Наук . вісник Ужгород . ун -ту ( Сер . Хімія ), 2017, № 1 (37) Nauk. vìsn. Užgorod. unìv., Ser. Hìm., 2017, № 1 (37) -5-

UDK: 547.5

Daniela Gru ľová 1, RNDr., PhD.; Vincenzo De Feo 2, Prof., PhD.

EUPHRASIA ROSTKOVIANA HAYNE - ACTIVE COMPONENTS AND BIOLOGICAL ACTIVITY FOR THE TREATMENT OF EYE DISORDERS

1Department of Ecology, Faculty of Humanities and Natural Sciences, University of Presov, Presov, Slovakia, e-mail:[email protected] 2Department of Pharmacy, University of Salerno, Via Giovanni Paolo II 132, 84084 Fisciano (Salerno), Italy, e-mail:[email protected]

Introduction at West Carpatian area in mountains regions. Medicinal are the oldest source of They present polyploids taxons with the high pharmacologically active compounds and range of hybridisation [8]. The species of the provided virtually the only source of medicinally genus perform a great variability and the useful compounds for centuries. According to differentiating characters are difficult to the World Health Organization, a medicinal recognise. The eyebrigh was characterised as is defined as any plant which contains stricta J. P. Wolff ex J. F. Lehm substances than can be used for therapeutic which was used in folk medicine for treatment of purposes or which are precursors of chemo- various eye problems [9]. The occurence of this pharmaceutical semisynthesis [1]. species is widespread in middle Europe. The The most frequently reported herbs used genus Euphrasia includes 14 species and 6 for treatment ocular diseases are ginkgo, bilberry hybrids growing in Slovakia. Most represented and ginseng. Another plant with the common growing in Slovakia are E. rostkoviana and E. name «eyebright» refers to the plant's use in stricta while Serbian flora recognizes eight treating eye infections. Although eyebright has species of Euphrasia genus [10]. These species been a part of the traditional folk medicine for are usually used as medicinal plants and the sold centuries, the literature of its constituents and product name is herba Euphrasiae . The different their way of acting is limited [2]. cytotypes or hybrids, respectivelly contain the The genus Euphrasia L. consists of high content of active components. The full around 450 species and their wild hybrids plants collected at flowering phase have always difficult to identify botanically belongs to the been used in phytomedicine for the treatment of family of , formerly included in various ocular problems [4]. the Scrophulariaceae [3]. It is an annual (rarely perennial) Uses hemiparasite species. This plant, with Hayne, synonym cosmopolitan distribution, is widespread on E. officinalis L., commonly known as alpine or sub-alpine meadows where snow is “eyebright”, “eyewort”, is a wild plant growing common and in pastures in many parts of in the temperate climatic zone [11]. The aerial European countries [4]. We can find this species parts of eyebright have been used since the also in Asia, Northern parts of America, in Middle Ages by pharmacists and physicians in mountains of Indonesia and New Zealand, and Europe in the treatment of various eye problems South America [5]. The occurance of the such as cataracts, conjunctivitis inflamed, and medicinal plant called „eyebright“ in temperate sore-eyes [4, 12, 13], disorders of the stomach, Himalayas, from Kashmir to Sikkim, Nilgiri’s, jaundice, diabetes and upper airway diseases Palestine, Israel and to Iran was noted [6]. [11]. The bright and shine in the eyes is done by The plant material is collected usually in eyebright. The Germans call it augentrost, Bulgaria, Hungary and the former states of Italians luminella and French people casse- Jugoslavia [7]. Most of the species are localised lunette. Eyebright reduce fatigue and soresness

