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Chemical composition of volatile and fixed oils from of Salvia argentea L. (Lamiaceae) growing wild in Sicily a
a
a
Luana Riccobono , Antonella Maggio , Sergio Rosselli , Vincenzo b
c
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Ilardi , Felice Senatore & Maurizio Bruno a
Dipartimento di Scienze e Tecnologie Biologiche Chimiche e Farmaceutiche (STEBICEF), Università di Palermo, Viale delle Scienze, Parco d'Orleans II, 90128 Palermo, Italy b
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Dipartimento di Scienze della terra e del Mare (DISTEM), Università di Palermo, Via Archirafi, 22, 90123 Palermo, Italy c
Dipartimento di Farmacia, Università di Napoli “Federico II”, Via D. Montesano, 49, 80131 Naples, Italy Published online: 16 Apr 2015.
To cite this article: Luana Riccobono, Antonella Maggio, Sergio Rosselli, Vincenzo Ilardi, Felice Senatore & Maurizio Bruno (2015): Chemical composition of volatile and fixed oils from of Salvia argentea L. (Lamiaceae) growing wild in Sicily, Natural Product Research: Formerly Natural Product Letters, DOI: 10.1080/14786419.2015.1030742 To link to this article: http://dx.doi.org/10.1080/14786419.2015.1030742
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Natural Product Research, 2015 http://dx.doi.org/10.1080/14786419.2015.1030742
Chemical composition of volatile and fixed oils from of Salvia argentea L. (Lamiaceae) growing wild in Sicily Luana Riccobonoa, Antonella Maggioa*, Sergio Rossellia, Vincenzo Ilardib, Felice Senatorec and Maurizio Brunoa
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a
Dipartimento di Scienze e Tecnologie Biologiche Chimiche e Farmaceutiche (STEBICEF), Universita` di Palermo, Viale delle Scienze, Parco d’Orleans II, 90128 Palermo, Italy; bDipartimento di Scienze della terra e del Mare (DISTEM), Universita` di Palermo, Via Archirafi, 22, 90123 Palermo, Italy; cDipartimento di Farmacia, Universita` di Napoli “Federico II”, Via D. Montesano, 49, 80131 Naples, Italy (Received 17 February 2015; final version received 15 March 2015)
The chemical compositions of the essential oil and of the non-polar extracts (petroleum ether, dichloromethane) of the aerial parts (flowers, leaves and stems) of Salvia argentea L. were determined by GC-FID and gas chromatography –mass spectrometry analysis. 14-Hydroxy-a-humulene (40.1%) was recognised as the main constituents of the essential oil of S. argentea, together with 1,3,8-p-menthatriene (12.1%), globulol (7.4%) and b-sesquiphellandrene (5.8%). Tritriacontane (9.9% and 14.1%), heptacosane (8.4% and 10.5%), hentriacontane (8.3% and 10.9%), tetradecanal (8.4% and 10.2%) and methyldotriacontane (7.9% and 7.6%) were recognised as the main constituents of the extracts in petroleum ether and dichloromethane, respectively, whereas methyl linolenate (36.6% and 13.5%) and methyl myristoleate (10.5% and 18.5%) were recognised as the main constituents of the methylated extracts. Keywords: Salvia argentea; Lamiaceae; volatile components; 14-hydroxy-ahumulene; fixed oils; fatty acids; linolenic acid
1. Introduction The genus Salvia is one of the largest members of the family Lamiaceae (subfamily Nepetoideae), comprising more than 500 species. It is widely distributed in various regions including the temperate and warmer zones of the world such as the Mediterranean, where it is represented by 36 species (Hedge 1972), Central Asia, the Pacific Islands, tropical Africa and America (Wu et al. 2012).
*Corresponding author. Email: [email protected] q 2015 Taylor & Francis
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L. Riccobono et al.
It is one of the most representative genus of the Labiatae that includes valuable species used in culinary preparations, phytotherapy and aromatherapy such as Menta piperita, Thymus capitatus, Rosmarinus officinalis and Salvia officinalis. The essential oils and extracts of these species hold important biological properties, in fact the antibacterial, antioxidant, hypoglycaemic, anti-inflammatory and cytotoxic activities besides an action against neurodegenerative disorders have been recently reported (Ben Jemia, Tundis, et al. 2013; Iauk et al. 2014; Sun et al. 2014; Kadioglu & Efferth 2015; Nazem et al. 2015). Several Salvia species are economically important because they have been used in therapy as antihydrotic, spasmolytic, antiseptic, anti-inflammatory and in the treatment of mental and nervous conditions (Baricevic & Bartol 2000) and furthermore as spices and flavouring agents in perfumery and cosmetics. Members of this genus have been shown to possess a significant array of pharmacological properties such as antimicrobial, antioxidant, cytotoxic, anti-HIV (Bisset 1994; Newall et al. 1996; Blumenthal 1998; Weiss 1998). The occurrence of the non-volatile secondary metabolites and the biological properties of all the studied species of Salvia have been recently reviewed (Wu et al. 2012). The essential oils of Salvia species are also applied in the treatment of a range of diseases, and it has been shown to possess antimicrobial, viricidal, cytotoxic, anti-mutagenic and antifungal activities (Jalsenjak et al. 1987). Salvia argentea L., (syn: S. tmolea Boiss.) is a perennial herb native to the Mediterranean region, in northwest Africa (Morocco, northern Algeria, Tunisia), southern Europe (Spain, Portugal, South Italy, Sicily, Malta, Albania, Bulgaria, Slovenia, Croatia, Bosnia, Kosovo, Montenegro, Serbia, Macedonia, and Greece) and the far west of Asia (Turkey). It occurs primarily on stony hillside meadows, basalt, volcanic soils and rocky bluffs. Usually, it is not found very near the sea or ocean, or at low altitudes, but it has often been found on highlands not far from the sea (http://ww2.bgbm.org/euroPlusMed/). S. argentea has a large basal leaves zone that measure 1 m wide and 30 – 60 cm high. The individual leaves are 20– 30 cm long and 15 cm wide. Both leaf surfaces are heavily covered with silky hairs that give it a wooly appearance. The leaves are soft to the touch, first emerging as a distinctive silvery white and then turning to greygreen after flowering. Cool weather in the fall turns the leaves silvery again (Clebsch & Barner 2003). In Lucania (Italy), where it is known as “l’erva du taglie`”, the young leaves of S. argentea were topically used as haemostatic (Pieroni et al. 2004), whereas the basal leaves, peeled and stewed, were consumed as food in Spain (“gordolobo”) (Tardı´o et al. 2006). Several biological properties have been reported for this species. In fact, a good antioxidant activity has been shown from the aqueous and methanolic extracts (Stagos et al. 2012) and from the methanolic extract (Salah et al. 2006; Ben Farhat et al. 2013a, 2013b). Furthermore, good acetylcholinesterase (AChE) and butyrylcholinesterase (BChE) inhibitory activity for the CH2Cl2 and methanolic extracts (Orhan et al. 2013), antibacterial activity on Staphylococcus aureus and Staphylococcus epidermidis for the ethanolic extract (Sarac & Ugur 2007) and larvicidal activity, against the mosquito Culex pipiens (S¸eref Gu¨n et al. 2011) for the hexane extract, were determined. Previous phytochemical studies of the plant indicated the presence of abietane diterpenoids in the roots (Michavila et al. 1986; Yang et al. 1996), whereas several flavones, from the exudates of S. argentea collected in Bulgaria (Nikolova et al. 2006) and from the acetone extract of plants cultivated in Poland (Sajewicz et al. 2012), and oleanane and ursane derivatives (Bruno et al. 1987; Janicsa`k et al. 2006) were identified in the aerial parts. Furthermore, several ursane triterpenoids with a new pattern of distribution of functional groups have been isolated from S. argentea var. aurasiaca (Pomel) Batt. & Trab., collected in Algeria (Lakhal et al. 2014) suggesting chemotaxonomic differences from other S. argentea variations. Some investigations have been published on the composition of the essential oil of S. argentea growing in Morocco (Holeman et al. 1984), Serbia (Couladis et al. 2001),
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Macedonia (Velicˇkovic´ et al. 2014) and Tunisia (Ben Farhat et al. 2013a), but nothing has been reported on Italian plants. In this study, as a continuation of our researches on Mediterranean plants (Zito et al. 2010; Rosselli et al. 2012; Maggio et al. 2013, 2014), we report the chemical composition of the essential oil and of the non-polar extracts from aerial parts of S. argentea L. growing wild in Sicily, a population not previously investigated.
