Amazonian Journal of Research ©2017 Universidade Federal do Pará This paper is available online free of all access charges – Faculdade de Engenharia Agronômica https://www.ajpr.online - Amaz. Jour. of Plant Resear. 4(2):517-523. 2020

ulture Mini Review

Hortic (Rhus coriaria L.) a spice and medicinal plant - a mini review

Mehdi Khoshkharam1, Mohamad Hesam Shahrajabian 1,2,3, Wenli Sun2,3 and Qi Cheng1,2

1 Department of Agronomy and Plant Breeding, Isfahan (Khorasgan) Branch, Islamic Azad University, Isfahan, Iran 2 Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China 3 Nitrogen Fixation Laboratory, Qi Institute, Building C4, No. 555, Chuangye Road, Jiaxing 314000, Zhejiang, China

Received: 02 April, 2020. Accepted: 04 May, 2020 First published on the web May, 2020 Doi: 10.26545/ajpr.2020.b00061x

Abstract Sumac is a famous spice in the Middle East, which is made from berries from a bush of the same name. In order to produce the spice from the plant, its is dried and crushed into a thin red-purple powder. The red berries are tangy and delicious, containing malic acid which is found in apples. As a spice, it is delicious on meat, in salad dressings, and makes a delicious infused vinegar if you macerate it in apple cider vinegar. The most important phenolic acids and flavonoids are catechin, ferulic acid, gallic acid, apigenin, gentisic acid, chlorogenic acid, P-coumaric acid, caffeic acid, isorhamnetin, quercetin, cinnamic acid, taxifolin, epicatechin, kaempferol, P-hydroxybenzoic acid, vanillic acid, vanillin, anisic acid, pyrogallol, sinapic acid, syringaldehyde, syringic acid and benzoic acid. Organic acids of Sumac are malic acid, citric acid, tartaric acid and fumaric acid. The fatty acid composition of sumac are myristic acid, palmitic acid, palmitoleic acid, stearic acid, oleic acid, linoleic acid and linolenic acid. The vitamin content of sumac fruits are thiamin, riboflavin, pyridoxine, cyanocobalamin, nicotinamide, biotin, and ascorbic acid. The most important health benefits of sumac are 1) anti-cancer: a super anti-oxidant, and packed with vitamin C which means it can help ward off diseases like diabetes, cardiovascular diseases and cancer, 2) anti-inflammatory: inflammation is thought to be the cause of most diseases and Sumac is an anti-inflammatory spice that helps fight various disorders, colds and the Flu, 3) it has been studies to be effective in regulating cholesterol levels and treating diabetes by reducing blood sugar, 4) anti-fungal and anti-microbial: Sumac is anti-microbial and anti-fungal spice which can help treat skin inflammation and disorders, it has also been studied to be effective in fighting bacteria like Salmonella and can be used to safely disinfect fruits and vegetables, 5) it can increase breast milk production and ease menstrual cramps, 6) Sumac is a diuretic which means it helps remove toxins from the body through urine and has been used traditionally to treat urine infections and digestive problems.

Key-words: Sumac, Functional Food, Herbal Remedy, Traditional Medicine

Introduction areas of the Middle East as a very popular flavoring spice. Sumac comes from a native to the Spice and herbal remedies have been used since Mediterranean, and its history dates to ancient times ancient times to treat a variety of disorders (Zargari, 1992). The Romans used sumac berries as a (Shahrajabian et al., 2019a,b,c,d,e; Sun et al., souring agent and flavoring before citrus fruits 2019a,b; Shahrajabian et al., 2020a,b). The word reached the region. Sumac still grows wild around the "sumac" is used to refer to the product of Mediterranean; major sources today include Turkey (Rhuscoriaria L.) spice recognized in Iran and other and the Middle East. There are many varieties of the Mehdi Khoshkharam and Mohamad Hesam Shahrajabian E-mail: [email protected], [email protected] 517

