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Asian Pac J Trop Med 2014; 7(Suppl 1):: S22-S28 S22

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Document heading doi: 10.1016/S1995-7645(14)60199-1 The chemical composition, botanical characteristic and biological activities of : a review 1 2 1 Majid Asadi-Samani , Mahmoud Bahmani , Mahmoud Rafieian-Kopaei * 1Medical Research Center, Shahrekord University of Medical Sciences, Shahrekord, Iran 2Razi Herbal Medicines Research Center, Lorestan University of Medical Sciences, Khorramabad, Iran

ARTICLE INFO ABSTRACT

Article history: Borago officinalis ( ) is an annual which is cultivated for medicinal and culinary uses, Received 2 Jun 2014 although it is commercially cultivated for . Borage seed oil is the rich in the Received in revised form 23 Aug 2014 gamma-linolenic acid (26%-38%) which is used as dietary or food supplement. Other than seed oil Accepted 17 Sep 2014 it contains a lot of fatty acids such as (35%-38%), (16%-20%), Available online 26 Sep 2014 (10%-11%), (3.5%-4.5%), eicosenoic acid (3.5%-5.5%) and (1.5%-3.5%). It is used for the treatment of various diseases such as multiple sclerosis, , heart diseases, and eczema. In this study different aspects of borage such as plant characteristics,’ production, applications in traditional medicine, clinical considerations, its effects on patients Keywords: blood and urine biochemistry, and also the effect of the its products on liver and kidney Borage performance tests are presented using published articles in scientific sites. Botanical characteristics Pharmacognosy Antioxidants Linolenic acid

1. Introduction in pharmaceutical, industrial and forage fields and is used in production of drinks and salads. This plant is known as Borago officinalis or borage is an annual herb which is high plant in Mediterranean regions. Borage is cultivated cultivated for medicinal and culinary uses, even though it around the world but is native to Europe, North Africa and is commercially cultivated for borage seed oil. Borage seeds Asia Minor[3,4]. Borage has oil seed which contains a high oil is the richest plant source of the gamma-linolenic acid amount of the GLA (30%-40%). GLA is one of the volatile fatty (GLA) which is used as dietary or food supplement. acids which is synthesized just by a few plant varieties and GLA is sometimes prescribed as anti-inflammatory drug often found in their seeds[5]. The main sources of the GLA with this belief that it lacks some of the common side- are borage and evening primrose[6,7]. Borage produces 300 effects of other anti-inflammatory drugs. GLA is also used to 600 kg seed in Britain so as to increase the amount of for the treatment of multiple sclerosis, diabetes, heart GLA in available crops and produce GLA in common oilseed diseases, arthritis, eczema, autoimmune disorders, cancer productions[7,8]. Ninety percent of selling rate of GLA oil is and premenstrual syndrome[1,2]. related to evening primrose. But borage is a better resource Borage is a medicinal plant which has different usages of the GLA since its seeds contain 30%-40% oil of which 20%-30% is GLA. This amount is approximately twice as many as that of in evening primrose. The oil of borage is *Corresponding author: Mahmoud Rafieian-Kopaei, Professor, PhD, Medical Plants Research Center, Shahrekord University of Medical Sciences, Shahrekord, Iran. more constant and its process is simpler than the oil of the Tel: 0098-3813346692 evening primrose[7,10]. Fax: 0098-3813349509 ’ E-mail: [email protected] In this study different aspects of borage such as plant s Foundation Project: Supported by Shahrekord University of Medical Sciences, history, characteristics, production, applications in Shahrekord, Iran. traditional medicine, clinical considerations, its effects on Majid Asadi-Samani et al./Asian Pac J Trop Med 2014; 7(Suppl 1): S22-S28 S23 ’ 2.3. Cultivation patients blood and urine biochemistry, and also effect of the its products on liver and kidney performance tests are presented. This plant is reproduced through seeding and each seed weights almost 17 to 19 g. Seeds are sown at 5-7 kg each hectare. The recommended suitable density to plant 2. History borage is equal to 100 000 shrubs per hectare. In another research in Isfahan, 30 cm distance between rows and 10 It was supposed that main sources of borage are from cm distance between shrubs on row has been defined as the Syria and Asia Minor while this plant is just found in very best attendance. Suitable cultivation time for this plant is little amounts. It seems that this plant has originated from in early spring, and it also can be cultivated in autumn and west Mediterranean areas, Spain and North Africa and late winter[21,23]. Researchers have shown that early seeding then has naturalized in many other locations. Historical increases seed