Indian Journal of Traditional Knowledge Vol. 16(2), April 2017, pp. 243-250

The ethnobotanical uses of Hyacinthaceae growing in and a review of pharmacological activities

Serpil Demirci Kayıran1* & Esra Eroğlu Özkan2 1Cukurova University Faculty of Pharmacy, Department of Pharmaceutical Botany, 01330, Adana, Turkey; 2Istanbul University Faculty of Pharmacy, Department of Pharmacognosy, 34116, Istanbul, Turkey E-mail: [email protected]

Received 28 March 2016, revised 25 November 2016

The Hyacinthaceae families have long been used in traditional medicine for a wide range of medicinal applications. This, together with some significant toxicity to livestock has led to the chemical composition of many of the species being investigated. The Hyacinthaceae family has represented 9 genera and 140 taxa of which 77 are endemic to Turkey. Especially species of Hyacinthaceae family have been mostly used as medicinal, for the treatment of rheumatism, cardiac, urinary infection, dermatological, stomach, hemorrhoid and prostate disease. An overview of the accessible 59 ethnobotany articles and 27 phytochemistry articles published since 1979 up to 2015 has been carried out. The most important databases have been consulted. All related works have been examined. This study is a review having traditional uses belonging to Turkish species and pharmacological activities of the Hyacinthaceae family in the world.

Keywords: Hyacinthaceae, Ethnobotany, Pharmacological activity, Turkey

IPC Int. Cl.8: A61K 36/00

The Hyacinthaceae (sense APGII) are bulbous , and benefits from the plants found in their own with approximately 900 species in about 70 genera, region. Initially, wild plants were collected from their can be divided into three main sub-families, the natural habitat, followed by the cultivation of those Hyacinthoideae, the Urgineoideae and the that were used most commonly. Turkish people are Ornithogaloideae, with a small fourth subfamily the quite interested in wild plants, due to the high Oziroeoideae, restricted to South America1,2. In proportion of people living in rural areas, and also for Turkey, the Hyacinthaceae family has represented economic reasons5-7. Local people in Turkey have a 9 genera (, , , long history of ethnobotanical usages for plants, Hyacinthus, , , , which was gained through long experiences, as the , and ) and 140 taxa of which 77 are dye, as ornamental plants, as perfume, as adhesive, as endemic to Turkey3. The plants included in this soap and as animal food in Turkey. In this study, family have long been used in traditional medicine for different uses of Hyacinthaceae family are presented a wide range of medicinal applications in the world. based on the ethnobotanical researches carried out in This, together with some significant toxicity to a different region in Turkey. livestock has led to the chemical composition of many of the species being investigated4. There is some Methodology activity working on Hyacinthaceae species in Turkey In this study, 36 ethnobotanical article and and in the world. Turkey is one of the most 27 phytochemical articles,62 usages of Hyacinthaceae floristically rich countries in the world with species by using international and national databases astonishing diversity. Its flora consists of about were funded. Domestic resources that were referenced 11000 vascular plants and approximately one-third of include the database of author’s doctoral theses its flora (34, 4 %) is endemic to the country. “Pharmaceutical Botanical Studies on the species Throughout history, humans have derived many uses of the family Hyacinthaceae (Kahramanmaraş)”. —————— A literature study was performed to collect data on the *Corresponding author use of Hyacinthaceae species parts in articles. In this 244 INDIAN J TRADIT KNOWLE, VOL 16, NO. 2, APRIL 2017