 Daniela Gru ľová, Vincenzo De Feo Наук . вісник Ужгород . ун -ту ( Сер . Хімія ), 2017, № 1 (37) Nauk. vìsn. Užgorod. unìv., Ser. Hìm., 2017, № 1 (37) -6- and eliminates watery eyes, runny nose caused despite serious risk of infection, some people by colds and hey fever [14]. Moreover a recent apply eyebright directly to the eye in the form of multinational prospective cohort trial proves the a lotion, poultice, or eye bath to treat a variety of anti-conjunctivitis effect of eyebright eye-drops. conditions including conjunctivitis, inflamma- Euphrasia single-dose eye drops can effectively tion of the eyelids at the edge of the lashes and safely be used for various conjunctival (blepharitis), eye fatigue, inflammation of the conditions by general practitioners and blood vessels, eyelids and conjunctiva, and for ophthalmologists. A dosage of one drop three "glued" and inflamed eyes. Eyebright is also times a day seems to be the general prescribed applied to the eyes to prevent mucous and dosage [15]. Iridoid glycosides, tannins and mucous membrane inflammation of the eyes. phenolic acids are the most important Additionally, eyebright is used as food compounds of this medicinal plant [11]. These being consumed as infusion and is listed by the compounds are known for anti inflammatory, Council of Europe as a natural flavouring [3] astringent, antioxidative, anti-apoptotic and however little scientific information was found weak antibiotic effects [3, 16]. Traditionally, to justify the reputed herbal uses.

Table 1. The list of the biological effects and disordes treated by the extracts of Euphrasia rostkoviana Hayne Biological effect Treated disorders anti-inflamatory ocular allergy symptoms antioxidant eye disorders antimicrobial palpebral margin inflammation anticancer conjunctivitis antifungal hordeolum antiviral dry eye hypotensive blepharitis hepatoprotectiver redness antiepileptic swelling anticatarrhal secretion regenerative burning of the conjunctiva immunomodulatory foreign body sensation

Phytochemical compositions The principal compounds in the aerial part spectrometry [24, 25], GC-MS [9, 11, 18], LC- of eyebright were defined as iridoids, phenolic MS [18, 26, 27] and LC-ESI-MS fragmentation acids, phenylpropane and flavonoid glycosides [4] and LC-TOF [2] were used for identification [2, 9, 17, 18]. phytochemicals. Iridoids, being described as 8- Different solvents (aqueous, methanol, (S)-7,8-dihydro-geniposide, geniposidic acid, ehanol, ethylacetate, heptane, n-hexane, chlo- aucubin, catalpol, euphroside, eurostoside, roform) were used to prepare the extracts from ixoroside, mussaenosidic acid [4, 13, 24, 25,]; aboveground parts of Euphrasia rostkoviana phenylethanoids: verbascoside, samioside and Hayne [4, 11, 17-19] (Table 2). crassifolioside [4]; phenyl-propanoid glycosides: Qualitative analyses included planar dehydroconiferyl alcohol-4-d-glucoside, eukovo- chromatography [20], differential spectro- side (3,4-dihydroxy-4-phenethyl-O-l-rhamnoside photometry [21-23], highperformance liquid (13)-4-O-isoferuoyl-d-glucoside), acteoside [2]; chromatography (HPLC) [4, 11], nuclear mag- phenolic compounds like hydroxytyrosol, netic resonance (NMR) spectroscopy and mass chlorogenic acid, caffeic acid, caffeic acid Наук . вісник Ужгород . ун -ту ( Сер . Хімія ), 2017, № 1 (37) Nauk. vìsn. Užgorod. unìv., Ser. Hìm., 2017, № 1 (37) -7- derivatives, coumaric acid and flavonoids: [9]. Identification of β-sitosterol was first done glycosidesof apigenin, luteolin, kaempferol by [20] and later [18] after GC-MS analysis (kaempferol-3-O-rutinoside), rhamnetin and mentioned the occurence of trans-phytol, quercetin-3-O-rutinoside (rutin) [2, 11, 28]. heptacosanes and nanocosanes along with Authors of [7] also mentioned a little amount of phytosterols. essential oil, which composition is descibed in

Table 2. Different solvents used extracts preparation for phytohemicals identification and biological activity of Euphrasia rostkoviana Hayne Solvent for extract preparation Authors methanol [4, 18, 19] ethanol [11, 17] ethyl acetate [17, 18] heptane [17] n-hexane [4, 18] chloroform [18] water [11]

