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ISSN: 1948-5948
Journal of Microbial & Biochemical Technology
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Tamarix nilotica (Ehrenb) Bunge: A Review of Phytochemistry and Pharmacology

Ahmed AM Abdelgawad*

Department of Medicinal and Aromatic Plants, Desert Research Center, Cairo, 11753, Egypt

*Corresponding Author:
Ahmed AM Abdelgawad
Department of Medicinal and Aromatic Plants
Desert Research Center, Cairo, 11753, Egypt
Tel: 0020119910661
E-mail: [email protected]

Received date: January 16, 2017; Accepted date: February 01, 2017; Published date: February 08, 2017

Citation: Abdelgawad AAM (2017) Tamarix nilotica (Ehrenb) Bunge: A Review of Phytochemistry and Pharmacology. J Microb Biochem Technol 9:544-553. doi:10.4172/1948-5948.1000340

Copyright: © 2017 Ahmed AMA. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Abstract

Tamarix nilotica (Ehrenb.) Bunge is known as Nile Tamarisk belonging to the Tamaricaceae family. This plant has diverse and potential medicinal uses in traditional herbal medicine for treating relieve headache, draw out inflammation, and as an antiseptic agent in Egypt. Tamarix nilotica have been occurs in Lebanon, Palestine, Egypt, Sudan, Somalia, Ethiopia and Kenya. Phytochemical investigation revealed that the major chemical constituents of Tamarix nilotica are flavonoids, tannins and phenolics. The hydro-alcoholic extracts of the leaves of T. nilotica exhibited significant antioxidant, anti-tumor, hepatoprotective and antiviral activities.

Keywords

Tamarix nilotica; Nile Tamarisk; Ellagitannins; Flavonoids; Antioxidant; Antitumor; Antiviral; Hepatoprotective; Antimicrobial; Antidiabetic

Introduction

Tamaricaceae is relatively a small family of 4 genera and 120 species [1]. Members of the family are chiefly temperate and sub-tropical, growing in maritime or sandy habitats in addition to halophytes or xerophytes that are distributed from the Mediterranean, North Africa and south-western Africa through Arabian Peninsula to Central and South Asia [2].

The genus Tamarix (tamarisk, salt cedar) is composed of about 50–60 species of flowering plants in the family Tamaricaceae, native to drier areas of Eurasia and Africa. Tamarix is represented in Egypt with two indigenous species which are T. aphylla (L.) H. Karst and T.nilotica (Ehrenb.) Bunge while, it is represented by 8 species in Saudi Arabia, namely: T. mascatensis Bunge.; T. ramosissima Leded., T.nilotica (Ehrenb.) Bunge., T. aphylla L., T. tetragyna Ehrenb., T. aucheriana Decne., T. pyconocarpa DC and T. passerinoides Del [2-4]. Another species of Tamarix include T. arabica, T. aralensis, T. boveana, T. chinensis, T. hohenackeri, T. karelinii, T. kotschyi, T. leptopetala, T. laxa var. araratica, T. laxa var. subspicata, T. mannifera var. persica, T. pycnocarpa, T. hampeana, T. mascatensis, T. bengalensis, T. gallica var. arborea, T. mannifera var. purpurascens, T. passerinoides var. macrocarpa and T. pallasii var. macrostemon [5].

Several species of plants belonging to the genus Tamarix have been employed in traditional medicine. The common traditional uses shown in various reports for some plant species of the genus are as a diaphoretic, diuretic and hepatotonic and to treat liver disorders, relieve headache, ease prolonged or difficult labor, and cure sores and wounds besides being an astringent and employed for tanning and dyeing purposes [6-10].

Among Tamarix plants, Tamarix nilotica (Ehrenb.) Bunge is a native plant in Egypt with a long history. Its leaves and young branches were used for reducing spleen edema, and it is mixed with ginger for uterus infections, while an aqueous decoction of its bark with vinegar is used as a licicidal lotion [9]. The aim of this review is to compile and document information on different aspects of Tamarix nilotica and highlight the need for research and development.

Botanical Description

Tamarix nilotica (Ehrenb.) Bunge is described as shrubs or trees of 2-5 m; multiform, glabrous, glaucescent or green, leaves with free distinct blade, ovate or deltoid-cordate, acute, half-clasping. Foliage is variable: green or grayish, dotted or not, sometimes covered with salt crystals. Racemes are loose, also much variable in size and shape. Pedicel is shorter than the calyx; petals are obovate-oblong; stamens 4-5; styles 3; capsule opening by 3 valves [11]. Seeds are numerous, elliptic with a tuft of hairs at the tip [3].