performance comparing with late seeding. documents shows that people from North Africa tribes There is an interaction between seed performance and GLA have transferred it to Spain and then to other regions[11-14]. level which could be related to the date of cultivation and However, most researchers say that this plant is native to the consumption of nitrogen fertilizer[1,29]. In early seeding Mediterranean areas[15]. grain filling was happened in warmer days of mid-June to late August. Obtained results is shown that the amount of 2.1. Botanical characteristics the GLA is reduced as temperature reduction during growth period in a way that matched other studies on oil seed Borago officinalis from family is known crops[30]. as borage, burrage, bourrache, and bugloss[16-19]. Borage Nitrogen fertilizer increases length of the plant, twigs is an annual, herbaceous and hairy plant which height and production efficiency. The most adequate amount of changes between 70 to 100 cm[3,20]. Stems are straight, fertilizer is 250 kg of Nitrogen per hectare but more amounts often branched[21], hollow, and covered by tough fibers. will decrease production efficiency. Mineral fertilizers Its are alternate and simple. Its leaves are covered are not usually used in planting borage. In order to grow with tough fibers[22]. The are blue and rarely appear this plant properly, not only the amount of nitrogen and white or rose colored[23]. Their calycle and corolla are five- phosphorus but the amount of potassium in soil should parts which are divided into some parts and make flowers be enough[23,31]. Since flowering twigs are medicinal it is polypetalous appearance. One of the features of the corolla necessary to collect them and then dry and pack according is that lamina parts lead to a tube which is almost seen to correct principles. This plant is harvested in flowering in plants in this family, which differentiates it from other period before the start of seed formation[5,9,32]. E T various plants. ach has five flags with anthers near hey should be dried° in fresh air in shadow or by dryer to each other and there is a vertical appendage in their tube in temperature of 40 C. Three or four harvest is done base. The pistil has a superior ovary which is changed to a according to climate condition. The yield of borage is fruit with 3 to 4 brownish nutlet after growing and there is a between 1 500-2 500 kg dried plants per hectare[5,32,33]. One dark but no albumin seed inside each. The fruit of borage is of the serious problems in producing seed of borage is a small brownish oval wrinkled nutlet[24]. Ripe nutlets are unlimited process of flower and seed falling. Seeds become dark without albumin[23]. mature about 3 weeks after pollination. Plant continues to flowering while seeds are falling. Average rate of seeding is 2.2. Ecology estimated about 400 kg per hectare of which 320 kg is fallen and 80 kg can be harvested[30]. It is a high plant with high resistance to cold which can 2.4. Chemical compounds grow well in wet soils with good drainage, weedy places and in complete exposure to sunlight. It cannot tolerate 2.4.1. Stems, leaves, and flowers poor dry soils but growth condition can be better in suitable conditions. It can also grow better in land exposed to Many researchers have reported about the fatty acids moderate sun. Intense sun can change plant to rosette available in leaves or the whole plant of borage, but there state[14,21,22,25]. This plant can grow in each type of soil are few information about changes in fatty acids during and in pH scale range from 4.5-8.2. The suitable pH for growth period. A research evaluates the quality and the this plant is 6.6. It has been reported that borage can be amount of fatty acids available in borage in different growth easily cultivated in medium or heavy soils with water. stages and reported as follows[4]. Regarding its high potential in taking sodium and chlorine, The amount of dry matter in all considered growth stages it is likely suitable to modify salt soils[23,26-28]. was very low. Chemical compound was closely related Majid Asadi-Samani et al./Asian Pac J Trop Med 2014; 7(Suppl 1): S22-S28 S24 2.4.2. Seed to the growth stages of plant and the amount of fiber was increasingly raised. The amount of raw protein decreased Boraginaceae family is one of the most known resources and the amount of lignin showed age-related increase. of GLA. In a chemotaxonomic study on 45 plant biomasses Indigestibility of the organic substance decreased in the from Boraginaceae family it was determined that all beginning of the seed formation stage. This decrease biomasses contain GLA and the lowest amount (7%) was major was attributed to interactions of some factors including related to L. and the highest amount significant increase in fibers parts, relative increase in related to borage