10/14

luteolin-7-O-glucoside and particularly its aglycone luteolin

were mainly responsible for the inhibition, whereas chloro-

genic acid was much less effective and caffeic acid, cynarin

and other dicaffeoylquinic acids did not exert significant ef-

fects. It has also been shown that inhibition of cholesterol

biosynthesis by artichoke extracts is enhanced by pre-treat-

ment with b-glucosidase, and further experiments showed

that cynaroside is indeed a substrate of b-glucosidase and

that the liberated luteolin is responsible for the inhibitory ef-

fect (luteolin also efficiently blocked the insulin effect on

cholesterol biosynthesis) (Gebhardt, 2002b).

Finally, endothelial dysfunction, which is more often ob-

served in conduit arteries such as the aorta, carotid, femoral,

and brachial arteries, is largely due to alterations in cellular

signal transduction initiated by an escalating cycle of damage

triggered by oxidative stress. This phenomenon is exacer-

bated in the elderly, where a progressive loss of vascular

endothelial function and concurrent loss of vasomotor con-

trol is frequent. In this connection,Rossoni et al. (2005)dem-

onstrated that the wild artichoke ( C. cardunculus) is able to

increase the production of the vasorelaxant factor nitric oxide

by cultured aortic endothelial cells. They also demonstrated

that luteolin and apigenin, the two flavone aglycones identi-

fied in wild artichoke, improve aortic relaxation when added

to the incubation bath. Moreover, the feeding of wild arti-

choke [10 mg (kg of polyphenols)1 day1] to aged rats signif-

icantly restored proper vasomotion to a level similar to that

observed in young animals.Li et al. (2004)focused their atten-

tion on production of nitric oxide (NO) by endothelial NO syn-

thase (eNOS) as an antithrombotic and anti-atherosclerotic

principle in the vasculature. Hence, an enhanced expression

of eNOS in response to pharmacological interventions could

provide protection against cardiovascular diseases. These

authors have shown that artichoke flavonoids are likely to

represent the active ingredients mediating eNOS upregula-

tion. They observed that in EA.hy 926 cells, a cell line derived

from human umbilical vein endothelial cells (HUVECs), an

artichoke leaf extract increased the activity of the human

eNOS promoter (determined by luciferase reporter gene as-

say). Interestingly, the flavonoids luteolin and cynaroside in-

creased eNOS promoter activity and eNOS mRNA

expression, whereas the caffeoylquinic acids cynarin and

chlorogenic acid were without effect. Thus, in addition to

the lipid-lowering and antioxidant properties of artichoke,

an increase in eNOS gene transcription may also contribute

to its beneficial cardiovascular profile.

6. Nutraceutical production

Considering together the findings within the existing litera-

ture concerning artichokes, it is evident that the by-products

originating from artichoke processing could be considered a

promising source of inulin and also of phenolics that can be

considered a raw material for food ingredient production.

Artichoke by-products such as leaves, external bracts and

stems produced by the artichoke processing industry repre-

sent a huge amount of discarded material (about 8085% of

the total biomass produced by the plant), which has the po-

tential to be used as a source of health-promoting inulin

and phenolics (Llorach et al., 2002; Lattanzio et al., 2005).

The current thinking in the field of diet and health research

is that non-nutrient components of diets, although not essen-

tial for life, can modulate various functions at the cell, tissue

and whole body levels in such ways that good health is main-

tained and age-related diseases are delayed or prevented. Re-

lated to this concept is that of functional foods. Following

regulatory changes in Europe, it will be necessary for func-

tional foods to have any claims relating to health benefits

authorised and it is envisaged that functional foods may be-

come thought of as foods for which a claim has been authorised.