2. Results and discussion Hydrodistillation of S. argentea aerial parts (HD) gave a yellow oil. Overall, 35 compounds were identified, representing 93.8% of the total oil composition. The components, listed in Table 1 according to their retention indices (RI) on an HP-5MS column, were divided into six classes on the basis of their chemical structures. 14-Hydroxy-a-humulene (40.1%) was recognised as the main constituent of the essential oil of S. argentea, together with 1,3,8-p-menthatriene (12.1%), globulol (7.4%) and b-sesquiphellandrene (5.8%). Generally, the oil consisted mainly of oxygenated sesquiterpenes (58.6%) and monoterpene hydrocarbons (21.4%), whereas sesquiterpene hydrocarbons (13.6%) were present in lower amounts and hydrocarbons, carbonylic compounds and specially oxygenated monoterpenes were almost absent. Four previous studies reported the chemical composition of S. argentea oils from plants collected in different regions (Holeman et al. 1984; Couladis et al. 2001; Ben Farhat et al. 2013a; Velicˇkovic´ et al. 2014), and their results have been inserted in Table 1. Caryophyllene oxide was reported as the main component of the oil from Macedonia (Ma) (37.6%), followed by a-copaene (8.5%), humulene epoxyde II (6.3) and b-caryophyllene (6.1%) (Velicˇkovic´ et al. 2014), whereas the major components of Serbian oil (S) were viridiflorol (32.4%), manool (14.6%), a-humulene (10.7%) and b-thujone (7.3%) (Couladis et al. 2001). The profile of the two Tunisian populations (T1 and T2) (Ben Farhat et al. 2013a) is quite similar to the Serbian one. In fact, although they were richer in monoterpene hydrocarbons (14.5% and 13.5%) with respect to S (0.5%) the main constituents were viridiflorol (26.9% and 18.7%), manool (6.1% and 13.6%), a-thujone (7.3% and 8.1%) and a-humulene (4.1% and 5.3%). On the other hand, the oil sample obtained from the Moroccan S. argentea (Mo) (Holeman et al. 1984) was characterised by camphor (45.1%), camphene (19.4%), a-pinene (9.3%) and borneol (9.0%). The composition of the essential oil of S. argentea collected in Sicily (HD) was found to be quite different from the composition of the oils of the other populations studied so far. In fact, although it had a high content in oxygenated sesquiterpenes such as Ma, S, T1 and T2, 14-hydroxy-a-humulene, 1,3,8-pmenthatriene, globulol and b-sesquiphellandrene, the main components of HD, were totally absent in the other populations. Furthermore, viridiflorol, manool, caryophyllene oxide, ahumulene, thujone, camphor and camphene, major compounds of the other oils were not present in the Sicilian population. Aerial parts S. argentea were extracted with petroleum ether and dichloromethane at room temperature for 1 week to give two residues: ETP1 and DCM1, respectively. In order to identify the free fatty acids, a portion of these extracts was successively treated with a solution of diazomethane in Et2O to afford ETP2 and DCM2. The analysis of the petroleum ether (ETP1) and dichloromethane (DCM1) extracts allowed the identification of 26 and 15 compounds, representing 90.2% and 93.2%, respectively, of the total composition, whereas in ETP2 and DCM2 21 and 26 compounds were identified, representing 90.5% and 90.1%, respectively, of the total composition. The components, listed in Table 2 according to their RI on an HP-5MS column, were divided into six classes on the basis of their chemical structures.
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Table 1. Chemical composition of essential oils of S. argentea collected in Sicily (HD) and reported in literature. RIa
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1358 2300 2500
925 928 938 953 980 1024 1025 1057 1108
1337 1351 1364 1396 1432 1487 1490 1522
RIb
Idc
1634 2300 2500
1, 2 1, 2, 3 1, 2, 3
1035 1014 1032 1076 1118 1150 1278 1256 1409
1468 1467 1527 1616 1612 1679 1694 1785
1, 2 1, 2 1, 2, 3 1, 2 1, 2, 3 1, 2, 3 1, 2, 3 1, 2, 3 1, 2
1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2
Compoundsd Hydrocarbons a-Ionene Tricosane Pentacosane Heptacosane Nonacosane 2-Methyltetradecane 2-Methyltetracosane Tetradecane Pentadecane Heneicosane 2-Methyldocosane Monoterpene hydrocarbons a-Thujene Tricyclene a-Pinene Camphene b-Pinene Limonene p-Cymene g-Terpinene 1,3,8-p-Menthatriene Myrcene Terpinolene d3-Carene a-Phellandrene a-Terpinene (E)-b-Ocimene (Z)-b-Ocimene Oxygenated monoterpenes 1.8-Cineole a-Terpineol a-Thujone b-Thujone Borneol Camphor Carvacrol Eugenol Isoborneol Linalool Terpinen-4-ol Thymol Bornyl acetate Sesquiterpene hydrocarbons d-Elemene a-Cubenene Silphiperfola-5,7(14)-diene 7-epi-Sesquithujene b-Cubebene a-Amorphene ar-Curcumene b-Sesquiphellandrene Valencene
HDe
Maf
Sg
T1h
T2i
Moj
0.1 t t 0.1
9.4
4.0
0.0
0.0
0.0
0.5
14.5 t
13.5 t
28.7
0.5 t t t t t
3.9 0.7 0.8 1.0 4.2 1.5
1.8 0.6 0.5 0.9 6.4 1.2
9.3 19.4
0.7 0.1 0.2 0.3 0.6 0.5
0.5 0.3 0.2 0.1 0.5 0.5 20.7 4.0 1.0 8.1 2.7 0.1 2.1 0.1 0.1
12.7
22.1 4.2 0.8 7.3 2.2 0.1 3.2 0.4 t 0.1 2.2 0.8 0.2 0.6 9.2
t
0.1
0.1
0.2
0.1
21.4 t 0.1 2.2 t 2.6 t 3.4 1.0 12.1
0.5 0.9 1.0 0.8 0.5 4.0 0.5 0.5 0.7 0.0 t
t
2.4 1.6
t
0.0
0.6
t
0.6
13.6 0.1 3.9 0.8 2.1 0.1 t 0.8 5.8
t 30.2
t 13.1 3.1 t 1.7 7.3 1.0 t t t t t t
1.3 0.8 0.2 0.2 13.1
64.1 2.5 7.5 9.0 45.1
0.0
t t
(Continued)
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Table 1. (Continued)
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RIa
1582 1585 1587 1593 1602 1634 1640 1642 1645 1716
1480 1619
1285 1950
RIb
2095 2135 2098 2103 2037 2089 2187 2209 2145 2478
1807 1934
1485 2622
Idc
1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2
1, 2 1, 2
1, 2 1, 2
Compoundsd -Muurolene -Cadinene d-Cadinene Cadalene cis-Calamenene b-Caryophyllene a-Calacorene b-Calacorene a-Copaene a-Humulene allo-Aromadendrene b-Bourbenene b-Elemene ?-Elemene 6,9-Guaiadiene Bicyclogermacrene Germacrene B Germacrene D E, E-a-Farnesene Sesquithujene a-Colocalene Oxygenated sesquiterpenes (E)-Sesquisabinene hydrate b-Copaen-4-a-ol Globulol Viridiflorol Salvial-4(14)-en-1-one; (mintketone) 1-epi-Cubenol t-Cadinol t-Muurolol Torreyol (a-muurolol) 14-Hydroxy-a-humulene Spathulenol Caryophyllene oxide Humulene epoxyde I Humulene epoxyde II b-Eudesmol a-Cadinol 10-peroxy-murolan-3,9(11)-diene Germacra-4(15),5,10(14)-trien-1-a-ol 10-nor-calamenen-10-one Carbonylic compounds Tridecan-2-one Tetradecanal Benzaldehyde Benzene acetaldehyde Nonanal Tetradecanoic acid Hexahydrofarnesyl acetone Others Dihydroedulan II (Z)-Phytol
HDe
Maf
1.9 3.0 6.1 1.3 1.1 8.5 0.6
58.6 4.1 1.4 7.4 0.3 t 3.1 1.1 0.2 0.9 40.1
0.6 0.4 t 1.2 t 1.3 3.9 t t 0.3 51.0
T1h
T2i
t t t
0.4 0.1 0.6
0.6 0.2 1.5
t 2.0
0.3 2.5 0.1
0.6 3.3 0.2
t 10.7 t
0.4 4.1 0.3
0.1 5.3 0.3
t
0.1
0.8
39.4
36.6
29.6
32.4
26.9
18.7
1.3 3.3
2.7 4.1
1.7 3.4
1.9 2.2
7.7
0.6
0.4
t 0.6
0.1 0.5
0.1 0.3
3.6 3.5 16.8
6.9
14.9
Moj
0.0
0.5 2.4 t
t 37.6 0.5 6.3
0.1 t 0.1
Sg
1.2 1.3 1.2 5.4
4.0 2.3 0.7
0.0
0.8 0.0 t t
4.6 3.1
0.0
(Continued)
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Table 1. (Continued) RIa
RIb
Idc
Compoundsd (E)-Phytol b-Ionone Manool Sclareol oxide Isocembrene Total
HDe
93.8
Maf
2.7 0.4 99.7
Sg
T1h
T2i
1.2 1.0 14.6
0.8 6.1
1.3 13.6
94.2
89.9
92.2
Moj
92.8
a
Retention index on a HP-5MS column. Retention index on a HP-Innowax column. Identification, 1 ¼ comparison of retention index; 2 ¼ comparison of mass spectra with MS libraries identification; 3 ¼ comparison with authentic compounds. d Correct isomer not identified. e t ¼ trace, less than 0.05%. f Ma ¼ collected in Macedonia (Velicˇkovic´ et al. 2014). g S ¼ collected in Serbia (Couladis et al. 2001). h T1 ¼ collected at Sers (Tunisia). i T2 ¼ collected at Makther (Tunisia) (Ben Farhat et al. 2013a). j Mo ¼ collected in Morocco (Holeman et al. 1984). b
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c
