Pharmacognostical and Pharmacological studies of Holoptelea integrifolia – An overview

About Authors:
Soujanya J, Silambujanaki P, Leela Krishna V
Department of Pharmacology, SRM College of Pharmacy,
SRM University, Kattankulathur-603203,
Kancheepuram Dist.,
Tamil Nadu, India

Abstract
Holoptelea integrifolia, Planch. is a widely used herb in traditional medical systems of India.It is an important pollen allergen of India andsensitizes almost 10% of the atopic population in Delhi.Various parts of Holoptelea integrifolia, a roadside plant, are indicated by Charaka Samhitha, Sushrutha Samhitha and other traditional systems for the treatment of inflammations, acid gastritis, dyspepsia, flatulence, colic, intestinal worms, vomiting, wounds, vitiligo, leprosy, filariasis, diabetes, haemorrhoids, dysmenorrhoea and rheumatism.The present review is therefore, an effort to give a detailed survey of the literature on its pharmacological, traditional and phytochemical properties

Reference Id: PHARMATUTOR-ART-1209

INTRODUCTION
Holoptelea integrifolia Planch. is traditionally used in Indian system of medicine. It thrives in deep porous soil with good drainage but becomes stunted and crooked on poor shallow soil. It is a moderate light demander and is not frost-hardy. It coppices well. The tree sheds its seeds during the hot season and they germinate at the commencement of the rains. Protection from the sun in early stages is beneficial. The rate of growth is fast. The bark and the leaves and twigs when crushed emit an unpleasant odor (WOA, 1997). The tree has a mucilaginous bark, which is boiled, and the juice squeezed out and applied to rheumatic swellings, the exhausted bark is then powdered and applied over the parts covered by the sticky juice.^[1]

Monkey’s favourite fruit It is a Monkey´s favourite seasonal fruit. During extensive surveys in Patalkot valley of Madhya Pradesh and Dangs in South Gujarat, came across many important uses of the trees and herbs by the local inhabitants. Tribals in both these remote areas of India use Holoptelea in many herbal practices. It has been used to cure rheumatoid, piles, laryngitis and many more. In an interesting conversation with a village head in Patalkot, came to know that Monkeys eat Holoptelea fruits after conceiving or delivering babies. It is assumed that it gives strength and immunity. ^[2]                                  

Description
The plant belongs to family Ulmaceae. It is commonly known as Indian Elm Tree. The flowering time of the tree is January to February, whereas, fruiting is seen in April to May. Holoptelea integrifolia is a large deciduous tree distributed throughout the greater part of India up to an altitude of 2,000 ft. It is sometimes grown on the road side. Trees or shrubs, evergreen or deciduous. Winter buds with scales, rarely naked; axillary budsdeveloped; terminal bud usually dying backearly.

Macroscopic characters
Leaves Leaves (7.5-12.5 by 3.2-6.3cm) are elliptic-ovate, acuminate, entire (those of the seedlings and shoots often serrate), glabrous, base rounded or subcordate in shape. Leaves simple, alternate or rarely opposite, usually distichous, petiolate; leaf blade pinnately veined, basally 3(or 5) -veined, margin entireor serrate. Stipules usually membranous, caduceus, upper epidermis dark green in colour, lower epidermis lighter in colour.

Flowers Flowers usually male and hermaphrodite mixed, greenish yellow, polygamous and found in short racemes or fascicles at the scars of fallen leaves. Monochlamydeous, bisexual, or rarely unisexual or polygamous. Perianth lobes 4-9, imbricateor rarely valvate, persistent or caducous. Stamensusually equal in number to and opposite perianth lobes, opposite, basally adnate to tepals; filaments distinct; anthers 2-celled, longitudinally fissured. Pistil2-carpellate, Inflorescences axillary. Style very short (2.5-4 mm.long); stigmas 2, linear. Sepals often 4, pubescent, 1.5-2.5 mm. long.

Fruits Fruits are sub-orbicular with membranous wing. Ovary superior, 1(or 2) -loculed; ovule1, suspended, anatropous; integuments2. Fruitsamara, drupes, or winged nutlets, apically usually with persistent stigmas. Endosperms canty or absent; embryo erect, curved, or involute; cotyledonsflat, curved, or flexed.

