ABSTRACT
The genus Avicennia comprises eight species of mangrove trees that occur in intertidal zones of estuaries and seabeds found in tropical and temperate regions spanning throughout the world. The plants belonging to the genus have both ecological and economic benefits. Different parts of the plants have ethnomedicinal applications for treatment of various diseases such as cancer, diabetes, malaria, rheumatism, asthma, small pox and ulcer. Pharmacological investigations have revealed antimicrobial, antioxidant, anticancer, antidiabetic, anti-inflammatory activities and so on in these plants. The genus possesses some unique metabolites of varied chemicals classes, which are responsible for their wide range of pharmacological activities. The presence of different bioactive compounds such as alkaloids, flavonoids, phenols, saponins, tannins, glycosides and terpenoids has been detected. Hence, there is a great scope to discover new biological active phytochemicals from different mangrove species of genus Avicennia. Although many research articles have been published on various pharmacological aspects of different plants of the genus, no comprehensive review is yet available pertaining to their ethnomedicinal uses, chemical constituents and pharmacological activities. The present article discusses the diversity as well as distribution of different species of genus Avicennia along with an in-depth coverage of their ethnomedicinal uses, phytochemical and pharmacological profiles.
Introduction
The mangroves are a taxonomically diverse group of halophytic plant communities that are found in the intertidal zones between land and sea of tropical and sub-tropical region of the world (Tomlinson Citation1986; Ravishankar et al. Citation2004). These plants are highly specialized, flourishing under inhospitable environment conditions of extreme tides, high salinity, high temperature, strong winds and anaerobic soil (Mazda et al. Citation2005). Exhibition of well-developed morphological and physiological features is the key to their survival in the adverse environmental conditions. Over the years, local communities inhabiting the mangrove forests exploit different mangrove plants for woods and disease treatment (Kathiresan & Ramanathan Citation1997). In medicinal literatures, only a handful of mangrove plants such as Acanthus illicifolius, Excoecaria agallocha, Rhizophora apiculata, R. mucronata and Sonneratia caseolaris are listed as endowed with medicinal properties (Bandaranayake Citation1998). However, in recent pharmacological investigations, different extracts prepared from other mangrove plants have proved their medicinal effect against a wide array of human, animal and plant diseases.
In total, there are about 84 mangrove plant species belonging to 24 genera and 16 families distributed throughout the world, out of which only 70 species are reported as true mangroves and the rest 14 as mangrove associates (Jun et al. Citation2008). Avicennia is the lone mangrove genus that occurs throughout the world. Along with Rizophora, they form the dominant plant communities of mangrove forests (Duke Citation1991). The wood of Avicennia plant is commonly used as fuel and for construction, while the high tannin content in the bark is used in dyeing and leather production. Leaves can be fed to cattle as fodder as well as used for the preparation of doors and mats. The fruits are used as an insect repellent and pneumatophores for the production of bottle stoppers and floats (Bandaranayake Citation1998, Citation2002; Kathiresan & Bingham Citation2001). There are also reports that document the importance of various parts of Avicennia species as ethnomedicinal. It has been mentioned in the ancient literatures that the tea prepared from the bark of some of its species is believed to treat a variety of digestive disorders like peptic ulcers, diarrhoea including haemorrhoids, rheumatic pain and so on (Bandaranayake Citation1998; Sumithra et al. Citation2011a; Thirunavukkarasu et al. Citation2011). Recent pharmacological investigations have also reported diverse medicinal properties of the plants belonging to the genus Avicennia against cancer, HIV, hepatitis, diabetes, inflammation, diarrhoea, oxidative stress-related diseases and so on (Rege et al. Citation2010; Sharief & Umamaheswararao Citation2011; Shafie et al. Citation2013). Besides, several metabolites, such as alkaloids, phenols, flavonoids, tannins, iridoid glucosides and terpenoids, have been identified from these plants, which could be attributed towards the medicinal properties of these plants (Bandaranayake Citation2002). The present review provides a comprehensive overview of distribution and diversity of the genus Avicennia along with updates on ethnomedicinal uses and bioactive profile of these groups of plants showing immense potential for their pharmaceutical applications. Besides, the present review will also provide a baseline of information on the medicinal potentials of these plants by bridging the gap between ethnomedicinal uses and modern scientific studies of the genus, by critically evaluating the available fragmented literatures on ethnomedicine, pharmacology and photochemistry.