The flavonoids were determined in were presented in the chromatographic profiles amount 0.38/100 g (hyperoside), polyphenols in of E. rostkoviana extracts (Table 3). amount 1.47/100 g (pyrogallol), tannins in High acteoside content in eyebright may amount 0.56/100 g (pyrogallol) and hydroxyl- give a reasonable explanation for its anti- cinnamic derivatives in amount 1.97/100 g inflammative action concerning eye-disorders. (rosmarinic acid) [18]. Fifteen phenolic com- Some biological properties were attributed to pounds were identified as six hydroxycinnamic quinic acid and its esters, like anti-inflammatory acids and derivatives and nine flavonoids, and antioxidant [29]. β-sitosterol is one of the distributed by flavones and flavonols were principal sterol in several plants materials, being identified [11]. Besides the chlorogenic and one of the most efficient compounds, acting in caffeic acids, quercetin-3-O-rutinoside and membranes to restrict the motion of fatty acyl apigenin which were previously reported by [2, chains, because of its stereochemistry, associated 18], they observed the presence of flavonoid with the presence of 24-ethyl group at C-24 [30]. glycosidesof apigenin (m/z 431), luteolin (m/z Hydroxycinnamic acids have been found to have 447), kaempferol (m/z 447 and m/z 593), good antioxidant activities [31]. The presence of rhamnetin (m/z 477) and quercetin (m/z 609) in the CH CH COOH group in the hydroxylcin- air-dried powdered E. rostkoviana . Regarding namic acids is considered to be a key for their the phenolic acids, they corresponded to ca. 67% significantly antioxidative efficiency [32]. and 55% of the total phenolics in hydroethanolic The promising bioactive compounds and infusion extracts. Continuously, they descrybed in eyebright are important to further identified seven organic acids: oxalic, aconitic, investigate their metabolite composition and to citric, malic, quinic, acetic and fumaric acids, compare extracts with different polarities focu- first time reported in this study. Quinic acid was sing their enrichment on active principles [11]. the main compound in E. rostkoviana leaves, representing 73% and 70% of the determined Antioxidant activity compounds in hydroethanolic and infusion Oxidative stress is a key feature of extracts, respectively. Also fatty acids were inflammation process and phenolic compounds herein reported for the first time. Nine fatty are potent antioxidant agents. Methanolic extract acids, which comprised four saturated (myristic, of Euphrasia rostkoviana Hayne and its pentadecanoic, palmitic, margaric) and five methanolic fractions were evaluated for unsaturated (linoleic, linolenic, stearic, cis11- antioxidant activity by [19]. Researchers [11] eicosenoic, docosahexaenoic) free fatty acids tested hydroethanolic and infusion extracts for and two sterols (cholesterol and β-sitosterol) scavenging activity against DPPH•, nitric oxide Наук . вісник Ужгород . ун -ту ( Сер . Хімія ), 2017, № 1 (37) Nauk. vìsn. Užgorod. unìv., Ser. Hìm., 2017, № 1 (37) -8-

Table 3. Identified phytochemicals in aerial parts of Euphrasia rostkoviana Hayne 8-(S)-7,8-dihydro-geniposide geniposidic acid aucubin catalpol iridoids [4, 13, 24, 25] euphroside eurostoside ixoroside mussaenosidic acid Verbascoside - acteoside phenylethanoids samioside [4] crassifolioside dehydroconiferyl alcohol-4-d- glucoside phenylpropanoid eukovoside (3,4-dihydroxy-4- glycosides phenethyl-O-l-rhamnoside(13)-4- [2] O-isoferuoyl-d-glucoside) phenyletanoid acteoside glycoside hydroxytyrosol chlorogenic acid phenolic caffeic acid compounds caffeic acid derivatives coumaric acid gylykosides of apigenin [2, 11, 28] luteolin kaempferol (kaempferol-3-O- flavonoids rutinoside) rhamnetin quercetin-3-O-rutinoside (rutin) hyperoside hydroxycinnamic [18] rosmarinic acid derivatives β-sitosterol [11, 18, 20] sterols cholesterol [11] trans-phytol heptacosanes [18]

nanocosanes oxalic aconitic citric organic acids malic quinic acetic fumaric myristic [11] pentadecanoic palmitic margaric fatty acids linoleic linolenic stearic cis11-eicosenoic docosahexaenoic

