1.  Introduction

Inflammation plays beneficial roles to maintain tissue homeostasis and protects organisms from harmful invasion of exogenous or endogenous toxins and pathogens. The primary response of inflammation is clinically characterized by local redness, swelling, heat, fever, pain, and loss of function [1-3]. However, chronic or uncontrolled inflammation leads to the development and progression of a number of diseases.  The common inflammatory diseases include asthma, rheumatoid arthritis, inflammatory bowel disease, cancer, atherosclerosis, type 2 diabetes, obesity, neurodegenerative diseases like Alzheimer’s disease, Parkinson’s disease, multiple sclerosis etc. which are the major threat to human health and considered to be responsible for 60% of global death [4-6]. At present, NSAIDs (non-steroidal anti-inflammatory drugs) as well as SAIDs (steroidal anti-inflammatory drugs) are commonly prescribed medications for inflammatory diseases. But the efficacy and tolerability of both can be overshadowed by their adverse effects. For instance, long term use of NSAIDs can cause ulcerations, hepatotoxicity and cardiovascular diseases etc., on the other hand, use of SAIDs are associated with hormonal disturbances, immunodeficiency, weight gain, diabetes, cataract and so on [7-10].

Numerous biochemical mediators work jointly to commence the inflammatory response, followed by recruitment and activation of other cells to resolve the response [11]. The potential inflammatory mediators include, enzymes (PLA₂, COX-1, -2); free radicals (ROS, RNS, and SOD); prostaglandins, leukotrienes, cytokines (TNF-α, IL-1,-6) and a number of transcription factors including nuclear factor (NF-κB). Plant extracts or pure compounds have been shown to exhibit significant anti‐inflammatory activity by inhibiting one or more of the aforementioned mediators and have paved the way from preclinical studies to clinical trials [9, 12]. The use of plant derived natural products in the treatment of inflammatory diseases represents a combined approach based on century old observations and experiences of traditional medicine, and modern techniques of pharmacology and phytochemistry [13]. The popularity and prescription rate of herbal medicine is increasing which indicates the shift of global trend from synthetic drugs towards medicines of natural origin which has also been considered as a promising future medicine [14] .

This review aims to summarize ten Bangladeshi plants belonging to eight different families [Abelmoschus esculentus (L.) Moench, Asparagus racemosus Willd., Blumea lacera (Burm.f.) DC., Butea monosperma (Lam.) Taub., Cheilocostus speciosus (J.Koenig) C.D.Specht., Mussaenda roxburghii Hook. f., Anthocephalus cadamba (Roxb.) Miq., Phyllanthus reticulatus Poir., Sesbania grandiflora (L.) Pers. and Spondias pinnata (L. f.) Kurz] which have been used extensively in folk medicine to heal or manage inflammation and related diseases, highlighting the anti-inflammatory molecules identified from these plants and their mode of action where reports are available. Toxicological information of these plants has also been overviewed in brief.     

2.  Materials and methods

A thorough literature search has been conducted using electronic databases like PubMed (https:// www.ncbi.nlm.nih.gov/pubmed/), ScienceDirect (https://www.sci encedirect.com/), and Google Scholar (https://scholar.google.com/) up to August 2023 for this study. The primary literature search was carried for anti-inflammatory activity and active constituents of selected plants whereas a secondary search was carried out for toxicity of the same plants namely A. esculentus, A. racemosus, B. lacera, B. monosperma, C. speciosus, M. roxburghii, A. cadamba, P. reticulatus, S. grandiflora and S. pinnata.  The figures of A. esculentus, A. racemosus, C. speciosus and  S. pinnata  were obtained from Wikimedia Commons under GNU free documentation license (https://en.wikipedia.org/wiki/GNU_Free_ Documentation_ License) whereas B. lacera, B. monosperma, S. grandiflora, M. roxburghii, N. cadamba and P. reticulatus were obtained from the web page ‘Flora of Bangladesh’, from the Survey of Vascular Flora of Chittagong and the Chittagong Hill Tracts Project, Bangladesh National Herbarium (https://bnh-flora.gov.bd), Ministry of Environment & Forest, People Republic of Bangladesh (Fig 1) These plants were selected based on their extensive therapeutic use in traditional medicine to manage and cure inflammatory disorders. The common name, local name and traditional uses of these plants included in Table 1 were extracted mainly from the books of Professor Abdul Ghani and Sarder Nasir Uddin, and from few other references.

