The caper (Capparis L.): Ethnopharmacology, phytochemical and pharmacological properties

The caper (Capparis L.): Ethnopharmacology, phytochemical and pharmacological properties

Fitoterapia 82 (2011) 93–101 Contents lists available at ScienceDirect Fitoterapia j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l ...

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Fitoterapia 82 (2011) 93–101

Contents lists available at ScienceDirect

Fitoterapia j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / f i t o t e

Review

The caper (Capparis L.): Ethnopharmacology, phytochemical and pharmacological properties Nizar Tlili a,c,⁎, Walid Elfalleh b, Ezzeddine Saadaoui c, Abdelhamid Khaldi c, Saida Triki a, Nizar Nasri a a b c

Laboratoire de Biochimie, Département de Biologie, Faculté des Sciences de Tunis, Université Tunis El-Manar, Tunis 2092, Tunisia Laboratoire d'Aridoculture et Cultures Oasiennes, Institut des Régions Arides de Médenine, 4119, Tunisia Unité de Recherche Gestion et Valorisation des Ressources Forestières, INRGREF, BP: 10 Ariana 2080, Tunisia

a r t i c l e

i n f o

Article history: Received 6 January 2010 Accepted in revised form 6 September 2010 Available online 16 September 2010 Keywords: Caper (Capparis) Ethnopharmacology Chemistry Biological activity

a b s t r a c t Caper (Capparis L.), a shrub plant with a large natural distribution, is used in traditional medicines to cure various illnesses. Phytochemicals studies have shown the presence of many beneficial compounds such as spermidine, rutin, quercetin, kaempferol, stigmasterol, campesterol, tocopherols, and carotenoids. Biological studies reveal important antimicrobial, anti-oxidative, anti-inflammatory, immunomodulatory and antiviral properties. The presented review summarizes information concerning the morphology, ethnopharmacology, phytochemistry, and biological activities of caper plants. © 2010 Elsevier B.V. All rights reserved.

Contents 1. 2. 3. 4. 5.

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Introduction . . . . . . . . . . . . . . . . . . . . . Origin and morphology . . . . . . . . . . . . . . . . Environmental condition and cultivation . . . . . . . . Ethnopharmacology . . . . . . . . . . . . . . . . . . Phytochemistry . . . . . . . . . . . . . . . . . . . . 5.1. Roots . . . . . . . . . . . . . . . . . . . . . 5.2. Seeds . . . . . . . . . . . . . . . . . . . . . 5.3. Aerial parts . . . . . . . . . . . . . . . . . . 5.4. Commercial caper . . . . . . . . . . . . . . . Biological activities . . . . . . . . . . . . . . . . . . 6.1. Immunostimulant and antitumural activity . . . . 6.2. Anti-diabetic activity . . . . . . . . . . . . . . 6.3. Antisclerosis activity . . . . . . . . . . . . . . 6.4. Antibacterial, antifungal and antiparasital activities 6.5. Antioxidant activity . . . . . . . . . . . . . . . 6.6. Other activities . . . . . . . . . . . . . . . . .

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⁎ Corresponding author. Laboratoire de Biochimie, Département de Biologie, Faculté des Sciences de Tunis, Université Tunis El-Manar, Tunis 2092, Tunisia. Tel.: + 216 21 22 30 08; fax: + 216 71 88 54 80. E-mail address: [email protected] (N. Tlili). 0367-326X/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.fitote.2010.09.006

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7. Conclusion . . Acknowledgments . Appendix A . . . . References . . . .