study, 62 different records and their used parts, used orientalis L. has a long history of cultivation as an purpose, uses, county and references were explained , grown across the Mediterranean in details in Table 1. Records of used species, used region, and later , the Netherlands and parts, used purpose showed in diagrams (Figs. 1-2). elsewhere. The of this species were collected The usage purposes of species could be split into and cultivated for the first time from Turkey.The food, medicinal, ornamental plants, dye, toys and bulbs of (L.) Stearnhave been used other usages. since a very long time. The sprouted were In our studies, the used plant parts most frequently hunged on a door as protection against evil spirits. are bulbs and leaves, whole plant, , scape, The bulbs of this species were reported to treatment of herba, bud, , and shoot. Record numbers of heart disease in the Materia Medica of Dioscorides. Hyacinthaceae members parts (leaves, whole plants, Today, bulbs of this species were used as medicinal in fruit, , herba, , scapes) for ethnobotanical Turkey9-11. As a result of this reviews, medicinal usages (food, medicinal, dye, ornamental, toys, utilizations of Hyacinthaceae species were determined adhesive, soap) were explained in details (Fig.1). in all 8 groups (Cancer diseases: tumor, prostate; Medicinal uses of Hyacinthaceae species could be urinary system diseases: urinary infections; listed below in 8 groups:1. Cancer diseases: Tumor, respiratory system disease: expectorant; circulatory prostate; 2. Urinary system diseases: Urinary system disease: cardiac disease, hemorrhoid; infections; 3. Respiratory system disease: analgesic: headache, kneepain; skin disease: boil, Expectorant; 4. Circulatory system disease: Cardiac acne; digestive system disease: as emetic, gastritis; disease, hemorrhoid; 5. Analgesic: A headache, other diseases: snake and scorpion bike, as antibiotic) kneepain; 6. Skin disease: Boil, acne; 7. Digestive for medicinal remedies. The usage of curing of snake system disease: As emetic, gastritis; 8. Other diseases: and scorpion bike or as antibiotic was classified under Snake and scorpion bike, as antibiotic. the group of “other usages”. The leaves, bulbs and of species by a majority for medicinal purposes, Results and discussion the whole plants and scape for ornamental purposes, Traditional uses in Turkey the herb for food and the flowers as dye were used. Total 62 items revealed the ethnobotanical uses of The leaves, bulbs, and flowers were used as food for 25 taxa (3 taxa of Bellevalia, 2 taxa of Hyacinthus, 5 all Bellevalia species in eastern Turkey12,13. The taxa of Muscari, 2 taxa of Leopoldia, 9 taxa of medicinal usage of bulbs of Muscari, Ornithogalum Ornithogalum, one taxon of Puschkinia, 2 taxa of and Drimia species were detected in the investigated Scilla and one taxon of Drimia) were recorded (Fig. publications. Only Ornithogalum oligophyllum 2). Ornithogalum and Muscari species were most E.D.Clarke was detected for the usage of shoots as used species of which record number is 26, where the soap. Usage of buds as soap was common of rest of the were at numbers 10, 7, 6, 6, 5 and 2 O. sphaerocarpum A.Kern and as a food of for Hyacinthus, Drimia, Bellevalia, Leopoldia, O. narbonense L.14-19. Four records of Hyacinthus Puschkinia and Scilla, respectively (Table 1). In this orientalis L. were recorded for curing prostate reviews, the most frequently used plant parts were, disease, wound healing, and hemorrhoids and as bulbs (20 records), leaves (20 records), followed by hemostatic where whole plant, leaves, bulbs, and whole plants (14 records), flowers (9 records), scape scapes are used parts20-21. (L.) Parl. (4 records), herb, bud and fruit (2 records) and shoot are determined as mostly used species as gastric, as an (1 record). (The multiple uses can be possible). The expectorant and as diuretic22. Two records of the fruit record numbers of the usage purpose and the parts of of M. neglectum Guss. ex Ten. have been used for the species were showed in Fig.1. A total of 26 curing of rheumatism disease23-25. We found for records were recorded as food, of 18 records as a skin disease curing of O. narbonense L. and medicinal plant, 6 records as ornamental plants, two O. umbellatum L. only in two investigated publication26. each record as soap and one record as toys, as adhesive or as honey plants. Apart from these, of 4 Pharmacological activities 8 species is reported to be as poisonous . Many of the Anti-inflammatory activity toxic compounds in bulbs of Hyacinthaceae species The extracts of leaves, bulbs and roots of have been known. The leaves of species mostly are autumnalis (Mill.) Chitt. [as Ornithogalum undulatum used as food, the bulbs are not used. Hyacinthus (Aiton) Thunb.] were tested by the inhibition of KAYIRAN & ÖZKAN: ETHNOBOTANICAL USES OF HYACINTHACEAE SPECIES GROWING IN TURKEY 245