A. esculentus, A. racemosus, C. speciosus and  S. pinnata  were obtained from Wikimedia Commons under GNU free documentation license (https://en.wikipedia.org/wiki/GNU_Free_Documentation_License) whereas B. lacera, B. monosperma, S. grandiflora, M. roxburghii, N. cadamba and P. reticulatus were obtained from the web page ‘Flora of Bangladesh’, from the Survey of Vascular Flora of Chittagong and the Chittagong Hill Tracts Project, Bangladesh National Herbarium (https://bnh-flora.gov.bd), Ministry of Environment & Forest, People Republic of Bangladesh.

Figure 1. Anti-inflammatory plants.

Table 1: Traditional uses of the selected plants

3. Results and discussion

3.1 Abelmoschus esculentus (L.) Moench

A. esculantus or okra is an annual herb and important vegetable crop which is grown in tropical, subtropical and warm temperate regions of Africa, Asia, Southern Europe and America [15]. The fruit is a common vegetable in tropical countries. Nevertheless, fruit as well as other parts of this plant demonstrated significant anti-inflammatory properties in several studies.  A. esculantus fruit extract suppressed LPS-induced NO, TNF-α, IL-1β and Akt (protein kinase B) mediated NF-κB pathway in murine microglial cells [16].  Fruit extracts as well as lectin (a protein) isolated from mature seeds of this plant inhibited carrageenan induced paw edema in both mice and rats [17-19]. Extract from whole plant has also been reported to inhibit hemolysis [20]. A. esculentus fruit extracts demonstrated wound healing properties in both in vivo and in vitro experimental models by down regulating inflammatory mediators [21, 22]. Raw and cooked extracts from this plant inhibited NO production, COX-2, iNOS expression, and the cytokines, TNF-α, IL-6 and IL-1β, in LPS and H₂O₂ induced RAW 264.7 cells confirming its anti-inflammatory properties [23]. The extracts were also found nontoxic in that study. However, in other studies, this plant has shown cytotoxic potential against BHK-21 cell [24]. The mRNA levels of pro-inflammatory cytokines (TNF-α, IL-6 and IL-1β) have been reduced by the leaf extract of A. esculentus but not by the fruit extract of this plant [25]. Polysaccharide isolated from this plant exhibited antidepressant effects by inhibiting the expression of TLR4, the nuclear translocation of NF-κB and high levels of proinflammatory cytokines (IL-6 and TNF-α), and also by enhancing the MAPKs (mitogen-activated protein kinases) signaling [26]. Different parts of okra i.e., flower, fruit, leaf and seed contain wide array of biologically active compounds among which β-sitosterol (1) [27], linolenic acid (2) and oleic acid (3) (Figure 2) [15] are reported anti-inflammatory molecules [28-31]. Phenolic constituents from A. esculentus exhibited high binding affinity to COX-2 and NF-κB in molecular docking studies where caffeic acid (4), vanillic acid (5) and ferulic acid (6) (Figure 2) were the lead molecules [32]. Anti-inflammatory molecule like quercetin-3-O-glucoside (7) (Figure 2) has been detected in this plant along with series of other molecules in GC-MS study [33].

Figure 2. Anti-inflammatory compounds isolated from A. esculentus

3.2 Asparagus racemosus Willd.

A. racemosus is an extensively used herb in Ayurvedic medicine system. This spinous under-shrub commonly grows at low altitudes of tropical and subtropical countries [49]. In in vivo experimental models, this species has shown significant reduction of rat paw edema induced by carrageenan and serotonin [50, 51]. Whereas in vitro assays demonstrated that this plant has promising RBC membrane stabilization activity [49, 52, 53]. A. racemosus extract demonstrated anti-inflammatory activity by reducing pathology of inflammatory bowel disease (IBD) in oxazolone induced zebra fish IBD (inflammatory bowel disease) model [54]. Sarsasapogenin (a steroidal saponin) isolated from this plant exhibited neuroprotective effect by inhibiting amyloid β protein (Aβ) fibrillation as well as acetylcholinesterase (AChE), butyrylcholinesterase (BuChE), beta site cleaving enzyme 1 (BACE1) and monoaminoxidase B (MAO-B) which are the key enzymes involved in the pathogenesis of Alzheimer’s disease [55]. The LD₅₀ of A. racemosus root extract has been found to be 505 mg/kg body weight of mice [56] and showed toxicity on liver and spleen tissues of rats on long term administration [57]. A broad range of biologically active constituents has been isolated from different parts of this plant [58] among which kaempferol (8) [59], quercetin (9) and rutin (10) (Figure 3) [60] are well studied anti-inflammatory bioflavonoids.