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1. Introduction Caper is a perennial shrub and is the common name of the genus Capparis, family Capparidaceae. This genus is represented by several species (about 250). It is known by various names, e.g. Caper (English), Kabbar (Arab), Alcaparro (Spain), and Gollaro (Pakistan). This perennial shrub plant has thick and deep roots, and is about 30–100 cm (high), and it can be thorny or inerm [1–4]. As a spontaneous plant, caper has a large natural distribution (Fig. 1). In the Mediterranean Sea Basin it grows from the Atlantic coasts of the Canary Islands and Morocco to the Black Sea to the Crimea and Armenia, and eastward to the Caspian Sea and into Iran [3,5–7]. The plants show strong resistance to harsh environmental conditions. Despite adverse conditions, plants of Capparis do not seem to show any water stresses or any symptoms of photo-inhibition, and the plant efficiently utilizes the high irradiance throughout the growth season [8]. Chemical studies on caper have reported the richness of different parts with many beneficial chemical compounds. Different parts of the caper plant can be used as a drug or in cosmetics. Before its commercialization, the immature flower buds are pickled in vinegar or preserved in salt. Additionally, the fruit with small soft seeds is preferred for the production of pickles. 2. Origin and morphology The origin of caper can be traced from a woody ancestor through an ecotypization on saline lowland substrate via gradual population processes, which possibly involve regula-

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tory genes [9,10]. Remains of caper were unearthed in archaeological sites as early as the lower Mesolithic [11]. Carbonized flower buds and unripe fruits were unearthed in a jar at the site of Telles-Sweyhat, Syria, dated to about 2400– 1400 B.C., and were considered to be stored as a condiment [12]. The genus Capparis is regarded by Zohary [13] in the Middle East as a relic of a woody xero-tropical flora widespread in Africa and south-western Asia during the Tertiary period. Jacobs [14] suggested that C. spinosa from Malaysia and Australia was introduced by humans. Caper is a shrub 30–100 cm tall. Its roots can be 6–10 m (long). Leaves are alternate, 2–5 cm long, oval to elliptic, with a rounded base and a mucronate, obtuse or emarginated apex. Flower bud appearance is continuous so that all transitional stages of development, from buds to fruit, can be observed simultaneously. Flowers are 5–7 cm across, axillary and solitary, with purplish sepals and white petals. The fruit (caberberry) is ellipsoid, with a thin pericarp. The fruit bursts when ripe, exosing seeds in a pale crimson flesh. Seeds are 3–4 mm across and reniform [1,2,4,15,16]. 3. Environmental condition and cultivation Caper is adapted to poor soils, and is widespread on rocky areas, mountains and grows on numerous soil types, including alfisols, regosols and lithosols. It shows a good response to volcanic or alkaline soils. Soil pH from 6.1 to 8.5 is tolerated [16–18]. Caper plants grow widely immediately after rain (April–May) and start disappearing in the beginning of the cold weather (September–October). It developed mechanisms that reduce the

Fig. 1. Natural distribution of caper based on Inocenio et al. [3].

