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      Antioxidant, antimicrobial, antiparasitic, and cytotoxic properties of various Brazilian propolis extracts

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          Abstract

          Propolis is known for its biological properties and its preparations have been continuously investigated in an attempt to solve the problem of their standardization, an issue that limits the use of propolis in food and pharmaceutical industries. The aim of this study was to evaluate in vitro antioxidant, antimicrobial, antiparasitic, and cytotoxic effects of extracts of red, green, and brown propolis from different regions of Brazil, obtained by ethanolic and supercritical extraction methods. We found that propolis extracts obtained by both these methods showed concentration-dependent antioxidant activity. The extracts obtained by ethanolic extraction showed higher antioxidant activity than that shown by the extracts obtained by supercritical extraction. Ethanolic extracts of red propolis exhibited up to 98% of the maximum antioxidant activity at the highest extract concentration. Red propolis extracts obtained by ethanolic and supercritical methods showed the highest levels of antimicrobial activity against several bacteria. Most extracts demonstrated antimicrobial activity against Staphylococcus aureus. None of the extracts analyzed showed activity against Escherichia coli or Candida albicans. An inhibitory effect of all tested ethanolic extracts on the growth of Trypanosoma cruzi Y strain epimastigotes was observed in the first 24 h. However, after 96 h, a persistent inhibitory effect was detected only for red propolis samples. Only ethanolic extracts of red propolis samples R01Et.B2 and R02Et.B2 showed a cytotoxic effect against all four cancer cell lines tested (HL-60, HCT-116, OVCAR-8, and SF-295), indicating that red propolis extracts have great cytotoxic potential. The biological effects of ethanolic extracts of red propolis revealed in the present study suggest that red propolis can be a potential alternative therapeutic treatment against Chagas disease and some types of cancer, although high activity of red propolis in vitro needs to be confirmed by future in vivo investigations.

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          Chemical diversity of propolis and the problem of standardization.

          Vassya Bankova (2005)
          Chemical variability of propolis is discussed with respect to the problem of standardization. Several chemical types of propolis are formulated, based on their plant source. Reliable criteria for chemical standardization of different propolis types are needed but such generally accepted criteria do not yet exist. The chemical profile of "poplar" propolis, typical for the temperate zone, can be characterized by the following parameters: total flavone and flavonol content, total flavanone and dihydroflavonol content, and total phenolics content. These parameters correlate better with the biological activity and are more informative that the quantification of individual components. There is still a lot of work to be done to achieve standardization of other propolis types. Working with standardized material will allow scientists to connect a particular chemical propolis type to a specific type of biological activity and formulate recommendations for mainstream practitioners.
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            Quantification of polyphenolics and their antioxidant capacity in fresh plums.

            Dae-Ok Kim, Ock Kyoung Chun, Young Jun Kim … (2003)
            Total phenolics, total flavonoids, and antioxidant capacity of 11 cultivars of fresh plums were determined using spectrophotometric methods. Identification and quantification of individual polyphenolics were performed using reversed-phase high-performance liquid chromatography equipped with a diode array detector. The total phenolic contents of various cultivars widely varied from 125.0 to 372.6 mg/100 g expressed as gallic acid equivalents. The level of total flavonoids in fresh plums ranged between 64.8 and 257.5 mg/100 g expressed as catechin equivalents. Antioxidant capacity, expressed as vitamin C equivalent antioxidant capacity (VCEAC), ranged from 204.9 to 567.0 mg/100 g with an average of 290.9 mg/100 g of fresh weight. Cv. Beltsville Elite B70197 showed the highest amounts of total phenolics and total flavonoids and the highest VCEAC. A positive relationship (correlation coefficient r (2)() = 0.977) was presented between total phenolics and VCEAC, suggesting polyphenolics would play an important role in free radical scavenging. The level of IC(50) value of superoxide radical anion scavenging activity of the plum cultivars ranged from 13.4 to 45.7 mg of VCEAC/100 g. Neochlorogenic acid was the predominant polyphenolic among fresh plums tested. Flavonols found in plum were commonly quercetin derivatives. Rutin was the most predominant flavonol in plums. Various anthocyanins containing cyanidin aglycon and peonidin aglycon were commonly found in all plums except for cv. Mirabellier and NY 101.
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              Botanical origin and chemical composition of Brazilian propolis.