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shrub, and some of them are poisonous. However, serves as a traditional medicine, which has Native Americans traditionally used sumac to make a pharmacological blood purifier, diuretic, stomachic refreshing drink, and they also used both and and tonic. Citric acid is a hydroxy acid and is used in berries in tobacco mixtures (Matloobi and the beverage, juice, cosmetics and pharmaceutical Tahmasebi, 2019). Sumac is widely used in cooking industries and flavoring, it also uses to regulate pH. in Turkey and the Middle East, especially in Lebanon, Iran, and Iraq (Moerman, 1998; Mohammadi et al., Sumac as a medicinal plant 2010). The dried whole berries must be soaked or ground before use; occasionally, the berries are Sumac has beenapplied as a medicinal plant or a soaked to soften them and then are strained out, spice for hundreds of years. It contains a wide range pressed to release all their juices, and the liquid used of medicinally active components, including organic as part of the cooking medium for a stew or other dish. acids, phenolic acids, flavonoids, anthocyanins, A simple salad of sliced onions seasoned with ground hydrolysable and terpenoids (Morshedloo et sumac is popular throughout the Middle East. Sumac al., 2018). Its scientific names are Rhus glabra L., flavors kebabs and grilled meats, fish, and chicken, , and Cashew family. Its common and it is added to marinades for foods that will be names are Blue glabrum, Dwarf sumac, Mountain roasted or grilled. It can be stirred into yogurt to make sumac, Indian salt (the powder on the berries), a marinade, or the seasoned yogurt can be served on Pennsylvania sumach, Scarlet sumac, Sleek sumach, its own as a dip or a condiment. Sumac is also Smooth sumac, and Upland sumach. sprinkled over rice, hummus, or baba ghanoush, along with a drizzle of olive oil, as a garnish and Identified metabolites of Sumac fruit flavoring (Lakshmi, 2016). Native Americans used the split and stems in basket-making and the All parts of the plant, including its fruit, contain for a yellow dye. In Iran, sumac is grown in significant amounts of (Glutamine). In a Mazandaran, Azadbayegan, Khorasan, Shiraz, general study of compounds found in sumac fruit, Ghazvin, Ghom and Hamedan. This study showed anthocyanins and fats have been identified as major that the water extracts of sumac could inhibit the constituents of sumac fruit (Fabroni et al., 2016). microbial growth in ground beef meat during refrigerated storage. Because the sumac is commonly Botany used as seasoning ingredients in muscle foods (kebab, chicken meat meal and so on), the application of their Anacardiaceae (the sumac family) includes extracts in these foods not only can improve sensory flowering , with about 80 genera and about 870 characteristics but also extend the shelf life. species20. Several species are economically Meanwhile, these extracts might have health- important fruit and nut crops.The fruits are commonly promoting effects on the consumers due to their fleshy drupes. Sumac, (genus Rhus), the genus of potential antimicrobial activities (Kamalinejad et al., and small , native to temperate and 2019). Studies have been done on fruit and oil subtropical areas of the world.Sumac leaves are mentions that the Sumac fruit contains flavonols, characteristically arranged in spirals and are usually phenolic acid, anthocyanins, and organic acids. The compound, though some species have simple leaves. sour taste is also due to the presence of organic acids The minute have five and are borne in such as malic acid, citric acid and tartaric acid dense panicles or spikes. The fruits are red drupes and (Chakraborty et al., 2009; Heydari et al., 2019). also are borne in dense upright clusters. All Syrian sumac (Rhus coriaria L.) is famously used in have a milky or resinous sap. Many species can Mediterranean region and the Middle East as a spice, spread asexually by rhizomes.The smooth, or scarlet, sauce and drink and Chinese sumac (Rhus typhina sumac (Rhus glabra), native to the eastern and central L.), is indigenous to the Eastern area of North United States, is a common species. It grows to a America, is not extensively cultivated in China ,s height of 6 meters (20 feet), with an open, flattened North, Northwest and many other regions such as crown and a few stout spreading branches. A Lanzhou, Beijing, Hebei, Shanxi where it is usually cultivated variety has dissected fern-like called huojushu (Kossah et al., 2009). The plant leaves.Sumac (R. typhina), grow up to 9 meters (29.5