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impact of high radiation and temperature and does not seem to show any water stresses or any symptoms of photo-inhibition [8,19,20]. Caper plants are used in almost all of the range of Capparis subgenus Capparis, extending from West Africa to the Norfolk Islands in the Pacific [21]. Most of the species are of alimentary or medicinal interest. The important sources are Turkey, Morocco [17], Spain, Greece, France and Italy (especially Sicily and the Aeolian island of Salina and the Mediterranean island of Pantelleria) [22]. The average annual production is estimated to be around 10,000 tonnes: 3500–4500 tonnes are produced in Turkey, 3000 tonnes in Morocco, 500–1000 tonnes in Spain and 1000–2000 tonnes in other countries [16]. In Tunisia the average annual production is estimated to be around 150 tonnes. The USA is one of the most important consumers [16]. The cultivation of this plant is less limited and most of the traditional and commercial uses of Capparis depend exclusively on the collections from the wild plants. Capers are cultivated in some countries, say, Spain, Italy, Turkey, Morocco, Tunisia, Algeria, Iran and the coastal areas of the Black Sea. Cultivation of caper started around 1970 in Spain and Italy, and later in Morocco, with a maximum of about 4000, 1000, and 2500 ha in cultivation, respectively [23]. To our knowledge, statistics for the other countries are not reported. The most important commercial species is mainly Capparis spinosa due to the fact that the main producer countries are from the Mediterranean Basin where this species is predominant [3,7,17,19]. Other species are also used as food like C. sicula [24], C. obvata [25], C. ovata [26,27], C. decidua [28], C. masaikai [29], C. sicula, C. orientalis, and C. zoharyi [22,30]. Indeed, Barbera and Di Lorenzo [30] reported that C. spinosa and C. sicula are cultivated as crop plants in Morocco, Italy, and Spain. C. orientalis is cultivated on the island of Pantelleria, Italy [22]. C. zoharyi is locally cultivated as crop plant around Sail, Morocco [22]. Treated seeds (with a dilute sulphuric acid or permanganate) are sown in sandy soil under glass in the spring; the plants are then transplanted outdoors during warm, settled weather. Capers may be also cultivated from cuttings of short shoots planted in a sandy soil in frames in a glasshouse [31]. Moreover, to develop a high quality product some producers (Italy for example) select the cultivar, especially the spineless (high harvesting). They also reduce the harvesting interval to assure the collection of the small buds and they use some strategic marketing to add value to the product (labelling the quality, product traceability…) [32]. 4. Ethnopharmacology Roots, leaves, buds, fruit, bark and seeds of caper were used by ancient people for medicinal purposes, to treat some diseases such as rheumatism, stomach problems, headache and toothache (Table 1). In ancient time, roots were consumed by ancient Egypt and Arab for treatment of kidney disease, liver disease, stomach problem and scorpion's stings. Leaves were used by ancient Arab against skin disease, to treat earache and kill worm in the ear. Buds were used by the ancient Arab against spleen disease. Ancient Romans used this part of caper plant to treat paralysis. Flowers could serve as a stimulant to increase erection and soothe pains. Fruits were used by ancient Greek to treat convulsions. Seeds served as a medication for gum problems by

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Table 1 Ancient medicinal uses of caper. Treated diseases

Consumer

References

Cure hemorrhoids, dispel bad odors spirits, dispel gases’ kidney disease, skin diseases, liver disease, diabetes Cleaning ulcers, pained teeth, protecting palsy and spleen ache, sciatica, all kinds of pains Menstruation Kill worms in the ears, rotting teeth and gums, stomach problems, accelerate menstruation’ scorpion stings, obstruction in the liver, arouse the appetite, kidney disease

Ancient Arab

[33,34]

Ancient Roman and Ancient Greek

[35]

Ancient Egypt

[35,36]

ancient Arab and to accelerate menstruation by ancient Egypt and ancient Greek [33–36]. Actually, in Morocco the fruit of C. spinosa is used to cure diabetic [37,38]. C. ovata is used in the Hugger (Algeria) as antiinflammatory, for headache, and for stomach ache [39]. In Libya C. orientalis is used as a remedy for stomachache [40]. Fruit of caper species (C. aegyptia) is used by Khushmaan Ma'aza Bedouins (Egypt) to make poultice for rheumatism and by Bischarin Bedouins (Egypt) to cure fever and headache [41]. Thulin [42] suggested that in Somalia they are consuming leaves to treat coughs. In Bahrain, people are using C. sicula as a tonic and an expectorant [43]. Iranian people use the roots, fruit and plant bark of C. spinosa as diuretics, tonics, against malaria and joint disease [44,45]. In Pakistan, people use all parts of C. decidua as anti-rheumatic, as diuretic, as kidney disinfectant, tonics, to reduce flatulence, to improve liver functions, to cure arteriosclerosis and migraine [46,47]; and they especially used leaves of C. spinosa as analgesic, anti-hemorrhoid, antirheumatic [48], aperients, deobstruent, depurative and diuretic [49]. In India, buds and roots of C. spinosa are useful in the treatment of boils; leaves are used as counter-irritant and as a cataplasm in swellings; roots are used to treat fever, rheumatism, paralysis, toothache and kill worm in the ear; the bark is used in the treatment of coughs, asthma and inflammation [50– 52]. In Indo-China the roots of C. micracantha are used to treating daily fever and the wood is used to cure ulcerated nose [53]. In Indonesia the root of this species is employed as diuretic and against bronchitis, and the wood is utilized to treat stomachache [53]. In the Philippines, the bark of C. zeylanica is employed to treat cholera and has stomachic properties [53]. In Hawaii, the entire plant (C. cordifolia) is used to repair broken bones [54]. Caper is one of the most common aromatic plants found in the Mediterranean Basin. The fresh aerial parts, specially the pickled flower buds, unripe fruits and shoots, are stored in salt, vinegar or brine and used as an appetizer with olives, cheese, and nuts or as a complement to meat, salads, pasta, and other foods.