Figure 3. Anti-inflammatory compounds isolated from A. racemosus

3.3 Blumea lacera (Burm.f.) DC.

B. lacera is an herbaceous weed that commonly grows in the uncultivated lands of Bangladesh, India, Australia, China, Malaya and tropical Africa. There are several reports on in vitro anti-inflammatory activity of B. lacera, studied using protein anti-denaturation and RBC membrane stabilization assays [61-63]. This species has demonstrated protective action against rat enterocolitis which is considered to be attributed mainly by the anti-inflammatory and anti-oxidant properties of the plant [64]. Aerial part extract of this plant inhibited writhing reflexes and ear edema in the experimental mice model and showed cytotoxicity (LC₅₀ = 5.4 μg/mL) in brine shrimp lethality bioassay [65]. Extract and compounds from this plant showed ulcer healing property investigated using in vivo and in silico models respectively and the extract did not show any sign of toxicity as well as abnormalities up to the dose of 5000 mg/kg of body weight [65, 66]. B. lacera leaf extract as well as its liposomal preparation were found effective against CCl₄-induced liver injury in rats [67]. B. lacera leaf extract demonstrated significant anti-hemorrhoid activity in croton oil-induced hemorrhoid rat model and also inhibited protein denaturation. In the same study, the extract did not show any sign of behavioral or neurological toxicity in rats and zero mortality up to a dose of 2000 mg/kg of body weight [68]. The plant is rich in flavonoids, alkaloids, glycosides, terpenoids, and essential oil components [69, 70] including anti-inflammatory molecules like quercetin (9) [68], 1,8-cineole (11), α-pinene (12), caryophyllene (13) (Fig. 4)  etc . GC-MS analysis revealed the presence of different components in this plant including neophytadiene, 1,2-epoxyundecane, hexadecanoic acid and phytol as major constituents [67, 71].

Figure 4. Anti-inflammatory compounds isolated from B. lacera

3.4 Butea monosperma (Lam.) Taub.

B. monosperma is indigenous to tropical and sub-tropical parts of Asia and is found throughout Bangladesh, India, Nepal, Sri Lanka, Myanmar, Thailand, Laos, Cambodia, Vietnam, Malaysia and Western Indonesia. This plant exhibited notable anti-inflammatory activities in several in vitro and in vivo studies. For instance, fixed oil from B. monosperma seed attenuated carrageenan induced paw edema in rats [72], flower extracts inhibited inflammatory mediators like IL-1β, IL-6 and IL-8, prostaglandin E₂ production and MMP-1, -2, -9 and -10 secretion as well as carrageenan induced paw edema and cotton pellet implanted granuloma in rats [73-75]. Extracts from this plant have also been found to protect RBC membrane from lysis [76, 77]. In acute oral toxicity assay the leaf extract of this plant was found safe up to a dose of 4,000 mg/kg rat body weight with no mortality [78]. A wide array of bioactive secondary metabolites has been isolated from different parts of the plant including β- sitosterol (1) (Fig. 2), lupeol (14), lupeonone etc. [79, 80]. Butrin (15), isobutrin (16) [81] and butein (17) (Fig. 5) [82] characterized from B. monosperma showed potent anti-inflammatory activity by down-regulating the synthesis of TNF-α, IL-6 and IL-8 via NF-κB inhibitory pathway in human mast cells [83].

