This study was conducted to evaluate the phenolic composition, toxicity, and antimicrobial activity of Licania rigida Benth, an underexploited wild Licania species. L. rigida leaf fractions (ethyl alcohol and ethyl acetate) were analyzed for their phenolic compound and flavonoid total, and high-performance liquid chromatography/ultraviolet spectra chromatographic profiles. Regarding the extract biological effects, toxicity was measured by acute oral toxicity in Wistar rats, MTT [3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide] method, and apoptosis indicators with DAPI in VERO cells, whereas well-agar diffusion and broth microdilution assays were applied to evaluate the antimicrobial ability. The phytochemical analysis resulted in significant amounts of phenolic compounds and total flavonoids in the extract and fraction, with flavonol-3-O-glycosylates as the main constituent. Regarding the extract and fraction antimicrobial activity, the results showed a significant effect against gram-positive bacteria and fungi, among which Staphylococcus epidermidis and Candida krusei displayed more susceptibility. No toxicity effects were observed in animals. Concerning the cytotoxicity assay, only the highest dose tested exhibited a minimal toxic effect on the analyzed cell lines. These results are relevant considering the increase of multiresistant microorganisms to conventional treatments applied. Therefore, investigating the pharmacological properties of the genus Licania is promising in the search for new sources of antimicrobial compounds.
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References
1.
FragaCG, CroftKD, KennedyDO, Tomás-BarberánFA: The effects of polyphenols and other bioactives on human health. Food Funct, 2019; 10:514–528.
2.
SilvaRFM, PogacnikL: Polyphenols from food and natural products: Neuroprotection and safety. Antioxidants, 2020; 9:1–13.
3.
LucaSV, MacoveiI, BujorA, et al.: Bioactivity of dietary polyphenols: The role of metabolites. Crit Rev Food Sci Nutr, 2020; 60:626–659.
4.
PilonAC, GuH, RafteryD, et al.: Mass spectral similarity networking and gas-phase fragmentation reactions in the structural analysis of flavonoid glycoconjugates. Anal Chem, 2019; 16:10413–10423.
5.
BorgesA, JoséH, HomemV, SimõesM: Comparison of Techniques and Solvents on the Antimicrobial and Antioxidant potential of extracts from Acacia dealbata and Olea europaea. Antibiotics, 2020; 9:1–19.
6.
BrimaEI: Toxic elements in different medicinal plants and the impact on human health. Int J Environ Res Public Health, 2017; 14:1–9.
7.
RibeiroNE, PereiraPS, OliveiraTBD, et al.: Acute and repeated dose 28-day oral toxicity of Chrysobalanus icaco L. leaf aqueous extract. Regul Toxicol Pharmacol, 2020; 113:104643.
8.
BrimaEI: Toxic elements in different medicinal plants and the impact on human health. Int J Environ Res Public Health, 2017; 14:1209.
World Health Organization: Worldwide country situation analysis: Response to antimicrobial resistance. Geneva, Switzerland, 2015. www.who.int/iris/bitstream/handle/(accessed August 1, 2019).
11.
ManilalA, SabuKR, ShewangizawM, et al.: In vitro antibacterial activity of medicinal plants against biofilm-forming methicillin-resistant Staphylococcus aureus: Efficacy of Moringa stenopetala and Rosmarinus officinalis extracts. Heliyon, 2020; 6:1–8.
12.
RevieNM, IyerKR, RobbinsN, CowenLE: Antifungal drug resistance: Evolution, mechanisms and impact. Curr Opin Microbiol, 2018; 45:70–76.
13.
ZacchinoSA, ButassiE, LibertoMD, RaimondiM, PostigoA, SortinoM: Plant phenolics and terpenoids as adjuvants of antibacterial and antifungal drugs. Phytomedicine, 2017; 37:27–48.
14.
