Hilliardiella elaeagnoides: Review of its Medicinal uses, Phytochemistry and Pharmacological properties

 

Alfred Maroyi

Department of Botany, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa.

 

ABSTRACT:

Hilliardiella elaeagnoides is a herbaceous plant species used as traditional medicine in southern Africa. The current investigation is aimed at reviewing the phytochemistry, pharmacological properties and medicinal uses of H. elaeagnoides. Results of the current study are based on literature search on phytochemistry, pharmacological properties and medicinal uses of H. elaeagnoides using several internet sources such as Scopus, Elsevier, SciFinder, Google Scholar, Pubmed, Science Direct and Web of Science. Other sources of information included pre-electronic sources such as journal articles, theses, book chapters, books and other scientific publications obtained from the University library. The current study showed that H. elaeagnoides is used as appetite stimulant, colic, protective charm and purgative, and traditional medicine for wounds, malaria, ulcerative colitis, dysentery, malaise, diarrhoea, stomach problems, constipation, rheumatism and abdominal pains. Ethnopharmacological research identified tannins, sesquiterpene lactones, steroids, alkaloids, amino acids, glycosides, flavonoids, polyphenols, saponins and triterpenoids from the aerial parts, leaves, roots, stems and whole plant parts of H. elaeagnoides. The leaf and root extracts of the species and compounds identified from H. elaeagnoides exhibited acetylcholinesterase (AChE), butyrylcholinesterase (BChE), antibacterial, antiplasmodial, antidiabetic, antioxidant, anti-inflammatory, antiprotozoal, antiulcer, cytotoxicity and bitterness activities. The crude extracts and compounds isolated from the species should be evaluated for detailed pharmacological and toxicological studies aimed at correlating the medicinal applications with ethnopharmacological properties of the species.

 

 

 

INTRODUCTION:

Hilliardiella elaeagnoides (DC.) N. Swelankomo and J.C. Manning is a perennial herb belonging to the Asteraceae or Compositae family. This species was originally treated under the genus Webbia DC., a generic name that was later treated as a homonym of Vernonia Schreb.¹, a genus that is known to be restricted to North America^2,3. Therefore, the species was later transferred to the genus Hilliardiella H. Rob.^2,3

 

 

Synonyms associated with the name H. elaeagnoides include Cacalia elaeagnoides (DC). Kuntze, Webbia oligocephala DC., Webbia elaeagnoides DC., Vernonia elaeagnoides (DC.) Sch. Bip. ex Walp., Vernonia krausii Sch. Bip. ex Walp., Hilliardiella oligocephala (DC.) H. Rob. and Vernonia oligocephala (DC.) Sch. Bip. ex Walp.^1,3,4 The English common names of H. elaeagnoides include “silver-haired vernonia” and “bicoloured-leaved vernonia”. The genus name Hilliardiella is in honour of Dr Olive May Hilliard (nee Hillary), a South African botanist and taxonomist. The epithet “elaeagnoides” means “resembling species Elaeagnus angustifolia L.” often known as oleaster, Russian olive or trebizond date⁵.

 

Hilliardiella elaeagnoides is a herbaceous perennial growing up to one metre in height⁴. Hilliardiella elaeagnoides has many erect stems growing from a perennial woody rootstock. The leaves of the species are almost stalkless, alternate, ovate to lanceolate in shape, upper surface smooth to thinly covered with hairs and the lower surface covered with silver hairs. This marked difference between the upper and lower surfaces is a useful characteristic, together with leaf shape that is often used to distinguish the plant species from its closely related species⁶. The bright violet flower heads are borne in large groups, clustered together in flat-topped groups at the ends of flowering shoots and bracts. The fruit is an achene with sub-cylindric, densely covered with silky hairs. Hilliardiella elaeagnoides has been recorded in wooded grassland, rocky grassland and open savanna areas in the Democratic Republic of Congo (DRC), Eswatini, Botswana, Lesotho, Namibia, South Africa, Zambia, Mozambique and Zimbabwe at altitude which ranged from sea level to 2338 m above sea level.^1,3,4,7-9 Hilliardiella elaeagnoides is possibly naturalized in the Cholistan desert in Pakistan^10-14 and India.¹⁵ The leaves, roots and twigs of H. elaeagnoides are used as tea and vegetable in southern Africa.^16-20 The stems, twigs and leaves of H. elaeagnoides are sold as traditional medicines in informal herbal medicine markets in Gauteng and KwaZulu-Natal provinces in South Africa.²¹. Research by Van Wyk²² carried out in South Africa revealed that the leaves of H. elaeagnoides have the potential in the pharmaceutical development of health products such as bitter tonic and stomachic in the country. Medicinal plants used to manage and treat human diseases play a crucial role in the primary healthcare of local communities in developing countries.^23-32 It is therefore, within this background that the current study was undertaken aimed at documenting the phytochemistry, pharmacological properties and medicinal uses of H. elaeagnoides.