Figure 5. Anti-inflammatory compounds isolated from B. monosperma

3.5 Cheilocostus speciosus (J.Koenig) C.D.Specht.

C. specious is a herbaceous ornamental plant distributed in the tropical and subtropical regions of Asia, Africa and the Americas [84]. Rhizome and aerial part extracts of this plant have been reported to possess strong activities against inflammation and arthritis [85, 86]. Extracts from different parts of this plant have shown RBC membrane stabilization and protein anti-denaturation action in vitro studies and inhibition of paw edema in animal models [87-90]. A large number of compounds have been characterized from this plant [84] among which 22, 23-dihydrospinasterone (18), dehydrocostus lactone (19), dehydrodihydrocostus lactone (20),  and stigmasterol (21) (Fig. 6) exhibited potent anti-inflammatory activity via lowering the levels of cytokines, PGE₂, lipoxgenase-5 and COX-2 [91] whereas a diosgenin (22) (Fig. 6) is found to inhibit NO and TNF-α in lipopolysaccharide (LPS) stimulated RAW 264.7 macrophages [92]. In a recent study, C. speciuosus extract has been found to ameliorate zearalenone (a non-steroidal estrogenic mycotoxin) induced toxicity in rats by modulating iNOS, inflammatory-related genes, and the Nrf₂ pathway. In the same study, GC-MS analysis of the extract revealed several compounds which azulene being the major one [93].

Figure 6. Anti-inflammatory compounds isolated from C. specious

3.6 Mussaenda roxburghii Hook. f.          

M. roxburghii is a wild perennial herb that grows in the foothills and moist shady places of Bangladesh, India, Nepal, Bhutan and Myanmar [94, 95]. Extracts from the leaf and roots of this plant have shown RBC membrane stabilization and protein anti-denaturation action in in vitro studies [96-98]. GC-MS analysis of the shoot ethanol extract has allowed characterizing compounds from M. roxburghii [95] including anti-inflammatory moieties for example, vitamin E (23) [99], neophytadiene (24)  [100] and squalene (25) (Fig. 7) [101, 102].

Figure 7. Anti-inflammatory compounds isolated from M. roxburghii

3.7 Anthocephalus cadamba (Roxb.) Miq.

A. cadamba (synonym: Neolamarckia cadamba) is an evergreen flowering tree distributed in different parts of Bangladesh, India, Nepal, Myanmar, Sri Lanka, Cambodia, Laos, Philippines, Malaysia, Indonesia, Papua New Guinea and Australia [103]. It is an important plant in Ayurveda due to the usefulness of its different parts for the management of a number of health hazards [45]. This plant has been investigated in several studies for its anti-inflammatory activities. Its stem bark extract exhibited potent anti-inflammatory properties in vivo experiments by suppressing histamine induced paw edema and cotton pellet induced granuloma whereas in vitro experiments, the bark fractions have shown protein anti-denaturation and human RBC membrane stabilization activities [104-107]. Again, extracts from leaf, fruit and flowering top of A. cadamba exhibited significant human RBC membrane stabilization action [108-111]. A. cadamba leaf extract exhibited accelerative wound-healing properties in diabetic rat model [112]. A wide variety of compounds has been revealed from this plant using GC-MS analysis and some of those have shown to be potential for the management of Alzheimer’s disease via in silico molecular docking analysis [113]. In a recent study, neocadambine D (26), 3β-dihydrocadambine (27) and 3β-isodihydrocadambine (28) (Fig. 8) isolated from A. cadamba showed better anti-inflammatory effects than that of the positive control, dexamethasone [114]. In another study, GC-MS analysis of bark extract revealed the presence of a series of phytoconstituents including  tetradecanoic acid, n-hexadecanoic acid, gamma-sitosterol, hexadecanoic acid, 2-hydroxy-1-(hydroxymethyl) ethyl ester, octadecanoic acid, 2,3-dihydroxypropyl ester, oleic acid, 9,12-octadecadienoic acid (Z,Z)- and 5-hydroxymethylfurfural as the major constituents [48]. Anti-inflammatory molecules like β–sitosterol (1), vanillic acid (5) (Fig. 2), ursolic acid (29), quinovic acid (30) (Fig. 8) etc. have been reported from this plant, where quinovic acid demonstrated potential anticancer property [115]. In another study, several other compounds have been reported from this plant including vincosamide-N-oxide and isodihydroamino cadambine, vincosamide, vallesiachotamine, iso-vallesiachotamine, and oleanolic acid etc., among which vallesiachotamine, iso-vallesiachotamine have shown potent anticancer activity against cancer cell line whilst all of the identified compounds did not show any toxic effect on normal cells [116].