5. Phytochemistry The chemical and bioactive components of the different parts of caper (roots, seeds, leaves, buds and fruits) were investigated and quantified by several researches.

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5.1. Roots A spermidine alkaloid, isocodonocarpine (1) (Fig. 2), was isolated from the roots of C. decidua [55,56], one is 14-Nacetylisocodonocarpine (2) and the second is 15-N-acetylcapparisine (3). 3-Hydroxy-3-methyl-4-methoxyoxindole was isolated from the roots of C. tomentosa [57]. 4-Methoxy-oxindole in roots was also identified [58]. 4,5,6,7-Tetrahydroxydecyl isothiocyanate were identified in C. grandis roots [59]. Indeed, the indole glucosinolate metabolites have been investigated for their potential as cancer chemoprotective agents [60]. Wu et al. (2003) [61] showed that roots of C. sikkimensis contain 2H-1,4benzoxazin-3(4H)-one, 6-methoxy-2-methyl-4-carbaldehyde, as an inhibitor in vitro tumor cell replication. Capparispine (4), capparispine 26-O-β-D-glucoside (5) and cadabicine 26-O-β-Dglucoside hydrochloride (6) were isolated from the root of C. spinosa [62] (Fig. 2). E-octadec-7-en-5-ynoic acid was isolated from chloroform extract of the roots of C. zeylanica [63]. Gupta and Ali [64] isolated oxygenated heterocyclic constituents from the alcoholic extract of root-bark of C. decidua. Roots of C. spinosa showed the presence of sugars: glucose, arabinose, mannose and galactose. Roots of this species showed also the existence of small amounts of lipid; the major fatty acid was linoleic acid followed by oleic acid [65]. The volatile oils of the root of C. spinosa were composed mainly of the methyl, isopropyl and sec-butyl isothiocyanates [45]. 5.2. Seeds Seeds of C. spinosa are rich in oil (ca. 30%) mainly unsaturated (ca. 70%) [66–68]. Oleic acid, linoleic acid (as ω-6 fatty acid) and linolenic acid (as ω-3 fatty acid) were also detected in high value. A high quantity of sterols; stigmasterol, sitosterol, campesterol, and avenasterol were also found in this plant [67,69]. Brassicasterol was also detected [67,69]. Caper seed oil is also rich in tocopherols (as vitamin E) with the presence of three isoforms: α-tocopherol, γ-tocopherol and δ-tocopherol [67,68]. Carotenoids (lutein and β-carotene) were also quantified in a large amount in seed oil of C. spinosa [68]. C. spinosa seed oil contains a good content of aliphatic and triterpenic alcohol (hexadecanol, octadecanol, tetracosanol, β-amyrin, gramisterol, cycloartanol and citrostadienol) [70]. These compounds have an important role in the prevention of many diseases and it can be used in many cosmetics and pharmaceutics products [71,72]. Glucosinolates

