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Journal of Medicinal

A Taxonomical, Morphological and Pharmacological Review of vulgare L., An Old Medicinal in Iran

Ahvazi M (Ph.D. Student)1, Balali GR (Ph.D.)1*, Jamzad Z (Ph.D.)2, Saeidi H (Ph.D.)1

1- Department of Biology, University of Isfahan, Isfahan, Iran 2- Research Institute of Forest and Rangelands, Tehran, Iran * Corresponding author: Department of Biology, University of Isfahan, Post code: 81746-73441 Tel: +98-313-7932493, Fax: +98-313-7932456 E-mail: [email protected]

Received: 28 Dec. 2016 Accepted: 15 May 2017

Abstract

Marrubium vulgare L. (common name: Horehound, hoarhound) is one of the medicinal plants which has been used in the treatment of stomach, arrhythmia, asthma, jaundice, lung diseases and liver disorders in Iranian . Other properties are expectorant, antispasmodic, tonic, anti-infective agent and externally, it has been used in ulcers and wounds. in M. vulgare generally appear in early spring and regularly visited by readily nectar gathering bees. The plant is a good candidate for phytoremediation of Hg contaminated soils. Previous phytochemical studies showed the presence of alkaloids, lactones, steroids, flavonoids, tannins, phenylpropanoid esters, and diterpenoids in M. vulgare. In this review we focused on the several aspects of , morphology, chemical composition and traditional medicine of horehound.

Keywords: Ethnobotany, , Medicinal plant, Phytochemistry, Taxonomy

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Introduction Taxonomy The Martinov (=Labiatae Plant name

Adans., the mint family) has a word-wide Horehound, hoarhound is the most well- distribution with more than 7200 species known English common name for this across approximately 240 genera [1]. The and common white horehound is English name genus Marrubium (Lamiaceae) is comprised of for M. vulgare in all of the distribution areas in about 49 accepted species. the world and is a name of Some of the species within Marrubium M. ballotoides Boiss. & Bal. [6, 7, 8, 9, 10]. It such as M. vulgare are used as medicinal plant is known with other regional names in traditionally [2]. M. vulgare L. (horehound) different parts of the world such as: has been known as a native species for , Persian= Faracion, Ghandnaye kohi, Shenar, and north of [2, 3]. Horehound Oftan-Sar, Korar [7, 9, 10, 11]. has been used as an expectorant cough remedy Grecian= Faracin, Berson [11]. since ancient Egyptian times. Its name comes Romanic= Madroptim [11]. from the word hoary, due to the white hairs Indian= Faracim, Shafar, shevir [10]. that cover horehound leaves, and hound, Arabic= Hashish el Kalb, Algama, Sogafol- because it was used in ancient Greek medicine Arz, Sharir [9, 10, 11, 12]. to treat bites from rabid dogs. Horehound is French: Marrube blanc [13]. used in Indian Ayurvedic medicine to treat Germany: Mauerandron, Weisse andorn, acute or chronic bronchitis and whooping Andorn [13]. cough. In Germany, horehound is used to treat dyspeptic complaints such as feeling of Botany repletion, flatulence and loss of appetite. It is The genus Marrubium L. belongs to also used for catarrh of the respiratory tract as subfamily. In data a component of some antitussive and base (http://www.theplantlist.org) there are expectorant drugs. It is a common expectorant 120 scientific plant names of species rank for component of European made cough the genus Marrubium, of these 49 are accepted remedies [4]. In a survey, an aqueous extract species names. The genus is distributed in of M. vulgare showed anti-diabetic activity temperate regions of Europe, North Africa and and effects on body weight properties [5]. The Asia to western China with a few species major chemical components of M.vulgare are naturalized in North and [14]. β- Cariophyllene (11 to 32%), Germacerene-D Many species of the Lamiaceae family are (9 to 20%), β-Bisabolene (25%), (E)-β- considered of high importance because of their Farnesene (8 to 11%), Carvacrol (14%), uses in medicine, culinary, and cosmetics [15]. β-Citronellol (8-9%), E-Caryophyllene (25%), Marrubium is present in Iran with 11 species -Amorphene (10%), -Eudesmol (11%). from which only one is endemic (M. procerum