Tritriacontane (9.9% and 14.1%), heptacosane (8.4% and 10.5%), hentriacontane (8.3% and 10.9%), methyldotriacontane (7.9% and 7.6%) and tetradecanal (8.4% and 10.2%) were recognised as the main constituents of the extracts ETP1 and DCM1. Generally, ETP1 and DCM1 consisted mainly of hydrocarbons (60.1% and 63.1%), carbonylic compounds (18.3% and 17.5%) and monoterpene hydrocarbons (4.0% and 5.5%), whereas other classes of compounds were absent. Methyl ester was, by far, the main class of ETP2 and DCM2 (63.7% and 50.4%) with methyl linolenate (36.6% and 13.5%) and methyl myristoleate (10.5% and 18.5%) as the major compounds together with methyl palmitate (8.0% and 1.9%). Among the hydrocarbons (17.0% and 26.8%), the second most abundant class, only tritriacontane (4.1% and 5.0%), heptacosane (2.9% and 4.6%) and hentriacontane (3.2% and 4.4%) are worthy of mention, whereas carbonylic compounds (8.9% and 11.4%) and other classes of compounds were present in lower amount. The compositions of petroleum ether and dichloromethane extracts were found to be quite similar. In fact, both ETP1 and DCM1 had a high content in hydrocarbons (60.1% and 63.1%) and the distribution of monoterpene hydrocarbons and carbonylic compounds appeared to be similar. The profile of ETP2 and DCM2 was also analogue. Both had a high rate of methyl esters (63.7% and 50.4%) and hydrocarbons, moreover a comparable quantity of carbonylic compounds was present. This large amount of free fatty acids (63.7%), which have been already proved to be very active against several mosquito species (Rahuman et al. 2008), probably explains the larvicidal activity of the hexane extract against the mosquito C. pipiens, as previously reported (S¸eref Gu¨n et al. 2011). 3. Experimental 3.1. Plant material Aerial parts of S. argentea L. were collected on the southern side of Monte delle Rose (Agrigento, Sicily, Italy) (378380 18.1900 N, 138250 6.6200 E, 1177 m s/L), in July 2014, from plants
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Table 2. Chemical composition of non-polar extracts of S. argentea collected in Sicily. RIa
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2300 2478 2500 2700 2863 2900 3052 3100 3264 3300 3500
RIb
Idc
2300 1, 2, 3 1, 2 2500 1, 2, 3 2700 1, 2, 3 1, 2 2900 1, 2, 3 1, 2 3100 1, 2, 3 1, 2 3300 1, 2, 3 3500 1, 2
938 1032 1, 2, 3 980 1118 1, 2, 3 1057 1256 1, 2, 3 1432 1612 1, 2 1494 1735 1, 2 1480 1517 1619 1703 1908
1807 1829 1934 2036 2219
1703
1, 2 1, 2 1, 2 1, 2 1, 2 1, 2
1712 2021 1, 2, 3 1891 2237 1, 2, 3 1928 2208 1, 2, 3 2085 2505 1, 2, 3 2135 2487 1, 2, 3 2139 2298 3132 3317 1472 1677 1893 2132
1, 2, 3 1, 2 1, 2 1, 2 1973 2193 2384 2625
1, 2 1, 2 1, 2 1, 2
Compoundd
ETP1 ETP2 DCM1 DCM2e
Hydrocarbons 60.1 Tricosane 1.5 Methyltetracosane# 3.2 Pentacosane 4.4 Heptacosane 8.4 Methyloctacosane# 2.8 Nonacosane 6.3 Methyltriacontane# 3.2 Hentriacontane 8.3 Methyldotriacontane# 7.9 Tritriacontane 9.9 Pentatriacontane 4.2 Monoterpene hydrocarbons 4.0 a-Pinene 1.2 b-Pinene 0.3 g-Terpinene 2.5 Sesquiterpene hydrocarbons 3.9 b-Cubebene 2.6 a-Zingiberene 1.3 Carbonylic compounds 18.3 Tridecan-2-one 2.5 Tridecanal 3.9 Tetradecanal 8.4 Pentadecan-2-one 2.7 Heptadecan-2-one 0.8 Methyl ester 0.1 9-Tetradecenoic acid methyl ester; methyl myristoleate Tetradecanoic acid methyl ester; methyl myristate (Z)-9-Hexadecenoic acid methyl ester; methyl palmitoleate Hexadecanoic acid methyl ester; 0.1 methyl palmitate (Z,Z)-9,12-Octadecadienoic acid methyl ester methyl linoleate (Z,Z,Z)-9,12,15-Octadecatrienoic acid methyl ester; Methyl linolenate Octadecanoic acid methyl ester; methyl stearate Methyl eicosenoate; methyl gadoleate Octacosanoic acid methyl ester Triacontanoic acid methyl ester; methyl melissate Others 3.8 Dodecanol 0.4 Tetradecanol 2.0 Hexadecanol 0.9 (E)-Phytol 0.5 Total 90.2
17.0
63.1
26.8
0.6 2.9 0.6 1.8 0.5 3.2 2.4 4.1 0.9 0.0
1.4 2.3 10.5 1.9 8.3 1.0 10.9 7.6 14.1 5.1 5.5 5.5
0.7 1.3 4.6 1.0 3.0 2.2 4.4 3.4 5.0 1.2 0.6
0.9 0.9
7.1 7.1
8.9 1.1 1.8 4.7 1.3
17.5
63.7 10.5
3.8 10.2 3.5 0.0
0.6 0.9 0.9 11.4 1.0 2.5 5.7 1.8 0.4 50.4 18.5 5.6
2.4 8.0
1.9
3.0
1.6
36.6
13.5
1.6 1.6
1.5 3.6 2.2 2.0
0.0
0.0
0.0
90.5
93.2
90.1
# Correct isomer not identified. a Retention index on an HP-5MS column. b Retention index on an HP-Innowax column. c Identification, 1 ¼ comparison of retention index; 2 ¼ comparison of mass spectra with MS libraries identification; 3 ¼ comparison with authentic compounds. d Correct isomer not identified. e t ¼ trace, less than 0.05%.
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at the full flowering stage. Typical specimens (SAF-P 200), identified by Prof. Vincenzo Ilardi, have been deposited Herbarium SAF, Department of Agricultural and Forest Science, University of Palermo, Palermo, Italy.
3.2. Isolation of the essential oil
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The air-dried samples were grounded in a Waring blender and then subjected to hydrodistillation for 3 h using n-hexane as solvent, according to the standard procedure previously described (Ben Jemia, Rouis, et al. 2013). The oil was dried over anhydrous sodium sulphate and then stored in sealed vials, at 2 208C, ready for the GC and gas chromatography– mass spectrometry (GC – MS) analyses. The sample yielded 0.27% (HD) of yellow oil (w/w) with a pleasant smell.
3.3. Preparation of the extracts Dried and finely powdered S. argentea (100 g) samples were extracted with petroleum ether and dichloromethane at room temperature for 1 week. The extracts were evaporated to dryness yielding a residue (1.098 and 0.496 g, respectively for ETP1 and DCM1). A portion of the extracts was treated with a solution of diazomethane in Et2O to afford ETP2 and DCM2.
3.4. Qualitative and quantitative analyses The essential oil and the four extract samples were analysed to determine the chemical components at the ‘Department of Pharmacy’ of the University of Naples ‘Federico II’ by GC and GC – MS. The GC analyses were carried out with a Perkin-Elmer Sigma 115 gas chromatograph fitted with an HP-5MS capillary column (30 m £ 0.25 mm i.d.; 0.25 mm film thickness) and equipped with a flame ionisation detector (FID). Analysis was also run by using a fused silica HP-Innowax polyethylenglycol capillary column (60 m £ 0.25 mm i.d.; 0.25 mm film thickness). GC – MS was recorded on an Agilent 6850 Ser. II apparatus fitted with a fused silica HP-5 capillary column (30 m £ 0.25 mm i.d.; 0.25 mm film thickness) and coupled to an Agilent Mass Selective Detector MSD 5973 as previously described (Loizzo et al. 2013). Identification of constituents was made as elsewhere reported (Zito et al. 2013) by comparison of their RI with either those of the literature (Jennings & Shibamoto 1980; Davies 1990) or with those of authentic compounds available in our laboratories. The RI were determined in relation to a homologous series of n-alkanes (C8 –C28) under the same operating conditions. Further identification was made by comparison of their mass spectra on both columns with either those stored in NIST 02 and Wiley 275 libraries or with mass spectra from the literature (Jennings & Shibamoto 1980; Adams 2007) and our home-made library. Component relative concentrations were calculated based on GC peak areas without using correction factors.
4. Conclusion In conclusion, with regard to S. argentea essential oil, the results presented herein indicate a quite different chemical profile of the Sicilian population with respect to the other ones studied so far and show that environmental conditions such as soil composition, climate can drastically influence the composition of the secondary metabolites. The previously reported larvicidal activity of the hexane extract against the mosquito C. pipiens, whose chemical composition was not reported, (S¸eref Gu¨n et al. 2011) could be explained by the huge presence of free fatty acids (63.7%), which have been already proved to be very active against several mosquito species (Rahuman et al. 2008).
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Acknowledgements GC – MS spectra were performed at the Pharmacy Department, University of Naples ‘Federico II’.
Disclosure statement No potential conflict of interest was reported by the authors.