ConfortinTC, ToderoI, SoaresJF, et al.: Extracts from Lupinus albescens: Antioxidant power and antifungal activity in vitro against phytopathogenic fungi. Environ Technol, 2019; 40:1668–1675.
15.
BlondeauD, St-PierreA, BourdeauN, BleyJ, LajeunesseA, Desgagné-PenixI: Antimicrobial activity and chemical composition of white birch (Betula papyrifera Marshall) bark extracts. Microbiol Open, 2020; 9:1–23.
16.
BarbosaAPO, SilveiraGDO, MenezesIACD, et al.: Antidiabetic effect of the Chrysobalanus icaco L. aqueous extract in rats. J Med Food, 2013; 16:538–543.
17.
FariasDF, SouzaTM, VianaMP, et al.: Antibacterial, antioxidant, and anticholinesterase activities of plant seed extracts from Brazilian semiarid region. BioMed Res Int, 2013; 2013(Article ID 510736):1–9.
18.
SantosES, OliveiraCDDM, MenezesIRA, et al.: Anti-inflammatory activity of herb products from Licania rigida Benth. Complement Ther Med, 2019; 45:254–261.
19.
FreitasMAD, AlvesAIS, AndradeJC, et al.: Evaluation of the antifungal activity of the Licania rigida leaf ethanolic extract against biofilms formed by candida sp. isolates in acrylic resin discs. Antibiotics, 2019; 8:1–11.
20.
GeorgéS, BratP, AlterP, AmiotMJ: Rapid determination of polyphenols and vitamin C in plant-derived products. J Agric Food Chem, 2005; 53:1370–1373.
21.
MiliauskasG, VenskutonisPR, BeekTAV: Screening of radical scavenging activity of some medicinal and aromatic plant extracts. Food Chem, 2004; 85:231–237.
22.
BritoNJN, LópezJA, NascimentoMAD, et al.: Antioxidant activity and protective effect of Turnera ulmifolia Linn. var. elegans against carbon tetrachloride-induced oxidative damage in rats. Food Chem Toxicol 2012;50:4340–4347.
23.
BhatiaS, SardanaS, SenwarKR, DhillonA, SharmaA, NavedT: In vitro antioxidant and antinociceptive properties of Porphyra vietnamensis. Biomedicine, 2019; 9:3.
24.
National Health Surveillance Agency: Ministry of Health Resolution No. RE 90/2004. Standards for toxicological studies of herbal products, Official Gazette of the Federative Republic of Brazil, Executive Branch. Brasília, DF, 2004.
25.
Organization for Economic Cooperation and Development: Guidelines for the Testing of Chemicals: Acute and Toxicity – Acute Toxic Class Method. OECD Guideline, Paris, 2001, p. 423.
26.
Clinical and Laboratory Standards Institute: Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts, Vol 22. CLSI, Wayne, PA, 2012, pp. 1–51.
27.
Clinical and Laboratory Standards Institute: Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard. Clinical and Laboratory Standards Institute, Wayne, PA, 2018, pp. M02A13:1–94.
28.
Clinical and Laboratory Standards Institute: Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard. Clinical and Laboratory Standards Institute, Wayne, PA, 2018, pp. M07-A11:1–13.
29.
Espinel-IngroffA, FothergillA, PeterJ, RinaldiMG, WalshTJ: Testing conditions for determination of minimum fungicidal concentrations of new and established antifungal agents for Aspergillus spp.: NCCLS Collaborative Study. J Clin Microbiol, 2002; 40:3204–3208.
30.
BiyuLV, YinW, GaoJ, et al.: Neo-5,22E-Cholestadienol derivatives from Buthus martensii Karsch and targeted bactericidal action mechanisms. Molecules, 2019; 24:1–17.
31.
LiberatoMCTC, MoraisSMD, SiqueiraSMC, et al.: Phenolic content and antioxidant and antiacetylcholinesterase properties of honeys from different floral origins. J Med Food, 2011; 14:658–663.
32.