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Bunge) [16, 17]. Most Marrubium species are medially notched, laterally reflexed, lower lip distributed in steppes, arid and semiarid areas spreading, 3-lobed with middle lobe larger. of Iran. M. vulgare L. is a perennial subshrub, Flowers are arranged perfect. Style included in C3, , reproduces by seeds and corolla tube. Stamens are arranged in 4, 2n = 34 [3, 18]. didynamous, lower pair usually larger; anther sacs divergent; included in corolla tube. Seeds Morphology are 4-parted, seed-like nutlets; each nutlet 1- Herbaceous, erect and ascending, perennial seeded, ovoid to oblong, 1-2 mm long, subshrub with stem bases becoming somewhat 3-angled, obtuse or truncate at apex, sublignescent; stems usually branched to form somewhat reticulate-roughened, brown to a rounded bushy plant; up to 100 cm tall, 20- black [3]. 100 cm wide. A tough, woody, branched taproot or having numerous fibrous lateral Trichomes roots. Stems have 20-100 cm tall, are Trichomes are one of the most important quadrangular except in old sublignescent characters for identification of the genera and growth. Leaves arranged opposite along stem, species in taxonomic studies in Lamiaceae [19, decussate. Leaf blades broadly ovate, oval, 20, 21, 22, 23, 24]. Trichomes show a range of suborbicular, or subreniform; 1-4 cm or up to variation within the family. Simple glandular 6 cm long, 1-5 cm wide, acute to rounded or and non- glandular as well as peltate are the truncate at apex, acute to cordate at base, most common types of trichomes, but stellate strongly corrugate and rugose, margins crenate and branched hairs are also characteristic of to dentate, pubescent above, gray-green above, some genera. Stellate and branched hairs are cinereous-lanate beneath, veins prominent on rather common in subfamily Lamioideae and lower surface; lower leaves on pedicels have been observed in many genera i. e. equaling blade or shorter, upper leaves Marrubium, , , , subsessile. Inflorescence in axils of upper Eremostachys and . In Lamiaceae leaves; flowers sessile and crowded in dense some genera are characterized by stellate whorls, these axillary subglobose multi- trichomes, i. e. in Marrubium & Lavandula. flowered verticals forming interrupted spikes Most of the long branches in stellate hairs are along stem; often subtended by leaves. Calyx four celled in upper surface in populations of is tubular, 3-6 mm long at anthesis, larger in M. vulgare that with altitude increase the fruit, 5-10 veined; short soft-hairy, 10-toothed, number of short branches are increased too each tooth with a small hooked spine/bristle, (from 7 to 14). The effect of the ecological recurved at maturity, alternately long and conditions i.e. arid areas and altitude are short; calyx spreading at maturity. Corolla is important factors for morphological variations white to pale lavender, tubular, bilabiate, and density of trichomes [14]. small, 5-10 mm long, tube about 2-4 mm longer than calyx; 2-lipped, upper lip erect,

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Anatomical characters adaxially and 1-2 layers of short cells on M. vulgare epidermis consists of one layer abaxial surface. Vascular bundles are collateral of large cells. Type of stomata is anomocytic and surrounded by parenchymatous bundle on adaxial surface. Isobilateral mesophyll sheaths [27]. includes 4-5 layers of long palisade cells

      

Figure 1- M. vulgare transversal section of leaf (details of mesophyll)

 Figure 2- white horehound [https://ast.wikipedia.org/wiki/Marrubium vulgare]   