Botanical description and distribution
The genus Avicennia (L.) is named after Avicenna or Abdallah Ibn Sina (980-1037 AD), a Persian physician (Quattrocchi Citation2000). The genus Avicennia has been placed in the division of Tracheophyta, sub-division Spermatophytina, class Magnoliopsida and order Lamiales. The assignment of family to the genus Avcennia has long been contagious. Earlier authors had reported that Avicennia belongs to family Verbenaceae (Fauvel et al. Citation1993; Green Citation1994). Over the years, many botanists have tried to elucidate the taxonomical classification of the genus through their classical investigations, accounting its propinquity to family Avicenniaceae (Bandaranayake Citation1998; Jun et al. Citation2008; Sharief et al. Citation2014a; http://www.iucnredlist.org/ [cited 2016 Jan 12]). On the contrary, modern molecular studies and phylogenetic relationships indicate that the genus has closer proximity towards the family Acanthaceae (Schwarzbach & McDade Citation2002; http://www.theplantlist.org2013 [cited 2016 Jan 12]). The diversity along with the distribution of the genus has evolved over the years. Earlier authors reported that distribution and occurrence of Avicennia species could broadly be classified into two geographical areas, Indo-Western Pacific (Old world) and Atlantic eastern Pacific (New world). Bakhuizen van den Brink (Citation1921) first reported the occurrence of two Avicennia species in these geographical locations. Later, botanical investigations carried out by Watson (Citation1928) reported the occurrence of four species. Since then, the diversity of the genus remained unchanged until Moldenke (Citation1980) reported additional taxa along with some new varieties. According to the botanical report, five species of the genus are confined to the area of Indo-western Pacific region (old world) and subsequently three more species were also reported in the region (Duke Citation1991). Later, Tomlinson (Citation1986) presented a detailed report on the diversity of genus Avicennia accounting eight species along with their putative ones and varieties. In a recent breakthrough, the phylogenetic analysis (www.theplantliest.org 2013) revealed that though genus Avicennia contains eight species, yet some of them that were reported earlier are either variety or have evolved differently with respect to their morphological adaptations pertaining to leaf and roots in different geographical locations. Based on the concurrence of phylogenetic evolution, the latest comprehensive and updated checklist database prepared by joint collaboration between the Royal Botanic Gardens, Kew and Missouri Botanical Garden and others states that the genus Avicennia consists of eight species, namely Avicennia balanophora Stapf & Moldenke., Avicennia bicolor Standl., Avicennia germinans (L.) L., Avicennia integra N.C. Duke., Avicennia marina (Forssk.) Vierh., Avicennia officinalis L., Avicennia schaueriana Stapf & Leechm. ex Moldenke and Avicennia tonduzii Moldenke (http://www.theplantlist.org/). The species variance has been reported in species A. germinans, A. marina and A. schaueriana (www.the plantlist.org 2013). Based on this this evidence, systematic details of species and species variance of the genus are prepared and presented in Table .
Table 1 . Avicennia species variance and distribution.
Avicennia plants have worldwide occurrence. They are densely distributed mangrove species found in both coastal river and seabeds of tropical as well as temperate regions (Tomlinson Citation1986). Five species of the genus viz A. bicolor, A. germinans, A. marina, A. officinalis and A. schaueriana are reported to have varied distribution in tropical and subtropical regions of both North and South America including Colombia, Costa Rica, Mexico; Panama, Brazil, Chile; coast of Africa; Middle East; South and South east Asia which includes Coast of India, Bangladesh, Malaysia, Vietnam, Thailand, Indonesia; and coast of TransAsia countries Australia and New Zealand (www.icunlist.org 2016). However, A. balanophora and A. integra, both have restricted distribution to coastline of Australia, whereas A. tonduzii is found only in pacific coast of Costa Rica. In these regions, the Avicennia species grow in pure and dense stands on mud flats along the coast, in brackish coastal swamps, and on riverbanks (Tomlinson Citation1986).
The different species of Avicennia have evolved differently and therefore have varied taxonomical descriptions. Among different species of the genus, A. germinans and A. integra are the largest and the smallest trees, respectively (Duke Citation1991). A. germinans, which may grow up to 30–50 m tall, has a thick bark which is dark brown or blackish colour with rough irregular flattened scales. The plant possesses special and modified pencil-like pneumatophores that reach 4–9 ft deep in oxygen-deficient (anaerobic) mud for sufficient aeration. Leaves are 3–15 cm long, elliptical, opposite, thick/ leathery with glands on the upper side and are dark green above and greyish beneath. Flowers form auxiliary clusters, 1–2 cm in diameter and are white in colour. Fruits are 2–3 cm in diameter, flat, dark green and with velvety pericarp beneath (Tomlinson Citation1986; Duke Citation1991). On the other hand, A. inetgra can grow either as a 2-m shrub or as a 7-m tall tree. Its bark is brown to reddish in colour, smooth in texture in small plants, whereas the same is pustular in larger ones. Roots produce 20–30 cm short, pencil-like pneumatophores. Leaves are 5–14 cm long, simple, opposite, ovate–elliptic in shape, shiny green upper, and pale and fine lower surface. Its flowers are zygomorphic, golden yellow or orange, 11–13 mm long with 4–5 calyx lobes, mostly 4 petals and 4–5 stamens. The fruits are pale green, furry, compressed ovoid pods, 21–23 mm long and 12–15 mm wide with a persisting calyx (Tomlinson Citation1986).