Наук . вісник Ужгород . ун -ту ( Сер . Хімія ), 2017, № 1 (37) Nauk. vìsn. Užgorod. unìv., Ser. Hìm., 2017, № 1 (37) -9-

Table 4. Some stoichiometrical formula of Euphrasia rostkoviana Hayne components (+)-geniposide geniposidic acid aucubin catalpol C17 H24 O10 C16 H22 O10 C15 H22 O9 C15 H22 O10

euphroside ixoroside mussaenosidic acid acteoside C16 H24 O10 C16 H24 O9 C16 H24 O10 C29 H36 O15

samioside eukovoside rosmarinic acid chlorogenic acid C34 H44 O19 C30 H38 O15 C18 H16 O8 C16 H18 O9

trans-caffeic acid o-coumaric acid hydroxytyrosol apigenin C9H8O4 C9H8O3 C8H10 O3 C15 H10 O5

luteolin kaempferol-3-O- rhamnetin rutin C15 H10 O6 rutinoside C 27 H30 O15 C16 H12 O7 C27 H30 O16 Наук . вісник Ужгород . ун -ту ( Сер . Хімія ), 2017, № 1 (37) Nauk. vìsn. Užgorod. unìv., Ser. Hìm., 2017, № 1 (37) -10-

hyperoside β-sitosterol cholesterol phytol C21 H20 O12 C29 H50 O C27 H46 O C20 H40 O

oxalic acid citric acid malic acid quinic acid C2H2O4 C6H8O7 C4H6O5 C7H12 O6

acetic acid fumaric acid myristic acid palmitic acid C2H4O2 C4H4O4 C14 H28 O2 C16 H32 O2

margaric acid linoleic acid linolenic acid eicosenoic acid C17 H34 O2 C18 H32 O2 C18 H30 O2 C20 H30 O3

and superoxide radicals, while ethanol, ethyl Fractionation dominated by a glycosilated acetate and heptane extract, was tested by in caffeic acid derivative, exhibited the strongest vitro tests on human corneal cells by [17]. antioxidant activity in DPPH and ABTS assays, Наук . вісник Ужгород . ун -ту ( Сер . Хімія ), 2017, № 1 (37) Nauk. vìsn. Užgorod. unìv., Ser. Hìm., 2017, № 1 (37) -11-