Taxonomy

The taxonomic classification of Tamarix nilotica is illustrated bellow [12,13]:

Kingdom: Plantae

Subkingdom: Tracheobionta

Division: Magnoliophyta

Class: Magnoliopsida

Order: Violales

Family: Tamaricaceae

Genus: Tamarix

Species: nilotica

Vernacular Names

The generic name originated in Latin: Tamarix may have referred to the Tamaris River in Hispania Tarraconensis (Spain) and nilotica, referred to the valley of the Nile. T.nilotica was known locally: in Egypt as Tarfa or Abal لبعلا or Nile tamarisk; in Saudi Arabia and Palestine as Athel لثلأا in Kenya as Uvari or Zizinda [14,15].

Geographical Distribution

T.nilotica widespread in Egypt, growing in saline sandy soils, on the edges of salt marshes, coastal and inland sandy plains, and Nile banks [4,16]. T.nilotica occurs in Lebanon, Palestine, Egypt, Sudan, Somalia, Ethiopia and Kenya [15,17].

Traditional Uses

Tamarix nilotica has been known since pharaonic times and has been mentioned in medical papyri to expel fever, relieve headache, to draw out inflammation, and as an aphrodisiac aperient, sudorific, ulcer, expectorant, carminative, astringent, diuretic [9,18]. In Egyptian traditional medicine, it has been used as an antiseptic agent [19]. Different parts of T.nilotica are used; the leaves and young branches are cooked for oedema of spleen and mixed with ginger for uterus infections, while the bark, when boiled in water with vinegar is used as lotion against lice. The bark used to treat eyes sore from a scratch or blow, also it is used for hemorrhoid [20,21]. The wood yields a locally made charcoal, also used as a fuel, said to be good firewood; the timber is sometimes used for inferior carpentry. Tamarix nilotica can help stabilize sand and may form nabkhas as part of the dune forming process [22].

Phytochemical Constituents

T.nilotica is a rich source of different classes of natural products with varying structural patterns. Many compounds have been isolated from T.nilotica including carbohydrates, phenols, flavonoids, terpenoids, steroids, tannins, and cardiac glycosides. Total phenolic and flavonoid contents in their chemical equivalents (gallic acid and quercetin, respectively) of the different extracts of the flowers of T.nilotica collected from Ismailia road, Egypt, in October, 2011were reported as in Table 1 [9].

Phenolics

Many phenolic compounds include Nilocitin, Ellagic acid, Gallic acid and some derivatives were isolated from leaves, flowers, roots and the aerial parts of T.nilotica [8,19,23-27]. All the chemical constituents that have been reported in the literature from T.nilotica were listed in Table 2 (Figure 1).

Flavonoids

Flavonoids are common constituents of numerous plants world-wide. The flavonoids isolated from the aerial parts of T.nilotica include kaempferol, Tamarixetin, quercetin, isoquercitrin, flavone, naringenin, dillenetin and its derivatives T.nilotica [8,26,28-31]. Flavonoids are the mostly biological active compounds found in plants, they are widely used in a variety of nutraceutical, cosmetic and pharmaceutical applications [32] (Figure 2).

Fraction Total phenolic (mg/g GAE) Total flavonoid (mg/g QE)
Chloroform 21.67 ± 2.1 0.79 ± 2.4
Ethyl acetate 20.6 ± 1 1.75 ± 1.5
Butanol 22.12 ± 2.4 0.58 ± 2.3
Aqueous 17.2 ± 1.4 -
Total 119.63 ± 0.09 2.55 ± 0.19

Table 1: Phenolic and flavonoid contents in T. nilotica flowers.

microbial-biochemical-technology-phenolic-compounds

Figure 1: The structure of phenolic compounds isolated from T. nilotica.