A. marina is a medium-length (3–11 m tall) Avicennia plant. The bark of the plant is mottled greenish yellow in colour, with smooth, flaky and peeling patches. The roots have short 10–15 cm pneumatophores that are slender with pointed tips. Leaves are shiny, leathery, yellowish green above and dull pale below. The flowers of A. marina are 4 mm in diameter and form tight bunches at the ends of a cross-like inflorescence with yellow petals. The fruits are 20–25 mm in diameter, pale grey green, compressed, oval-shaped and two-valved capsule (Tomlinson Citation1986; Sharief et al. Citation2014a, Citation2014b). These are botanical features commonly found in different A. marina species or varieties. However, complexity arose during taxonomical classification of one of its varieties, A alba. Over the years, many researchers have placed the variety as one of the species of genus Avicennia (Bandaranayake Citation2002; Jun et al. Citation2008; Sharief & Umamaheswararao Citation2011). New findings and phylogenetic analysis have revealed that A. alba has close resemblance to A. marina and taxonomically has been placed as one of latter’s variety (www.theplantlist.org 2013).
A. officinalis is a 12-m tall tree with smooth lenticels, light coloured but do not have fissured barks. It has 8–20 cm long, pencil-like pneumatophores, aerial stilt roots. The leaves are 8–10 cm long, spoon-shaped, upper side glossy green, underside finely hairy, with salt crystals found in the surface, especially in dry weather. The flower of A. officinalis is 1 cm in diameter, being the largest among all the species of its genus. The flower is orange–yellow, globular in shape with rancid or fetid smell. The fruits of the plant are 2–3 cm long, oval slightly beaked, smooth velvety, contains a single seed which completely fills the capsule (Tomlinson Citation1986; Sharief et al. Citation2014a, Citation2014b).
A. bicolor is 8–20 m tall tree and can be recognized by its dense and dark green crown. Its flowers are distinctly zygomorphic and like those of A. germinans have petals which are hairy inside, but are much smaller, scarcely 5–6 mm in diameter, and expanded. The white corolla sometimes has yellow throat, hence the name bicolour. A distinctive feature is the inequality of the stamens, formed inside at the same level as in the flower. The filaments of outer pair are at least 1 mm long compared with the inner pair, which is 0.5 mm long (Tomlinson Citation1986).
A. schauerina has flowers larger than of A. bicolor, the corolla being 10–12 mm long and almost as wide, and resemble those of A. germinans in size, but the inner face of the corolla is glabrous or at most slightly hairy. The lobes are narrow and are not reflexed and so enclose the equal stamens with filaments 1.5 to 2 mm long. The ovary is uniformly hairy but not beaked. The fruit is pale sap green, seldom with purple tinge, and is flatter and more pointed than that of A. germinans (Tomlinson Citation1986).
In comparison to other previously reported species, not much detailed morphological analysis has been carried out on remaining two species, A. tonduzii and A. balanosphora. Earlier reports had taxonomically addressed A. tonduzii as a variant of A. biolor. However, A. tonduzii was later considered and placed as a separate Avicennia species for its narrow leaves, and the paniculate assemblages of floral axes with the individual flower pairs, which remain distant from each other. A. balanosphora is distinguished from other species of its genus by its characteristic fruit. It is recognizable by its oblong, acorn (fruit) and the corolla limb growing to 6 mm wide during anthesis (Tomlinson Citation1986).
Ethnomedicinal uses
The available literatures have reported that most of the Avicennia species have been traditionally used as a medicine for a wide array of diseases worldwide by the local communities inhabiting the mangrove forests (Bandaranayake Citation2002, Das et al. Citation2016). From many of the ethnomedicinal uses of the genus, the widest applications have been in the treatment of rheumatism, pregnancy, ulcer and smallpox (Bandaranayake Citation2002). Different parts of the plant such as leaf, bark/stem, seeds, roots and fruits have been exploited over the years for the treatment of various diseases (Shilpi et al. Citation2012; Simlai & Roy Citation2013). Plants like Avicennia alba Blume (a variant to A. marina), A. marina, A. nitida and A. officinalis are reported to have been widely used against treatment of many diseases which are documented and presented in Table . A number of reports are available for ethnomedicinal uses of different species of Avicennia plants for the treatment of different diseases (Rollet Citation1981; Fauvel et al. Citation1993, Citation1995; Bandaranayake Citation1998, Citation2002; Ito et al. Citation2000; Sumithra et al. Citation2011a; Thirunavukkarasu et al. Citation2011; Kar et al. Citation2014b). In addition, inhabitants of Soutt east Asia use the flowers of Avicennia rumphiana Hallier f to produce some of the best honey in the world, which is enriched with antibacterial as well as antioxidant properties (Field Citation1995).