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feet), fall foliage is orange-red to purple. It also has a to 11.09 mg ascorbic acid equivalents per g dry variety of finely cut leaves. Edible sumac varieties weight (Fereidoonfar et al., 2019). The aqueous and include smooth sumac (Rhus glabra), staghorn sumac aqua-methanol extracts of Sumac parts were analyzed (Rhustyphina), sweet sumac (Rhusaromatica), dwarf by HPLC to unfold the deferent tannins derivatives, or winged sumac (Rhuscopallina), lemonade gallotannins methyl gallate, digallic acid, tri-gallic (Rhusintegrifolia), southwestern sumac acid, and ellagic acid, and dodecagallolyl glycoside (Rhusmicrophylla), sugar bush (Rhus ovata), and derivatives as representative tannins present in R. squaw berry (Rhustrilobata). All nonpoisonous coriaria (Regazzoni et al., 2013). The components of species contain red berries when ripe and are sumac ethanolic extract gained by GC/MC is shown sometimes inaccurately and collectively called red in Table 1. sumac. R. coriaria, the only species of Rhus genus that is most prevalent in Iran, is a large shrub or small Sumac as a spice (1–3 m high), with pinnately compound leaves, greenish-white flowers, and brown to red fruits. Rhuscoriaria has long been used as a spice. Sumac fruit consists of pulp (outcrop and shortcut), Sumac has long been used as a pure spice or in the endocarp and nuclei, which reportedly have the combination with other spices, as a complement to highest percentage of oil, the endocarp has the lowest drinks, sauces and as a natural stimulant in food oil content (Ahmad et al., 2014). In China, millions of recipes (Abu-Reidah et al., 2015). It is also of tons of sumac are produced annually. Sumac fruit particular economic importance due to its use in the contains12 to 20.8% oil that linoleic acid is the cosmetics, dyeing, food preservation, and animal skin predominant fatty acid (47.4%). Linoleic acid is an processing technology (Abu-Reida et al., 2014). The unsaturated fatty acid and can reduce cholesterol and sumac oil could be mixed with vinegar or olive or the risks associated with heart disease. In Turkey, the sesame oil, depending on the type of native recipes. sumac fruit's oil content has been reported in the Nowadays, the most common edible consumed form range of 10% to 15%, but in other studies, oleic acid of sumac is as an additive to food as a spice or water. has been identified as the dominant fatty acid content of 34-40%. Oleic acid (Omega-9), an essential fatty Traditional usages acid in the body which forms a major part of the body's fatty acids, but it is low in the liver and A vast proportion of the important metabolites neurons. for nutrients and pharmacology (such as tannins, phenolic acids, anthocyanins, organic acids, proteins, Sumac chemical component essential oils, fatty acids, fiber, and minerals) have already been identified from various parts of sumac. Studies mention that a high degree of variation Based on the Canon of Medicine of Avicenna (Ibn- was found in the chemical characteristics and the Sina) Sumac as a remedy plant used in the treatment results revealed significant differences among the of stroke. Sumac has been utilized in traditional accessions in Sumac. Titratable acidity by variation medicine for the treatment of blood disease as from 2.01 to 7.84% and pH ranged from 2.66 to 3.90 diabetes diuresis, stroke and cancer, gastrointestinal (r = 0.56). Ascorbic acid ranged from 10.00 to diseases such as ulcer, diarrhea, stomach tonic, 45.00 mg per g of dry weight, phenolic content varied stomachache, and hemorrhoids pain, Hemorrhoids, from 77.54 to 389.30 mg gallic acid equivalents per g anorexia, measles, smallpox, hyperglycemia, dry weight (r = 0.32). the flavonoid content ranged atherosclerosis, hypertension Diarrhea, Conjunctiva, from 2.19 to 7.54 mg quercetin equivalents per g dry Hematosis, Hemoptysis, and Leukorrhea, Dermatitis, weight, while tannin content ranged from 52.00 to Ocular, and Liver Disease (Wu et al., 2020). Other 189.80 mg gallic acid equivalents per g dry weight. medicinal usages have also been studied, including Free amino acid content ranged from 25.01 to 166.38 weight loss, skin treatment, hair, burns, digestive mg glycine equivalents per g dry weight, while tract, headache, and temperature reduction (Ali- anthocyanin content varied from 3.57 to 66.14 mg Shtayeh et al., 2013). In traditional Iranian medicine, cyanidin-3-glucoside equivalents per g dry weight. sumac has been used as a hemostasis factor, anti- Furthermore, antioxidant capacity ranged from 1.55 diarrhea, anti-pus, and trachea treatment, and also pre

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Table 1. The components of sumac ethanolic extract gained by GC/MC.