species (28%). This is available lignin during growth stages and changes in the ratio of plant in plant in a few amounts but is very important due to its tissues components. The amount of total energy was almost nutritional and medicinal value[43]. SDA is other fatty acid constant in first three stages and then increased a little. which is found in plants in a little amount but it is found in Since nutritional value during growth period was constant Boraginaceae family in amount of 2%[7]. Several studies have optimum harvest stage of the borage is in the beginning been conducted on combination of fatty acid available in of seed formation stage when performance of dry matter is seed oil of planted and wild species of Boraginaceae. The minimum. The profile of the fatty acids changes upon growth amount of linoleic acid, ALA, GLA, SDA and erucic acid are α stages. -Linolenic acid (ALA) and stearidonic acid (SDA) of special importance in chemotaxonomic inside this family. are the main compounds in germination stage which then Tocopherols are also natural effective antioxidants and δ decreased later. In the beginning of seed formation stage borage species have high amount of -tocopherols[44,45]. LA is in highest level and the amounts of GLA and acid oleic Phenolic compounds exist in oil seeds and various increase. studies have proved their antioxidant properties. Borage is The leaves of borage contains following compounds: a few important due to high amount of GLA available in its seed amount of pyrrolizidine alkaloids, licosamin, intermedin, oil. In a comprehensive research, antioxidants properties sopinin, sopindian, yezan, colin; fatty acids including ALA of borage extracts have been reported[46,47]. These excellent (55%) and GLA (more than 4%); silicic acid (1.5%-22.0%); antioxidants properties of borage are attributed to phenolic potassium, calcium, nitrate potassium (3%), acetic, lactic compounds. It has been determined that rosmarinic δ and malic acid; -bornesitol, cianozhens; fresh leaves acid, synergic acid and synaptic acid are main phenolic also contain mucilage hydrolysable to glucose, galactose, compounds available in extract of borage seed. Rosmarinic arabinose and alantoein up to 30%; leaves of borage in acid is the main component of extract which is seeding stage contain 2.5-5.0 mg GLA and 5.7-9.0 mg used extensively in food industries. On the other hand SDA[34,35]. The most amount of the gama-linolenic fatty acids synergic acid and synaptic acid are included in phenol and are seen in May or June and the most amount of that in main antioxidants of rapeseed and canola[39,48,49]. upper leaves of the stem in August or September[36]. There is potential for borage antioxidants to be used in The amount of gum and mucilage available in leave and food formulations and in skin health products as compounds stem is 3.8% and in is 5.4%. The amounts which absorb UV. It has been suggested that linoleic acid of potassium and calcium are reported 5.3% and 6.2% and palmitic acid are dominant fatty acids available in respectively[11,37,38]. Compared to inflorescence, less amounts mature seeds of borage[42]. Borage oil due to high amount of potassium, gum and mucilage are present in stem and of GLA is investigated by food and pharmaceutical research leave but more calcium is in stem and leave. Inflorescence groups[50]. Oils containing GLA is used to treat some diseases of borage contains mucilage, tannin, calcium, potassium resulted from lack of GLA in human[51]. and ash insoluble in acid and alkaloid but has not saponins, 2.5. Pharmaceutical applications flavonoids and cyanogenic glycosides[1,19,20,38]. The flowers of borage and generally all parts of the plant contain 30% mucilage. Green parts of the plant contain nitrate potassium, Raw obtained from borage is used as anticonvulsant, resin, malate and a little amount of essence, manganese, bronchodilator, vasodilator. It also has cardio-depression phosphoric acid and allantoin[39-41]. property. SDA is a precursor for synthesis which is Today GLA and SDA supplements and oils containing these found a little in oil of the borage seed while SDA is second fatty acids are used in diet to meet the shortage of necessary frequent fatty acid in leaves of borage[11,42]. Since animals fatty acids and prostaglandin. They also are used in treating have very low ability to synthesize this kind of necessary , and cancer[51,52]. fatty acids, they must be included in daily diet. This vital Atopic is an inherited and regressive disease compounds bearing therapeutic value could increase which is seen in 5%-10% of children and now local animals health and quality of life[4]. Linolenic acid and corticosteroid is oftern used to remove inflammatory and palmetic acid are collected from flowers and high levels of itchy rashes seen in patients. Results of recent researches ALA is