Table 2. Ethnomedicinal uses of Avicennia sp.
Phytochemistry
In search of novel and natural drugs from natural resources, recent focus has been made on marine plants, especially mangrove as an alternative source of therapeutically important chemicals (Harvey Citation2000). Many reports have documented that the genus Avicennia possesses some unique metabolites of varied chemical classes, which may be responsible for their wide range of pharmacological activities (Ganesh & Jannet Citation2011; Shanmugapriya et al. Citation2012; Poompozhil & Kumarasamy (Citation2014). Phytochemical screening of various solvent extracts from the genus such as methanol, ethanol, ethyl ether, acetone, hexane, chloroform, benzene, aqueous, and ethyl acetate has indicated the presence of diverse and novel phytochemicals like alkaloids, terpenoids, steroids, phenolics, saponins, flavonoids, tannins, steroid and glycosides. The detailed list of isolated phytochemcials from different solvent extracts has been complied and presented in Table .
Table 3. List of various classes of phytochemicals present in Avicennia sp.
The first investigation on the chemistry of genus Avicennia can be traced back to 1913, when Bournot characterized lapachol from the wood of the Indian and West African A. tomentosa (Bournot Citation1913). As listed in Table , a total of 14 flavonoids including flavones, 19 naphthalene derivatives, 5 terpenoids, 7 steroids, 23 tannins 6 fatty acids, 31 glucosides from wide variety of secondary metabolite classes have been listed to date in genus Avicennia (Majumdar et al. Citation1981; Sharaf et al. Citation2000; Jia et al. Citation2004; Feng et al. Citation2007). Phytochemical studies have revealed that most chemically investigated Avicennia species till now are rich in phytochemicals, namely terpenoids, glucosides and naphthalene derivatives (Konig & Rimpler Citation1985; Sutton et al. Citation1985; Shaker et al. 2001; Han et al. Citation2007). These naturally occurring compounds are found to be concentrated in the plant’s leaf, stem/bark and aerial roots. A number of pharmacologically important phyto-constituents belonging to different classes of phytochemicals which have been isolated include flavonoids (3); naphthalene derivatives (20, 22 23, 24, 30, 31); tannins (35, 36, 37, 38); steroids (41); terpenoids (49, 55, 56, 67); and fatty acids (69, 70, 71, 73, 74) (Konig et al. Citation1994; Gonzales et al. Citation2000; Ramirez & Roa Citation2003; Han et al. Citation2007, Citation2008; Manilal et al. Citation2009, Sumithra et al. Citation2011b; Hossain et al. Citation2012; Mahera et al. Citation2013; Jain et al. Citation2014; Ramanjaneyulu et al. Citation2015). A detailed report on their occurrence, chemical structure and bioactivity has been presented in Table . In the context of phytochemistry, though occurrence of many phytochemicals and biologically active phytoconstituents has been reported in the genus, it can only be conclusive when the same has been evaluated in all remaining solvent extracts along with other phytochemically unexplored species of the genus as well. In view of this, an extensive phytochemical investigation is necessary for isolating chemical compounds/constituents from each solvent extract and for understanding their biological/pharmacological action for pharmacological use.
Table 4. Phytoconstituents isolated from Avicennia sp.
Table 5. Important phytoconstituents of Avicennia sp. with pharmacological properties.
Pharmacological activities
In recent times, a number of pharmacological studies have reported medicinal uses of Avicennia plants, through validation and exploring bioactivity of each plant through in vitro and in vivo studies. Among eight species along with their synonyms or variants, A. alba, A. marina and A. officinalis are the plants with maximum pharmacological reports. However, bioactive principle(s) responsible for exhibiting such pharmacological effects need(s) to be reported and studied in detail. Undertaking detailed pharmacological studies involving elucidation of active chemical constituents will contribute immensely to medicinal science for the treatment of different diseases. The pharmacological activity and mode of action of extracts prepared from different parts of Avicennia plants are presented in Table .
Table 6 Pharmacological activity of Avicennia sp.