MedeirosJLD, AlmeidaTSD, NetoJJL, et al.: Chemical composition, nutritional properties, and antioxidant activity of Licania tomentosa (Benth.) fruit. Food Chem, 2020; 313:0308–8146.
33.
SenT, SamantaSK: Medicinal plants, human health and biodiversity: A broad review. Adv Biochem Eng Biotechnol, 2014; 147:59–110.
34.
ZhuM, ChenG, WuJ, LiN, LiuZ, GuoM: Recent development in mass spectrometry and its hyphenated techniques for the analysis of medicinal plants. Phytochem Anal, 2018; 29:365–374.
35.
NugrahaAS, TriatmokoB, WangchukP, KellerPA: Vascular epiphytic medicinal plants as sources of therapeutic agents: Their ethnopharmacological uses, chemical composition, and biological activities. Biomolecules, 2020; 10:1–66.
36.
Alvarado-CastilloC, EstradaO, CarvajalE: Pomolic acid, triterpenoid isolated from Licania pittieri, as competitive antagonist of ADP-induced aggregation of human platelets. Phytomedicine, 2012; 19:484–487.
37.
EstradaO, ContrerasW, AchaG, et al.: Chemical constituents from Licania cruegeriana and their cardiovascular and antiplatelet effects. Molecules, 2014; 19:21215–21225.
38.
PessoaIP, NetoJJL, AlmeidaTSD, et al.: Polyphenol composition, antioxidant activity and cytotoxicity of seeds from two underexploited wild Licania species: L. rigida and L. tomentosa. Molecules, 2016; 21:1–16.
39.
LuzJRD, NascimentoTESD, SilvaGA, et al.: Licania rigida Benth leaf extracts: Assessment of toxicity and potential anticoagulant effect. S Afr J Bot, 2021; 139:217–225.
40.
MoghadamtousiSZ, KadirHA, HassandarvishP, TajikH, AbubakarS, ZandiK: A review on antibacterial, antiviral, and antifungal activity of curcumin. BioMed Res Intl, 2014; 2014(Article ID 186864):1–12.
41.
VestergaardM, IngmerH: Antibacterial and antifungal properties of resveratrol. Int J Antimicrob Agents, 2019; 53:716–723.
42.
OthmanL, SleimanA, Abdel-MassihRM: Antimicrobial activity of polyphenols and alkaloids in middle eastern plants. Front Microbiol, 2019; 10:1–28.
43.
SantosECG, DonniciCL, CamargosERS, et al.: Interaction of Pseudobombax marginatum Robyns stem bark extract on the cell surface of Bacillus cereus and Staphylococcus aureus. J Bacteriol Mycol, 2018; 5:1–7.
44.
BadisaRB, ChaudhuriSK, PilarinouE, RutkoskiNJ, HareJ, LevensonCW: Licania michauxii Prance root extract induces hsp 70 mRNA and necrotic cell death in cultured human hepatoma and colon carcinoma cell lines. Cancer Lett, 2000; 149:8–61.
45.
RosaSSS, SantosFO, LimaHG, et al.: In vitro anthelmintic and cytotoxic activities of extracts of Persea willdenovii kosterm (Lauraceae). J Helminthol, 2018; 92:674–680.
46.
ElishaIL, BothaFS, McGawLJ, EloffJN: The antibacterial activity of extracts of nine plant species with good activity against Escherichia coli against five other bacteria and cytotoxicity of extracts. BMC Complement Altern Med, 2017; 17:1–10.
BelwalT, EzzatSM, RastrelliL, et al.: A critical analysis of extraction techniques used for botanicals: Trends, priorities, industrial uses and optimization strategies. Trends Anal Chem, 2018; 100:82–102.
50.
KharbachM, MarmouziI, JemliME, BouklouzeA, HeydenYV: Recent advances in untargeted and targeted approaches applied in herbal-extracts and essential-oils fingerprinting - A review. J Pharm Biomed Anal, 2020; 177:112849.