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References Adams RP. 2007. Identification of essential oil components by gas chromatography/mass spectrometry. 4th ed. Carol Stream, IL: Allured Publishing Co. Baricevic D, Bartol T. 2000. Sage: the genus Salvia. In: Kintzios SE, editor. Pharmacology: the biological/ pharmacological activity of the Salvia genus. New York, NY: Harwood Academic Publishers; p. 143 –184. Ben Farhat M, Landoulsi A, Chaouch-Hamada R, Sotomayor JA, Jorda´n MJ. 2013a. Profiling of essential oils and polyphenolics of Salvia argentea and evaluation of its by-products antioxidant activity. Ind Crops Prod. 47:106–112. doi:10.1016/j.indcrop.2013.02.007. Ben Farhat M, Landoulsi A, Chaouch-Hamada R, Sotomayor JA, Jorda´n MJ. 2013b. Characterization and quantification of phenolic compounds and antioxidant properties of Salvia species growing in different habitats. Ind Crops Prod. 49:904–914. doi:10.1016/j.indcrop.2013.06.047. Ben Jemia M, Rouis Z, Maggio A, Venditti A, Bruno M, Senatore F. 2013. Chemical composition and free radical scavenging activity of the essential oil of Achillea ligustica growing wild in Lipari (Aeolian Islands, Sicily). Nat Prod Commun. 8:1629–1632. Ben Jemia M, Tundis R, Maggio A, Rosselli S, Senatore F, Menichini F, Bruno M, Kchouk ME, Loizzo MR. 2013. NMR-based quantification of rosmarinic and carnosic acids, GC –MS profile and bioactivity relevant to neurodegenerative disorders of Rosmarinus officinalis L. extracts. J Funct Foods. 5:1873–1882. doi:10.1016/j.jff. 2013.09.008. Bisset NG. 1994. Herbal drugs and phytopharmaceuticals. Stuttgart: CRC Press. Blumenthal M. 1998. The complete German commission E monographs. Austin, TX: American Botanical Council. Bruno M, Savona G, Hueso-Rodrı´guez JA, Pascual C, Rodrı´guez B. 1987. Ursane and oleanane triterpenoids from Salvia argentea. Phytochemistry. 26:497– 501. doi:10.1016/S0031-9422(00)81441-7. Clebsch B, Barner CD. 2003. The new book of Salvias: sages for every garden. Portland, OR: Timber Press. Couladis M, Tzakou O, Stojanovic D, Mimica-Dukic N, Jancic R. 2001. The essential oil composition of Salvia argentea L. Flavour Frag J. 16:227–229. doi:10.1002/ffj.989. Davies NW. 1990. Gas chromatographic retention indices of monoterpenes and sesquiterpenes on methyl silicon and Carbowax 20M phases. J Chromatogr A. 503:1– 24. doi:10.1016/S0021-9673(01)81487-4. Hedge IC. 1972. Salvia L. In: Tutin TG, Heywood VH, Burges NA, Valentine DH, Walters SM, Webb DA, editors. Flora Europaea. Vol. 3. Cambridge: Cambridge University Press; p. 188. Holeman MA, Berrada M, Bellakhdar J, Ilidrissi A, Pinel R. 1984. Comparative chemical study on essential oils from Salvia officinalis, S. aucheri, S. verbenaca, S. phlomoides and S. argentea. Fitoterapia. 55:143–148. Iauk L, Acquaviva R, Mastrojeni S, Amodeo A, Pugliese M, Ragusa M, Loizzo MR, Menichini F, Tundis R. 2014. Antibacterial, antioxidant and hypoglycaemic effects of Thymus capitatus (L.) Hoffmanns. Et Link leaves’ fractions. J Enzyme Inhib Med Chem. 17:1– 6. doi:10.3109/14756366.2014.930453. [Epub ahead of print]. Jalsenjak V, Peljnajk S, Kustrak D. 1987. Microcapsules of sage oil, essential oils content and antimicrobial activity. Pharmacology. 42:419–420. Janicsa`k G, Veres K, Zoltan Kaka`sy A, Ma`the´ I. 2006. Study of the oleanolic and ursolic acid contents of some species of the Lamiaceae. Biochem Syst Ecol. 34:392–396. Jennings W, Shibamoto T. 1980. Qualitative analysis of flavour and fragrance volatiles by glass capillary gas chromatography. New York, NY: Academic Press. Kadioglu O, Efferth T. 2015. Pharmacogenomic characterization of cytotoxic compounds from Salvia officinalis in cancer cells. J Nat Prod. doi:10.1021/np501007n. [Epub ahead of print]. Lakhal H, Kabouche A, Alabdul Magid A, Voutquenne-Nazabadioko L, Harakat D, Kabouche Z. 2014. Triterpenoids from Salvia argentea var. aurasiaca (Pomel) Batt. & Trab. and their chemotaxonomic significance. Phytochemistry. 102:145–151. Loizzo M, Jemia M, Senatore F, Bruno M, Menichini F, Tundis R. 2013. Chemistry and functional properties in prevention of neurodegenerative disorders of five Cistus species essential oils. Food Chem Toxicol. 59:586–594. doi:10.1016/j.fct.2013.06.040. Maggio A, Bruno M, Formisano C, Rigano D, Senatore F. 2013. Chemical composition of the essential oils of three species of the Apiaceae family growing wild in Sicily: Bonannia graeca, Eryngium maritimum and Opopanax chironium. Nat Prod Commun. 8:841–844.
Downloaded by [University of Victoria] at 04:42 25 April 2015
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L. Riccobono et al.
Maggio A, Riccobono L, Bancheva S, Bruno M, Senatore F. 2014. Chemical composition of the essential oil of the local endemics Centaurea davidovii and C. parilica (Asteraceae, sect. Lepteranthus) from Bulgaria. Nat Prod Commun. 9:1373–1376. Michavila A, De la Torre MC, Rodrı´guez B. 1986. 20-nor-abietane and rearranged abietane diterpenoids from the root of Salvia argentea. Phytochemistry. 25:1935–1937. doi:10.1016/S0031-9422(00)81178-4. Nazem F, Farhangi N, Neshat-Gharamaleki M. 2015. doi:10.1016/j.jcjd.2014.11.003 Beneficial effects of endurance exercise with Rosmarinus officinalis Labiatae leaves extract on blood antioxidant enzyme activities and lipid peroxidation in streptozotocin-induced diabetic rats. Can J Diabetes.. Newall CA, Anderson LA, Phillipson JD. 1996. Herbal medicines: a guide for healthcare professionals. London: Pharmaceutical Press. Nikolova MT, Grayer RJ, Genova E, Porter EA. 2006. Exudate flavonoids from bulgarian species of Salvia. Biochem Syst Ecol. 34:360– 364. doi:10.1016/j.bse.2005.11.006. Orhan I, Senol F, Ercetin T, Kahraman A, Celep F, Akaydin G, Sener B, Dogan M. 2013. Assessment of anticholinesterase and antioxidant properties of selected sage (Salvia) species with their total phenol and flavonoid contents. Ind Crops Prod. 41:21–30. doi:10.1016/j.indcrop.2012.04.002. Pieroni A, Quave CL, Santoro RF. 2004. Folk pharmaceutical knowledge in the territory of the Dolomiti Lucane, inland southern Italy. J Ethnopharmacol. 95:373– 384. doi:10.1016/j.jep.2004.08.012. Rahuman AA, Venkatesan P, Gopalakrishnan G. 2008. Mosquito larvicidal activity of oleic and linoleic acids isolated from Citrullus colocynthis (Linn.) Schrad. Parasitol Res. 103:1383–1390. doi:10.1007/s00436-008-1146-6. Rosselli S, Maggio AM, Canzoneri M, Simmonds MSJ, Bruno M. 2012. Sesquiterpenes from Onopordum illyricum and their antifeedant activity. Nat Prod Commun. 7:1131–1132. Sajewicz M, Staszek D, Wro`bel MS, Waksmundzka-Hajnos M, Kowalska T. 2012. The HPLC/DAD fingerprints and chemometric analysis of flavonoid extracts from the selected sage (Salvia) species. Chromatogr Res Int., Article ID 230903: 1–8. Salah KBH, Mahjoub MA, Ammar S, Michel L, Millet-Clerc J, Chaumont JP, Mighri Z, Aouni M. 2006. Antimicrobial and antioxidant activities of the methanolic extracts of three Salvia species from Tunisia. Nat Prod Res. 20:1110–1120. doi:10.1080/14786410600834230. Sarac N, Ugur A. 2007. Antimicrobial activities and usage in folkloric medicine of some Lamiaceae species growing in Mugla, Turkey. EurAsia J BioSci. 4:28–37. ¨ z E, C S¸eref Gu¨n S, C ¸ inbilgel I˙, O ¸ etin H. 2011. Larvicidal activity of some Salvia L. (Labiatae) plant extracts against the mosquito Culex pipiens L. (Diptera: Culicidae). Kafkas Univ Vet Fak Derg. 17:S61–S65. Stagos D, Portesis N, Spanou C, Mossialos D, Aligiannis N, Chaita E, Panagoulis C, Reri E, Skaltsounis L, Tsatsakis AM, Kouretas D. 2012. Correlation of total polyphenolic content with antioxidant and antibacterial activity of 24 extracts from Greek domestic Lamiaceae species. Food Chem Toxicol. 50:4115–4124. doi:10.1016/j.fct.2012. 08.033. Sun Z, Wang H, Wang J, Zhou L, Yang P. 2014. Chemical composition and anti-inflammatory, cytotoxic and antioxidant activities of essential oil from leaves of Mentha piperita grown in China. PLoS One, doi:10.1371/journal. pone.0114767. Tardı´o J, Pardo-De-Santayana M, Morales R. 2006. Ethnobotanical review of wild edible plants in Spain. Bot J Linnean Soc. 152:27–71. Velicˇkovic´ DT, Ristic´ MS, Milosavljevic´ NP, Davidovic´ DN, Bogdanovic´ SZ. 2014. Chemical composition of the essential oil of Salvia argentea L. Agro Food Ind Hi Tech. 25:70–72. Weiss RF. 1998. Herbal medicine. Beaconsfield: Beaconsfield Publishers. Wu YB, Ni ZY, Shi QW, Dong M, Kiyota H, Gu YC, Cong B. 2012. Constituents from Salvia species and their biological activities. Chem Rev. 112:5967–6026. doi:10.1021/cr200058f. Yang MH, Blunden G, Xu YX, Nagy G, Mathe I. 1996. Diterpenoids from Salvia species. Pharm Sci. 2:69– 71. Zito P, Sajeva M, Bruno M, Maggio A, Rosselli S, Formisano C, Senatore F. 2010. Essential oil composition of stems and fruits of Caralluma europaea NEBr. (Apocynaceae). Molecules. 15:627–638. doi:10.3390/molecules15020627. Zito P, Sajeva M, Bruno M, Rosselli S, Maggio A, Senatore F. 2013. Essential oils composition of two sicilian cultivars of Opuntia ficus-indica (L.) Mill. (Cactaceae) fruits (prickly pear). Nat Prod Res. 27:1305– 1314. doi:10.1080/ 14786419.2012.734823.