Wood The wood is light yellow with an unpleasant odour when freshly cut, lustrous, somewhat interlocked-grained, medium and even-textured, moderately heavy. It can be kiln-seasoned successfully and retains its brightness and colour. Well seasoned wood is fairly durable in sheltered and well ventilated locations; for use in exposed places the wood requires to be given a pressure antiseptic treatment.

Bark Bark of the tree remains grey, pustular, exfoliating in somewhat corky scales. It may be pulped and made into hard boards and insulation boards. It contains lignin, cellulose, pentosans and ash. It is mucilaginous and used in external applications for rheumatism.

Seed Seedling epigeous. It yields 37.4% of yellow oil. The seed cake contains lysine, glutamic acid and histidine.

Timber It is used for brush backs and handles of dusting brooms, for which it is very suitable. It is also used for indoor building purposes, cheap furniture, cabinet work, carving, ploughs, yokes, carts and carriages, combs, shoe heels, mathematical instruments, warper bobbins for jute mills, cotton reels, dugout boats and for making charcoal.

Microscopic characters
Leaf
The upper epidermis consists of small barrel shaped paranchymatous cells. In surface view they appear wavy in outline and trichomes are present on both the surfaces of leaf, more along the midrib region and less along the lamina. The covering trichomes are simple, unbranched, uniseriate, unicellular structures, apex blunt and walls smooth.  Stomata are present on the lower surface. Leaf type is dorsiventral. The palisade consists a single layer of regular, long,  columnar cells, beneath which is a 3 to 4 layered mass of closely packed cells filled with chloroplast. Stomata represented by anomocytic type. Some oil glands are present in the lower epidermis
In the midrib region cortex consists of 5 to 7 layers of paranchymatous cells. The vascular bundle is ovoid in shape. Mass of xylem and phloem shows different structures. Below the vascular bundle a zone of sclerenchymatous tissues are present. In between the upper epidermis and the vascular bundle 6 to 7 layer of irregular shaped collenchyma cells are present. The vascular bundle is collateral and open endark. There are few layers of cambium in between the xylem and phloem. The phloem consists of sieve tubes, companion cells and phloem parenchyma. Xylem consists of xylem vessels, tracheids and parenchyma. Xylem is seen on the upper side whereas phloem is seen towards the lower side of the epidermis. ^[3]  

Stem
The outline of the transverse section of the stem is nearly circular covered with many unicellar, uniseriate trichomes. The outermost multilayered periderm consists cork cambium and secondary cortex. The cork layer is interrupted at many places due to the presence of lenticels. The cortex is multilayered consists of parenchymatous cells. The primary phloem remains as patches of crushed tissue. The secondary phloem consists of sieve tubes, companion cells, phloem parenchyma and phloem rays. Vessels are present in broken conditions and crushed form. The xylem is represented by both primary and secondary xylem tissue. It consists of vessels and tracheids. The primary xylem towards pith. The secondary xylem consists of large vessels and xylem parenchyma. Xylem is found in the form of continuous medullary rays. The pith is large and remains to the central part of the stem. It consists of thin walled parenchymatous cells having many intercellular spaces. The pith regions have oil droplets. The vascular bundle is collateral and open endark.

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Leaf constant studies
The stomata are present only in lower surface of leaf. They are anomocytic type. The stomatal index is 14.83 mm and the stomatal frequency range is 34.25.

Quantitative Leaf Microscopy

Palisade ratio: 7.00 – 10.00

Stomata number Upper surface: 7.00 – 9.00

Stomata number Lower surface: 4.00 – 8.00

Stomata index Upper surface: 14.08 – 20.34

Stomata index Lower surface: 12.44 – 18.40

Vein islet number: 4.00 – 5.75

Veinlet termination number: 3.00 – 3.50 ^[4]

Powder analysis
The organoleptic evaluations means conclusions drawn from studies resulted due to impression on organs of senses. The color, texture, odour and taste of the plant powder were analyzed [Table 1].

