Research Article
No access
Published Online: 14 July 2014

Topical Anti-Inflammatory Activity of a Monofloral Honey of Mimosa scabrella Provided by Melipona marginata During Winter in Southern Brazil

Publication: Journal of Medicinal Food
Volume 17, Issue Number 7

Abstract

Melipona marginata is an endangered species of stingless bee from Brazil that produces honey with particular physicochemical features and a remarkable exotic flavor. To the best of our knowledge, this is the first report devoted to exploring the medicinal potential of this honey. Thus, the aim of this paper was to investigate the potential anti-inflammatory activity of honey extract from M. marginata on skin inflammation. The honey sample was classified as a monofloral honey of Mimosa scabrella. The presence of 11 phenolic compounds as kaempferol and caffeic acid was detected using the high-performance liquid chromatography-electrospray ionization-tandem mass spectrometry (HPLC-UV-ESI-MS) method. The anti-inflammatory activity was measured using a 12-O-tetradecanoylphorbol-13-acetate-induced ear edema model of inflammation in mice. The topical application of the M. marginata honey extract (1.0 mg/ear) was able to reduce ear edema with an inhibitory effect of 54±5%. This extract decreased the myeloperoxidase activity in 75±3%, which suggests a lower leucocyte infiltration that was confirmed by histological analysis. This extract also provided a reduction of 55±14% in the production of reactive oxygen species. This anti-inflammatory activity could be due to a synergic effect of the phenolic compounds identified in the honey sample. Taken together, these results open up new possibilities for the use of M. marginata honey extract in skin disorders.

Get full access to this article

View all available purchase options and get full access to this article.