Natural Product Research: Formerly Natural Product Letters Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/gnpl20
Chemical composition of volatile and fixed oils from of Salvia argentea L. (Lamiaceae) growing wild in Sicily a
a
a
Luana Riccobono , Antonella Maggio , Sergio Rosselli , Vincenzo b
c
a
Ilardi , Felice Senatore & Maurizio Bruno a
Dipartimento di Scienze e Tecnologie Biologiche Chimiche e Farmaceutiche (STEBICEF), Università di Palermo, Viale delle Scienze, Parco d'Orleans II, 90128 Palermo, Italy b
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Dipartimento di Scienze della terra e del Mare (DISTEM), Università di Palermo, Via Archirafi, 22, 90123 Palermo, Italy c
Dipartimento di Farmacia, Università di Napoli “Federico II”, Via D. Montesano, 49, 80131 Naples, Italy Published online: 16 Apr 2015.
To cite this article: Luana Riccobono, Antonella Maggio, Sergio Rosselli, Vincenzo Ilardi, Felice Senatore & Maurizio Bruno (2015): Chemical composition of volatile and fixed oils from of Salvia argentea L. (Lamiaceae) growing wild in Sicily, Natural Product Research: Formerly Natural Product Letters, DOI: 10.1080/14786419.2015.1030742 To link to this article: http://dx.doi.org/10.1080/14786419.2015.1030742
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Natural Product Research, 2015 http://dx.doi.org/10.1080/14786419.2015.1030742
Chemical composition of volatile and fixed oils from of Salvia argentea L. (Lamiaceae) growing wild in Sicily Luana Riccobonoa, Antonella Maggioa*, Sergio Rossellia, Vincenzo Ilardib, Felice Senatorec and Maurizio Brunoa
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a
Dipartimento di Scienze e Tecnologie Biologiche Chimiche e Farmaceutiche (STEBICEF), Universita` di Palermo, Viale delle Scienze, Parco d’Orleans II, 90128 Palermo, Italy; bDipartimento di Scienze della terra e del Mare (DISTEM), Universita` di Palermo, Via Archirafi, 22, 90123 Palermo, Italy; cDipartimento di Farmacia, Universita` di Napoli “Federico II”, Via D. Montesano, 49, 80131 Naples, Italy (Received 17 February 2015; final version received 15 March 2015)
The chemical compositions of the essential oil and of the non-polar extracts (petroleum ether, dichloromethane) of the aerial parts (flowers, leaves and stems) of Salvia argentea L. were determined by GC-FID and gas chromatography –mass spectrometry analysis. 14-Hydroxy-a-humulene (40.1%) was recognised as the main constituents of the essential oil of S. argentea, together with 1,3,8-p-menthatriene (12.1%), globulol (7.4%) and b-sesquiphellandrene (5.8%). Tritriacontane (9.9% and 14.1%), heptacosane (8.4% and 10.5%), hentriacontane (8.3% and 10.9%), tetradecanal (8.4% and 10.2%) and methyldotriacontane (7.9% and 7.6%) were recognised as the main constituents of the extracts in petroleum ether and dichloromethane, respectively, whereas methyl linolenate (36.6% and 13.5%) and methyl myristoleate (10.5% and 18.5%) were recognised as the main constituents of the methylated extracts. Keywords: Salvia argentea; Lamiaceae; volatile components; 14-hydroxy-ahumulene; fixed oils; fatty acids; linolenic acid
1. Introduction The genus Salvia is one of the largest members of the family Lamiaceae (subfamily Nepetoideae), comprising more than 500 species. It is widely distributed in various regions including the temperate and warmer zones of the world such as the Mediterranean, where it is represented by 36 species (Hedge 1972), Central Asia, the Pacific Islands, tropical Africa and America (Wu et al. 2012).
*Corresponding author. Email: [email protected] q 2015 Taylor & Francis
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It is one of the most representative genus of the Labiatae that includes valuable species used in culinary preparations, phytotherapy and aromatherapy such as Menta piperita, Thymus capitatus, Rosmarinus officinalis and Salvia officinalis. The essential oils and extracts of these species hold important biological properties, in fact the antibacterial, antioxidant, hypoglycaemic, anti-inflammatory and cytotoxic activities besides an action against neurodegenerative disorders have been recently reported (Ben Jemia, Tundis, et al. 2013; Iauk et al. 2014; Sun et al. 2014; Kadioglu & Efferth 2015; Nazem et al. 2015). Several Salvia species are economically important because they have been used in therapy as antihydrotic, spasmolytic, antiseptic, anti-inflammatory and in the treatment of mental and nervous conditions (Baricevic & Bartol 2000) and furthermore as spices and flavouring agents in perfumery and cosmetics. Members of this genus have been shown to possess a significant array of pharmacological properties such as antimicrobial, antioxidant, cytotoxic, anti-HIV (Bisset 1994; Newall et al. 1996; Blumenthal 1998; Weiss 1998). The occurrence of the non-volatile secondary metabolites and the biological properties of all the studied species of Salvia have been recently reviewed (Wu et al. 2012). The essential oils of Salvia species are also applied in the treatment of a range of diseases, and it has been shown to possess antimicrobial, viricidal, cytotoxic, anti-mutagenic and antifungal activities (Jalsenjak et al. 1987). Salvia argentea L., (syn: S. tmolea Boiss.) is a perennial herb native to the Mediterranean region, in northwest Africa (Morocco, northern Algeria, Tunisia), southern Europe (Spain, Portugal, South Italy, Sicily, Malta, Albania, Bulgaria, Slovenia, Croatia, Bosnia, Kosovo, Montenegro, Serbia, Macedonia, and Greece) and the far west of Asia (Turkey). It occurs primarily on stony hillside meadows, basalt, volcanic soils and rocky bluffs. Usually, it is not found very near the sea or ocean, or at low altitudes, but it has often been found on highlands not far from the sea (http://ww2.bgbm.org/euroPlusMed/). S. argentea has a large basal leaves zone that measure 1 m wide and 30 – 60 cm high. The individual leaves are 20– 30 cm long and 15 cm wide. Both leaf surfaces are heavily covered with silky hairs that give it a wooly appearance. The leaves are soft to the touch, first emerging as a distinctive silvery white and then turning to greygreen after flowering. Cool weather in the fall turns the leaves silvery again (Clebsch & Barner 2003). In Lucania (Italy), where it is known as “l’erva du taglie`”, the young leaves of S. argentea were topically used as haemostatic (Pieroni et al. 2004), whereas the basal leaves, peeled and stewed, were consumed as food in Spain (“gordolobo”) (Tardı´o et al. 2006). Several biological properties have been reported for this species. In fact, a good antioxidant activity has been shown from the aqueous and methanolic extracts (Stagos et al. 2012) and from the methanolic extract (Salah et al. 2006; Ben Farhat et al. 2013a, 2013b). Furthermore, good acetylcholinesterase (AChE) and butyrylcholinesterase (BChE) inhibitory activity for the CH2Cl2 and methanolic extracts (Orhan et al. 2013), antibacterial activity on Staphylococcus aureus and Staphylococcus epidermidis for the ethanolic extract (Sarac & Ugur 2007) and larvicidal activity, against the mosquito Culex pipiens (S¸eref Gu¨n et al. 2011) for the hexane extract, were determined. Previous phytochemical studies of the plant indicated the presence of abietane diterpenoids in the roots (Michavila et al. 1986; Yang et al. 1996), whereas several flavones, from the exudates of S. argentea collected in Bulgaria (Nikolova et al. 2006) and from the acetone extract of plants cultivated in Poland (Sajewicz et al. 2012), and oleanane and ursane derivatives (Bruno et al. 1987; Janicsa`k et al. 2006) were identified in the aerial parts. Furthermore, several ursane triterpenoids with a new pattern of distribution of functional groups have been isolated from S. argentea var. aurasiaca (Pomel) Batt. & Trab., collected in Algeria (Lakhal et al. 2014) suggesting chemotaxonomic differences from other S. argentea variations. Some investigations have been published on the composition of the essential oil of S. argentea growing in Morocco (Holeman et al. 1984), Serbia (Couladis et al. 2001),
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Macedonia (Velicˇkovic´ et al. 2014) and Tunisia (Ben Farhat et al. 2013a), but nothing has been reported on Italian plants. In this study, as a continuation of our researches on Mediterranean plants (Zito et al. 2010; Rosselli et al. 2012; Maggio et al. 2013, 2014), we report the chemical composition of the essential oil and of the non-polar extracts from aerial parts of S. argentea L. growing wild in Sicily, a population not previously investigated.