Table 1:  Powder analysis

Fluorescence analysis
Fluorescence analysis of the leaf and stem power in various solvents have been studied ^[5] [Table 2]. It can be as a diagnostic tool for testing the adulterations.

Table 2: Fluorescence analysis of the extracts

Physico - chemical analysis
Ash values are helpful in determining the quality and purity of crude drugs, especially in the powered form. The different physico-chemical standards and solvent extractive value were obtained by employing standard methods of analysis as described in Pharmacopoeia of India (1996) ^[6] [Table 3].

Table 3:  Physico - chemical analysis

Extractive value of leaf is high in methanol extract whereas very low in benzene extract. Extractive value of stem is high in methanol extract while very low in chloroform extract.

Vernacular names
The common vernacular names of the plant in India are Kanjho, Waola (Gujarati), Kanju, Papri, Banchilla, Chilbil, Dhamna, Begana (Hindi), Thavasai, Rasbija, Kaladri, Nilavahi (Kannada), Aval (Malayalam), Vavli, Papara (Marathi), Dauranja, Turuda (Oriya), Rajain, Khulen, Arjan (Punjabi); Chirabilva (Sanskrit), Aya, Ayil, Kanci, Vellaya (Tamil), and Thapasi, Nemali, Pedanevili (Telugu). ^[7]

Distribution
A small genus of trees distributed in tropical and sub-tropical parts of Asia and Africa. One species occurs in India [Figure 1.Holopteleaintegrifolia]. It is found in Punjab, M.P, Bihar, Assam, Bundelkhand, Tamil Nadu and Sub Himalayas region in India. It is also distributed in Burma, Ceylon, China. ^[1],[7]

Medicinal uses
The plant has several medicinal properties. In India, decoction of the bark of this plant is externally used in rheumatism. ^[8] Oral application of the bark is used to treat intestinal tumours. ^[9] Dried bark is useful as an oxytocic in pregnant ladies. ^[10] Decoction of the leaves is orally given to regulate fat metabolism. ^[11] Leaves along with garlic are externally used to treat ringworm eczema and cutaneous diseases. ^[12] Leaves of the plant, Garlic (Allium sativum) and Black Pepper (Piper nigrum) are mixed and crushed to make tablet. One tablet per day can be given to the patient suffering from jaundice. ^[13] Paste of the stem bark is externally applied to treat the inflammation of lymph glands. Holoptelea integrifolia stem bark powder is externally applied on the forehead of the patient suffering from common fever. ^[14] Moreover, paste of the stem bark is externally applied in cases of ringworm and scabies. Stem bark acts as an anti-inflammatory agent specifically for eyes. ^[15] In Nepal, bark is externally used to relieve rheumatic swellings. ^[16] Bark and leaf paste of Holoptelea integrifolia plant are applied externally on the white patches or leucoderma. ^[17]

Scientific classification

Domain                       :  Eukaryota

Kingdom                     :  Plantae

Subkingdom                :  Viridaeplantae

Phylum                        :  Tracheophyta

Subphylum                  :  Euphyllophytina. 

Infraphylum                 :  Radiatopses

Class                            :  Magnoliopsida

Subclass                      :  Dilleniidae

Superorder                  :  Urticanae

Order                           :  Urticales

Family                         :  Ulmaceae

Genus                          :   Holoptelea

Specific epithet           :   integrifolia

Botanical name           :  Holoptelea integrifolia (Roxb.) Planch.      

Parts used Leaves, Root and Stem bark.