A food can be regarded as functional if it is satisfactorily dem-

onstrated to affect beneficially one or more target functions in

the body, beyond adequate nutritional effects, in a way which

is relevant to either the state of well-being and health or the

reduction of the risk of a disease. In this connection, the func-

tional food components of artichoke are inulin-type fructans

and various secondary metabolites, especially polyphenolic

compounds. Inulin-type fructans are non-digestible oligosac-

charides that are classified as dietary fibre. The targets for

their functional effects are the colonic microflora that use

them as selective fertilizers; the gastrointestinal physiology;

the immune functions; the bioavailability of minerals; and

the metabolism of lipids. Potential health benefits may also

concern reductions in the risk of some diseases like intestinal

infections, constipation, non-insulin-dependent diabetes,

obesity, osteoporosis or colon cancer (Roberfroid, 1999b; Rob-

erfroid, 2002). As far as artichoke phenolic components are

concerned, much of the research has focused on the antioxi-

dant activity of artichoke leaf extracts. Leaf extracts have

been reported to show antioxidative and protective properties

against hydroperoxide-induced oxidative stress in cultured

rat hepatocytes (Gebhardt, 1997), to protect lipoprotein from

oxidation in vitro (Brown& Rice-Evans, 1998), to inhibit hemo-

lysis induced by hydrogen peroxide, and to inhibit oxidative

stress when human cells are stimulated with agents that gen-

erate reactive oxygen species such as hydrogen peroxide (Per-

ez-Garcia et al., 2000). Nowadays there is a growing interest

towards dietary supplements together with natural non-toxic

food additives. Foods are among the most rapidly growing

sectors in the food and personal care product industry. This

development is due to the loss of consumer confidence in

the modern diet, the aging population, and finally an overall

enhancement in health awareness and disease prevention

among customers (Schutz et al., 2006b).

Lopez-Molina et al. (2005)have prepared a high molecular

weight inulin from artichoke agro-industrial wastes using

environmentally benign aqueous extraction procedures.

Physico-chemical analysis of the properties of artichoke inu-

lin was reported. The average degree of polymerization was

46, which is higher than for Jerusalem artichoke, chicory,

and dahlia inulins. GCMS confirmed that the main constitu-

ent monosaccharide in artichoke inulin was fructose and its

degradation by inulinase indicated that it contained the ex-

pectedb-2,1-fructan bonds. The FT-IR spectrum was identical

to that of chicory inulin. These data indicate that artichoke

inulin is likely to be suitable for use in a wide range of food

applications. In this connection, fat and carbohydrate

replacement with artichoke inulin could offer the advantage

of not compromising taste and texture, while delivering nutri-

tionally enhanced products.



11/14

Artichoke by-products are also a potential good source of

antioxidant activity because it contains large amounts of

polyphenols that possess high antioxidant activity. Llorach

et al. (2002)have used fast and commercially feasible proto-

cols to extract antioxidant phenolics from artichoke by-prod-

ucts: raw artichoke (RA), blanched (thermally treated)

artichoke (BA), and artichoke blanching waters (ABW). Two

protocols, with possible industrial applicability, based on both

methanol and water extractions have been described. Pheno-

lic contents (expressed as caffeic acid derivatives) (grams per

100 g of dry extract) were 15.4 and 9.9 for RA when extracted

with methanol and water, respectively; 24.3 and 10.3 for BA

when extracted with methanol and water, respectively; and

finally, 11.3 g of phenolics/100 mL of ABW. The higher amount

of phenolics in BA could be due to the inactivation of polyphe-

nol oxidase (PPO) at the industrial scale (due to blanching pro-

cess), avoiding PPO-catalyzed oxidation of these phenolics, a

phenomenon that could occur in RA by-products. The authors

suggest that the functionalization of foodstuffs by adding

artichoke by-product extracts should be considered. To this

purpose, sensory modification of foodstuffs, as well as the

stability and activity of artichoke extracts within food matri-

ces, should be investigated. In addition, toxicological studies

should be carried out to ascertain the boundary between

health-beneficial effects and risk of harm.

Lattanzio et al. (2005) have evaluated methanolic extracts

of artichoke by-products (offshoots, leaves and external

bracts of artichoke heads) for their phenolic antioxidants.

The artichoke extracts were assessed for their protective role

in the control of oxidative damage to biological molecules

(proteins, lipids and DNA), caused by free radicals such as

RCOO and/or OH, using the b-carotene/linoleate assay, the

deoxyribose assay and the metmyoglobin assay. Artichoke

by-products are rich in phenolic compounds, especially chlor-

ogenic acid and 1,5-O-dicaffeoylquinic, 3,5-O-dicaffeoylquinic

and 3,4-O-dicaffeoylquinic acids. When the biological activity

of artichoke extracts is considered, the presence of luteolin-7-

glucoside and hydrolysable tannins, besides caffeoylquinic

derivatives, in the phenolic fraction of these extracts must

be taken into account: all these phenolics possess a good anti-

oxidant activity against peroxyl and hydroxyl radicals when

assessed using the b-carotene/linoleate assay and the met-

myoglobin assay.