Table 1—Traditional usages of Hyacinthaceae members in Turkey Used parts Used purpose Uses County References forniculatum (Fomin) Garbari Leaves, bulb Food Eaten cooked Iğdır 12 (syn. Bellevalia forniculata Deloney) Bellavalia paradoxa (Fisch. & C.A.Mey.) Leaves Food Eaten cooked Iğdır 12 Boiss. [syn. Bellevalia pycnantha (K.Koch) Losinsk.] Bellevalia speciosa Woronow Flower, bulb Food Eaten fresh Kars 13 ex Grossh. (syn. Bellevalia sarmatica (Pall. ex Leaves Food Eaten cooked Iğdır 12 Miscz.) L. - - - South Anatolia 5 - - Cultivated İzmir 58 Hyacinthus orientalis L.subsp. chionophilus Whole plant Medicinal Hemostatic Tunceli 20 Wendelbo Leaves, scape Medicinal Prostate disease Kahramanmaraş 11 Bulb Medicinal Wound healing Kahramanmaraş 20 Leaves Medicinal Hemorrhoids disease East Anatolia 21 Leichtlin Flower Dye - Düzce 59 ex Baker Whole plant Dye, poison - Amasya 8 Flower Dye Egg coloring K.maraş 60, 61 Whole plant Ornamental plants - Mersin 57 Whole plant Ornamental plants - Iğdır 12 Muscari bourgaei Baker Whole plant Dye, poison - Amasya 8 Sweet Bulb Medicinal Gastric, expectorant, - 5 diuretic Muscarir acemosum Mill. Whole plant Ornamental plants Garden decoration 5 (syn. Muscari muscarimi Medik.) Guss. ex Ten. Leaves, Flower Dye, Toys Egg coloring, hairpin İzmit 62 Fruit Medicinal Rheumatic disease Manisa 25 Whole plant Dye Coloring Amasya 8 Flower Medicinal Wart disease Yalova 24 Fruit Medicinal Rheumatic disease Isparta 7, 23 Leaves Food Animal food Aksaray 6 Bulb Food Eaten West Anatolia 63 Leopoldia comosa (L.) Parl. Bulb Medicinal Gastric,expectorant, İstanbul 22 [syn. Muscari comosum (L.) Mill.] diuretic Whole plant Food Eaten fresh Aksaray 9 Ornamental plants Bulb Medicinal Gastric,expectorant, - 5 diuretic Bulb Food Eaten fresh Erzurum 18 Leopoldia tenuiflora (Tausch) Heldr. (syn. Bulb Medicinal Antibiotic, rheumatism Hakkari 64 Muscari tenuiflorum Tausch) and tumor disease Whole plant Food Animal food Aksaray 9 Ornithogalum armeniacum Baker Leave, Flower Food Eaten cooked Antalya 10 Ornithogalum lanceolatum Labill. Whole plant Food Eaten as vegetable Mersin 5 Ornithogalumn arbonense L. Bulb, Leaves Food Eaten as vegetable Iğdır 12 Bulb Food Eaten cooked Erzurum 18 Leaves Food Eaten cooked Sakarya 16 Medicinal Acne disease, emetic, 14 diuretic, cardioactive Leaves, bud Food Eaten cooked Adana 14 Leaves Food Eaten as vegetable Siirt 19 Herb Food Food Inner Anatolia 58 (Contd.) 246 INDIAN J TRADIT KNOWLE, VOL 16, NO. 2, APRIL 2017