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Phytochemicals
The pharmacognostic investigations were carried out in terms of organoleptic, microscopic and physical parameters. The dried leaves and bark were subjected to successive Soxhlet extraction using petroleum ether, chloroform, ethyl acetate and methanol. The phytochemical analyses indicate that the plant contains carbohydrates, proteins, amino acids, steroids, glycosides, alkaloids, flavanoids, terpenoids, anthraquinones, saponins, tannins, catachin and phenolics. ^{[18],[19],[20],[21],[22]} The chemical constituents of stem bark are friedelin, friedelin-3-β-ol, β-sitosterol, hederagenin (heart wood), hexacosanol, fatty acid esters, holoptelin A and B and β-amyrin (leaves). ^[23] By the application of reversed-phase partition chromatography, the oil from the seeds of Holoptelea integrifolia (Urticaceae) is found to contain the acids such as lauric 0.2%, myristic 3.5%, palmitic 35.1%, stearic 4.5%, arachidic 1.1%, behenic 0.4%, hexadecenoic 1.9% and oleic 53.3%. ^[24] Leaves of the plant has shown the occurrence of Friedelin, Friedelanols and associated friedelanes and pentacyclic triterpenes.
Physicochemical data of the stem bark of Holoptelea integrifolia analysis showed ash content of 11.75% and water soluble ash of 10.5% indicating the presence of inorganic matter. Acid insoluble ash 0.36% shows the presence of silicates in the bark. Water soluble extractive value (10.52%) is due to the presence of sugars, acids, polar constituents, glycosides of steroid, alkaloids and coumarines. n-Hexane soluble extractive value (0.62%) reveals the presence of less polar straight chain compounds and waxy materials. Alcohol soluble extractive value (2.18%) shows the presence of fewer amounts of polar substances like phenols, tannins, glycosides and flavonoids in the stem bark.
Heavy metals viz. lead (0.11), cadmium (0.03) and mercury (0.001) of the stem bark was found to be within the permissible limits as per WHO guidelines. The stem bark was free from arsenic, thereby proving the safety of its utilization in Ayurveda and Siddha systems. Mineral elements such as iron (2.17), copper (0.05), manganese (0.08), zinc (0.93), nickel (0.02), cobalt (0.11), chromium (0.13) are found in considerable amount which may be directly or indirectly helpful in the management of many diseases. Thus some traditionally used Indian medicinal plants particularly the stem bark of Holoptelea integrifolia are promising source of potential antioxidants. ^[23]

Pharmacological activities

Anti-inflammatory effect
The anti-inflammatory activity of Holoptelea integrifoliawas evaluated by the carrageenan-induced paw edema test in the male Wistar strain rats.Measurements of paw volume (ml) were made by mercury displacing techniques using plethysmometer. Immediately before and 1, 2, 3 and 4 h after carrageenan injection, percentage increment of paw volume after 1, 2, 3 and 4 h was calculated by Newbould method. The extract administered orally at doses of 250 and 500 mg/kg p.o. produced a significant (P < 0.05) dose dependent inhibition of edema formation. ^[25] A significant % inhibition of paw edema by the aqueous extract of leaves of H. integrifolia, Planch. and its almost nearby same % inhibition with indomethacin suggest its usefulness as an anti-inflammatory agent.

Wound healing activity
Wound-healing activity was evaluated by taking wound contraction, wound closure, tensile strength and collagen formation as parameters.Excision modelwas adopted indicating that both extracts are showing wound-healing property comparable to that of standard group. Breaking strength of the skin was measured using the Universal testing machine (Shimadzu, Switzerland). Both MLE (methanolic extract of leaves) and MSBE (methanolic extract of stem bark) extracts have shown high breaking strength than that of control group. MSBE has shown higher breaking strength and higher collagen content. Hydroxyprolinecontents were found to be increased significantly in the groups treated with MLE and MSBE which implies more collagen deposition in treated groups than the control group. Finally, histopathology studies conformed wound-healing activity of Holoptelea integrifolia.^[26]

Antimicrobial activity
The antimicrobial property of the Holoptelea was studied against the six bacterial (Bacillus subtilis, Bacillus cerculences, Staphylococcus aureus, Escherichia coli, Pseudomonas aeruginosa and Klebsiella aeruginosa) and five fungal strains (Candida albicans, Saccharomyces serviseae, Aspergillus niger, Candida Tropicana and Candida krusei) using the agar well diffusion method and minimum microbicidal concentration(MMC) and minimum inhibitory concentration(MIC) were determined for each strain, ^[26] in which methanolic extract of stem bark (MSBE) has shown bigger zone of inhibition (11.3–20.4 mm) than methanolic extract of leaves (MLE) (9.6–14.9 mm).