 

MATERIALS AND METHODS:

Results of the current study are based on literature search on phytochemistry, pharmacological properties and medicinal applications of H. elaeagnoides using information derived from several internet sources which include Google Scholar, Scopus, Elsevier, SciFinder, Pubmed, Science Direct and Web of Science. Other sources of information such as pre-electronic sources which included journal articles, theses, books, book chapters and other scientific articles were gathered from the University library. The keywords used in the search included “Hilliardiella elaeagnoides”, the synonyms of the species “Cacalia elaeagnoides”, “Webbia oligocephala”, “Webbia elaeagnoides”, “Vernonia elaeagnoides”, “Vernonia krausii”, “Vernonia oligocephala” and “Hilliardiella oligocephala”, English common names “silver-haired vernonia” and “bicoloured-leaved vernonia”. The other searches carried out used the keywords “biological properties + H. elaeagnoides”, “ethnobotany + H. elaeagnoides”, “ethnomedicinal uses + H. elaeagnoides”, “ethnopharmacological properties + H. elaeagnoides”, “indigenous knowledge + H. elaeagnoides”, “medicinal uses + H. elaeagnoides”, “pharmacological properties + H. elaeagnoides”, “phyochemistry + H. elaeagnoides” and “traditional uses + H. elaeagnoides”.

 

RESULTS AND DISCUSSION:

Medicinal uses of Hilliardiella elaeagnoides:

The roots, flowers, stems, leaves, whole plant parts and twigs of H. elaeagnoides are widely used as appetite stimulant, colic, protective charm and purgative, and traditional medicines for wounds, malaria, ulcerative colitis, dysentery, malaise, diarrhoea, stomach problems, constipation, rheumatism and abdominal pains (Table 1; Figure 1). Other minor medicinal uses of the species recorded in a single country and based on a single literature record included anthritis³³, asthma²⁸, headache³⁴, hypertension³⁴, nausea³⁵, pain³⁴, sores³⁶, venereal diseases³⁷ and worms³⁵ (Table 1). Hilliardiella elaeagnoides is an important medicinal plant species in South Africa, and the plant species is included in the monograph of “medicinal plants in South Africa”.⁶

 

Table 1: Medicinal uses of Hilliardiella elaeagnoides

Medicinal uses	Parts used	Country	References
Abdominal pain	Leaves and flowers	Eswatini, South Africa and Zimbabwe	[6,10,11,17-19,34-45]
Anthritis	Leaves	South Africa	[33]
Appetite stimulant	Leaves	South Africa	[35,44]
Asthma	Leaves	South Africa	[18]
Colic	Leaves	South Africa	[6,10,11,18,34-36,38,42,43]
Constipation	Leaves	South Africa	[34,35,44,45]
Diabetes	Leaves, roots and twigs	Eswatini and South Africa	[6,16,17,19,33,34,36,38,40,42-54]
Diarrhoea	Leaves and roots	Eswatini and South Africa	[34-37,43-45,55,56]
Dysentery	Leaves	South Africa	[6,33-36,38,40,42-44,47]
Headache	Leaves	South Africa	[34]
Hypertension	Leaves	South Africa	[34]
Malaise	Leaves	Eswatini and South Africa	[16,43,44]
Malaria	Leaves	South Africa	[43,57-59]
Nausea	Leaves	South Africa	[35]
Pain	Leaves	South Africa	[34]
Protective charm	Whole plant	Eswatini, Lesotho and South Africa	[16-19,40,60-63]
Purgative	Leaves	South Africa	[34,38,45]
Rheumatism	Leaves	Eswatini, South Africa and Zambia	[6,16,19,34-36,38,40,42-45,47,50]
Sores	Leaves	South Africa	[36]
Stomach problems	Leaves	Lesotho and South Africa	[6,11,17-19,34,38,40,43,47,50,53,64-67]
Ulcerative colitis	Leaves	South Africa	[6,10,17,35,38,43-45,47]
Venereal diseases	Roots	Eswatini	[37]
Worms	Leaves	South Africa	[35]
Wounds	Leaves and stems	South Africa	[18,68]

 