2. Results and discussion Hydrodistillation of S. argentea aerial parts (HD) gave a yellow oil. Overall, 35 compounds were identified, representing 93.8% of the total oil composition. The components, listed in Table 1 according to their retention indices (RI) on an HP-5MS column, were divided into six classes on the basis of their chemical structures. 14-Hydroxy-a-humulene (40.1%) was recognised as the main constituent of the essential oil of S. argentea, together with 1,3,8-p-menthatriene (12.1%), globulol (7.4%) and b-sesquiphellandrene (5.8%). Generally, the oil consisted mainly of oxygenated sesquiterpenes (58.6%) and monoterpene hydrocarbons (21.4%), whereas sesquiterpene hydrocarbons (13.6%) were present in lower amounts and hydrocarbons, carbonylic compounds and specially oxygenated monoterpenes were almost absent. Four previous studies reported the chemical composition of S. argentea oils from plants collected in different regions (Holeman et al. 1984; Couladis et al. 2001; Ben Farhat et al. 2013a; Velicˇkovic´ et al. 2014), and their results have been inserted in Table 1. Caryophyllene oxide was reported as the main component of the oil from Macedonia (Ma) (37.6%), followed by a-copaene (8.5%), humulene epoxyde II (6.3) and b-caryophyllene (6.1%) (Velicˇkovic´ et al. 2014), whereas the major components of Serbian oil (S) were viridiflorol (32.4%), manool (14.6%), a-humulene (10.7%) and b-thujone (7.3%) (Couladis et al. 2001). The profile of the two Tunisian populations (T1 and T2) (Ben Farhat et al. 2013a) is quite similar to the Serbian one. In fact, although they were richer in monoterpene hydrocarbons (14.5% and 13.5%) with respect to S (0.5%) the main constituents were viridiflorol (26.9% and 18.7%), manool (6.1% and 13.6%), a-thujone (7.3% and 8.1%) and a-humulene (4.1% and 5.3%). On the other hand, the oil sample obtained from the Moroccan S. argentea (Mo) (Holeman et al. 1984) was characterised by camphor (45.1%), camphene (19.4%), a-pinene (9.3%) and borneol (9.0%). The composition of the essential oil of S. argentea collected in Sicily (HD) was found to be quite different from the composition of the oils of the other populations studied so far. In fact, although it had a high content in oxygenated sesquiterpenes such as Ma, S, T1 and T2, 14-hydroxy-a-humulene, 1,3,8-pmenthatriene, globulol and b-sesquiphellandrene, the main components of HD, were totally absent in the other populations. Furthermore, viridiflorol, manool, caryophyllene oxide, ahumulene, thujone, camphor and camphene, major compounds of the other oils were not present in the Sicilian population. Aerial parts S. argentea were extracted with petroleum ether and dichloromethane at room temperature for 1 week to give two residues: ETP1 and DCM1, respectively. In order to identify the free fatty acids, a portion of these extracts was successively treated with a solution of diazomethane in Et2O to afford ETP2 and DCM2. The analysis of the petroleum ether (ETP1) and dichloromethane (DCM1) extracts allowed the identification of 26 and 15 compounds, representing 90.2% and 93.2%, respectively, of the total composition, whereas in ETP2 and DCM2 21 and 26 compounds were identified, representing 90.5% and 90.1%, respectively, of the total composition. The components, listed in Table 2 according to their RI on an HP-5MS column, were divided into six classes on the basis of their chemical structures.
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Table 1. Chemical composition of essential oils of S. argentea collected in Sicily (HD) and reported in literature. RIa
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1358 2300 2500
925 928 938 953 980 1024 1025 1057 1108
1337 1351 1364 1396 1432 1487 1490 1522
RIb
Idc
1634 2300 2500
1, 2 1, 2, 3 1, 2, 3
1035 1014 1032 1076 1118 1150 1278 1256 1409
1468 1467 1527 1616 1612 1679 1694 1785
1, 2 1, 2 1, 2, 3 1, 2 1, 2, 3 1, 2, 3 1, 2, 3 1, 2, 3 1, 2
1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2
Compoundsd Hydrocarbons a-Ionene Tricosane Pentacosane Heptacosane Nonacosane 2-Methyltetradecane 2-Methyltetracosane Tetradecane Pentadecane Heneicosane 2-Methyldocosane Monoterpene hydrocarbons a-Thujene Tricyclene a-Pinene Camphene b-Pinene Limonene p-Cymene g-Terpinene 1,3,8-p-Menthatriene Myrcene Terpinolene d3-Carene a-Phellandrene a-Terpinene (E)-b-Ocimene (Z)-b-Ocimene Oxygenated monoterpenes 1.8-Cineole a-Terpineol a-Thujone b-Thujone Borneol Camphor Carvacrol Eugenol Isoborneol Linalool Terpinen-4-ol Thymol Bornyl acetate Sesquiterpene hydrocarbons d-Elemene a-Cubenene Silphiperfola-5,7(14)-diene 7-epi-Sesquithujene b-Cubebene a-Amorphene ar-Curcumene b-Sesquiphellandrene Valencene
HDe
Maf
Sg
T1h
T2i
Moj
0.1 t t 0.1
9.4
4.0
0.0
0.0
0.0
0.5
14.5 t
13.5 t
28.7
0.5 t t t t t
3.9 0.7 0.8 1.0 4.2 1.5
1.8 0.6 0.5 0.9 6.4 1.2
9.3 19.4
0.7 0.1 0.2 0.3 0.6 0.5
0.5 0.3 0.2 0.1 0.5 0.5 20.7 4.0 1.0 8.1 2.7 0.1 2.1 0.1 0.1
12.7
22.1 4.2 0.8 7.3 2.2 0.1 3.2 0.4 t 0.1 2.2 0.8 0.2 0.6 9.2
t
0.1
0.1
0.2
0.1
21.4 t 0.1 2.2 t 2.6 t 3.4 1.0 12.1
0.5 0.9 1.0 0.8 0.5 4.0 0.5 0.5 0.7 0.0 t
t
2.4 1.6
t
0.0
0.6
t
0.6
13.6 0.1 3.9 0.8 2.1 0.1 t 0.8 5.8
t 30.2
t 13.1 3.1 t 1.7 7.3 1.0 t t t t t t
1.3 0.8 0.2 0.2 13.1
64.1 2.5 7.5 9.0 45.1
0.0
t t
(Continued)
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Table 1. (Continued)
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RIa
1582 1585 1587 1593 1602 1634 1640 1642 1645 1716
1480 1619
1285 1950
RIb
2095 2135 2098 2103 2037 2089 2187 2209 2145 2478
1807 1934
1485 2622
Idc
1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2 1, 2
1, 2 1, 2
1, 2 1, 2
Compoundsd -Muurolene -Cadinene d-Cadinene Cadalene cis-Calamenene b-Caryophyllene a-Calacorene b-Calacorene a-Copaene a-Humulene allo-Aromadendrene b-Bourbenene b-Elemene ?-Elemene 6,9-Guaiadiene Bicyclogermacrene Germacrene B Germacrene D E, E-a-Farnesene Sesquithujene a-Colocalene Oxygenated sesquiterpenes (E)-Sesquisabinene hydrate b-Copaen-4-a-ol Globulol Viridiflorol Salvial-4(14)-en-1-one; (mintketone) 1-epi-Cubenol t-Cadinol t-Muurolol Torreyol (a-muurolol) 14-Hydroxy-a-humulene Spathulenol Caryophyllene oxide Humulene epoxyde I Humulene epoxyde II b-Eudesmol a-Cadinol 10-peroxy-murolan-3,9(11)-diene Germacra-4(15),5,10(14)-trien-1-a-ol 10-nor-calamenen-10-one Carbonylic compounds Tridecan-2-one Tetradecanal Benzaldehyde Benzene acetaldehyde Nonanal Tetradecanoic acid Hexahydrofarnesyl acetone Others Dihydroedulan II (Z)-Phytol
HDe
Maf
1.9 3.0 6.1 1.3 1.1 8.5 0.6
58.6 4.1 1.4 7.4 0.3 t 3.1 1.1 0.2 0.9 40.1
0.6 0.4 t 1.2 t 1.3 3.9 t t 0.3 51.0
T1h
T2i
t t t
0.4 0.1 0.6
0.6 0.2 1.5
t 2.0
0.3 2.5 0.1
0.6 3.3 0.2
t 10.7 t
0.4 4.1 0.3
0.1 5.3 0.3
t
0.1
0.8
39.4
36.6
29.6
32.4
26.9
18.7
1.3 3.3
2.7 4.1
1.7 3.4
1.9 2.2
7.7
0.6
0.4
t 0.6
0.1 0.5
0.1 0.3
3.6 3.5 16.8
6.9
14.9
Moj
0.0
0.5 2.4 t
t 37.6 0.5 6.3
0.1 t 0.1
Sg
1.2 1.3 1.2 5.4
4.0 2.3 0.7
0.0
0.8 0.0 t t
4.6 3.1
0.0
(Continued)