  Isolated compounds Extract/Fraction Plant part References
Phenolics
1 1,2,6-Tri-O-galloyl-ß-D-glucose Aq Ac LP [35]
2 3,4,8,9,10-pentahydroxy-dibenzo-[b,dlpyran-6-one Aq Ac FP [23,24]
3 Coniferyl alcohol 4-O-sulphate n-Bu LP [26]
4 Dehydrodigallic acid Et Ac RP [19]
5 Ellagic acid Aq Ac FP [23,24]
6 Ellagic acid 3,3'-dimethyl ether 4-O-ß-D-glucopyranoside Et Ac RP [19]
7 Ellagic acid-3-methyl ether Et AP [8]
8 Ferulaldehyde    (4-hydroxy-3-methoxycinnamaldehyde) Pet Eth RP [25]
9 Isoferulaldehyde    (3-hydroxy-4-methoxycinnamaldehyde) Pet Eth RP [25]
10 Isoferulic acid Bn RP [19]
11 Isoferulic acid methyl ester Et AP [8]
12 Methyl ferulate 3-O-sulphate n-Bu LP [26]
13 Gallic acid Et Ac RP [19]
14 Methyl gallate Aq Ac FP [23,24]
15 Methyl gallate 4-methylether Aq Ac FP [23,24]
16 Nilocitin   (2,3-digalloyl-D-glucopyranose) Aq Ac FP [23,24]
17 Niloticol    (l-ferulloyl-3-pentacosanoylglycerol) Pet Eth RP [25]
18 N-trans-Feruloyltyramine Et AP [8]
19 Syringaresinol Bn RP [19]
Flavonoids
20 5,7,4'-trihydroxy-5'-methoxylflavone Bu LP [30]
21 Flavone Bu LP [31]
22 Clematine Et AP [8]
23 Dihydroflavonol Bu LP [31]
24 Dillenetin Et AP [8]
25 Kaempferide Et AP [8]
26 Kaempferol n-Bu LP [26]
    Et LP [28]
27 Kaempferol-3-glucoside (Astragalin) Aq Ac FP [29]
    Et LP [28]
28 Kaempferol 3-O-sulphate-7,4'-dimethyl ether Aq Ac FP [29]
29 Kaempferol 3-O-ß-D-glucuronide 6"-ethyl ester Aq Ac FP [29]
30 Kaempferol-4', 7-dimethyl ether Aq Ac FP [29]
    Et LP [28]
    Et AP [8]
31 Kaempferol-4',7-dimethyl   ether-3-glucoside Et LP [28]
32 Naringenin Et AP [8]
33 Quercetin Aq Ac FP [29]
34 Quercetin 3-O-ß-D-glucupyranuronide n-Bu LP [26]
35 Quercetin 3-O-ß-D-glucuronide 6"-ethyl ester Aq Ac FP [29]
36 Quercetin 3-O-ß-D-glucuronide 6"-methyl ester Aq Ac FP [29]
37 Quercetin-3-glucoside (Isoquercitrin) Et LP [28]
38 Tamarixetin n-Bu LP [26]
39 Tamarixin (tamarixetin-3-glucoside) Et LP [28]
  Ellagitannins      
40 1,3-Di-O-galloyl-4,6-O-(S)-hexahydroxydiphenoyl-ß-D-glucose Aq Ac LP [34]
41 Gemin D Aq Ac LP [34]
42 Hippomanin A Aq Ac LP [34]
43 Hirtellin A Aq Ac LP [34]
44 Hirtellin B Aq Ac LP [35]
45 Hirtellin C Aq Ac LP [35]
46 Hirtellin D Aq Ac LP [37]
47 Hirtellin F Aq Ac LP [35]
48 Hirtellin T1 Aq Ac LP [10]
49 Hirtellin T2 Aq Ac LP [37]
50 Hirtellin T3 Aq Ac LP [10]
51 Isohirtellin C Aq Ac LP [35]
52 Nilotinin D1 Aq Ac LP [34]
53 Nilotinin D2 Aq Ac LP [34]
54 Nilotinin D3 Aq Ac LP [34]
55 Nilotinin D4 Aq Ac LP [36]
56 Nilotinin D5 Aq Ac LP [36]
57 Nilotinin D6 Aq Ac LP [36]
58 Nilotinin D7 Aq Ac LP [35]
59 Nilotinin D8 Aq Ac LP [35]
60 Nilotinin D9 Aq Ac LP [35]
61 Nilotinin D10 Aq Ac LP [37]
62 Nilotinin M1 Aq Ac LP [34]
63 Nilotinin M2 Aq Ac LP [36]
64 Nilotinin M3 Aq Ac LP [36]
65 Nilotinin M4 Aq Ac LP [35]
66 Nilotinin M5 Aq Ac LP [37]
67 Nilotinin M6 Aq Ac LP [37]
68 Nilotinin M7 Aq Ac LP [37]
69 Nilotinin Q1 Aq Ac LP [10]
70 Nilotinin T1 Aq Ac LP [37]
71 Nilotinin T2 Aq Ac LP [10]
72 Nilotinin T3 Aq Ac LP [10]
73 Remurin A Aq Ac LP [34]
74 Remurin B Aq Ac LP [34]
75 Tamarixinin A Aq Ac LP [35]
76 Tamarixinin B Aq Ac LP [37]
77 Tamarixinin C Aq Ac LP [37]
78 Tellimagrandin I Aq Ac LP [35]
79 Tellimagrandin II Aq Ac LP [35]
Terpenoids
80 3-O-trans-caffeoylisomyricadiol Et AP [8]
81 3a-(3",4"-dihydroxy-trans-cinnamoyloxy)-D-friedoolean-14-en-28-oic      acid n-Hn LP [26,27]
Steroids
82 ß-Sitosterol Et AP [8]

Table 2: Isolated compounds from the different parts of T. nilotica.