in mature leaves[42]. have shown that patients affected by this disease due to lack Majid Asadi-Samani et al./Asian Pac J Trop Med 2014; 7(Suppl 1): S22-S28 S25 necessary fatty acids. Borage is one of the rich resources and their medicinal use is approved. Generally GLA is used of these acids and seems to be beneficial to these patients. as food supplement and drug prescript to treat diseases like Borage also has effect on the treatment of obsessive- local eczema, heart diseases, cyclical mastalgia, diabetes, [58,59] compulsive disorder. It has been determined that the arthritis and multiple sclerosis . High validity of extract of this plant is effective on stress models in mouse. borage and its increasing demand is related to increase in Studies have shown that patients affected to psoriasis due documents about fatty acids quality and also their amount in human diet regarding health and effect of improving to lack free fatty acids and if this lack is removed symptoms atherosclerosis. Polyunsaturated fatty acids are not will be decreased and even recovered. Borage plant is one synthesized by human body and must be supplied by special GLA of the rich resources of which effect on recovery of diets. They are the most important precursor for active inflammatory chronic diseases is approved. Borage seed Psoriasis vulgaris physiological compounds like prostaglandin, thromboxanes oil has been affective on recovery of and leucotrienes[60]. Human body skin cannot biosynthesize [53-55] rashes . GLA from linolenic acid or arachidonic acid precursor. So Researches about borage seed oil analysis show that daily consumption of borage seed oil which is rich in GLA existence of alkaloids induced side effects is possible. significantly improves skin condition. After using this oil Borage seed oil is also used for chronic skin inflammatory skin dryness and itch are decreased[61]. disease in order to prevent manifestation of these effects. Skin itch and stimulation problems are also ameliorated 2.7. Antioxidant effects [49,56] S B by this plant extract . everal plants in oraginaceaeEchium B I ( family,amoenum specially orage and its ranian variety Fat oxidation is one of the main reasons of decrease in ), have been used in Iranian traditional medicine the quality of fatty foods. This process affect on color, favor, as tranquillizer from ancient times. Phytochemical studies tissue and nutritional value of foods[62]. Free radicals such as have shown presence of flavonoids in this plant and they superoxide, hydroxyl, hydroperoxyl and nitric oxide radicals [63] can produce benzodiazepine like effects by attachingEchium to can cause fat oxidation . Using synthetic antioxidants M benzodiazepineamoenum receptors. ethanol extract of in foods could delay oxidation but using them in food has also shown anticonvulsant effects in products is subject to limitation regarding rules since these mouse. The main effective substances in this plant are compounds have anti-health potential. This subject causes pyrrolizidine alkaloids, flavonoides, rosmarinic acid, us to prefer natural antioxidants instead of them. Medicinal anthocyanins, saponins, unsaturated terpenoides and sterol. plants with natural antioxidants have been shown to be Likely anticonvulsant effects of this plant are performed beneficial in a variety of complications such as cancer[64- by flavonoids, rosmarinic acid and some of the above 66], burn[67,68], diabetes[69-71], hyperlipidemia[72-74], and [57] substances . Of course proof of this subject requires amnesia[75,76], These compounds are able to prevent or cure special researches on these substances. the side effects of other compounds[71,77-80]. Borage plant causes increase in urine excretion, decrease Many natural antioxidants already have been extracted [38,56] in blood pressure and kidney function benefits . from different kinds of plant materials such as oilseeds, [81] 2.6. Effects related to GLA vegetables, leaves, roots, , cereal and plants leaves . Among natural antioxidants, phenolic antioxidants are extensively available in plants[66,82-84]. Borage oil is rich in GLA is one of the compounds available in borage and unsaturated fatty acids like GLA which is high resistance some other plants seed oil which is extensively used in food to oxidation. This resistance is resulted from existence supplements and to treat different diseases. Unsaturated of tocopherols and several phenol compounds in tissues fatty acids are very important in animals cells since they containing oil. When oil is extracted antioxidants such as are affected in maintaining structure and function of cell tocopherols are extracted with oil which are main factors in membrane, adjusting synthesis and transfer of cholesterol protecting the oil. Borage flour contains large amounts of and in avoiding water loss from skin and precursor of phenol