Antimicrobial
Antibacterial activities of species like A. alba, A. marina, A. officinalis and A. schaueriana have been widely studied. Using agar well and disc diffusion methods, the antibacterial activity of leaf and bark extracts of A. alba in different solvents has been studied against eight Gram-positive and six Gram-negative bacteria. The acetone, benzene, chloroform, ethyl acetate, hexane and methanol leaf and bark extracts of the plant are reported to exhibit antibacterial activity selectively against S. entrica, A. proptophormiae, A. tumefaciens, P. mirabilis, P. aeruginosa, R. rhodochrous, B. subtilis, P. vulgaris, S. mutans, S.aureus and A. faecalis, in comparison with standard tested bacterial antibiotics (Nagababu & Umamaheswararao Citation2012; Satyaveni et al. Citation2013; Bakshi & Chaudhuri Citation2014). The leaf extracts of A. marina (acetone, chloroform, hexane, methanol, ethanol, ethyl acetate) have been reported to exhibit antibacterial activity selectively against bacteria such as A. tumefaciens, Bacillus cereus, E. faecalis, E. coli, S. aureus, S. mutans, K. pneumonia, P. aeruginosa, B. subtilis, Staphylococcus sp., Proteus sp., Pseudomonas sp. and Shigella sp (Kumar et al. Citation2011; Afzal et al. Citation2011, Devi et al. Citation2012; Shanmugapriya et al. Citation2012; Bakshi & Chaudhuri Citation2014; Sharief & Umamaheswararao Citation2014). However, later, the charcoal-treated leaf extracts of A. marina were seen to exhibit higher growth inhibition against the same bacterial strains (reference). In another study, various stem extracts (petroleum ether, benzene, ethyl acetate and ethanol) of A. marina have been reported for their antibacterial activity against P. mirabilis, S. paratyphi, E. coli, S. aureus and B. subtilis (Ruba et al. Citation2013). Various solvent extracts of A. officinalis leaf are also reported with a high percentage of antibacterial activity. The acetone, ethyl acetate and methanol leaf extracts of A. officnials plant showed antimicrobial activity with 21–25 mm zone of inhibition against various human pathogenic strains such as A. tumefaciens, S. mutans S. aureus, K. pneumonia, P. aeruginosa, B. subtilis and E. coli (Valentin et al. Citation2010; Shanmugapriya et al. Citation2012; Bakshi & Chaudhuri Citation2014). Methanol and ethanol extracts from its fruit also exhibited higher antibacterial activity with MIC values ranging between 1.25 and 5.0 mg/100 μl against bacterial species, namely E. coli, E. Aerogenes, K. pneumonia, L. delbrueckii, P. aeruginosa, B. subtilis, S. aureus and S. pyogenes (Sharief & Umamaheswararao Citation2014). Similarly, stem extracts of A. officinalis in acetone, methanol, ethanol, benzene, ethyl acetate were also active against E coli, E. aerogenes, K. pneumoniae, P. aeruginosa, B. subtilis, L. delbrueckii, S. aureus and S. pyogenes with varying zone of inhibition ranging from 11.33 to 18.00 mm (Sharief & Umamaheswararao Citation2011). The various fruit and root solvent extracts of A. officinalis also showed strong antimicrobial activity against various pathogenic bacteria as listed in Table against E. coli, E. aerogenes, K. pneumoniae, P. aeruginosa, B. subtilis, L. delbrueckii, S. aureus and S. pyogenes, B. cereus and E. Faecalis, E. cloacae, P. vulgaris and so on (Sharief & Umamaheswararao Citation2011; Sharief et al. Citation2014b, Citation2015).
Fardin and Young (Citation2015) evaluated a high growth inhibition of A. schaueriana leaf extracts against plant fungal Colletotrichum and Cladosporium sp.. Using thin layer chromatography bioautography, petroleum ether and chloroform fractions of ethanolic stem extract of this plant showed antifungal activity against C. sphaerospermum, C. cladosporioides and C. lagenarium with many active bands in the range of Rf = 0·72 to Rf = 0·55. In another study using agar dilution assay, the ethanolic, petroleum ether crude extract of A. schauceriana stem and column chloroform fractions showed growth inhibition against C. gloeopsporioides. Antifungal activity is also reported in A. marina against Pencillium digitatum, one of the devastating pathogens of citrus fruit. Using agar diffusion method, the ethanol extract of this plants leaf showed 80% inhibition against the pathogen (Behbahani et al. Citation2012). There is a report that hydroalcholic extract of A. marina’s showed inhibitory effect on human fungal pathogen C. albicans. The results showed that the MIC and MFC values for the fungus have noticeable anticandida effects on different species of C. albicans (Panahai et al. Citation2014). Similarly, other extracts such as ethyl acetate and acetone extract of this plant have been reported to exhibit antifungal activity as seen against A. flavus with 6.5 mm zone of inhibition. Antifungal action has also been reported in A. alba. The ethyl acetate leaf extract of the plant was reported to be effective against fungus T. rubrum (Bakshi & Chaudhuri Citation2014).
Few studies have been undertaken to characterize and identify the bioactive principle responsible of antimicrobial activity in Avicennia plants (Han et al. Citation2007, Citation2008; Manilal et al. Citation2009; Chinnappan et al. Citation2013). The antimicrobial effect can be corroborated with the presence of naphthalene derivatives (20, 22, 23, 24), terpenoids (55, 56) in stem extracts and fatty acids (69, 70, 71, 72, 73, 74) in leaf and flower extracts of A. marina. The presence of terpenoid (67) in A. officinalis has also been reported to exhibit the antimicrobial activity.