References

1.
Fernández-Torres R, Pérez-Bernal JL, Bello-López MÁ, Callejón-Mochón M, Jiménez-Sánches JC, Guiraúm-Pérez A: Mineral content and botanical origin of Spanish honeys. Talanta 2005;65:686–691.
2.
Ouchemoukh S, Louaileche H, Schweitzer P: Physicochemical characteristics and pollen spectrum of some Algerian honeys. Food Control 2007;18:52–58.
3.
Arráez-Román D, Gómez-Caravaca AM, Gómez-Romero M, Segura-Carretero A, Fernández-Gutiérrez A: Identification of phenolic compounds in rosemary honey using solid-phase extraction by capillary electrophoresis-electrospray ionization-mass spectrometry. J Pharm Biomed Anal 2006;41:1648–1656.
4.
Borsato DM, Vargas T, Koop L, Farago PV, de Almeida MM: Physicochemical quality control of bee honeys from Campos Gerais region of Paraná—Brazil. B Ctr Pesqui Proc Al 2010;28:205–212.
5.
Alvarez-Suarez J, Tulipani S, Romandini S, Bertoli E, Battino M: Contribution of honey in nutrition and human health: a review. Med J Nutrition Metab 2010;3:15–23.
6.
Bogdanov S, Jurendic T, Sieber R, Gallmann P: Honey for nutrition and health: a review. J Am Coll Nutr 2008;27:677–689.
7.
Pérez E, Rodríguez-Malaver AJ, Vit P: Antioxidant capacity of Venezuelan honey in Wistar rat homogenates. J Med Food 2006;9:510–516.
8.
Garedew A, Schmolz E, Lamprecht I: Microcalorimetric investigation on the antimicrobial activity of honey of the stingless bee Trigona spp. and comparison of some parameters with those obtained with standard methods. Thermochim Acta 2004;415:99–106.
9.
Guerrini A, Bruni R, Maietti S et al.: Ecuadorian stingless bee (Meliponinae) honey: a chemical and functional profile of an ancient health product. Food Chem 2009;114:1413–1420.
10.
de Almeida-Muradian LB, Matsuda AH, Bastos DHM: Physicochemical parameters of amazon Melipona honey. Quim Nova 2007;30:707–708.
11.
Torres A, Garedew A, Schmolz E, Lamprecht I: Calorimetric investigation of the antimicrobial action and insight into the chemical properties of “angelita” honey—a product of the stingless bee Tetragonisca angustula from Colombia. Thermochim Acta 2004;415:107–113.
12.
Boorn Kl, Khor YY, Sweetman E, Tan F, Heard TA, Hammer KA: Antimicrobial activity of honey from the stingless bee Trigona carbonaria determined by agar diffusion, agar dilution, broth microdilution and time-kill methodology. J Appl Microbiol 2010;108:1534–1543.
13.
Irish J, Carter DA, Blair SE, Heard TA: Antibacterial activity of honey from the Australian stingless bee Trigona carbonaria. Int J Antimicrob Agents 2008;32:89–90.
14.
Moure JS, Urban D, Melo GAR (Orgs.): Catalogue of bees (Hymenoptera, Apoidea) in the Neotropical region. Sociedade Brasileira de Entomologia, Curitiba, Brazil, 2007.
15.
Alves DFS, Cabral Júnior F das C, Cabral PP de AC, de Oliveira Junior RM, do Rego ACM, Medeiros AC: Efeitos da aplicação tópica do mel de Melipona subnitida em feridas infectadas de ratos. Rev Col Bras Cir 2008;35:188–193.
16.
Marques AAB, Fontana CS, Vélez E, Bencke GA, Schneider M, Dos Reis RE: Lista das espécies da fauna ameaçadas de extinção no Rio Grande do Sul. Decreto no. 41672, de 11 de junho de 2002. FZB/MCT-PUCRS/PANGEA, PUCRS, Porto Alegre, Brazil, 2002.
17.
Silveira FA, Melo GAR, Almeida EAB: Abelhas brasileiras: sistemática e identificação, 1 ed. Editoração eletrônica, Belo Horizonte, Brazil, 2002.
18.
Araujo ED, Costa M, Chaud-Netto J, Fowler HG: Body size and flight distance in stingless bees (Hymenoptera: Meliponini): inference of flight range and possible ecological implications. Braz J Biol 2004;64:563–568.
19.
Kleinert A de MP: Colony strength and queen replacement in Melipona marginata (Apidae: Meliponini). Braz J Biol 2005;65:469–476.
20.
Ferreira-Caliman MJ, Nascimento FS, Turatti IC, Mateus S, Lopes NP, Zucchi R: The cuticular hydrocarbons profiles in the stingless bee Melipona marginata reflect task-related differences. J Insect Physiol 2010;56:800–804.