Table 1—Traditional usages of Hyacinthaceae members in Turkey Botanical name Used parts Used purpose Uses County References Ornithogalum oligophyllum E.D.Clarke Bulb, Leaves Food Eaten cooked Iğdır 12 Leaves, shoot Soap - Amasya 8 Scape, Leaves Food Eaten cooked Blacksea region 17 Ornithogalumm ontanum Cyr. (syn. Bulb, Leaves Food Eaten cooked İzmit 62 Ornithogalum platyphyllum Boiss.) Scape, Leaves Food Eaten cooked Blacksea region 17 L. Whole plant - Animal food Aksaray 6 Ornithogalum sigmoideum Freyn & Sint. Whole plant Food Eaten cooked İzmit 62 Scape, Leaves Food Eaten cooked Blacksea region 17 Ornithogalum sp. Whole plant Food Eaten as vegetable Ordu 65 Ornithogalum sphaerocarpum A.Kern. Leave, bud Soap - Amasya 8 L. Whole plant Poison - Aksaray 6 Bulb Medicinal Boil and acne disease Uşak 26 Adams Leaves, Flower Food Eaten fresh Iğdır 12 Ornamental plants Home decoration 12 Herb Food Food East Anatolia 64 L. Bulb Medicinal Wound healing, Kırklareli 66 herniated disc disease Haw.subsp. armena (Grossh.) Flower Ornamental plants Home decoration Iğdır 12 Mordak Drimia maritime (L.) Stearn Flower, Bulb Adhesive, Adhesive, honey plant Mersin 57 [syn. Urginea maritima (L.) Baker] Honeyplant Bulb Medicinal Snake or scorpion bike Bodrum 9 Bulb Medicinal Headache and kneepain Antalya 10 disease Bulb Medicinal Diuretic, cardio active Kahramanmaraş 11 Bulb Medicinal, poison Diuretic, expectorant, Aegean 5 cardio active Mediterranean cyclooxygenase enzymes COX-1 and COX-227.Two Antimicrobial activity homo isoflavanones and a xanthone isolated from The purified protein extract of ovatifolia (Baker) Jessop exhibited (Mill.) Chitt. [as Ornithogalum undulatum (Aiton) significant activity against COX-2 with an IC50 of Thunb.] has good activity against Bacillus subtilis at 2.87 μM28.The bulb extract of plumbea MIC of 0.2 mg/ml29. Antibacterial activity of homo (Lindl.) Speta (as Scilla plumbea Lindl.) exhibited isoflavanones isolated from and moderate inhibitory activity against COX-129.The Eucomis schiffii have been tested. Some of these dichloromethane and hexane extracts of Merwilla compounds showed activity against Staphylococcus plumbea (Lindl.) Speta showed good inhibition aureus32. The bulbs of Leopoldia comosa (L.) Parl. against both COX-1 and COX-230.The methanol (as Muscari comosum Mill.) were tested for the extracts of nervosus (Burch) van der inhibition of the methicillin-resistant Staphylococcus Merwe [as Scilla nervosa (Burch.) Jessop] bulbs were aureus (MRSA) biofilms. Leopoldia comosa (L.) tested in a mouse model of acute croton oil-induced Parl.(as Muscari comosum Mill.) showed a significant auricular contact dermatitis for anti-inflammatory dose dependent biofilm inhibition with an IC50 of 16 activity. After treatment with the extract, oedema was µg/ml34. According to Goktas et al. ethanol extract of significantly reduced 3 hrs (~66 %) and 6 hrs Muscari neglectum Guss. ex Ten. showed antifungal (~40 %). The result showed that the extract has strong activity against Postia placenta and Trametes but short acting effect31. The water extract of the bulb versicolor35. A 29 kDa glycoprotein isolated of Drimi aelata Jacq. (as Drimi arobusta Baker) from (Roxb.) Jessop [as Urginea showed percentage inhibition of COX-1 that was indica (Roxb.) Kunth] bulbs demonstrated inhibition over 70 %33. the germination of spores and hyphal growth of KAYIRAN & ÖZKAN: ETHNOBOTANICAL USES OF HYACINTHACEAE SPECIES GROWING IN TURKEY 247