Antidiarrhoeal
Amongst many species of Avicennia, antidiarrhoeal study has been carried only in A. alba and A. officinalis. The methanol extract of leafs of A. alba was investigated for its possible antidiarrhoeal effect on diarrhoeal animal models. The extract exhibited considerable antidiarrhoeal activity on castor oil-induced diarrhoea in mice, increasing the mean latent period and reducing the frequency of defecation significantly at the oral dosage of 500 mg/kg body weight (p < .001) in comparison with the standard drug Loperamide (50 mg/kg b.w) (Rahman et al. Citation2011). Flavonoids present in the A. officinalis methanol leaf extract are reported to inhibit release of autacoids and prostaglandins, which in turn can inhibit motility and secretion induced by castor oil in castor oil induced diarrhoeal animal model (Ahmed et al. Citation2008). In addition, saponins steroids, alkaloids and glycosides can also exhibit antidiarrhoeal effect (Roome et al. Citation2008). The presence of these phytochemicals was reported through phytochemical screening in methanolic leaf extract of A. alba Table ).
Analgesic and antipyretic
The analgesic and antipyretic properties of A. alba was reported by Kar et al. (Citation2014a). Its methanol leaf extract at a dosage of 200 mg/kg b.w exhibited significant analgesic activity in Albino (Wister) rat model. The radiant heat and tail immersion study showed that the extract modulated the action potential and signal transmission generated from the sensory mediators like delta and C fibres sensory neurons to relive pain (Kar et al. Citation2014a). In another study, the same extract at an oral dosage of 200 mg/kg b.w exhibited significant anti-pyretic effect in yeast-induced rat model. The extract could inhibit prostaglandin by blocking the activity of cyclooxygenase enzyme that causes pyrexia (Shaik et al. Citation2013). The presence of flavonoids in A. alba leaf extracts could be responsible for its antipyretic activity (Kar et al. Citation2014b).
Antiulcer
Peptic ulcer is one of the major gastro-intestinal disorders which occur due to an imbalance between the gastric acid secretion and gastric mucosal integrity factors (Hoogerwerf & Pasricha Citation2006). The antiulcer potential has been reported only in A. officinalis plant. The ethanol (Sura et al. Citation2011), hot and cold aqueous (Thirunavukkarasu et al. Citation2011) and methanol (Aparna et al. Citation2014) leaf extracts of this plant have been reported for antiulcerogenic activities. The ethanol leaf extract at 250 and 500 mg/kg b.w dosages decreased the ulcerative lesion index of indomethacine-induced ulcerative rat by 11.6% and 25.3%, respectively. The antiulcer activity might be due to the antioxidant effect of the plant extract that could reduce glutathione in the gastric mucosa (Sura et al. Citation2011). Furthermore, the ethanol leaf extracts also exhibited dose-dependent antiulcer protection in aspirin-induced ulcer rat model by preventing increased acid secretion in mucosa (Sura et al. Citation2011). Similarly, the gastro protective effect of both hot and cold aqueous leaf extracts at 125 mg/kg dosages was reported in nonsteroidal anti-inflammatory drugs (NSAID)-induced albino Wister rat ulcer model (Thirunavukkarasu et al. Citation2011). In another study, the ulcer protective effect of methanol leaf extract at 200 and 400 mg/kg b.w dosages has been reported in Pylorus Ligated and Ethanol–HCl-induced Wistar albino rats model (Aparna et al. Citation2014). The presence of flavonoids and tannins in leaf extracts was attributed to the antiulcerogenic and cytoprotective effects (Augwa & Nwako Citation1988; Maira et al. Citation2006). In addition, the major polyphenols, polymeric tannins and hydrosable tannins (35), (36), (37), (38) are known for their cytoprotective and antiulcerogenic properties in A. officinalis (Konig et al. Citation1994; Gonzales et al. Citation2000; Ramirez & Roa Citation2003).
Antinoceptive
The antinoceptive property has been reported in A. alba and A. officinalis. The methanol leaf extract of A. alba at an oral dosage of 500 mg/kg b.w increased the levels of PGE2 and PGF2α in the peritoneal using acetic acid-induced writhing mice model (Derardt et al. Citation1980). The extract produced significant writhing inhibition, which was at par with standard drug diclofenac sodium (Rahman et al. Citation2011). Similarly, the ethanol leaf extract of A. officinalis at 250 and 500 mg/kg dosages produced significant writhing inhibition (Shahid et al. Citation2007). The presence of polyphenolic compounds such as flavonoids and tannins, pentacyclic triterpenes, steroids, alkaloids and glycosides in the leaf extracts could be responsible for their antinociceptive activity (Roome et al. Citation2008).