Antioxidant activity
The methanolic extract of leaves (MLE) and stem bark (MSBE) of Holoptelea integrifolia were screened for antioxidant activity against 1,1-diphenyl-2-picrylhydrazyl (DPPH) free radical scavenging activity, and total phenolic content was also estimated. Antioxidant activity was assessed by DPPH scavenging method where MSBE was found to be most potent antioxidant than the MLE. The higher phenolic content of MSBE might have contributed to higher antioxidant activity of MSBE than MLE. ^[26]

Antitumour activity
The antitumour activity of the ethanolic extract of leaves of Holoptelea integrifolia (EHI) has been evaluated against Dalton’s ascitic lymphoma (DAL) in Swiss albino mice at the dose of 250 and 500 mg/kg, body weight. The experimental parameters were evaluated like tumour volume, tumour cell count, viable tumour cell count, mean survival time and increase in life span to assess antitumour activity. The extract was administered orally for 14 consecutive days to tumour bearing group of animals. The extract increased the life span of DAL treated mice ^[27] and restored the hematological parameters as compared with the DAL bearing mice in a dose-dependant manner. All these data point to the possibility of developing an ethanolic extract of leaves of Holoptelea integrifolia as a novel, potential agent in the area of cancer chemotherapy.

Antidiarrhoeal activity
The ethanolic extract of leaves of Holoptelea integrifolia was studied for its antidiarrhoeal properties in experimental diarrhoea, induced by castor oil and magnesium sulphate in mice. At the doses of 250 and 500 mg/kg per oral, the ethanolic extract showed significant and dose-dependent antidiarrhoeal activity in both models. ^[28] The extracts also significantly reduced the intestinal transit in charcoal meal test when compared to atropine sulphate (5 mg/kg; i.m.). Thus ethanolic extract of leaves of Holoptelea integrifolia have a significant antidiarrhoeal activity and supports its traditional uses in herbal medicine.

Antiemetic activity
Treatment of nausea/vomiting caused by cisplatin, a potent chemotherapeutic agent and one of the most emetogenic stimuli, requires a combination of different antiemetic drugs. Pica was measured in rats to quantify cisplatin-induced nausea, and the antinausea effect of pretreatment with ethanolic extract of leaves of Holoptelea integrifolia, Planch (HIE) when given orally was seen. Cisplatin at 3 mg/kg (i.p) induced significant pica accompanied by reduced food intake, suggesting the presence of nausea. Cisplatin-induced pica decreased significantly when animals were pretreated with HIE at doses of 250 mg/kg p.o and 500 mg/kg p.o (P<0.01). HIE pretreatment decreased cisplatin induced kaolin intake in the rat model of simulated nausea, suggesting that HIE and its active constituent(s) may play a therapeutic role in chemotherapy-induced emesis. ^[29]

Anti-obesity activity
Protective Effect of Holoptelea integrifolia Against Diet Induced Obesity was carried out by selecting healthy Sprague-Dawley rats. The treatment group of animals was given oral administration of 250 mg/kg or 500 mg/kg of Holoptelea integrifolia alcohol extract in 10 mL of 0.5% CMC, using gastric tube for 5 week study duration. Sibutramine (7 mg/kg body weight) is used as a positive control. The control group of animals were given 10 ml/kg of 0.5% CMC. The weight gain for different groups compared at weekly intervals. The reduction in body weight gain of animals in treatment groups corresponding to 250 mg/kg and 500 mg/kg doses are about 98.1% and 130.8% respectively compared to those in the untreated control group. Sibutramine exhibited 123.1% reduction in weight gain compared to the control group. The treatment group of animals also showed significant reduction in serum triglycerides and lipid profile (anti-hyperlipidemic activity) when compared to the control group. ^[30]

Antiviral activity
In an ethnopharmacological screening, plants used in Nepalese traditional medicine were evaluated for antiviral activity. Methanolic and methanolic-aqueous extracts were assayed in two in vitro viral systems, influenza virus/MDCK cells and herpes simplex virus/Vero cells. Holoptelea integrifolia exhibited considerable antiviral activity against herpes simplex virus. None of these extracts showed cytotoxic effects. Additionally partial protease inhibitory activity was estimated.^[16]