Ready-to-eat foods such as soups are in great demand by

consumers. In this context, the addition of new health-pro-

moting active ingredients such as polyphenols could repre-

sent an important way to increase the dietary intake of

these compounds.Llorach et al. (2005)analysed an artichoke

by-products aqueous extract and reported that it contained a

high level of polyphenols (100 mg of polyphenols/g of dry ex-

tract), comprising mainly of caffeic acid derivatives. A sensory

panel with four trained judges evaluated soups to which dif-

ferent amounts of the extracts had been added and discov-

ered that up to 10 mg of extract/mL of soup could be added

without compromising the acceptability of the soup, which

was compared to an unadulterated soup. Further, the antiox-

idant capacity, evaluated as free radical scavenging activity

(ABTS+ assay) and ability to reduce the 2,4,6-tripyridyl-S-tri-

azine (TPTZ)-Fe(III) complex to TPTZ-Fe(II) (FRAP assay), was

substantially increased with addition of the extracts.

7. Conclusions

Globe artichoke is a large immature flower rich in medicinal

substances. It is considered one of the most important veg-

etable crops in the countries bordering the Mediterranean

basin. Globe artichoke is also cultivated, although to a lesser

extent, in the Near East, North Africa, South America, and

the United States. Globe artichoke has important nutritional

values due to its particularly high content of bioactive phe-

nolic compounds, such as caffeoylquinic derivatives and

flavonoids, but also due to substantial amounts of inulin, fi-

bres and minerals. The economic use of the crop is currently

mainly focussed on the consumption of the edible immature

flower heads (capitula), commonly referred to as heads, ea-

ten as a fresh, canned or frozen vegetable, and more re-

cently, demand has been increased because of its

reputation as a health food. Furthermore leaves, stems,

and roots are used to feed livestock. These raw material

may be exploited for either the extraction of inulin, a

water-soluble and low caloric carbohydrate, whose beneficial

effects have been reported to be associated with gut flora-

mediated fermentation and production of butyrate, or phe-

nolic compounds, especially caffeoylquinic derivatives, bio-

active substances which are reported to exert beneficial

effects in the treatment of hepato-biliary diseases, hyperlip-

idaemia, dropsy, rheumatism and cholesterol metabolism.

Clinical and pre-clinical trials have confirmed the therapeu-

tic potential of this plant: among all the plants used in folk

medicine against liver complaints artichoke can be consid-

ered the most effective.

As a consequence, due to the considerable interest in pre-

ventive medicine and in the food industry in the development

of natural antioxidants from botanical sources, research has

focussed on elucidating the composition of the artichoke phe-

nolic fraction from a qualitative (four mono-caffeoylquinic

isomers, six dicaffeoylquinic isomers, six flavonoid glyco-

sides, and at least seven anthocyanins have been identified)

and quantitative viewpoint, as well as the mechanisms

underlying the therapeutic activity of artichoke extracts.

These studies confirm the popular use of artichoke for the

treatment of several ailments and reveal that this therapeuti-

cal activity is probably primarily due to the phenolic structure

of these substances, which may function to inhibit free radi-

cal-mediated processes.

Besides the external bracts, the fleshy and developed arti-

choke root system could be used as a source of inulin. Cur-

rently, commercially available inulins are obtained mainly

from chicory, Jerusalem artichoke, and dahlia. Artichoke inu-

lin presents similar physico-chemical properties to high per-

formance chicory inulin but an even higher degree of

polymerization, which makes artichoke inulin desirable for

applications in the food industry. Fat and carbohydrate

replacement with artichoke inulin could offer the advantage

of not compromising taste and texture, while delivering nutri-

tionally enhanced products.

As far as the functionalization of foodstuffs through use

ofartichoke by-products is concerned, sensory modification of

foodstuffs, as well as the stability and activity of artichoke ex-

tracts within food matrices, should be investigated. In addi-

tion, toxicological studies should be also carried out to



12/14

ascertain the boundary between health-beneficial effects and

the risk of toxicity.

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