Anti-inflammatory
The anti-inflammatory activity was exhibited by A. marina A. alba, A. officinalis A. and A. tomentosa species. Shafie et al. (Citation2013) reported anti-inflammatory effect of hydro-alcoholic leaf extract of A. marina by using rheumatoid arthritis in Wistar rat model. The extract at 400 mg/kg dosage showed significant reduction in inflammatory markers and improvement in joint lesions (Shafie et al. Citation2013). Polyphenolic compounds present in mangroves can prevent harmful effects of oxidative damage, which are reported to play a critical role in rheumatoid arthritis (Araujo et al. Citation1998). The investigation on anti-inflammatory activity of crude methanol extract of A. officinalis leaf was performed on acute (carrageenin), subacute (Formalin) and chronic (Freunds Complete Adjuvant) rat paw oedema models. The extract at 400 mg/kg dose was found to be more effective and induced significant inhibition in all the three anti-inflammatory models (Sumithra, Anbu et al. Citation2011a). The structural analysis of bioactive principles of the A. officinailis methanol leaf extract displayed the presence of triterpene - betulinic acid (49), which exhibits anti-inflammatory activity in other medicinal plants (Sumithra, Anbu et al. Citation2011a). Betulinic acid was also reported to exhibit anti-inflammatory effect in A. alba A. marina and A. tomentosa (Sumithra, Janjanam et al. Citation2011b; Hossain et al. Citation2012).
Diuretic
Diuretic effect had been reported in A. officinalis. The methanol leaf extract of this plant at 200 and 400 mg/kg dosages showed significant diuretic effect in Swiss Albino using Lipschitz diuretic assay. The extract was able to increase urine volume along with high amount of Na+ and Cl− load, which was comparable to that of standard drug furosemide. (Hossain et al. Citation2012). After treatment with the plant extract, there was also noticeable decrease in the concentration ratio of excreted sodium and potassium ions. This effect marks that the extract has lesser hyperkalaemic side effect but possess essential quality of being a good diuretic agent. Diuretic action of the extract may be due to its effect on the rate of glomerular filtration and inhibitory effect on the reabsorption mechanism of salt.
Neuropharmacological
The neuropharmacological activity has been reported in A. officinalis. The methanolic leaf extracts exhibited the neuropharamacological effect by reducing the onset of sleep and potentiating the sleeping time in pentobarbital-induced mice (Ahmed et al. Citation2008). Furthermore, the leaf extract showed central sedative properties in Swiss-albino mice model by inducing a reduction in behavioural exploration of mice as evidenced by open field, hole cross and head dip test (Hossain et al. Citation2012). The extract reduced the onset of sleep and potentiated the pentobarbital-induced sleeping time in mice, suggesting its probable tranquilizing action (Capasso et al. Citation1996). Later, Ahmed et al. (Citation2008), at an oral dosage of 500 mg/kg b.w methanolic leaf extracts, tested exploratory behaviour in animals in the open field, hole cross and head dip Swiss albino mice models. The result confirmed that the extract has CNS depressant action, as it exerted central sedative properties and reduced exploratory behaviours in mice (Perez et al. Citation1998).
Antiviral/Anti-HIV
The antiviral activity has been reported in leaf extracts of A. marina and A. officinalis. The leaf extracts of A. marina were reported for their antiviral activity against hepatitis B virus (Beula et al. Citation2012) and Encephalomyocarditis virus (Premanathan et al. Citation1999). A. marina’s leaf ethanol extracts have profound antiviral activity against the hepatitis B virus. A. marina’s leaf ethanol extracts displayed inhibitory potential against surface antigen, DNA polymerase and reverse transcriptase of Hepatitis B with IC50 values of 403.91, 489.39 and 372.09 ug/mL, respectively (Beula et al. Citation2012). The leaf extracts of A. officinalis exhibited inhibitory potential against HIV’s reverse transcriptase enzyme, binding of gp120 and interaction of gp120/CD4 (Rege et al. Citation2010).
Anticancer
The anticancer potential has been reported in A. marina and A. officinalis. The ethanol, methanol and aqueous leaf extracts of A. marina were reported for their cytotoxicity activities against HL60, MDA-MB 231, and NCI-H23 cell lines (Karami et al. Citation2012; Sukhramani & Patel Citation2013; Momtazi-borojeni et al. Citation2013) using MTT assay. The cytotoxicity activity can be attributed to the presence of flavonoids (3) having anticancer activity that can kill human promyelocytic leukaemia cells by apoptosis mechanism (Ramanjaneyulu 2015). In addition, the plant is also reported to possess anticancer compounds such (20), (22), (23), (31), (55) and (56) in its stem as well as (49) in its root (Han et al. Citation2007; Sumithra et al. Citation2011b; Hossain et al. Citation2012). Sumithra et al. (Citation2011a), in another anticancer study, reported cytotoxicity activity of A. officinalis in Ehrlich ascitic carcinoma cell lines. The methanol leaf extract of this plant exhibited significant antitumour activity. Increase in life span and normal haematological parameters were seen restored in the affected animals (Sumithra et al. Citation2011a). The anticancerous effect of the plant can be attributed to the presence of tannins (35) (36) (37) (38) in leaf and bark and terpenoid (67) in the root (Konig et al. Citation1994; Gonzales et al. Citation2000; Ramirez & Roa Citation2003; Han et al. Citation2008).