              Regina Aguiar, Cecília S. Alencar, Christopher Y. Park (2002)
              Brazilian propolis has been classified into 12 groups based on physicochemical characteristics: five in the southern Brazil group (group 3), one in the southeastern Brazil group (group 12), and six in the northeastern Brazil group (group 6). The plant origins of these groups were investigated using reversed-phase high-performance thin-layer chromatography (RPHPTLC), reversed-phase high-performance liquid chromatography (RPHPLC), and gas chromatography-mass spectrometry (GC-MS). It was concluded that the origins of propolis group 3, group 6, and group 12 are resins of the poplar tree, Hyptis divaricata, and Baccharis dracunculifolia, respectively.
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                Author and article information

                Contributors
                Vijai Gupta: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 30 March 2017
                Publication date Collection: 2017
                Volume: 12
                Issue: 3
                Electronic Location Identifier: e0172585
                Affiliations
                [1 ]Department of Pharmacy, Federal University of Bahia, Salvador, Bahia, Brazil
                [2 ]Department of Biotechnology and Food, Faculty of Technology, SENAI/CIMATEC, National Service of Industrial Learning – SENAI, Salvador, Bahia, Brazil
                [3 ]Institute of Technology in Health, Faculty of Technology, SENAI/CIMATEC, National Service of Industrial Learning – SENAI, Salvador, Bahia, Brazil
                [4 ]Department of Physiology, Federal University of Sergipe, São Cristovão, Sergipe, Brazil
                [5 ]Department of Pharmacy, Federal University of Sergipe, Lagarto, Sergipe, Brazil
                [6 ]Institute of Research and Technology, Tiradentes University, Aracaju, Sergipe, Brazil
                [7 ]Department of Biotechnology, Federal University of Bahia, Salvador, Bahia, Brazil
                Tallinn University of Technology, ESTONIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: RPDS BASM GAB SSC MAUG.

                • Data curation: RPDS BASM GAB FFP MAUG.

                • Formal analysis: RPDS BASM GAB SSC LNA RGA AAC.

                • Funding acquisition: RPDS BASM FFP MAUG JDVB.

                • Investigation: RPDS BASM MAUG.

                • Methodology: GAB SSC LNA RGA AAC FFP.

                • Project administration: RPDS BASM FFP MAUG JDVB.

                • Resources: RPDS BASM GAB SSC LNA RGA AAC JDVB.

                • Software: RPDS RGA AAC FFP MAUG JDVB.

                • Supervision: RPDS BASM SSC MAUG.

                • Validation: RPDS BASM GAB SSC MAUG.

                • Visualization: RPDS BASM SSC LNA RGA AAC.

                • Writing – original draft: RPDS BASM MAUG.

                • Writing – review & editing: RPDS BASM MAUG JDVB.

                ‡ These authors also contributed equally to this work.

                Article
                Publisher ID: PONE-D-16-11243
                DOI: 10.1371/journal.pone.0172585
                PMC ID: 5373518
                PubMed ID: 28358806
                SO-VID: ac252da6-42c3-4fec-afcd-77a6c0ed4651
                Copyright © © 2017 Dantas Silva et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 9 April 2016
                Date accepted : 7 February 2017
                Page count
                Figures: 2, Tables: 3, Pages: 18
                Funding
                The authors would like to thank Serviço Nacional de Aprendizagem Industrial – Departamento Nacional (SENAI DN), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), APIS Nativa Produtos Naturais LTDA Company, Laboratório de Oncologia Experimental (Universidade Federal do Ceará) and the Gonçalo Moniz Research Centre – FIOCRUZ (Rio de Janeiro). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Antioxidants
                Subject: Research and Analysis Methods
                Subject: Extraction Techniques
                Subject: Supercritical Fluid Extraction
                Subject: People and places
                Subject: Geographical locations
                Subject: South America
                Subject: Brazil
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Protozoans
                Subject: Parasitic Protozoans
                Subject: Trypanosoma
                Subject: Trypanosoma Cruzi
                Subject: Biology and Life Sciences
                Subject: Developmental Biology
                Subject: Life Cycles
                Subject: Protozoan Life Cycles
                Subject: Epimastigotes
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Protozoology
                Subject: Protozoan Life Cycles
                Subject: Epimastigotes
                Subject: Medicine and Health Sciences
                Subject: Pharmacology
                Subject: Drugs
                Subject: Antimicrobials
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Microbial Control
                Subject: Antimicrobials
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Staphylococcus
                Subject: Staphylococcus Aureus
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Medical Microbiology
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Staphylococcus
                Subject: Staphylococcus Aureus
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Pathogens
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Staphylococcus
                Subject: Staphylococcus Aureus
                Subject: Physical Sciences
                Subject: Chemistry
                Subject: Chemical Compounds
                Subject: Organic Compounds
                Subject: Alcohols
                Subject: Ethanol
                Subject: Physical Sciences
                Subject: Chemistry
                Subject: Organic Chemistry
                Subject: Organic Compounds
                Subject: Alcohols
                Subject: Ethanol
                Custom metadata
                Data Availability All relevant data are within the paper and its Supporting Information files.

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