21.
Ramirez SR, Nieh JC, Quental TB, Roubik DW, Imperatriz-Fonseca VL, Pierce NE: A molecular phylogeny of the stingless bee genus Melipona (Hymenoptera: Apidae). Mol Phylogenet Evol 2010;56:519–525.
22.
Moraes EHF, Alvarenga MA, Ferreira ZMGS: As bases nitrogenadas de Mimosa scabrella Bentham. Quim Nova 1990;13:308–309.
23.
Louveaux J, Maurizio A, Vorwohl G: Methods of melissopalynology. Bee World 1970;5:125–138.
24.
Barth OM: O pólen no mel brasileiro. Luxor, Rio de Janeiro, Brazil, 1989.
25.
Nair PKKA: A modification in the method of pollen preparation. J Sci Ind Res 1960;19:26–27.
26.
Melhen TS, Cruz-Barros MAV, Corrêa AMS, Makino-Watanabe H, Silvestre-Capelato MSF, Gonçalves-Esteves V: Variabilidade polínica em plantas de Campos do Jordão (São Paulo, Brasil). Bol Inst Bot 2003;16:1–104.
27.
Ferreres F, Tomás-Barberán FA, Gil MI, Tomás-Lorente F: An HPLC technique for flavonoid analysis in honey. J Sci Food Agr 1991;56:49–56.
28.
Kassim M, Achoui M, Mustafa MR, Mohd MA, Yusoff KM: Ellagic acid, phenolic acids, and flavonoids in Malaysian honey extracts demonstrate in vitro anti-inflammatory activity. Nutr Res 2010;30:650–659.
29.
Jasicka-Misiak I, Poliwoda A, Deren M, Kafarski P: Phenolic compounds and abscisic acid as potential markers for the floral origin of two Polish unifloral honeys. Food Chem 2012;131:1149–1156.
30.
Committee for the Update of the Guide for the Care and Use of Laboratory Animals, National Research Council: Guide for the Care and Use of Laboratory Animals, 8th ed. The National Academy Press, Washington, DC, 2011.
31.
Otuki MF, Bernardi CA, Prudente AS et al.: Garcinia gardneriana (Planchon & Triana) Zappi. (Clusiaceae) as a topical anti-inflammatory alternative for cutaneous inflammation. Basic Clin Pharmacol Toxicol 2011;109:56–62.
32.
Swingle KF, Reiter MJ, Schwartzmiller DH: Comparison of croton oil and cantharidin induced inflammations of the mouse ear and their modification by topically applied drugs. Arch Int Pharmacodyn Ther 1981;254:168–176.
33.
Tragni E, Tubaro A, Melis S, Galli CL: Evidence from two classic irritation tests for an anti-inflammatory action of a natural extract, Echinacina B. Food Chem Toxicol 1985;23:317–319.
34.
Suzuki K, Ota H, Sasagawa S, Sakatani T, Fujikura T: Assay method for myeloperoxidase in human polymorphonuclear leukocytes. Anal Biochem 1983;132:345–352.
35.
de Young LM, Kheifets JB, Ballaron SJ, Young JM: Oedema and cell infiltration in the phorbol ester-treated mouse ear are temporally separate and can be differentially modulated by pharmacologic agents. Agents Actions 1989;26:335–341.
36.
Recio MC, Giner RM, Uriburu L et al.: In vivo activity of pseudoguaianolide sesquiterpene lactones in acute and chronic inflammation. Life Sci 2000;66:2509–2518.
37.
Boller S, Soldi C, Marques MC et al.: Anti-inflammatory effect of crude extract and isolated compounds from Baccharis illinita DC in acute skin inflammation. J Ethnopharmacol 2010;130:262–266.
38.
Keston AS, Brandt R: The fluorometric analysis of ultramicro quantities of hydrogen peroxide. Anal Biochem 1965;11:1–5.
39.
Driver AS, Kodavanti PR, Mundy WR: Age-related changes in reactive oxygen species production in rat brain homogenates. Neurotoxicol Teratol 2000;22:175–181.
40.
Larrosa M, Luceri C, Vivoli E, et al.: Polyphenol metabolites from colonic microbiota exert anti-inflammatory activity on different inflammation models. Mol Nutr Food Res 2009;53:1044–1054.
41.
Crespo I, García-Mediavilla MV, Gutiérrez B, Sánchez-Campos S, Tuñón MJ, González-Gallego J: A comparison of the effects of kaempferol and quercetin on cytokine-induced pro-inflammatory status of cultured human endothelial cells. Br J Nutr 2008;100:968–976.
42.
Funakoshi-Tago M, Nakamura K, Tago K, Mashino T, Kasahara T: Anti-inflammatory activity of structurally related flavonoids, apigenin, luteolin and fisetin. Int Immunopharmacol 2011;11:1150–1159.