6
L. Riccobono et al.
Table 1. (Continued) RIa
RIb
Idc
Compoundsd (E)-Phytol b-Ionone Manool Sclareol oxide Isocembrene Total
HDe
93.8
Maf
2.7 0.4 99.7
Sg
T1h
T2i
1.2 1.0 14.6
0.8 6.1
1.3 13.6
94.2
89.9
92.2
Moj
92.8
a
Retention index on a HP-5MS column. Retention index on a HP-Innowax column. Identification, 1 ¼ comparison of retention index; 2 ¼ comparison of mass spectra with MS libraries identification; 3 ¼ comparison with authentic compounds. d Correct isomer not identified. e t ¼ trace, less than 0.05%. f Ma ¼ collected in Macedonia (Velicˇkovic´ et al. 2014). g S ¼ collected in Serbia (Couladis et al. 2001). h T1 ¼ collected at Sers (Tunisia). i T2 ¼ collected at Makther (Tunisia) (Ben Farhat et al. 2013a). j Mo ¼ collected in Morocco (Holeman et al. 1984). b
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c
Tritriacontane (9.9% and 14.1%), heptacosane (8.4% and 10.5%), hentriacontane (8.3% and 10.9%), methyldotriacontane (7.9% and 7.6%) and tetradecanal (8.4% and 10.2%) were recognised as the main constituents of the extracts ETP1 and DCM1. Generally, ETP1 and DCM1 consisted mainly of hydrocarbons (60.1% and 63.1%), carbonylic compounds (18.3% and 17.5%) and monoterpene hydrocarbons (4.0% and 5.5%), whereas other classes of compounds were absent. Methyl ester was, by far, the main class of ETP2 and DCM2 (63.7% and 50.4%) with methyl linolenate (36.6% and 13.5%) and methyl myristoleate (10.5% and 18.5%) as the major compounds together with methyl palmitate (8.0% and 1.9%). Among the hydrocarbons (17.0% and 26.8%), the second most abundant class, only tritriacontane (4.1% and 5.0%), heptacosane (2.9% and 4.6%) and hentriacontane (3.2% and 4.4%) are worthy of mention, whereas carbonylic compounds (8.9% and 11.4%) and other classes of compounds were present in lower amount. The compositions of petroleum ether and dichloromethane extracts were found to be quite similar. In fact, both ETP1 and DCM1 had a high content in hydrocarbons (60.1% and 63.1%) and the distribution of monoterpene hydrocarbons and carbonylic compounds appeared to be similar. The profile of ETP2 and DCM2 was also analogue. Both had a high rate of methyl esters (63.7% and 50.4%) and hydrocarbons, moreover a comparable quantity of carbonylic compounds was present. This large amount of free fatty acids (63.7%), which have been already proved to be very active against several mosquito species (Rahuman et al. 2008), probably explains the larvicidal activity of the hexane extract against the mosquito C. pipiens, as previously reported (S¸eref Gu¨n et al. 2011). 3. Experimental 3.1. Plant material Aerial parts of S. argentea L. were collected on the southern side of Monte delle Rose (Agrigento, Sicily, Italy) (378380 18.1900 N, 138250 6.6200 E, 1177 m s/L), in July 2014, from plants
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Table 2. Chemical composition of non-polar extracts of S. argentea collected in Sicily. RIa
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2300 2478 2500 2700 2863 2900 3052 3100 3264 3300 3500
RIb
Idc
2300 1, 2, 3 1, 2 2500 1, 2, 3 2700 1, 2, 3 1, 2 2900 1, 2, 3 1, 2 3100 1, 2, 3 1, 2 3300 1, 2, 3 3500 1, 2
938 1032 1, 2, 3 980 1118 1, 2, 3 1057 1256 1, 2, 3 1432 1612 1, 2 1494 1735 1, 2 1480 1517 1619 1703 1908
1807 1829 1934 2036 2219
1703
1, 2 1, 2 1, 2 1, 2 1, 2 1, 2
1712 2021 1, 2, 3 1891 2237 1, 2, 3 1928 2208 1, 2, 3 2085 2505 1, 2, 3 2135 2487 1, 2, 3 2139 2298 3132 3317 1472 1677 1893 2132
1, 2, 3 1, 2 1, 2 1, 2 1973 2193 2384 2625
1, 2 1, 2 1, 2 1, 2
Compoundd
ETP1 ETP2 DCM1 DCM2e
Hydrocarbons 60.1 Tricosane 1.5 Methyltetracosane# 3.2 Pentacosane 4.4 Heptacosane 8.4 Methyloctacosane# 2.8 Nonacosane 6.3 Methyltriacontane# 3.2 Hentriacontane 8.3 Methyldotriacontane# 7.9 Tritriacontane 9.9 Pentatriacontane 4.2 Monoterpene hydrocarbons 4.0 a-Pinene 1.2 b-Pinene 0.3 g-Terpinene 2.5 Sesquiterpene hydrocarbons 3.9 b-Cubebene 2.6 a-Zingiberene 1.3 Carbonylic compounds 18.3 Tridecan-2-one 2.5 Tridecanal 3.9 Tetradecanal 8.4 Pentadecan-2-one 2.7 Heptadecan-2-one 0.8 Methyl ester 0.1 9-Tetradecenoic acid methyl ester; methyl myristoleate Tetradecanoic acid methyl ester; methyl myristate (Z)-9-Hexadecenoic acid methyl ester; methyl palmitoleate Hexadecanoic acid methyl ester; 0.1 methyl palmitate (Z,Z)-9,12-Octadecadienoic acid methyl ester methyl linoleate (Z,Z,Z)-9,12,15-Octadecatrienoic acid methyl ester; Methyl linolenate Octadecanoic acid methyl ester; methyl stearate Methyl eicosenoate; methyl gadoleate Octacosanoic acid methyl ester Triacontanoic acid methyl ester; methyl melissate Others 3.8 Dodecanol 0.4 Tetradecanol 2.0 Hexadecanol 0.9 (E)-Phytol 0.5 Total 90.2
17.0
63.1
26.8
0.6 2.9 0.6 1.8 0.5 3.2 2.4 4.1 0.9 0.0
1.4 2.3 10.5 1.9 8.3 1.0 10.9 7.6 14.1 5.1 5.5 5.5
0.7 1.3 4.6 1.0 3.0 2.2 4.4 3.4 5.0 1.2 0.6
0.9 0.9
7.1 7.1
8.9 1.1 1.8 4.7 1.3
17.5
63.7 10.5
3.8 10.2 3.5 0.0
0.6 0.9 0.9 11.4 1.0 2.5 5.7 1.8 0.4 50.4 18.5 5.6
2.4 8.0
1.9
3.0
1.6
36.6
13.5
1.6 1.6
1.5 3.6 2.2 2.0
0.0
0.0
0.0
90.5
93.2
90.1
# Correct isomer not identified. a Retention index on an HP-5MS column. b Retention index on an HP-Innowax column. c Identification, 1 ¼ comparison of retention index; 2 ¼ comparison of mass spectra with MS libraries identification; 3 ¼ comparison with authentic compounds. d Correct isomer not identified. e t ¼ trace, less than 0.05%.
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at the full flowering stage. Typical specimens (SAF-P 200), identified by Prof. Vincenzo Ilardi, have been deposited Herbarium SAF, Department of Agricultural and Forest Science, University of Palermo, Palermo, Italy.
3.2. Isolation of the essential oil
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The air-dried samples were grounded in a Waring blender and then subjected to hydrodistillation for 3 h using n-hexane as solvent, according to the standard procedure previously described (Ben Jemia, Rouis, et al. 2013). The oil was dried over anhydrous sodium sulphate and then stored in sealed vials, at 2 208C, ready for the GC and gas chromatography– mass spectrometry (GC – MS) analyses. The sample yielded 0.27% (HD) of yellow oil (w/w) with a pleasant smell.
3.3. Preparation of the extracts Dried and finely powdered S. argentea (100 g) samples were extracted with petroleum ether and dichloromethane at room temperature for 1 week. The extracts were evaporated to dryness yielding a residue (1.098 and 0.496 g, respectively for ETP1 and DCM1). A portion of the extracts was treated with a solution of diazomethane in Et2O to afford ETP2 and DCM2.
3.4. Qualitative and quantitative analyses The essential oil and the four extract samples were analysed to determine the chemical components at the ‘Department of Pharmacy’ of the University of Naples ‘Federico II’ by GC and GC – MS. The GC analyses were carried out with a Perkin-Elmer Sigma 115 gas chromatograph fitted with an HP-5MS capillary column (30 m £ 0.25 mm i.d.; 0.25 mm film thickness) and equipped with a flame ionisation detector (FID). Analysis was also run by using a fused silica HP-Innowax polyethylenglycol capillary column (60 m £ 0.25 mm i.d.; 0.25 mm film thickness). GC – MS was recorded on an Agilent 6850 Ser. II apparatus fitted with a fused silica HP-5 capillary column (30 m £ 0.25 mm i.d.; 0.25 mm film thickness) and coupled to an Agilent Mass Selective Detector MSD 5973 as previously described (Loizzo et al. 2013). Identification of constituents was made as elsewhere reported (Zito et al. 2013) by comparison of their RI with either those of the literature (Jennings & Shibamoto 1980; Davies 1990) or with those of authentic compounds available in our laboratories. The RI were determined in relation to a homologous series of n-alkanes (C8 –C28) under the same operating conditions. Further identification was made by comparison of their mass spectra on both columns with either those stored in NIST 02 and Wiley 275 libraries or with mass spectra from the literature (Jennings & Shibamoto 1980; Adams 2007) and our home-made library. Component relative concentrations were calculated based on GC peak areas without using correction factors.
4. Conclusion In conclusion, with regard to S. argentea essential oil, the results presented herein indicate a quite different chemical profile of the Sicilian population with respect to the other ones studied so far and show that environmental conditions such as soil composition, climate can drastically influence the composition of the secondary metabolites. The previously reported larvicidal activity of the hexane extract against the mosquito C. pipiens, whose chemical composition was not reported, (S¸eref Gu¨n et al. 2011) could be explained by the huge presence of free fatty acids (63.7%), which have been already proved to be very active against several mosquito species (Rahuman et al. 2008).
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Acknowledgements GC – MS spectra were performed at the Pharmacy Department, University of Naples ‘Federico II’.
Disclosure statement No potential conflict of interest was reported by the authors.