Figure 8. Anti-inflammatory compounds isolated from A. cadamba

3.8 Phyllanthus reticulatus Poir.

P. reticulatus is a shrub and grows throughout tropical areas of Bangladesh, India, China and the Malay Islands. This plant has been reported to attenuate carrageenan induced paw edema in both mice and rats treated with bark and leaf extracts [117-120]. In in vitro investigations this plant inhibited lysis of RBC membrane [121].  P. reticulatus extract and fractions have been investigated for gastroprotective effects in several studies. The plant down regulated mRNA levels of IL-8 and TNF-α in ulcer rat models and thus claimed to possess anti-inflammatory and immunomodulatory activities [122]. Again this plant has decreased ulcer index in pylorus ligation-induced, ethanol-induced and swim stress-induced ulcer rat models [123]. Ethyl 9,12,15-octadecatrienoic acid, ethyl 9,12,15-octadecatrienoate, n-hexadecanoic acid and tocopherol have been detected as major constituents in this plant by GC-MS analysis  [124]. In a different investigation, a wide range of compounds have been identified from P. reticulatus extract using UPLC-ESI-QTOF/MS analysis including well documented anti-inflammatory molecules like gallic acid (31),  catechin (32) (Fig. 9),  quercetin (9) (Fig. 3) etc. [125]. Other anti-inflammatory moieties isolated from P. reticulatus are rutin (10) (Fig. 3), lupeol (14) (Fig. 5), ellagic acid (33), betulinic acid (34) (Fig. 9), vanillic acid (5) (Fig. 2) etc. [126, 127].

Figure 9. Anti-inflammatory compounds isolated from P. reticulatus

3.9 Sesbania grandiflora (L.) Pers.

S. grandiflora is a soft wooded flowering tree that grows in Asian countries including Bangladesh, India, Malaysia and Indonesia [128, 129]. In the in vitro RBC membrane stabilization assay, this plant protected the cell membrane from lysis [129-131]. In different in vivo study models like carrageenan induced paw edema, cotton pellet induced granuloma and adjuvant-induced arthritis model, the flower [132], bark [128, 133] and root extract [134] of S. grandiflora successfully attenuated inflammation. In acetic acid induced ulcerative colitis this plant has been found to suppress inflammatory cytokines like TNF-α and IL-6 [135]. In acute oral toxicity assay the root extract of this plant was found safe up to a dose of 2,000 mg/kg rat body weight with no mortality [136]. Molecular docking study revealed that phytoconstituents (β-amyrin, linolenic acid and L-α-terpineol) present in the leaves of this plant have a high binding affinity to prostaglandin 3 receptor E₂, which may be useful to develop peptic ulcers therapy [137]. Along with different bioactive constituents, betulinic acid (34) (Fig. 9) and tocopherols have been reported from this plant [138, 139].

3.10 Spondias pinnata (L. f.) Kurz

S. pinnata is a deciduous tree distributed in different parts of Bangladesh, India, Sri Lanka, China, and other Southeast Asian countries [140, 141]. Both bark and stem heart wood extracts of S. pannata have reduced carrageenan induced rat paw edema in a dose dependent manner [142, 143]. Whereas leaf extracts of this species demonstrated strong anti-hemolytic activity in RBC membrane stabilization assay [140, 144-146]. S. pinnata bark extract exhibited protective effects against the oxidative and inflammatory changes that occur during the development of mucositis [147]. The seed extract of this plant did not show any signs of toxicity in mice at a dose of 2,000 mg/kg body weight [148]. In recent years, the GC-MS technique has enabled to identify of a wide range of components from the essential oil of this plant including caryophyllene (13) (Fig. 4) and α-pinene (12) (Fig. 4) and the essential oil itself demonstrated strong anti-inflammatory activity [144]. A quinolone (7-hydroxy-6-methoxyquinolin-2(1H)-one) (35) (Fig. 10) isolated from S. pinnata has been reported to down regulate several inflammatory mediators like NO, TNF-α, IL-6, IL-1β, ROS, iNOS and COX-2, and also found to retain cytoplasmic concentration of NF-κB by inhibiting its activation in LPS stimulated RAW 264.7 cells [141]. A series of glycosides, caffeoylquinic acid and coumarin derivatives have also been reported from the fruits of this plant [149].