Figure 1: Medicinal applications of Hilliardiella elaeagnoides derived from literature records

 

Phytochemistry of Hilliardiella elaeagnoides:

Bohlman et al.⁶⁹ isolated three sesquiterpene lactones, 8α-(2-hydroxymethyl acryloyloxy)-hirsutinolide-13-O-acetate and glaucolides 17,18-epoxyvernonataloide and stilpnotomentolide-8-O-[4-hydroxy-methacrylate] from the aerial parts of H. elaeagnoides. Riaz et al.¹⁰ identified 3β-acetoxyneohop13(18)-ene, β-sitosterol, 3β-hydroxylup-20,29-ene, 3β-hydroxyolean-12-en-28-oic acid and β-sitosterol-3-O-β-D-glucopyranoside from the whole plant parts of H. elaeagnoides. Mustafa⁷⁰ identified 3β-acetoxyneohop13(18)-ene, β-sitosterol, 3β-hydroxyolean-12-en-28-oic acid, 5,7,4'-trihydroxyflavone, apigenin-7-p-coumerate, kaemferol, isorhamnetin, β-sitosterol 3-O-β-D-glucopyranoside and quercetin from the whole plant parts of H. elaeagnoides. Other phytochemicals identified from the roots of H. elaeagnoides include alkaloids, flavonoids, glycosides, polyphenols, saponins, steroids, tannins, terpenoids and triterpenoids.^11,12,14,55. The leaves and stems of H. elaeagnoides are rich in amino acids with high amounts²⁵ and these include tryptophan (10.8–28.0 mg/g), isoleucine (2.1–31.4mg/g), allo-isoleucine (5.2– 35.2mg/g), Threonine (<0.2–36.3mg/g), alanine (0.7– 48.6mg/g), aspartic acid (0.6–58.2mg/g), phenylalanine (8.6–62.4mg/g), glutamic acid (3.1–73.7mg/g), serine (0.9–78.5mg/g), Valine (2.3–104.3mg/g), asparagine (13.5–361.1mg/g) and proline (12.1–489.5mg/g) (Table 2), giving the species a high nutritional value.

 

Table 2: Amino acid content of Hilliardiella elaeagnoides leaves and stems³⁵

Amino acid	Value (mg/g)
Alanine	0.7 – 48.6
Allo-isoleucine	5.2 – 35.2
α-Aminoadipic acid	2.4 – 7.6
α-Aminobutyric acid	0.8 – 3.1
γ-Aminobutyric acid	1.0 – 7.4
β-Aminoisobutyric acid	2.8 – 5.0
Asparagine	13.5 – 361.1
Aspartic acid	0.6 – 58.2
Cysteine	9.3 – 9.5
Glutamic acid	3.1 – 73.7
Glutamine	3.3
Glycine	<0.02 – 7.3
Histidine	9.0 – 12.2
Isoleucine	2.1 – 31.4
Lysine	9.6 – 17.3
Ornithine	8.1 – 9.6
Phenylalanine	8.6 – 62.4
Proline	12.1 – 489.5
Sarcosine	<0.02
Serine	0.9 – 78.5
Threonine	<0.2 – 36.3
Tryptophan	10.8 – 28.0
Tyrosine	4.5 – 17.9
Valine	2.3 – 104.3

 

Pharmacological properties of Hilliardiella elaeagnoides:

The following biological activities have been reported from the leaf and root extracts of H. elaeagnoides and compounds isolated from the species: acetylcholinesterase (AChE) and butyrylcholinesterase (BChE)^13,14, antibacterial^12;71, antidiabetic¹⁰, antioxidant^12,14, anti-inflammatory¹⁴, antiplasmodial^57,72, antiprotozoal⁷², antiulcer^11,14, bitterness⁷³ and cytotoxicity⁷² activities.

 

Acetylcholinesterase (AChE) and butyrylcholinesterase (BChE) activities:

Mahmood et al.¹³ evaluated the acetylcholinestrase (AChE) and butyrylcholinestrase (BChE) enzyme inhibitory activities of methanol, n-hexane, dichloromethane, ethyl acetate and n-butanol extracts of H. elaeagnoides leaves using the ELISA microtiter plate reader assay. All the extracts were moderately active against both enzymes with the ethyl acetate extract showing the highest inhibition against AChE and BChE with half maximal inhibitory concentration (IC₅₀) values of 128.8µg/mL and 145.7µg/mL, respectively.¹³ Mahmood et al.¹⁴ evaluated the acetylcholinesterase (AChE) and butyrylcholinesterase (BChE) enzyme inhibitory activities of methanol, dichloromethane, ethyl acetate, n-hexane and n-butanol extracts of H. elaeagnoides roots using acetylcholinesterase inhibitory enzyme from eel fish and butyrylcholinesterase inhibitory enzyme from equine serum assays with eserine as a positive control. The hexane and ethyl acetate extracts showed maximum AChE inhibition with IC₅₀ values of 215.0μg/mL and 302μg/mL, respectively. Whereas, the n-hexane and n-butanol fractions showed highest BChE inhibition with IC₅₀ values of 159.1 μg/mL and, 163.9μg/mL, respectively.¹⁴