Fig. 2—Records number of ethnobotanical usages according to taxa

Antioxidant activity Antioxidant potential of some homo isoflavanones isolated from Mill.has been determined by lipid peroxidation assay. Strong antioxidant activity was observed with an IC50 value between 0.94 µM and 7.98 µM38.Two homo isoflavanones, namely ledebourin B and ledebourin C were isolated from the bulbs of Ledebouria floribunda (Baker) Jessop have shown good antioxidant activity against DPPH radical and β-carotene/linoleic acid system39. The bulbs of Leopoldia comosa (L.) Parl. [as Muscari comosum (L.) Mill.] were tested for antioxidant activity by DPPH screening and lipid

peroxidation assays. In both antioxidant assays, strong Fig. 1—Record numbers of Hyacinthaceae members parts (leaves, activity was shown for Leopoldia comosa (L.) whole plants, fruit, bulb, herba, flowers, scapes) for Parl. [as Muscari comosum (L.) Mill.]40. The ethnobotanical usages (food, medicinal, dye, ornamental, toys, adhesive, soap) ethanolic extract of the bulbs of Ledebouria revoluta L.f.) Jessop [as Scilla indica (Wight) Baker] showed Fusarium oxysporum36. The ethanol extract of root 49 % protection against the lipid peroxidation induced of japonica (Thunb.) Schult. & Schult.f. by ferrous sulphate at a concentration of 250 µg/ml41. [as Scilla scilloides (Lindl.) Druce] showed Antioxidant activity of the bulb of Ornithogalum antimicrobial activity against Staphylococcus aureus, alpigenum Stapf was determined using β– Salmonella enteritidis, Escherichia coli and carotenelinoleic acid model system. The methanol Candida parapsilosis37. Some homo isoflavanones extract showed the highest antioxidant activity of 42 isolated from barteri Baker were 88.12 ± 0.9 % . tested against the methicillin-resistant Staphylococcus aureus (MRSA), one of them showed significant Cyclic AMP phosphodiesterase activity inhibitory activity with an MIC of 0.47 nM32. The One of the triterpenoid oligosaccharides, dichloromethane fraction of the methanol extract of Scillasaponin A isolated from Baker Schizocarphus nervosus (Burch) van der Merwe has been found to inhibit cyclic AMP phosphoesterase -5 2 (as Scilla nervosa (Burch.) Jessop showed inhibitory with an IC50 value of 11.5x10 M . Peruvianoside A activity against Staphylococcus aureus, Klebsiellla and scillasaponin B isolated from L. pneumoniae and Candida albicans with an IC50 showed moderate inhibitory activity against cyclic -5 values of 1.8 µg/ml, 2.0 µg/ml and 1.0 µg/ml, AMP phosphodiesterase with an IC50 of 23.5x10 and respectively31. 14x10-5, respectively43.

Antihelmintic activity Cytotoxic activity Aqueous extracts of (Lindl.) Some triterpenoid oligosaccharides isolated from Speta (as Scilla natalensis Planch.) had good activity Eucomis bicolor Baker have been found to be toxic to against Schistosoma haematobium, with a MIC of HeLa cells with the concentration between 5 µg/ml and 30 44 0.4 mg/ml . 50 µg/ml . Ethanol and dichloromethane extracts of 248 INDIAN J TRADIT KNOWLE, VOL 16, NO. 2, APRIL 2017