Figure 10. Anti-inflammatory compounds isolated from S. pinnata

In the present paper, we have reviewed a total of 10 plants that possess pharmacological potential to combat inflammatory disorders. These plants are used extensively in various systems of traditional medicines in the management of inflammation and inflammatory diseases like bronchitis, asthma, rheumatism, tumor etc. Different parts of the selected plants have been evaluated for their anti-inflammatory activities using in vitro and in vivo experimental models. The commonly used in vitro experiments were found to be RBC membrane stabilization and protein anti-denaturation assays and assays to examine inhibition of activated inflammatory mediators, for example, prostaglandin, enzymes (COX-2 and LOX), nitric oxide (NO), cytokines (TNF-α and ILs), NF-κB etc. Whereas the commonly used in vivo assays include carrageenan induced rodent paw edema, cotton pellet implemented granuloma, adjuvant-induced arthritis and acetic acid induced ulcerative colitis along with other inflammatory disease models in animals. Each of the selected plants demonstrated significant anti-inflammatory action in at least two or more of the above preclinical investigations. A number of anti-inflammatory compounds have been reported from these plants and several of them were found to suppress numerous inflammatory mediators. Among these β-sitosterol (1), linolenic acid (2), oleic acid (3), caffeic acid (4), kaemferol (8) quercetin (9), gallic acid (31), catechin (32), ellagic acid (33), betulinic acid (34) etc. are well documented anti-inflammatory molecules. Evaluation of toxicity is also crucial for the safe use of medicinal plants. Extracts from different parts of these plants demonstrated varying levels of toxicity. For example, A. racemosus root extract showed toxicity on liver and spleen tissues of rats on long term administration and aerial part of B. lacera showed toxicity to brine shrimp [57, 65]. Whereas leaf extract of B. monosperma, root extract of S. grandiflora and seed extract of S. pinnata were found safe in acute oral toxicity assay [78, 116, 136].

4. Conclusions

Plants have proved their remarkable therapeutic potential with time and through rigorous pharmacological and phytochemical investigations which led to the discovery of a variety of drug candidates with promising anti-inflammatory activities. The selected Bangladeshi plants reviewed in this paper possess a rich history of being used by traditional healers of the country to combat various inflammatory disorders. However, intensive research focus has yet been required for these plants for their detailed chemical investigations followed by a precise understanding of molecular mechanisms as well as toxicological evaluation.   

Abbreviations

Aβ: amyloid beta; AChE, acetylcholinesterase; BACE, beta site cleaving enzyme; BuChE, butyrylcholinesterase; CCl₄, carbon tetrachloride; COX, cyclooxygenase; GC-MS, gas chromatography – mass spectroscopy; H₂O₂, hydrogen peroxide; IBD, inflammatory bowel disease; iNOS, inducible nitric oxide synthase; IL, interleukin; INF-γ, interferon-γ; LC₅₀, lethal concentration 50;  LD₅₀, lethal dose 50; LPS, lipopolysaccharide; MAO-B, monoaminoxidase B; MAPKs, mitogen-activated protein kinases; MMP,  matrix metalloproteinase; NF-κB, nuclear factor- κB; ng, nano gram; NO, nitric oxide; Nrf-2, nuclear factor erythroid 2-related factor-2; NSAIDs, non-steroidal anti-inflammatory drugs; PLA₂, phospholipase A₂; PGE₂, prostaglandin E₂; RBC, red blood cell; RNS, reactive nitrogen species; ROS, reactive oxygen species; SAIDs, steroidal anti-inflammatory drugs; SOD, superoxide dismutase; TLR4, toll-like receptor 4; TNF-α, tumor necrosis factor-α, UPLC-ESI-QTOF/MS, Ultra-performance liquid chromatography with electrospray ionization quadruple time-of-flight mass spectrometry.

Authors’ contributions

Conceptualization, investigation, data curating, writing original draft & visualization, M.A.A.; Formal analysis, review and editing, M.A. and R.Z.

Acknowledgements

We would like to thank Dr. Shumaia Parvin (Department of Pharmacy, University of Rajshahi, Bangladesh) for her careful review and insightful suggestions to improve the paper.

Funding

Not applicable

Availability of data and materials

All data will be made available on request according to the journal policy.

Conflicts of interest

All authors declare that they have no financial or commercial conflicts of interest.

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