1, R1 = CH3-O-, R2 = R3 = H 2, R1 = CH3-O-, R2 = H, R3 = CH3-CO3, R1 = H, R2 = CH3-O-, R3 = CH3-CO-

were identified and quantified in seed oil, and the main glucosinolate was glucocapperin (7) [73] (Fig. 3). 2-Hydroxyethyl glucosinolate was isolated and characterized from the seed of this specie [74]. Seeds of C. spinosa are rich in proteins [70,75]. Liu et al. [76] extracted a heat-stable sweet protein, named mabinlin II, from the seeds of C. spinosa. 5.3. Aerial parts Quaternary ammonium compounds and alkaloids were isolated from leaves of Capparis [77,78]. p-Methoxy benzoic acid was isolated from the aerial part of C. spinosa and it possesses significant antihepatotoxic activity against carbon tetrachloride and paracetamol induced hepatotoxicity in vivo and thioacetamide and galactosamine induced hepatotoxicity in isolated rat hepatocytes, using in vitro technique [79]. Leaves and buds of C. spinosa are rich in phenolic compounds [80]. Sharaf et al. [81] isolated quercetin triglycoside, and 3-O-[6 -αL-rhamnosyl-6″-β-D-glycosyl]-β-D-glucoside (8) from the aerial part of this plant (Fig. 3). From the leaves and stems of three Capparis species (C. cartilogenia, C. deciduas and C. spinosa) flavonoid glycosides were isolated and identified as kaempferol-7-rhamnoside (9), kaempferol-3-rutinoside, kaempferol3,7-dirhamnoside, kaempferol 3-glucoside-7-rhamnoside, kaempferol-3-rhamnoside-7-glucoside, quercetin-7-rhamnoside, quercetin-3-rutinoside, quercetin-7-rutinoside, quercetin3,7-dirhamnoside, quercetin-3-glucoside-7-rhamnoside, isorhamnetin 3-rutinoside, isorhamnetin 3,7-dirhamnoside, and apigenin 6,8-di-C-glucoside [82]. Moreover, flavonol aglycones were isolated and identified as kaempferol, quercetin, isorhamnetin, and their 7-O-methyl derivatives (rhamnocitrin, rhamnetin, and rhamnazin) from leaves of three Capparis species [83]. Glucosinolates were identified and quantified in young shoots and buds of C. spinosa; the main component was glucocapperin [73]. Kjær and Schuster [84] reported the existence in the leaves of C. flexuosa of the 3-hydroxybutyl-, 4-hydroxybutyl-, 3-butenyl-, and 2-hydroxy-3-butenyl glucosinolate. Indeed, it has been reported that certain glucosinolates (e.g. benzyl-, p-hydroxybenzyl- and 2-hydroxybut-3-enyl glucosinolates) act as cancer chemoprotective [85]. 1H-indole-3-acetonitrile 4-O-β-glucopyranoside, 1H-indole3-acetonitrile 4-O-β-(6′-O-β-glucopyranoyl)-glucopyranoside, (6S)-hydroxy-3-oxo-α-ionol glucosides, and a prenyl glucoside (10) (Fig. 3) were isolated from the fruits of C. spinosa [86,87]. The

4, R = OH 5, R = O-β β-D-glucose 6, R = O-β-D-glucose hydrochloride

Fig. 2. Structures of compounds 1–6.

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7, R = CH3

9

10

8

11, R = isopropyl Fig. 3. Structures of compounds 7–11.