IC 50 : 11.88 µg/ml and 4.24 µg/ml, respectively, was the most active against Gram-positive and which are notable results if compared to the Gram-negative bacteria, presenting the lowest investigated standards. Fractions of flavonoid MIC and MLC values. S. epidermidis and P. glycosides proved to have similarly strong, but mirabilis were the most susceptible species for lower effect [19]. Infusion showed stronger both extracts. The E.rostkoviana extracts showed activity than hydroethanolic extract in DPPH bacteriostatic and bactericidal activities against assay and ainst both radicals O 2• and NO•, all of the studied strains. Results obtained for respectively. The reduction result of ethyl hydroethanolic and infusion extracts revealed acetate extracts was lower by almost half than in that Gram-positive bacteria as more sensitive ethanolic extract. The heptane extract did not than Gram-negative ones. show DPPH reduction activity and lower ethanol extract concentration reduced the NO x level to a Cytotoxic and immunomodulatry effect on greater extent than the higher one. However, all human corneal epithelial (10.014 pRSV-T) results were lower than the radical level obtained cells in the control. Inversely, a higher concentration It has been shown that flavonoids and of the ethyl acetate and heptane extracts led to polyphenols possess an inflammation reducing stronger NO x reducing activity [17]. Extracts effect. Their anti-inflammatory properties are obtained using a polar solvent (ethanol) manifested mainly through the modulation of the increased corneal cell NO x production, while the cytokine network. Cytokines are a group of inverse, i.e. extracts obtained with ethyl acetate multifunctional substances involved in immune- and heptane, decreased the NO x level. Ethanol logical processes. One of the classifications and ethyl acetate extracts were not toxic to distinguishes pro- and anti-inflammatory human corneal cells even at a concentration of cytokines; IL-1β, IL-6 or TNF-α represent the 125 g/mL. However, mixtures of fractions former group while e.g. IL-10 the latter [33]. obtained after heptane extraction were toxic to Extract from eyebright application to cells when the concentration exceeded 10.014 pRSV-T cells generally decreased pro- 75 g/mL, while cellular mitochondrial metabo- inflammatory cytokine levels. Inhibition of lism was significantly limited at a concentration inflammation should be considered to be a of only 25 g/ml. Undesirable effects on the positive therapeutic effect, considering the fact eyes may exert when non-polar solvents are used that prolonged inflammation is the result of for the extraction of the active components. much pathology. Cytokines released by corneal Important positive roles in the maintenance of cells treated with E. rostkoviana extracts in tests eye surface health may be observed. This may be exert immunomodulatory activity rather than a beneficial effect in some chronic eye diseases typical anti- or pro-inflammatory properties. such as dry eye or ocular allergies. The ethanol (at low concentrations) and ethyl acetate extracts Conclusions were the most useful E. rostkoviana Hayne. The use of different techniques of Extracts for supplemental clinical ocular extraction affects the chemical composition of E. medicine due to their effects on the free radical rostkoviana extracts and consequently their balance [17]. The achievement of better results biological activities. with infusion may be related with the presence Uppermentioned properties of the main of higher amounts in phenolic compounds and components occured in aerial parts of the E. organic acids [11, 32]. rostkoviana present the potential benefits of the plant which may be interesting for the future Antibacterial activity research. Its ecological aspect as a hemiparasite Biological assays for antibacterial activity plant could lead to the beginning of the new of eyebright hydroethanolic and water extracts investigation of the relation between the host and were investigated by [11] for the first time. MIC the production of secondary metabolites. and MLC values were determined in three Gram-positive ( S. aureus , S. epidermidis and M. Acknowledgement luteus ) and in six Gram-negative ( E. faecalis , B. The work was supported by the projects cereus , P. mirabilis , E. coli , P. aeruginosa and ITMS: 26220220182 and Project number S. typhimurium ) bacterial strains. Water extract 003PU-2-3/2016. Наук . вісник Ужгород . ун -ту ( Сер . Хімія ), 2017, № 1 (37) Nauk. vìsn. Užgorod. unìv., Ser. Hìm., 2017, № 1 (37) -12-

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Paper received on: 19.05.2017.

EUPHRASIA ROSTKOVIANA HAYNE - ACTIVE COMPONENTS AND BIOLOGICAL ACTIVITY FOR THE TREATMENT OF EYE DISORDERS

Daniela Gru ľová, Vincenzo De Feo.

Euphrasia rostkoviana Hayne is an annual hemiparasite wild grow in mountain medows. It is a medicinal plant also known as Aufraise, Augentrostkraut, Casse-Lunettes, Eufrasia, Euphraise, Euphrasia, Herbe d'Euphraise, Luminet, eyebright and other names. Folk medicine have known this plant and used the leaf, the stem, and small pieces of the flowers for the treatment of eye diseases. Herbalists use eyebright as a poultice with or without concurrent administration of a tea for the redness, swelling, and visual disturbances caused by blepharitis and conjunctivitis. The herb is also used for eyestrain and to relieve inflammation caused by colds, coughs, sinus infections, sore throats and hay fever. Short review aimed on the scientific facts which were publish in last decades. The principal compounds in the aerial parts were identified as iridoids, phenolic acids, phenylpropane-, and flavonoid-glycosides. The content of flavonoids, polyphenols, tannins and hydroxycinnamic derivatives were also determined. The antioxidant and antibacterial activity as well as imunomodulatory effect was performed. Despite its potential in treatment of eye diuseases, there are still less knowledge presented.