Ellagitannins

The tamaricaceous plants produce a unique class of ellagitannins with diverse structures [33]. The review of literature reported the isolation of monomeric (Isohirtellin C, Remurin A-B, Gemin D, Nilotinin, Nilotinin M2-7, Hippomanin A, and Tellimagrandin I-II), dimeric (Nilotinins D1-D10, Tamarixinin A-C and Hirtellin A-D and F), trimeric (Nilotinin T1-T2, Hirtellin T1-T3) and tetrameric ellagitannins (Nilotinin Q1) from the aqueous acetone extracts of leaves of T.nilotica growing in Egypt [10,34-37]. Interest in the ellagitannin constituents due to their marked antiviral, antimicrobial, immunomodulatory, antitumor, and hepatic protective activities, which are largely dependent on the tannin structures [38] (Figure 3).

Terpenoids and steroids

To date, two terpenoids and one steroid compounds from T.nilotica have been reported. In 2009, 3α-(3",4"-dihydroxy-transcinnamoyloxy)- D-friedoolean-14-en-28-oic acid, was isolated from the leaves of T.nilotica growing in Egypt [26]. Furthermore, 3-O-transcaffeoylisomyricadiol and β-sitosterol were isolated from the ethanolic extract of the aerial parts of T.nilotica growing in Saudi Arabia [8] (Figure 4).

Pharmacological Activities

Scientific studies on T. niloyica indicate that it has wide-reaching pharmacological activities, including the effects as anti-tumor, antioxidant, antidiabetic, antiviral, antimicrobial and hepatoprotective activity.

Antioxidant activity

Free radicals are involved in a number of pathological conditions such as inflammatory diseases, atherosclerosis, cerebral ischemia, AIDS, and cancer [39]. The free radicals are produced in the human body due to environmental pollutants, chemicals, physical stress, radiations, etc. Catalase and hydroperoxidase enzymes are among the important antioxidants produced by the immune system. Consumption of antioxidants or free radical scavengers is necessary to compensate depletion of antioxidants of the immune system.

In 2008, AbouZid et al., reported that, the aqueous alcoholic extracts of leaves and flowers of Tamarix nilotica grown in Egypt had a significant antioxidant activity (73-96%) [7]. The in vitro antioxidant assays used in this study were 1,1-diphenyl-2-picryl hydrazyl (DPPH) radical scavenging activity, superoxide anion scavenging activity and iron chelating activity [26,40].

DPPH free radical scavenging activity of different T.nilotica subextracts has been screened at 100 μg/ml. EtOAc (100%), BuOH (93%) and total extract (90%) exhibited potential antioxidant activity while CHCl3 exhibited the lowest effect (26%). Comparing the IC50 of promising subextracts (>90%) with ascorbic acid as positive control (IC50 4.8 ± 0.54 μg/ml), EtOAc showed the best effect (7.25 ± 0.86 μg/ ml), with lower IC50 followed by BuOH (8.25 ± 0.65μg/ml) and total extract (45 ± 0.73μg/ml) [9]. When antioxidant assay was performed by TLC using DPPH, a significant antioxidant activity was related to butanol fractions of Tamarix nilotica grown in Sudan [31].

Cytotoxic and anti-angiogenic activity

Ellagitannins from the leaves of T.nilotica grown in Egypt were reported to exhibit significant host-mediated antitumor activities against sarcoma-180 in mice and strong cytotoxic effects with higher tumor specificity against four tumor cell lines [35,37]. T.nilotica showed a selective cytotoxic potential against liver (HUH-7), colon (HCT-116), lung and breast (MCF-7) carcinoma cell, while being non-toxic to other cancer cells [9,40].

A considerable number of cancers have been reported to be dependent on angiogenesis and respond well to anti-angiogenic therapies. These include cancers of the colon, breast, lung, and bladder as well as renal cell carcinoma and non-small cell lung cancer (NSCLC). Anti-angiogenic therapies target angiogenesis by two major mechanisms: blocking the receptor tyrosine kinases intracellularly or neutralizing angiogenic factors such as VEGF or its receptors [41].