known compounds cappariloside A and stachydrin, an adenosine nucleoside, and the known compounds hypoxanthine and uracil were isolated from the fruit of the same species [88]. Sarragiotto et al. [89], showed that the aerial part of C. humilis (branch and leaves) contains 3-carbomethox-N-methylpyridinium and N-methylproline. Leaves, buds and flowers of C. spinosa are rich in tocopherols (α- and γ-tocopherol) and carotenoids [19]. The leaf oil of this species is composed of isothiocyanates, n-allcanes, terpenoids, a phenyl propanoid, an aldehyde and a fatty acid. The main components of this oil are thymol, 2-hexenal butyl isothiocyanate and isopropyl isothiocyanate (11) [45] (Fig. 3). The distribution of minerals in buds and fruits of this species shows high content of potassium, phosphorus, magnesium and calcium with the presence of sodium, manganese and iron [90–93]. Lipids and proteins are also quantified in buds and fruits [90,94]. 5.4. Commercial caper Phenolic compounds are present in a high level in commercial caper [95]. Content of rutin, quercetin, 3-rutinoside, kaempferol 3-rutinoside; and kaempferol 3-rhamnosyl-rutinoside was reported in commercial caper [95,96]. The absence of free aglycones in the original buds indicates that they were produced during the brining process [96]. Carotenoids, tocopherols and vitamin C were detected in commercial caper [95]. Storage conditions did not affect phenolic compounds but they decrease dramatically carotenoids, tocopherols and vitamin C content of caper (data not published); as cited by other authors for other

plants [97–100]. Volatile compounds were identified and quantified in salted capers; aldehydes and esters are the most abundant chemical classes; methyl-isothiocyanate is the major one, followed by benzyl-isothiocyanate [7]. 6. Biological activities Recently it has been reported that caper possesses some medicinal properties and antioxidant activities. 6.1. Immunostimulant and antitumural activity C. zeylanica leaves extract is a potent immunostimulant, stimulating both the specific and non-specific immune mechanisms [101]. Methanolic extract of C. spinosa buds may contribute in improving immune surveillance of human peripheral blood mononuclear cells toward virus infection by up-regulating expression of peculiar pro-inflammatory cytokines; it suppressed the replication of herpes simplex virus type 2 and increased the expression of pro-inflammatory cytokines including interleukin-12, interferon-γ and tumor necrosis factor-α [102]. Moreover, an inhibitor of in vitro tumor cell replication was isolated from the roots of C. sikkimensis [61]. More recently, a protein with potent anti-proliferate activity toward tumor cells and inhibitory activity toward HIV-1 reverse transcriptase and some antifungal activity have been isolated from seeds of C. spinosa [103]. These important biological activities were probably due to the important quantity of the antioxidants which have an excellent activity against these

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diseases. Indeed, some carotenoids were reported to inhibit chemically induced carcinogenesis in the hamster buccal pouch [104]. Tocopherols play an important preventive role against cancer [105]. Phenolic compounds have an anti-tumor effect [106]. The biological activities mentioned above may also be due to some aldehydes which act as an inhibitor in vitro tumor cell replication [61]. 6.2. Anti-diabetic activity The powdered fruit of C. decidua possesses a positive action against alloxan-induced oxidative stress and diabetes in rat; it decreases SOD activity in the liver and kidney (contrary to the diabetic group). The treatment with Capparis also decreased GSH-reactivity in the kidney and heart due to the decrease of GSH content [107]. It was reported that aqueous extracts of C. spinosa exhibit a potent anti-hyperglycemic activity in diabetic rats without affecting basal plasma insulin concentrations [108,109]. These results were possibly due to the alkaloids’ presence in this plant. Indeed, Sharma et al. [110] demonstrated the action of alkaloids from Capparis on various targets for the treatment of diabetes and their multiple therapeutic effects. These facts explain the use of caper by old people to treat diabetic disease [37]. 6.3. Antisclerosis activity Yue-lan et al. [111] bring attention to the notable protective activity of C. spinosa against oxidative stress and interrupting of ROS in systemic sclerosis dermal fibroblasts. It is suggested that extracts of C. decidua fruit and shoot have anti-atherosclerotic and preventing plaque formation potent [112,113]. Ethanolic extract from C. spinosa can effectively inhibit the fibroblast proliferation and type I collagen production in progressive systemic sclerosis [114]. Aqueous extract of C. spinosa can also act by decreasing the cholesterol biosynthesis [109]. Moreover, the diets of 15 hyperlipidemic adults supplemented with unripe fruit of C. decidua reduce their plasma triglycerides, total lipids and phospholipids concentration [115]. This is probably due to the vitamins, alkaloids and phenolics especially flavonoids. It was reported that these compounds induce a significant lipid lowering activity and improves dyslipidemia to hypercholesterolemic and hypertriglyceridemic rats [116,117]. This finding supports its use to cure arteriosclerosis by people [46,47]. 6.4. Antibacterial, antifungal and antiparasital activities C. decidua seeds extract showed antibacterial activity against Vibrio cholerae ogava, inaba, and ettor [118]. Petroleum ether, chloroform, ethanol and water extract of C. zeylanica roots exhibited in vitro antibacterial activity. Petroleum ether extract inhibit S. aureus, B. subtilis, K. pneumoniae and P. vulgaris and produces inhibition zone ranging from 10 to 16 mm at a concentration of 16.5 μg/ml, whereas chloroform, ethanol and water extracts show inhibitory activity against bacterial strains at concentrations of 13.5, 14 and 14 μg/ml, respectively [119]. Moreover, Ali-Shtayeh and Abu Ghdeib [120] brought attention to the antifungal activity of the caper extract against Trichophyton mentagrophytes and Trichophyton violaceum. Jacobson and Schlein [121] reported that caper extract agglutinated and