Antioxidant
The antioxidant activity has been reported in A. marina and A. officinalis. Acetone, methanol, ethyl acetate and ethanol extracts of A. marina fruit and leaf were reported for their antioxidant potential, as these could scavenge the ABTS (2,2′-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid)), CrO5 (Chromium peroxide) and FRAP (Ferric reducing ability of plasma) molecules (Sharief et al. Citation2014a, Citation2014b). In another study, the ethyl acetate, ethanol, methanol extracts of pneumatophores (Packia Lincy et al. Citation2013) along with aqueous and ethanolic bark extracts (Packia Lincy et al. Citation2013) of this plant exhibited strong antioxidant activity by scavenging DPPH (2,2-diphenyl-1-picrylhydrazyl), superoxide and ABTS radicals (Selvasundhari et al. Citation2014). Similarly, the acetone, methanol and ethanol fruit extracts of A. officinalis were reported for their capacity to scavenge ABTS, CrO5, DPPH and FRAP (Sharief et al. Citation2014b). Besides, ethanolic leaf extract of the plant was reported for its DPPH, hydroxyl and ABTS scavenging activity (Thirunavukkarasu et al. Citation2011).
Antidiabetic
Out of the different Avicennia plants, the antidiabetic potential is only reported in A. marina species. The leaves (Babuselvam et al. Citation2013) and pneumatophores (Mahera et al. Citation2011, Citation2013) were reported for their antihyperglycaemic activities. Babuselvam et al. (Citation2013) reported antihyperglycaemic activity of the ethanolic leaf extracts of A. marina in alloxan-induced diabetic rats. Significant decrease in the blood glucose levels, urea and increase in total haemoglobin (Hb), total protein and serum insulin were observed in alloxanized diabetic rats upon administration of 250 and 500 mg/kg leaf extracts. Furthermore, the other biochemical parameters like serum phosphorous, albumin and globulin were also reported to be ameliorated. The antidiabetic properties of A. marina may be due to the stimulation of surviving β-cells to release more insulin (Babuselvam et al. Citation2013). In another study, the methanolic pneumatophore extracts were also reported for their AGE inhibition potential that indicates the potential of this plant to control the post diabetic complications (Mahera et al. Citation2011, Citation2013).
Toxicity studies
Toxicological evaluation has been reported in two Avicennia species, namely A. marina and A. officinalis. A. marina aqueous leaf extracts at of 500 and 1000 mg/kg dosages showed no behavioural changes, zero mortality rate and normal of biochemical indices (SGOT, SGPT, ALP and urea) in experimental rats (Beula et al. Citation2012). Furthermore, the methanol and aqueous leaf extracts of this plant showed no toxicity effect against normal cell line, HEK-293 T (Sukhramani & Patel Citation2013). The ethanolic leaf extract of A. officinalis also showed no toxicity in Wistar albino mice at 250 and 500 mg/kg dosages (Sura et al. Citation2011).
Conclusion
The genus Avicennia is a pioneer group of dominant mangrove plant species having eight species including their varieties and synonyms with potential medicinal values. The plants belonging to the genus Avicennia are ecologically and phytochemically diverse with ethnomedicinal uses. Most species or species synonyms with genus Avicennia are valued for their traditional medicinal applications. Out of eight reported species, the ethnomedicinal investigation of A. balanophora, A. bicolor and A. integra has not been reported so far. Although most of the pharmacological studies have been validated recently for Avicennia, there are still many areas where our current knowledge could be improved.
The different extracts and compounds isolated from species like A. alba, A. officinalis and A. marina exhibited various pharmacological activities. Some of the active phyto-constituents responsible for such bioactivity that are reported in these plants belong to group of flavonoids, tannins, terpenoids, fatty acids and naphthoquinones. The species/species variants, namely A. alba, A. officinalis and A. marina have been investigated in detail for their phytochemical and therapeutic studies for which Avicennia is considered as a genus of medicinal importance. However, pharmacological studies of other species have not been carried out so far. There is a need for a detailed analysis of phytochemical and pharmacological properties of these species. This will enable to establish their medicinal importance and therapeutic potential, if any. In addition, the effectiveness of bioactive compounds or active chemical constituents found in plants of genus Avicennia needs to be explored further for future drug development.
Disclosure statement
No potential conflict of interest was reported by the authors.
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