The results indicated that the leaves extract of Tamarix nilotica grown in Sudan exhibited remarkable anti-angiogenic activity by inhibiting the sprouting of micro-vessels more than 60% by using ex vivo rat aortic ring assay [42].

Hepatoprotective activity

Hepatoprotective activity of T.nilotica grown in Egypt was assessed using carbon tetrachloride- induced hepatic injury in rats by monitoring biochemical parameters. Aqueous ethanol extract of flowers of T.nilotica ameliorated the adverse effects of carbon tetrachloride and returned the altered levels of biochemical markers near to the normal levels [40]. In this study, carbon tetrachloride was used to induce liver damage and hence enhancing the levels of SGOT, SGPT and ALP. Carbon tetrachloride is biotransformed by liver enzymes to a highly reactive free radical. This free radical can lead to lipid peroxidation, disruption of Ca2+ homeostasis, elevation of hepatic enzymes, and finally results in cell death [43]. Carbon tetrachloride has been used in animal models to investigate chemical toxininduced liver damage. The extent of hepatic damage is assessed by the increased level of cytoplasmic enzymes (SGOT, SGPT and ALP).

Antidiabetic activity

The leaves aqueous extracts of T.nilotica were used effectively to reduce the serum glucose level as the experimental period progressed and demonstrated a marked hypolipidemic effect evidenced by the lower serum triglyceride and total cholesterol levels. The overall effect of the plant extracts was significantly better than the synthetic drug, metformin in terms of antihyperglycemia and antihyper triacylglycerolaemia. Also, the results suggest that the plant extract are potential phytotherpeutic agents which could be used for the management of diabetes type 2 and dyslipidemia associated with it [44]. The hypoglycemic activity may result from both pancreatic and extrapancreatic mechanisms, on the other hand, enhanced by high antioxidant capacity [45]. The actual role of these interesting compounds in the antidiabetic properties of T.nilotica still requires elucidation. These polyphenolic compounds act as monomers or oligomers, responsible for in vitro insulin enhancing activity in epididymal fat cells and shown in vitro to have insulin-like activity as well as an antioxidant effect.

Antiviral effect

Infectious viral diseases are still major threat to public health and remain as an important problem due to viruses have resisted prophylaxis or therapy longer than any other form of life [46]. Egyptian medicinal plants have diverse uses in traditional folk medicine to cure various ailments including infectious diseases.

The Hydro-alcoholic extracts of the aerial parts of Tamarix nilotica are found to have virucidal effect against herpes simplex-1 virus (HSV) at concentration of 1000 μg/ml with Rf 104 [47]. The antiviral bioassay is carried out by the end point titration technique (EPTT) that builds on the ability of plant extract dilutions to inhibit the produced cytopathogenic effect (CPE) and expressed as reduction factor (Rf) of the viral titer.

Antimicrobial activity

microbial-biochemical-technology-flavonoid-compounds

Figure 2: The structure of flavonoid compounds isolated from T. nilotica.

microbial-biochemical-technology-structure-ellagitannins

Figure 3: The structure of ellagitannins isolated from T. nilotica.

microbial-biochemical-technology-steroids-isolated

Figure 4: Structures of terpenoids and steroids isolated from T. nilotica.

A significant antibacterial and antifungal activity was related to butanol extract from Tamarix nilotic growing in Sudan. The other extracts showed moderate to weak inhibition on fungi (Aspergillus niger and Candidas albicans). The pure compounds (flavone and dihydroflavonol) isolated from butanol extract of Tamarix nilotica also revealed significant antibacterial activity and antifungal activity. This study demonstrated that the butanol fraction of Tamarix nilotica is potential candidate for antimicrobial activity and deserves further optimization [31]. Evaluation of the antimicrobial activities of different extracts and isolated compounds was carried out by the disc diffusion method, measured by the diameter of the zone of inhibition.

Endophytic fungi, which have been reported in numerous plant species, are important components of the forest community and contribute significantly to the diversity of natural ecosystems. Tamarix nilotica grown in Saudi Arabia showed the highest endophytic diversity with a relative frequency of 27.27%, the most frequently isolated species was Penicillium chrysogenum with an overall colonization rate of 98.57% [48].

Conclusion

T.nilotica could be considered as promising candidates for the discovery of novel chemopreventive or chemotherapeutic formulations with reduced side effects. The literature endorses further investigations on this plant to determine the active principles and their mode of action.

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