killed the parasites Leishmania. Upadhyay et al. [122] showed that different extracts isolated from C. decidua can significantly kill or influence the egg delivery response of Bruchus chinensis a serious pest of stored food grains and causes damage to cow pea, gram, soybean, and pulses. These activities were probably due to the quaternary ammonium and glucosinolate. Indeed, certain quaternary ammonium compounds are good against fungi, amoeba, and enveloped viruses; and especially those containing long alkyl chains are used as antimicrobials and disinfectants [123,124]. Other authors suggested that many plants increase their secondary metabolites including glucosinolate in response to attack by insects and microbes [125]. These results can explain the use of this plant by people to kill worm in the ear [33,50]. 6.5. Antioxidant activity The lyophilized and methanolic extract of C. spinosa showed a significant antioxidant effect [126,127]. Extract at 100 and 1000 g/ml concentrations inhibits significantly (pb 0.01) lipid peroxidation by 71.50% and 90%, respectively. These antioxidant activities of the methanolic extract are related to the high level of phenolic compounds [80,95,127]. Capparis buds extract caused a dose-dependent inhibition of lipid auto-oxidation in heated red meat, incubated with simulated gastric fluid. The extract at 3.5 and 7 μM GAE exhibited a dose-dependent peroxyl radical scavenging activity in a methyl linoleate methanol solution oxidized by an azoinitiator, and reduced hypervalent iron myoglobin species formed from met-Mb and H2O2, at 180 μM GAE. The hydrophilic extract, at 70–280 μM GAE, caused a dose-dependent inhibition of lipid autooxidation in heated red meat, incubated with simulated gastric fluid for 180 min [128]. Indeed, this protective effect may be due to the richness of phenolic compounds, tocopherols and carotenoids. Many authors suggested that these compounds have an excellent anti-oxidative property [106,129–131]. 6.6. Other activities Gadgoli and Mishra [132] suggested that C. spinosa extract possesses significant antihepatotoxic activity against carbontetrachloride and paracetamol which induced hepatotoxicity in vivo and thioacetamide and galactosamine which induced hepatotoxicity in isolated rat hepatocytes, using in vitro technique. This result supports the use of caper by the ancient people to treat liver disease and improve liver functions [34,46]. Caper extract was found to possess significant antiinflammatory activity against carrageenan induced oedema in rats [133]. Moreover, Panico et al. [134] showed that lyophilised extract of C. spinosa protects human chondrocytes cultures stimulated by pro-inflammatory cytokine. This finding represents an experimental confirmation of the traditional use of these plants as anti-inflammatory [39,50]. And it's probably due to the anti-inflammatory effect of phenolic compounds [106]. Trombetta et al. [135] suggested that caper extracts displayed marked antiallergic effectiveness and showed a good protective effect against the bronchosperm induced by antigen challenge in sensitized guinea pigs. Leaves extract of C. zeylanica possesses analgesic and antipyretic effects [136]. It was reported that the C. spinosa extract has the ability to maintain skin homeostasis and can be used as a possible