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Ecology with dormancy differing across continents, and Origin even between populations. After collection of The genus Marrubium (Lamiaceae) is the mature M. vulgare seeds in October, comprised of about forty species. M. vulgare is germination rate was less than 35% at trial native to Asia (Afghanistan, Armenia, temperatures between 10-30°C, with the Azerbaijan, China (Xinjiang), Cyprus, Iran, majority of germination occurring between Kazakhstan, Lebanon, Russian Federation 1826°C. Following 1 month of storage under 3 (Ciscaucasia), Syria, Turkey, Turkmenistan, sets of conditions (26°C-dry, 0°C-dry, 0°C- Uzbekistan into Pakistan), Europe (Albania, moist), 78% germination occurred for the Austria, Belarus, Belgium, Bulgaria, seeds which have been kept at 32°F-moist Czechoslovakia, Denmark, Estonia, England, (0°C). It took 3 months of dry storage at 26°C France including Corsica, Greece including Crete, for 80% germination to occur. Seeds stored Hungary, Italy including Sardinia and Sicily, under 0°C needed 4 months of storage to reach Latvia, Lithuania, Netherlands, Poland, Portugal, 80% germination. Some studies have shown Romania, Russian Federation (southwest that germination rates of un-stratified seeds European areas), Spain including Baleares, south were highest when temperatures fluctuated at Sweden, Switzerland, Ukraine including Krym, least 15°C diurnally when tested at intervals Yugoslavia), and northern Africa (north Algeria, over a year. Optimum temperature regimes of north Libya, Morocco, Azores, Madeira Islands, un-stratified seeds were 15/40°C and 20/40°C. Canary Islands, Tunisia). This plant is being used It was also found that the seeds of M. vulgare since ancient as a medicinal plant [2, 3]. are poor germinators at very cold temperatures

Hg absorption from environment in seedbeds. Cold and moist stratification for Mercury (Hg) is an environmental pollutant 4-8 weeks enhanced the germination rate over which is mainly supplied via anthropogenic a wide range of temperatures, with lower sources to the soil. It is harmful because of its germination rates if stratification period was toxicity, mobility, bioaccumulation, shorter or longer as several responses to methylation process and transport in the temperature regimes were observed between atmosphere [26]. Recent studies have shown populations from differing locations. Crops that M. vulgare can absorb high Hg from soil. grow appropriately in well-drained, neutral to Moreno-Jimenez et al. have shown the plant alkaline soil in sun. M. vulgare generally has a high resistance to Hg and is able to flowers early in the spring, readily foraged by extract around 10–30 g Hg ha_1 year_1 in aerial bees for the nectar. It has been reported that parts, so can be a good candidate for Hg this plant also has the potential of self- phytoremediation of contaminated soils [27]. fertilization, although there is a lack of adequate researches to identify the seeding Cultivation potential by self-pollination. Plants are cut Seeds from a specific location seem to have when are in flowering stage and used fresh or location-dependent germination requirements, dried [3, 28].

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Phytochemical components illustrates the main components (percentage up M. vulgare and other species in Iran to 1%) of various species of Marrubium. Prior to the introduction of chemical medicines, man relied on the healing properties of medicinal plants [29]. The knowledge of herbal remedies in traditional cultures has contributed significantly to the development of the use of drugs derived from plants, considering their widespread use, with 80% of the world’s population relying on such medicines for their health care [2]. The Figure 3-Conversion of pre-marrubiina to Phenolic acids, caffeic acid, and rosmarinic marrubiina [35] acid, are common constituents of the family Lamiaceae. Forty percent of the species of There are several studies about the species Lamiaceae family are thought to contain components and their percentages that are compounds that possess aromatic properties. related to several factors such as collection Caffeic acid plays a central role in the time, drying conditions, altitude, soil, climatic biochemistry of this family. Previous and geographic factors. The chemical phytochemical studies have also showed the compositions of M. vulgare essential oil from presence of alkaloids, lactones, steroids, various origins have been the subject of many flavonoids, tannins, phenylpropanoid esters, studies. For example the major constituents of vitamin C and diterpenoids in M. vulgare [2, M. vulgare essential oil grown in Egypt from 30, 31, 32, 33]. Marrubium is an important the aerial parts were carvacrol, β- phellandrene medicinal plant in Iranian medicine with 10 and carvyl acetate with 36.28, 15.49, 11.52 species. The genus is known to produce many percentage respectively [50]. While the major diterpenoids such as marrubiina (Figure 3), composition of the essential oil obtained from identified in 1842, which was the first the dried flowering aerial parts of M. vulgare diterpenoid and major compound to be isolated from Iran were β-bisabolene (20.4%), δ- and characterized from M. vulgare leaves. cadinene (19.1%) and isocaryophyllene Marrubiin exists in high concentrations in (14.1%). In Tunisia, the main constituents of many traditionally important Lamiaceae M. vulgare essential oil were y-Eudesmol species and has demonstrated excellent (11.93%), β-Citronellol (9.90%), Citronellyl pharmacological properties with high safety formate (9.50%) and Germacrene-D (9.37%) margins in different inflammation models [2, [46]. From Poland E-Caryophyllene, 30, 34]. Moreover, some studies demonstrated Germacrene D, Carvacrol and δ-Amorphene the considerable antioxidant activity of were the main components of M. vulgare M. vulgare is associated with the presence of essential oil [42]. Germacrene D and marrubiin along with phenolics and flavonoids Caryophyllene oxide are two dominant exerting a synergistic effect [34]. Table 1 components of the oils obtained from other