compounds after extracting oil. These antioxidants eicosanoids like and leucotrienes. In animals can be concentrated as raw extracts or be used as phenol these fatty acids are synthesized from necessary fatty acid compounds in unsaturated oils like seed oils[46,47]. Borage linolenic acidΔ and first stage of this process is desaturation flour and its extracts have concentration-related antioxidant - [43] of GLA by Desaturase . Synchronous decrease in activity properties. Products containing high amount of antioxidant of this enzyme and advancement of age, stress, eczema, can be obtained from borage flour under optimum condition. diabetes, and some infections or increase in GLA catabolism Maximum antioxidant activity of extract is° resulted if simultaneously due to oxidation or fast cell division leads to extraction is performed with 52% ethanol in 74 C for 60 min. GLA lack. Clinical experiments have shown that consumption The ability of this extract to delay fat oxidation is attributed of food supplements containing GLA could be useful in the to the phenol compounds to eliminate reactive species treatment of some diseases such as local eczema, mastalgia, of oxygen. Borage extract may be added to oils and meat diabetes, virus infections and some kind of cancers. Oils products instead of antioxidants to delay fats oxidation. But, containing GLA are used vastly as health public supplement low amount of the hydrophobic phenols may lead to weak Majid Asadi-Samani et al./Asian Pac J Trop Med 2014; 7(Suppl 1): S22-S28 S26 [2] A l-Khamees WA, Schwartz MD, Alrashdi S, Algren AD, Morgan antioxidant in oil emulsion systems in water. J Transition metal ions like iron, magnesium, manganese BW. Status epilepticus associated with borage oil ingestion. Med Toxicol 7 are also found frequently in living beings and foods with 2011; : 154-157. plant and animal origin. These metals interfere directly [3] G hahreman A. Flora of Iran. Tehran: Research Institute of Forests or indirectly in the beginning of fat oxidation. It has and Rangelands; 1978. Persian. [4] P eiretti PG, Palmegiano GB, Salamano G. Quality and fatty acid been determined that chelated form of metal ions to fat Borago officinalis peroxidation is less available. Since raw extract of borage content of borage ( L.) during the growth cycle. Ital J Food Sci 16 and its components have chelating property of metals in 2004; : 177-184. watery experimental environment, this extract could be [5] Y ang W, Sokhansanj S, Tang J, Winter P. Determination of considered as a good chelating factor for food and other thermal conductivity, specific heat and thermal diffusivity of Biosyst Eng 82 products[49,85-87]. borage seeds. 2002; : 169-176. Regarding ability of borage extract to scavenge reactive [6] S ayanova O, Smith MA, Lapinskas P, Stobart AK, Dobson G, DPPH Christie WW, et al. Expression of a borage desaturase cDNA oxygen species and radical, it could be used as relative b drug to treat diseases related to free radicals which might containing an N-terminal cytochrome 5 domain results in the Δ6 hurt tissues[88]. Borage meal imposes an antioxidant activity accumulation of high levels of -desaturated fatty acids in Proc Natl Acad Sci 94 which is dependent on concentration in meat model system. transgenic tobacco. 1997; : 4211-4216. A [7] S ayanova O, Shewry PR, Napier JA. Characterization and ntioxidant compounds are concentrated in a meal in the Borago officinalis J best condition of extraction which is predicted by response expression of a fatty acid desaturase from . ° Exp Bot 50 surface methodology that is 52% ethanol at 74 C for 60 1999; : 411-412. min[85]. [8] D e Spirt S, Stahl W, Tronnier H, Sies H, Bejot M, Maurette JM, et al. Intervention with flaxseed and borage oil supplements Br J Nutr 101 modulates skin condition in women. 2009; : 440-445. 3. Conclusion [9] S impson MJ. Comparison of swathing and desiccation of borage Borago officinalis ( ) and estimation of optimum harvest date stage. Ann Appl Biol 123 Borage is cultivated for medicinal and culinary uses, 1993; : 105-108. even though it is commercially cultivated for borage seed [10] B elch JJ, Hill A. Evening primrose oil and borage oil in Am J Clin Nutr 71 oil. Borage seed oil is rich in GLA which is used as dietary rheumatologic conditions. 2000; (1 Suppl): 352s- O 6s. or food supplement. ther than seed oil it contains lots of í ‐ ‐ ó [11] D el-R o Celestino M, Font R, de Haro Bail n A. Distribution of fatty acids such as linoleic acid, oleic acid, palmitic acid, Borago stearic acid, eicosenoic acid and erucic acid. It is used for fatty acids in edible organs and seed fractions of borage officinalis J Sci Food Agric 88 the treatment of various diseases such as multiple sclerosis, L. 2008; : 248-255. diabetes, heart diseases, arthritis and eczema. 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