 

Antibacterial activities:

Rana¹² evaluated the antibacterial activities of the aqueous methanolic crude extract of roots of H. elaeagnoides against Bacillus subtilis, Bacillus pumilus, Escherichia coli, Staphylococcus aureus and Pseudomonas aeruginosa using broth microdilution assay with moxifloxacin (5µg/disc) and gentamicin (10 µg/disc) as positive controls. The extract exhibited activities against all tested pathogens with the exception of Escherichia coli with minimum inhibitory concentration (MIC) values ranging from 14.0µg/ml to 16.4µg/ml.¹² Nkala et al.⁷¹ evaluated antibacterial activities of methanol, dichloromethane and acetone extracts of H. elaeagnoides leaves against Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus and Enterococcus faecalis using microplate dilution method with gentamycin as a positive control. The extracts exhibited activities with MIC values ranging from 1.0mg/ml to 2.0mg/ml against tested pathogens which were comparable to MIC values ranging from 0.9 mg/ml to 2.0mg/ml exhibited by the positive control. The minimum bactericidal concentration (MBC) values ranged from 0.5mg/ml to 2.0mg/ml against tested pathogens compared to MBC values ranging from 0.06 mg/ml to 2.0mg/ml exhibited by the positive control.⁷¹

 

Antidiabetic activities:

Riaz et al.¹⁰ evaluated the antidiabetic activities of the compounds 3β-acetoxyneohop13(18)-ene, β-sitosterol, 3β-hydroxylup-20,29-ene, 3β-hydroxyolean-12-en-28-oic acid and β-sitosterol-3-O-β-D-glucopyranoside isolated from H. elaeagnoides using the α-glucosidase inhibition assay with acarbose as the standard. Only 3β-acetoxyneohop13(18)-ene exhibited inhibitory activities against enzyme α-glucosidase with IC₅₀ value of 18.5 µM.¹⁰

 

Antioxidant activities:

Rana¹² evaluated the antioxidant activities of the aqueous methanolic crude extract of roots of H. elaeagnoides using the 2,2-diphenyl1-picrylhydrazyl (DPPH) free radical scavenging assay with quercetin as a positive control. The extract exhibited activities with IC₅₀ value of 62.7µg/ml which was higher that IC₅₀ value of 15 µg/ml exhibited by the positive control.¹² Mahmood et al.¹⁴ evaluated the antioxidant activities of methanol, dichloromethane, ethyl acetate, n-hexane and n-butanol extracts of H. elaeagnoides roots using DPPH assay, FRAP (ferric reducing antioxidant power) assay, and total antioxidant capacity using the phosphomolybdenum assay with ascorbic acid as a positive control. In DPPH assay, the ethyl acetate extract exhibited the best activities with IC₅₀ value of 39.1μg/mL in comparison to IC₅₀ value of 17.0μg/mL exhibited by the positive control. The methanol extract exhibited the highest ferric reducing power of 71.9mg GAE/g while ethyl acetate and methanol extracts exhibited the highest total antioxidant capacities of 73.1mg GAE/g and 71.1mg GAE/g, respectively.¹⁴

 

Anti-inflammatory activities:

Mahmood et al.¹⁴ evaluated the anti-inflammatory activities of methanol, dichloromethane, ethyl acetate, n-hexane and n-butanol extracts of H. elaeagnoides roots using the soybean lipoxygenase assay with baicialin as a positive control. Only n-butanol extract exhibited activities with IC₅₀ value of 132.2μg/mL.¹⁴

 