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16 Journal of Medicinal Plants, Volume 17, No. 65, Winter 2018 Ahvazi & et al. plant species of the genus Marrubium. and total cholesterol levels in treated animals Comparison of different studies confirms that [51]. Ghlissi et al. mentioned that hypoglycemic the differences in the volatile composition of effect and the improvement of hepatorenal the plants could be attributed to genetic damage by M. vulgare infusion on alloxan- (genus, species, and ecotype), chemotype, diabetic rats may in part be due to its antioxidant distinct environmental and climatic conditions, activity [54]. Some references have mentioned seasonal sampling periods, geographic origins, that M. vulgare is also used for the treatment of plant populations, vegetative plant phases, soil, type 2 diabetes, hypercholesterolaemia and climate, extraction and quantification methods hypertension [54, 55]. [43].  Anti-bacterial activity Biological activity of M. vulgare It was shown that the ethanol extract and Marrubiin, a furane labdane diterpene, is the essential oil of M. vulgare had inhibitory the main analgesic compound present in effect against most Staphylococcus aureus M. vulgare. It was mentioned that Marrubiinic isolates plates. The least MIC value of the acid is a derivative component of Marribin, extract M. vulgare was 2.5 mg/mL and the which exhibited significant analgesic effect highest MIC value of the essential oil M. against the writhing test in mice. In addition, vulgare was 2.5 mg/mL [47]. Whereas, the Marrubiinic acid showed better activity and essential oil of M. vulgare was effective on excellent yield, and its analgesic effect was antibiotic resistance Klebsiella pneumoniae confirmed in other experimental models of strains [58]. Another study showed that the pain in mice. The results showed that essential oil of M. vulgare inhibited the growth Marrubiinic acid could be used as a model to of Gram (+) and Gram (-) bacteria (Listeria obtain new and more potent analgesic drugs monocytogene, Pseudomonas aeruginosa, [51]. Many researchers have indicated the Agrobacterium tumefaciens and Salmonella multifaceted therapeutic activities of enterica), along with IC50 and MIC values M. vulgare, which some of them are given ranging from 0.1-15 μl/ml, respectively [57]. It below. was reported that the total phenolic and flavonoid contents of this plant have an Anti-diabetic activity antibacterial efficacy on Candida albicans In a study, an aqueous extract of M. vulgare (yeast) [58]. In Morocco, the leaves and showed anti-diabetic activity and effects on flowering tops of M. vulgare are used for body weight properties [52]. In another study, diabetes treatment [55]. an infusion of M. vulgare exhibited a decline in blood glucose levels by 50% and more than Anti-oxidant activity 60% concentrations of 100 mg/kg, 200 and Medicinal plants are a source of a wide 300 mg/kg respectively, as well as a variety of natural antioxidants. A significant significant lowering of total lipids, triglycerides radical scavenging effect of M. vulgare was