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tanning agent or as a treatment for hair de-pigmentation [137]; this effect may be attributed to phenolic compounds, especially quercetin. This compound can stimulate melanogenesis in human melanocytes and melanoma [138]. Using tablets containing extract of C. masaikai is beneficial for enhancing oral moisture and is a possible way to improve oral dryness [27,139]. Ethanolic extract of C. decidua has a central nervous system depressant and anticonvulsant activities [26]. 7. Conclusion Capparis species, as a large spontaneous plant, have a wide range of applications in the traditional medicine. Recently, the pharmacology and chemistry of this plant have been extensively studied. Chemical studies of the different parts of Capparis, both fermented and non-fermented, have shown the presence of many beneficial compounds. Biological studies have revealed significant anti-diabetic, antisclerosis, antimicrobial, anti-oxidative, anti-inflammatory, immunomodulatory and antiviral activities providing a support to the ancient uses. Nevertheless, despite the important and varied pharmacological studies available, clinical tests are necessary to confirm the use of this species in medical practice. Acknowledgments The authors wish to thank Mr. W. Rezgui (Tunisia), Mr. D. Allaire (Canada), Dr. D. Zope (India), Dr. L. Janeš (Slovenia) and Pr. H. Y. Aboul-Enein (Egypt) for providing language help and constructive remarks. The authors are also grateful to anonymous referees and the editor for helpful comments on an earlier draft. Appendix A. Supplementary data Supplementary data to this article can be found online at doi:10.1016/j.fitote.2010.09.006. References [1] Zohary M. The species of Capparis in the Mediterranean and the near Eastern countries. Bull Res Counc Isr 1960;8:49–64. [2] Hewood VH, Capparis L. In: Tutin TG, Heywood VH, Buugres NA, Valentine DH, Walters SM, Webb DA, editors. Flora Europaea, 1. 1st ed. Cambridge: Cambridge University Press; 1964. p. 259. [3] Inocenio C, Rivera D, Obon MC, Alcaraz F, Barrena J-A. A systematic revision of Capparis section Capparis (Capparaceae). Ann Mo Bot Gar 2006;93:122–49. [4] Saadaoui E, Khaldi A, Khouja ML, El-Gazzah M. Etude de la variabilité morphologique du câprier (Capparis spp.) en Tunisie. Revue des régions arides, 2; 2007. p. 523–7. [5] Jacobs M. The genus Capparis (Capparaceae) from the Indus to the Pacific. Blumea 1965;12:385–541. [6] Fici S. Micromorphological observations on leaf and pollen of Capparis L. section Capparis (Capparaceae). Plant Biosyst 2004;138:125–34. [7] Romeo V, Ziino M, Giuffrida D. Flavour profile of capers (Capparis spinosa L.) from the Eolian Archipelago by HS-SPME/GC-MS. Food Chem 2007;101:1272–8. [8] Levizon E, Drilias P, Kyparissis A. Exceptional photosynthetic performance of Capparis spinosa L. under adverse conditions of Mediterranean summer. Photosynthetica 2004;42:229–35. [9] Mayr E. The growth of biological thought. Diversity, Evolution and Inheritance. Cambridge, MA: Harvard University Press; 1982. [10] Cronquist A. The Evolution and Classification of Flowering Plants. Lawrence, Kansas: Allen Press; 1988. [11] Hansen JM. The Palaeoethnobotany of Franchthi Cave. Bloomington: Indiana University Press; 1991. p. 38–9.

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