Ledebouria ovatifolia (Baker) Jessop showed good Hypoglycemic activity antibacterial activity against Gram-positive bacteria A polyhydroxypyrrolizidine alkaloid isolated from with a MIC value between 0.8 mg/ml and Muscari armeniacum Leichtlin ex Baker was found to 12.5 mg/ml30.Thirtheen homo isoflavanones have been be an inhibitor of intestine lactase, L-fucosidase isolated from Schizocarphus nervosus (Burch) van der and amyloglucosidase with an IC50 value of 4.4 µM, 52 Merwe [as Scilla nervosa (Burch.) Jessop] and tested 46 µM and 25 µM, respectively . A pyrrolidine against colon cancer (HT-29) and breast cancer (MDA- alkaloid isolated from Scilla siberica Haw. was MB-435) cell lines. One of these compounds was found to be a potent inhibitor β-glucosidase and found to be highly active with an ED50 value of 0.88 β-galactosidase with an IC50 of 3.2 µg/ml and 53 µg/ml and 0.42 µg/ml, respectively45. Some 4.4 µg/ml, respectively . The bulb of Scilla peruviana L. compounds isolated from (Boiss.) Speta contains pyrrolidins and A pyrrolizidines. Two of were tested for their cytotoxic activity against HSC-2 pyrrolizidine alkaloids showed significant inhibition 54 cells by using MTT assay. Four compounds showed of yeast α-glucosidase and bacterial β-glucosidase . cytotoxic activity with LD50 values ranging from 10 to Some polyhydroxy alkaloid isolated from Hyacinthus 23 mg/ml46. A 15-deoxoeucosterol oligosaccharide orientalis L., one of them was found to be a good isolated from Scilla peruviana L. was found to be toxic inhibitor bacterial β-glucosidase and mammalian 43 to HeLa cells at the concentration of 5 µg/ml . The galactosidase trehalases with an IC50 of 3.8 µg/ml and bufadienolide, riparianin isolated from the bulbs of 4.0 µg/ml, respectively. The other one inhibited rice Drimia macrocentra (Baker) Jessop and Drimia α-glucosidase and rat intestinal maltase with an IC50 55 calcarata (Baker) Stedje (as Urginea riparia Baker) of 2.2 µg/ml and 2.5 µg/ml, respectively . showed moderate activity against MCF7 (breast), This study is composed of traditional uses, TK10 (renal) and UACC62 (melanoma) cell lines47. pharmacological and phytochemical data of members Some bisdesmosidic cholestane glycosides isolated of Hyacinthaceae family. The medicinal and aromatic from the bulbs of Jacq. were plants of Turkey is extraordinarily rich. The richness tested on HL-60 leukemia cells. Two of these of medicinal and aromatic plants was decreasing with compounds were extremely cytotoxic with IC50 values three different phytogeographical regions (European- between 0.00013 and 0.00016 µg/ml48. Four water- Siberian, Mediterranean, and Iran-Turano), altitudes, soluble polysaccharide fractions extracted from the different climates and soil structures. That is a bracteata (Thunb.) J.C.Manning & Goldblatt positive correlation between floristic richness and 56 (as Ornithogalum caudatum Aiton) exhibited ethnobotanically useful of plants . The reported significantly higher antitumor activity against solid number of medicinal plants in the native folklore tumor Sarcoma 180 in vivo than control. Three remedies seems very significant the vegetation cover fractions significantly inhibited the growth of K562 of Turkey as the area has very rich flora. The cells in vitro49. The cytotoxic effects of Ornithogalum members of Hyacinthaceae family have a long history cuspidatum Bertol. methanolic fractions (40 %, 60 %, of traditional use in Turkey. The total number of 80 %, 100 %) were determined on PC-3, prostate population in Turkey also justifies the low number of cancer cells and WEHI-164 fibrosarcoma cells. The them under medicinal use. Ethnobotanically uses of 80 % and 100 % methanolic fractions showed Hyacinthaceae species of Turkey have comparatively significant antiproliferative and apoptotic effects on been studied more scientifically. Ethnobotanical PC-3 and WEHI-164 cells with IC50 value of 65 μg/ml, studies open the way for further investigation of new 45μg/ml and 76 μg/ml, 73μg/ml, rspectively50. Ethanol future prospects for the better healthcare of human and dichloromethane extracts of Ledebouria ovatifolia being regarding various diseases. Many folk remedies (Baker) Jessop showed good antibacterial activity used in traditional medicine are used as the first line against Gram-positive bacteria with a MIC value of healthcare. The literature survey showed that the between 0.8 mg/ml and 12.5 mg/ml30. pharmacological studies support the ethnobotanical usage of Hyacinthaceae species. As a result, these Eustrogenic activity species have a great therapeutic potential and it will The ether extract of bulb Muscari racemosum Mill. be evaluated for the medical treatment. Many of them exhibited estrogenic activity by inducing proliferation have been unconfirmed by pharmacological studies of MCF7 cells in a dose-dependent manner51. in vitro and in vivo. The toxicity of members of this

KAYIRAN & ÖZKAN: ETHNOBOTANICAL USES OF HYACINTHACEAE SPECIES GROWING IN TURKEY 249

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