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A Taxonomical, … reported by Fadel et al. [49]. In a study about traditional uses such as expectorant, the antioxidant potential of some Morocco antispasmodic properties, antiasthmatic, anti- medicinal plants the finding showed that infective agent and externally, it has been used phenolics in M. vulgare provided a substantial to treat ulcers and wounds [31]. The plant is antioxidant activity [55]. reported to possess hypoglycemic, antihypertensive, analgesic, anti-inflammatory, Gastroprotective activity antioxidant, and antibacterial activities [30]. S. It was reported that the extract of Dall’Acqua et al. has mentioned some of the M. vulgare and marrubiin displays antiulcer traditional usage of the leaves of the plant such activity and this effect can be partly attributed as Maltese fever, malarial fever, asthma, to the isolated diterpene [59]. diaphoretic, dental abscesses, expectorant, emmenagogue, cirrhosis, hepatopathy, Respiratory tract infection sedative, stomachic and dysmenorrhea, Horehound has been used as an expectorant antipyretic and stomach disorders [62]. In a cough remedy since ancient Egyptian times recent study about the antioxidant capacity and [60]. Several usage of M. vulgare such as phenolic contents of some of the respiratory catarrh, acute and chronic Mediterranean medicinal plants some of the bronchitis, whooping cough has been reported traditional uses of M. vulgare such as by Spiteri M. [54]. The leaves and flowering treatment of gastroenterical and respiratory tops of M. vulgare are also used for bronchitis diseases, antinociceptive, anti-inflammatory, treatment in Morocco [55]. hypoglycemic and insecticidal effects were mentioned. Tonic, aromatic, expectorant, Traditional medicine (Ethnobotany) diaphoretic and diuretic activities have also Years ago, humans have relied on nature been stated [63]. M. vulgare is used in folk for their basic needs for the production of food medicine in Europe, Pakistan, Brazil, and stuff, shelters, clothing, means of Tunisia to treat respiratory infections, transportation, fertilizers, flavors, and including bronchitis, coughs and asthma [30]. fragrances, and not the least, medicines. Indigenous people have been using the unique M. vulgare in Iranian Traditional approach of their traditional system of Medicine medicine for centuries [61]. Medicinal plants The crude extract of M. vulgare is widely are the “backbone” of traditional medicine, used as antihypertensive in traditional which means more than 3.3 billion people in medicine [50]. M. vulgare (Horehound, the less developed countries utilize medicinal hoarhound) is one of the medicinal plants plants on a regular basis. There are nearly which is used in the treatment of stomach 2000 ethnic groups in the world, and almost tonic, arrhythmia, asthma, jaundice, every group has its own traditional medical pulmonary diseases and liver disorders in knowledge and experiences [29]. M. vulgare Iranian traditional medicine [10, 64, 65]. In as the most representative species has several Alamut region of Ghazvin province in Iran the

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plant are used traditionally for asthma, catarrh, hepatoprotective properties [71], cough, typhoid fever by the indigenous people antispasmodic [74], poor digestion, loss of [66]. appetite, bloating and flatulence, treatment of diarrhoea, jaundice and painful menstruation. Other effects and Medicinal uses Additionally, externally is used for treatment The medicinal properties of M. vulgare of ulcers, skin damage, mouth and throat have been reported by many studies as follow: infections [54]. inflammatory and anti-oedematogenic effect [67], pulmonary affections and expectorant Conclusion [68], source of natural antioxidants and Since metabolic diseases count as the main increase of the anti-atherogenic potential of dilemma in societies, so paying attention to the HDL (high-density lipoprotein) [69], cytotoxic traditional medicine and medicinal plants for activity [70], hepatoprotective activity [71], their treatment seems necessary. This study reducing the elevated blood glucose level and gives support to the traditional use of M. lipid profile of streptozotocin (STZ)-induced- vulgare as a multipurpose herbal medicine and diabetic rats [72], anti-tyrosinase effects [73], may justify its use in folk medicine.