Antiplasmodial activities

Clarkson et al.⁵⁷ evaluated antiplasmodial activities of aqueous, dichloromethane, dichloromethane-methanol (1:1) extracts of H. elaeagnoides leaves and roots against Plasmodium falciparum using the parasite lactate dehydrogenase (pLDH) assay. The dichloromethane-methanol (1:1) extract of the roots exhibited activities with IC₅₀ value of 20.0µg/ml while dichloromethane and dichloromethane-methanol (1:1) extracts of the leaves exhibited activities with IC₅₀ values of 3.5µg/ml and 5.5 µg/ml, respectively.⁵⁷ Mokoka et al.⁷² evaluated antiplasmodial activities of dichloromethane and dichloromethane: methanol (1:1) extracts of H. elaeagnoides leaves against Plasmodium falciparum with benznidazole chloroquine (IC₅₀ = 0.05μM) as a positive control using the ³H-hypoxanthine incorporation assay. The dichloromethane and dichloromethane: methanol (1:1) extracts exhibited activities with IC₅₀ values of 7.7μg/mL and 9.5μg/mL, respectively.⁷²

 

Antiprotozoal activities:

Mokoka et al.⁷² evaluated antiprotozoal activities of dichloromethane and dichloromethane: methanol (1:1) extracts of H. elaeagnoides leaves against Trypanosoma cruzi, Trypanosoma brucei rhodesiense and Leishmania donovani with benznidazole (IC₅₀ = 0.5μg/mL), melarsoprol (IC₅₀ = 0.03μM) and miltfosine (IC₅₀ = 0.2 μg/mL) as reference drugs. Determination of the activities of the extracts against these pathogens was done using Almar Blue, resazurin assay. The extracts exhibited activities with IC₅₀ values ranging from 4.7 μg/mL to 44.5μg/mL.⁷²

 

Antiulcer activities:

Mubashar¹¹ evaluated the antiulcer activities of aqueous methanolic extracts of roots of H. elaeagnoides against aspirin-induced peptic ulcer model with anti-ulcer drug cimetidine (100mg/kg) as the positive control. The extracts exhibited protective activities on the gastric mucosa by reducing the number and severity of lesions in a dose-dependent manner.¹¹ Mahmood et al.¹⁴ evaluated the antiulcer activities of methanol, dichloromethane, ethyl acetate, n-hexane and n-butanol extracts of H. elaeagnoides roots using the jack-bean urease assay with kojic acid as a positive control. The ethyl acetate extract showed activities with IC₅₀ value of 55.9μg/mL followed by n-hexane (IC⁵⁰ = 75.4μg/mL and methanol (IC₅₀ = 145.8μg/mL).¹⁴

 

Bitterness activities:

Olivier and Van Wyk⁷³ evaluated the bitterness values of leaves of H. elaeagnoides using procedures prescribed by the World Health Organisation⁷⁴ and the European Pharmacopoeia⁷⁵ and compared to the bitterness value of quinine hydrochloride set at 200 000. The bitterness value of 10032 was obtained for H. elaeagnoides leaves. Olivier and Van Wyk⁷³ argued that the physiological effects associated with bitter taste of herbal medicines are ascribed to the bitter tonic (amarum) effect which result in the stimulation, secretion of saliva, secretion of gastric juices and secretion of bile through taste stimuli via the nervus vagus. The amarum effect is illustrated by an extremely bitter plant species, Gentiana lutea L. with bitterness value of 10 000 – 30 000⁷⁶. Therefore, the bitterness value of 10032 exhibited by H. elaeagnoides leaves was categorized as extremely bitter by Olivier and Van Wyk.⁷³

 

Cytotoxicity activities:

Mokoka et al.⁷² evaluated the cytotoxicity activities of dichloromethane and dichloromethane: methanol (1:1) extracts of H. elaeagnoides leaves against the rat myoblast L6 cells with podophyllotoxin (IC₅₀ = 0.05 μM) as a reference drug. The dichloromethane and dichloromethane: methanol (1:1) extracts exhibited activities with IC₅₀ values of 6.5μg/mL and 22.3μg/mL, respectively.⁷²

 

CONCLUSION:

The present review summarizes the medicinal uses, phytochemistry and pharmacological properties of H. elaeagnoides. Although H. elaeagnoides has been the subject of phytochemical and pharmacological research, there is not yet enough data correlating the ethnomedicinal uses of the species with its phytochemical and pharmacological properties. Detailed studies on the pharmacokinetics, in vivo and clinical research involving both extracts and compounds isolated from the species are required. Therefore, future research should focus on the molecular modes or mechanisms of action, pharmacokinetics and physiological pathways for specific extracts of the species including identification of the bioactive compounds of the species and their associated pharmacological activities.

 

CONFLICT OF INTEREST:

No conflict of interest is associated with this work.

 

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Received on 16.02.2020           Modified on 01.04.2020

Accepted on 13.05.2020         © RJPT All right reserved