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References Adams RP. 2007. Identification of essential oil components by gas chromatography/mass spectrometry. 4th ed. Carol Stream, IL: Allured Publishing Co. Baricevic D, Bartol T. 2000. Sage: the genus Salvia. In: Kintzios SE, editor. Pharmacology: the biological/ pharmacological activity of the Salvia genus. New York, NY: Harwood Academic Publishers; p. 143 –184. Ben Farhat M, Landoulsi A, Chaouch-Hamada R, Sotomayor JA, Jorda´n MJ. 2013a. Profiling of essential oils and polyphenolics of Salvia argentea and evaluation of its by-products antioxidant activity. Ind Crops Prod. 47:106–112. doi:10.1016/j.indcrop.2013.02.007. Ben Farhat M, Landoulsi A, Chaouch-Hamada R, Sotomayor JA, Jorda´n MJ. 2013b. Characterization and quantification of phenolic compounds and antioxidant properties of Salvia species growing in different habitats. Ind Crops Prod. 49:904–914. doi:10.1016/j.indcrop.2013.06.047. Ben Jemia M, Rouis Z, Maggio A, Venditti A, Bruno M, Senatore F. 2013. Chemical composition and free radical scavenging activity of the essential oil of Achillea ligustica growing wild in Lipari (Aeolian Islands, Sicily). Nat Prod Commun. 8:1629–1632. Ben Jemia M, Tundis R, Maggio A, Rosselli S, Senatore F, Menichini F, Bruno M, Kchouk ME, Loizzo MR. 2013. NMR-based quantification of rosmarinic and carnosic acids, GC –MS profile and bioactivity relevant to neurodegenerative disorders of Rosmarinus officinalis L. extracts. J Funct Foods. 5:1873–1882. doi:10.1016/j.jff. 2013.09.008. Bisset NG. 1994. Herbal drugs and phytopharmaceuticals. Stuttgart: CRC Press. Blumenthal M. 1998. The complete German commission E monographs. Austin, TX: American Botanical Council. Bruno M, Savona G, Hueso-Rodrı´guez JA, Pascual C, Rodrı´guez B. 1987. Ursane and oleanane triterpenoids from Salvia argentea. Phytochemistry. 26:497– 501. doi:10.1016/S0031-9422(00)81441-7. Clebsch B, Barner CD. 2003. The new book of Salvias: sages for every garden. Portland, OR: Timber Press. Couladis M, Tzakou O, Stojanovic D, Mimica-Dukic N, Jancic R. 2001. The essential oil composition of Salvia argentea L. Flavour Frag J. 16:227–229. doi:10.1002/ffj.989. Davies NW. 1990. Gas chromatographic retention indices of monoterpenes and sesquiterpenes on methyl silicon and Carbowax 20M phases. J Chromatogr A. 503:1– 24. doi:10.1016/S0021-9673(01)81487-4. Hedge IC. 1972. Salvia L. In: Tutin TG, Heywood VH, Burges NA, Valentine DH, Walters SM, Webb DA, editors. Flora Europaea. Vol. 3. Cambridge: Cambridge University Press; p. 188. Holeman MA, Berrada M, Bellakhdar J, Ilidrissi A, Pinel R. 1984. Comparative chemical study on essential oils from Salvia officinalis, S. aucheri, S. verbenaca, S. phlomoides and S. argentea. Fitoterapia. 55:143–148. Iauk L, Acquaviva R, Mastrojeni S, Amodeo A, Pugliese M, Ragusa M, Loizzo MR, Menichini F, Tundis R. 2014. Antibacterial, antioxidant and hypoglycaemic effects of Thymus capitatus (L.) Hoffmanns. Et Link leaves’ fractions. J Enzyme Inhib Med Chem. 17:1– 6. doi:10.3109/14756366.2014.930453. [Epub ahead of print]. Jalsenjak V, Peljnajk S, Kustrak D. 1987. Microcapsules of sage oil, essential oils content and antimicrobial activity. Pharmacology. 42:419–420. Janicsa`k G, Veres K, Zoltan Kaka`sy A, Ma`the´ I. 2006. Study of the oleanolic and ursolic acid contents of some species of the Lamiaceae. Biochem Syst Ecol. 34:392–396. Jennings W, Shibamoto T. 1980. Qualitative analysis of flavour and fragrance volatiles by glass capillary gas chromatography. New York, NY: Academic Press. Kadioglu O, Efferth T. 2015. Pharmacogenomic characterization of cytotoxic compounds from Salvia officinalis in cancer cells. J Nat Prod. doi:10.1021/np501007n. [Epub ahead of print]. Lakhal H, Kabouche A, Alabdul Magid A, Voutquenne-Nazabadioko L, Harakat D, Kabouche Z. 2014. Triterpenoids from Salvia argentea var. aurasiaca (Pomel) Batt. & Trab. and their chemotaxonomic significance. Phytochemistry. 102:145–151. Loizzo M, Jemia M, Senatore F, Bruno M, Menichini F, Tundis R. 2013. Chemistry and functional properties in prevention of neurodegenerative disorders of five Cistus species essential oils. Food Chem Toxicol. 59:586–594. doi:10.1016/j.fct.2013.06.040. Maggio A, Bruno M, Formisano C, Rigano D, Senatore F. 2013. Chemical composition of the essential oils of three species of the Apiaceae family growing wild in Sicily: Bonannia graeca, Eryngium maritimum and Opopanax chironium. Nat Prod Commun. 8:841–844.
Downloaded by [University of Victoria] at 04:42 25 April 2015
10
L. Riccobono et al.
Maggio A, Riccobono L, Bancheva S, Bruno M, Senatore F. 2014. Chemical composition of the essential oil of the local endemics Centaurea davidovii and C. parilica (Asteraceae, sect. Lepteranthus) from Bulgaria. Nat Prod Commun. 9:1373–1376. Michavila A, De la Torre MC, Rodrı´guez B. 1986. 20-nor-abietane and rearranged abietane diterpenoids from the root of Salvia argentea. Phytochemistry. 25:1935–1937. doi:10.1016/S0031-9422(00)81178-4. Nazem F, Farhangi N, Neshat-Gharamaleki M. 2015. doi:10.1016/j.jcjd.2014.11.003 Beneficial effects of endurance exercise with Rosmarinus officinalis Labiatae leaves extract on blood antioxidant enzyme activities and lipid peroxidation in streptozotocin-induced diabetic rats. Can J Diabetes.. Newall CA, Anderson LA, Phillipson JD. 1996. Herbal medicines: a guide for healthcare professionals. London: Pharmaceutical Press. Nikolova MT, Grayer RJ, Genova E, Porter EA. 2006. Exudate flavonoids from bulgarian species of Salvia. Biochem Syst Ecol. 34:360– 364. doi:10.1016/j.bse.2005.11.006. Orhan I, Senol F, Ercetin T, Kahraman A, Celep F, Akaydin G, Sener B, Dogan M. 2013. Assessment of anticholinesterase and antioxidant properties of selected sage (Salvia) species with their total phenol and flavonoid contents. Ind Crops Prod. 41:21–30. doi:10.1016/j.indcrop.2012.04.002. Pieroni A, Quave CL, Santoro RF. 2004. Folk pharmaceutical knowledge in the territory of the Dolomiti Lucane, inland southern Italy. J Ethnopharmacol. 95:373– 384. doi:10.1016/j.jep.2004.08.012. Rahuman AA, Venkatesan P, Gopalakrishnan G. 2008. Mosquito larvicidal activity of oleic and linoleic acids isolated from Citrullus colocynthis (Linn.) Schrad. Parasitol Res. 103:1383–1390. doi:10.1007/s00436-008-1146-6. Rosselli S, Maggio AM, Canzoneri M, Simmonds MSJ, Bruno M. 2012. Sesquiterpenes from Onopordum illyricum and their antifeedant activity. Nat Prod Commun. 7:1131–1132. Sajewicz M, Staszek D, Wro`bel MS, Waksmundzka-Hajnos M, Kowalska T. 2012. The HPLC/DAD fingerprints and chemometric analysis of flavonoid extracts from the selected sage (Salvia) species. Chromatogr Res Int., Article ID 230903: 1–8. Salah KBH, Mahjoub MA, Ammar S, Michel L, Millet-Clerc J, Chaumont JP, Mighri Z, Aouni M. 2006. Antimicrobial and antioxidant activities of the methanolic extracts of three Salvia species from Tunisia. Nat Prod Res. 20:1110–1120. doi:10.1080/14786410600834230. Sarac N, Ugur A. 2007. Antimicrobial activities and usage in folkloric medicine of some Lamiaceae species growing in Mugla, Turkey. EurAsia J BioSci. 4:28–37. ¨ z E, C S¸eref Gu¨n S, C ¸ inbilgel I˙, O ¸ etin H. 2011. Larvicidal activity of some Salvia L. (Labiatae) plant extracts against the mosquito Culex pipiens L. (Diptera: Culicidae). Kafkas Univ Vet Fak Derg. 17:S61–S65. Stagos D, Portesis N, Spanou C, Mossialos D, Aligiannis N, Chaita E, Panagoulis C, Reri E, Skaltsounis L, Tsatsakis AM, Kouretas D. 2012. Correlation of total polyphenolic content with antioxidant and antibacterial activity of 24 extracts from Greek domestic Lamiaceae species. Food Chem Toxicol. 50:4115–4124. doi:10.1016/j.fct.2012. 08.033. Sun Z, Wang H, Wang J, Zhou L, Yang P. 2014. Chemical composition and anti-inflammatory, cytotoxic and antioxidant activities of essential oil from leaves of Mentha piperita grown in China. PLoS One, doi:10.1371/journal. pone.0114767. Tardı´o J, Pardo-De-Santayana M, Morales R. 2006. Ethnobotanical review of wild edible plants in Spain. Bot J Linnean Soc. 152:27–71. Velicˇkovic´ DT, Ristic´ MS, Milosavljevic´ NP, Davidovic´ DN, Bogdanovic´ SZ. 2014. Chemical composition of the essential oil of Salvia argentea L. Agro Food Ind Hi Tech. 25:70–72. Weiss RF. 1998. Herbal medicine. Beaconsfield: Beaconsfield Publishers. Wu YB, Ni ZY, Shi QW, Dong M, Kiyota H, Gu YC, Cong B. 2012. Constituents from Salvia species and their biological activities. Chem Rev. 112:5967–6026. doi:10.1021/cr200058f. Yang MH, Blunden G, Xu YX, Nagy G, Mathe I. 1996. Diterpenoids from Salvia species. Pharm Sci. 2:69– 71. Zito P, Sajeva M, Bruno M, Maggio A, Rosselli S, Formisano C, Senatore F. 2010. Essential oil composition of stems and fruits of Caralluma europaea NEBr. (Apocynaceae). Molecules. 15:627–638. doi:10.3390/molecules15020627. Zito P, Sajeva M, Bruno M, Rosselli S, Maggio A, Senatore F. 2013. Essential oils composition of two sicilian cultivars of Opuntia ficus-indica (L.) Mill. (Cactaceae) fruits (prickly pear). Nat Prod Res. 27:1305– 1314. doi:10.1080/ 14786419.2012.734823.