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22 Journal of Medicinal Plants, Volume 17, No. 65, Winter 2018 Ahvazi & et al. and marrubiin obtained from leaves of 67. Stulzer H.K, Tagliari M.P, Zampirolo J.A, Marrubium vulgare L. (Lamiaceae). J.P.P. Cechinel-Filho V and Schlemper V. 2011; 63: 1230 - 1237. Antioedematogenic effect of marrubiin 60. Blumenthal M, Goldberg A, Brinckmann J. obtained from Marrubium vulgare. Journal of Herbal Medicine: Expanded Commission E Ethnopharmacol. 2006; 108: 379 - 384. Monographs. American Botanical Council. 68. Molina-Salinas G.M, Ramos-Guerra M.C, 2000; Newton, 233 - 236. Vargas-Villarreal J, Mata-Ca´rdenas B.D, 61. Karunamoorthi K, Jegajeevanram K, Becerril-Montes P and Said-Fernandeza S. Vijayalakshmi J and Mengistie E. Traditional Bactericidal Activity of Organic Extracts from Medicinal Plants: A Source of Flourensia cernua DC against Strains of Phytotherapeutic Modality in Resource- Mycobacterium tuberculosis. Archives of Constrained Health Care Settings. Journal of Medical Res. 2006; 37: 45 - 49. Evidence-Based Complementary & Alternative 69. Berrougui H, Isabelle M, Cherki M and Khalil Medicine 2013, 18 (1): 67-74. A. Marrubium vulgare extract inhibits human- 62. Acqua S.D, Cervellati R, Loi M.C and LDL oxidation and enhances HDL-mediated Innocenti G. Evaluation of in vitro antioxidant cholesterol efflux in THP-1 macrophage. Life properties of some traditional Sardinian Sciences 2006; 80: 105 - 112. medicinal plants: Investigation of the high 70. Nawal H.M and Atta E.M. Cytotoxic and antioxidant capacity of Rubus ulmifolius. Food Antioxidant Activity of Marrubium vulgare Chem. 2008; 106: 745 - 749. and its Flavonoid Constituents. 2nd 63. Amessis-Ouchemoukh N, Madani K, L.V. International Conference on Chemical, Fale P, Serralheiro M.L and Eduarda M. Environmental and Biological Sciences Araujo M. Antioxidant capacity and phenolic (ICCEBS 2013). 2013, 17-18, Dubai (UAE). contents of some Mediterranean medicinal 71. Akther N, Shawl A.S, Sultana S, Chandan plants and their potential role in the inhibition B.K and Akhter M. Hepatoprotective activity of cyclooxygenase-1 and acetylcholinesterase of Marrubium vulgare against paracetamol activities. Industrial Crops and Products 2014; induced toxicity. Journal of Pharmacy Res. 53: 6 - 15. 2013; 7: 565 - 570. 64. Bahmanyar A and Mahbobi Ardekani H. 72. Azzi R, Lahfa F and Djaziri R. Movafgh-Aldin. Abomansor Ali Alheravi. Phytochemical, antihyperglycemic and Tehran University Press (1ed). Iran. 1967, P: antihyperlipidemic study of crude 244. hydroalcoholic extract of aerial parts of 65. Momen Tonekaboni S.M. Tohfat-Alhakim. Marrubium vulgare L. in normal and Nashre Shahre Tehran. Iran. 2007, P: 321. strptozotocin induced-diabetic wistra rats. 66. Ahvazi M, Mozaffarian V, Nejadsatari T, IJPSR 2014; 5 (5): 2006 - 2013. Mojab F, Charkhchiyan M.M, Khalighi- 73. Namjoyan F, Jahangiri A, Azemi M.E, Sigaroodi F and Ajani Y. Medicinal Arkian E and Mousavi H. Inhibitory Effects of Application of Native Plants (Lamiaceae and Physalis alkekengi L., Alcea rosea L., Bunium Rosaceae Family) in Alamut Region in Gazvin persicum B. Fedtsch. and Marrubium vulgare Province. J. Med. Plants 2007; 6 (24): 74 - 84. L. on Mushroom Tyrosinase. Jundishapur J.

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