51.
AzwanidaNN: Review on the extraction methods used in medicinal plants, principle, strength and limitation. Med Arom Plants, 2015; 4:196.
52.
RosatoA, CarocciA, CatalanoA, et al.: Elucidation of the synergistic action of Mentha piperita essential oil with common antimicrobials. PLoS One, 2018; 13:1–13.
53.
Van VuurenS, ViljoenA: Plant-based antimicrobial studies - Methods and approaches to study the interaction between natural products. Planta Med, 2011; 77:1168–1182.
54.
AyazM, UllahF, SadiqA, et al.: Synergistic interactions of phytochemicals with antimicrobial agents: Potential strategy to counteract drug resistance. Chem-Biol Interact, 2019; 308:294–303.
55.
Álvarez-MartínezFJ, Barrajón-CatalánE, Herranz-LópezM, MicolV.: Antibacterial plant compounds, extracts and essential oils: An updated review on their effects and putative mechanisms of action. Phytomedicine, 2021; 90:153626.
56.
YangY, ZhngT: Antimicrobial activities of tea polyphenol on phytopathogens: A review. Molecules, 2019; 24:1–8.
57.
OkwuMU, OlleyM, AkpokaAO, IzevbuwaOE: Methicillin-resistant Staphylococcus aureus (MRSA) and anti-MRSA activities of extracts of some medicinal plants: A brief review. AIMS Microbiol, 2019; 5:117–137.
58.
CascioferroS, CarboneD, ParrinoB, et al.: Therapeutic strategies to counteract antibiotic resistance in MRSA Biofilm-associated infections. Chem Med Chem, 2020; 10:1–18.
59.
TaeiM, ChadeganipourM, MohammadiR: An alarming rise of non-albicans Candida species and uncommon yeasts in the clinical samples; a combination of various molecular techniques for identification of etiologic agents. BMC Res Notes, 2019; 12:1–7.
60.
JakobekL: Interactions of polyphenols with carbohydrates, lipids and proteins. Food Chem, 2015; 175:556–567
61.
Bouarab-ChibaneL, ForquetV, LantériP, et al.: Antibacterial properties of polyphenols: Characterization and QSAR (quantitative structure-activity relationship) models. Front Microbiol, 2019; 10:829.
62.
JamiuAT, AlbertynJ, SebolaiOM, PohlCH: Update on Candida krusei, a potential multidrug-resistant pathogen. Med Mycol, 2020; 59:14–30.
63.
DagliaM: Polyphenols as antimicrobial agents. Curr Opin Biotechnol, 2012; 233:174–181.
64.
OlszewskaaMA, GędasA, SimõesM: Antimicrobial polyphenol-rich extracts: Applications and limitations in the food industry. Food Res Int, 2020; 134:109214.
65.
EvensenNA, BraunPC: The effects of tea polyphenols on Candida albicans: Inhibition of biofilm formation and proteasome inactivation. Can J Microbiol, 2009; 55:1033–1039.
66.
ShahzadM, SherryL, RajendranR, EdwardsCA, CombetE, RamageG: Utilising polyphenols for the clinical management of Candida albicans biofilms. Int J Antimicrob Agents, 2014; 44:269–273.
67.
NassimaB, NassimaB, RiadhK: Antimicrobial and antibiofilm activities of phenolic compounds extracted from Populus nigra and Populus alba buds (Algeria). Braz J Pharm Sci, 2019; 55:e18114.
68.
Álvarez-MartínezFJ, Barrajón-CatalánE, EncinarJA, Rodríguez-DíazJC, MicolV: Antimicrobial capacity of plant polyphenols against gram-positive bacteria: A comprehensive review. Curr Med Chem, 2018; 27:2576–2606.
Yong-ShengJ: Recent advances in natural antifungal flavonoids and their derivatives. Bioorg Med Chem Lett, 2019; 29:1–13.
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