Name of component Percent of Total Retention Time (min) Trans-Caryophyllene 7.84 12.858 Butanedioic acid, diethyl ester 22.01 13.87 1,7-Nonadien-4-ol,4,8- 1.06 15.869 dimethyl Malate 39.7 17.873 Tricyclo[6.3.1.02,5]dodecane- 1.18 17.941 8-ol Cembrene 5.84 19.198 Palmitate 7.64 19.808 9-Octadecenoic acid 2.61 21.78 Ethyl Linoleic acid 4.04 22.187 Ethyl Linoleolate 6.32 22.743 Phytol 1.76 22.858

vention of smallpox in the eye (Tohma et al., 2019). soup and can be considered as a natural preservative Studies have shown the effects of the hyperglycemic in some foods. Shidfar et al. (2014) found that the and uric acid lowering effects of sumac (Candan, favorite effect of sumac consumption on serum 2003). Sumac inhibits the α-amylase enzyme glycemic status, apoB, apoA-I and TAC levels in type significantly. Alpha-amylase is responsible for 2 diabetic patients. The sumac ethanolic extract breaking down starch into simpler sugars and showed a high antioxidant effect, the predominant inhibiting this enzyme increases glucose tolerance in compounds in the essential oil were malate (39.7%), diabetic patients. In addition, the sumac can indirectly Butanedioic acid, and diethyl ester (22.01%); on the inhibit xanthine oxidase, which is one of the ways to basis of their findings, the possibility of using the fruit reduce blood uric acid levels in patients with gout. In of R. coriaria L. as a novel source of natural recent years, due to the emergence of microbial antimicrobial and antioxidant agents for the food and resistance, the global tendency to investigate the pharmaceutical industries are suggested. Abdallah et antimicrobial effects of biological materials has been al. (2019) concluded that R. coriaria extract could increasingly increased and Sumac has also been no potentially induce its anti-cancer effects, and it is a exception (Mahdavi et al., 2018). Sumac reduces promising to involve R. coriaria as a therapeutic drug blood sugar and uric acid (Cowman, 1999). candidate for uterus cervix cancer. The most important health benefits of sumac is presented in Modern Pharmaceutical Science Table 2.

The methanol extract of Sumac fruits as a rich Industry source of natural antioxidant phenols and tannins, utilized as an inhibitory function on vascular smooth Some herbal plants are also use in Industry muscle cell migration. Studies have shown that (Shahrajabian et al., 2019). In the past, the leaves, tannins have anti-carcinogenic effects. Sumac has skin, roots, and branches of the sumac were used as been utilized as anti-bacterial, anti-fungal, natural dyes in dyeing. In the food industry, on the antioxidant, anti-inflammatory, antidiabetic and other hand, antioxidants are used to prevent oxidative anticholinergic, vascular smooth muscle cell degradation of fats by inhibiting the formation of free migration inhibition (Schulze-Kaysers et al., 2015), radicals. Synthetic antioxidants such as butylated hypoglycemic, and hypolipidemic activities, tumor hydroxy anisole (BHA), butylated hydroxy toluene growth inhibitor on breast cancer (Isik et al., 2019). (BHT) and propyl gallate (PG) are widely used. Ahmadi et al. (2017) showed that the water extract of However, the use of synthetic antioxidants in food sumac has retention effect against Bacillus cereus in products has been abused (Kizil and Turk, 2010).

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Table 2. The most important health benefits of sumac. Balance blood sugar levels Reduce cholesterol Rich in antioxidants Reduces the chance of bone depletion Calms muscle aches Can help in the fight against cancer

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Cite this article as:

Khoshkharam, M.; Shahrajabian, M.H.; Sun, W.; Cheng, Qi. 2020. Sumac (Rhus coriaria L.) a spice and medicinal plant - a mini review. Amaz. Jour. of Plant Resear. 4(2): 517-523.

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