Pollen allergy
Holoptelea integrifoliais an important pollen allergen of India and sensitizes almost 10% of the atopic population in Delhi. It was assessed on the basis of skin prick tests and ELISA, ELISA inhibition and immunoblot inhibition studies. Out of 44 atopic Indian patients skin prick tested with H. integrifolia extract, 34% were found to be sensitized. ELISA and ELISA inhibition studies suggested strong cross-reactivity between H. integrifolia and Parietaria judaica pollen. Immunoblot inhibition studies revealed that 14-, 16-, 28-, 38-, 42- and 46-kDa proteins are the cross-reactive proteins in H. integrifolia and P. judaica. However, Par j 1, the major allergen of P. judaica, is absent in H. integrifolia pollen. ^[31]

Antidiabetic activity
The leaf extracts of (Planch) was tested at a dose of 200mg/kg body weight orally for antidiabetic activity using alloxan induced diabetic rats on acute and prolonged treatment. The extracts showed significant (p<0.01) antidiabetic results. The results obtained were comparable with the standard drug Glibenclamide.^[32]

Exposure of sulphur dioxide on the metabolism of plant
Two-month-old chilbil Holoptelea integrifolia plants were exposed to 0·06, 0·1 and 0·8 μl litre⁻¹ sulphur dioxide (SO₂) for 4 h in a continuous flow exposure chamber. Symptoms mapped 48 h after exposure indicated no visible injury. The biochemical changes included accumulation of free sugars, especially reducing sugars in tissue associated with depletion of starch, and enhanced acid phosphatase in exposed plants. Constancy in chlorophyll level and rate of CO₂ fixation, together with the absence of visual symptoms, suggest the resistant nature of the chilbil tree. ^[33]

Inhibition of beta-lactamase by 1,4-naphthalenedione
The most important mechanism of the beta-lactam antibiotic resistance is the destruction of the antibiotics by the enzyme beta-lactamase. Use of beta-lactamase inhibitors in combination with antibiotics is one of the successful antibacterial strategies. The inhibitory effect of a phytochemical, 1,4-naphthalenedione, an antibacterial principle, isolated from the plant Holoptelea integrifolia on beta-lactamase is reported. This compound was found to have a synergistic effect with the antibiotic amoxicillin against a resistant strain of Staphylococcus aureus. Hence, the compound can serve as a potential lead compound for the development of effective beta-lactamase inhibitor that can be used against beta-lactam-resistant microbial strains. ^[34]

Antibacterial activity
Klebsiella pneumoniae is lately emerging as an important cause of neonatal nosocomial infection. Klebsiella pneumoniae is clinically the most important member of the Klebsiella genus of Entereobacteriaceae. New antibiotic resistant strains of Klebsiella pneumoniae are appearing and it is increasingly found as a nosocomial infection. Klebsiella pneumoniae can cause bacterial pneumonia, though it is more commonly implicated in hospital acquired urinary track and would infections, particularly in immunocompromised individuals. It is an opportunistic pathogen for patients with chronic pulmonary disease, enteric pathogenicity, nasal mucosa atrophy and rhinoscleroma. Ethnobotanical information of the plant species showed that the acetone extracts’s antibacterial activity against K. pneumonia. ^[35]

CONCLUSION
Holoptelea integrifolia (Roxb) Planch, the versatile medicinal plant is the unique source of various types of compounds having diverse chemical structure. The multidisciplinary approach to the study of fresh mature leaf of H. integrifolia does help in understanding their identification, taxonomical features and medicinal importance. The chromogenic testing showed the presence of terpenoid, steroids, tannins, saponins, carbohydrates and protein in the leaves. These identification standards suggest that it could be helpful in utilization of this plant in herbal formulations, as a medicine and as pharmaceutical raw material. A significant amount of research has already been carried out during the past few decades in exploring the chemistry of different parts of the plant, which generates enough encouragement among the scientists in exploring more information about this medicinal plant. An extensive research and development work should be undertaken on plant and its products for their better economic and therapeutic utilization. Therefore this review might be helpful for scientists and researches to find out new chemical entities responsible for its claimed traditional activities.

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