43.
Fabrowski FJ, Nakashima T, Muñiz GIB, Mazza MCM, Klock U. Caracterização químico-qualitativa das variedades populares da bracatinga (Mimosa scabrella Bentham). Bol Pesq Fl 2002;44:13–28.
44.
De Young LM, Kheifets JB, Ballaron SJ, Young JM. Oedema and cell infiltration in the phorbol ester-treated mouse ear are temporally separate and can be differentially modulated by pharmacologic agents. Agents Actions 1989;26:335–341.
45.
Gábor M. Mouse ear inflammation models and their pharmacological applications. Akadémiai Kiadó, Budapest, 2001.
46.
Otuki MF, Vieira-Lima F, Malheiros Â, Yunes RA, Calixto JB. Topical anti-inflammatory effects of the ether extract from Protium kleinii and α-amyrin pentacyclic triterpene. Eur J Pharmacol 2005;507:253–259.
47.
Rahman S, Ansari RA, Rehman H, Parvez S, Raisuddin S. Nordihydroguaiaretic acid from creosote bush (Larrea tridentata) mitigates 12-O-tetradecanoylphorbol-13-acetate-induced inflammatory and oxidative stress responses of tumor promotion cascade in mouse skin. Evid Based Complement Alternat Med 2011;2011:734–785.
48.
Denning MF. Epidermal keratinocytes: regulation of multiple cell phenotypes by multiple protein kinase C isoforms. Int J Biochem Cell Biol 2004;36:1141–1146.
49.
Winyard PG: Key stages in the acute inflammatory response and their relevance as therapeutic targets. In: Inflammation Protocols (Winyard PG, Willoughby DA, ed.) Humana Press, Totowa, NJ, 2003, pp. 3–4.
50.
Bradley PP, Priebat DA, Christensen RD, Rothstein G: Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 1982;78:206–209.
51.
Okayama Y: Oxidative stress in allergic and inflammatory skin diseases. Curr Drug Targets 2005;4:517–519.
52.
Shahidi F: Funtional foods: their role in health promotion and disease prevention. J Food Sci 2004;69:146–149.
53.
Nakamura Y, Kozuka M, Naniwa K et al.: Arachidonic acid cascade inhibitors modulate phorbol ester-induced oxidative stress in female ICR mouse skin: differential roles of 5-lipoxygenase and cyclooxygenase-2 in leukocyte infiltration and activation. Free Radic Biol Med 2003;35:997–1007.
54.
Park KK, Park JH, Jung YJ, Chung WY: Inhibitory effects of chlorophyllin, hemin and tetrakis(4-benzoic acid)porphyrin on oxidative DNA damage and mouse skin inflammation induced by 12-O-tetradecanoylphorbol-13-acetate as a possible anti-tumor promoting mechanism. Mutat Res 2003;542:89–97.
55.
Slaga TJ: Overview of tumor promotion in animals. Environ Health Perspect 1983;50:3–14.
56.
Furstenberger G, Sorg B, Marks F: Tumor promotion by phorbol esters in skin: evidence for a memory effect. Science 1983;220:89–91.
57.
Slaga TJ: Multistage skin carcinogenesis: a useful model for the study of the chemoprevention of cancer. Acta Pharmacol Toxicol 1984;55:107–124.

Information & Authors

Information

Published In

cover image Journal of Medicinal Food
Journal of Medicinal Food
Volume 17Issue Number 7July 2014
Pages: 817 - 825
PubMed: 24650139

History

Published online: 14 July 2014
Published in print: July 2014
Published ahead of print: 20 March 2014
Accepted: 3 January 2014
Received: 29 January 2013

Permissions

Request permissions for this article.

Topics

Authors

Affiliations

Débora M. Borsato
Department of Pharmacy, Federal University of Paraná, Curitiba, Brazil.
Arthur S. Prudente
Department of Pharmacology, Federal University of Paraná, Curitiba, Brazil.
Patrícia M. Döll-Boscardin
Department of Pharmaceutical Sciences, State University of Ponta Grossa, Ponta Grossa, Brazil.
Aurélio V. Borsato
Brazilian Agricultural Research Corporation, Embrapa Pantanal, Corumbá, Brazil.
Cynthia F. P. Luz
Institute of Botany, São Paulo, Brazil.
Beatriz H. L. N. S. Maia
Department of Chemistry, Federal University of Paraná, Curitiba, Brazil.
Daniela A. Cabrini
Department of Pharmacology, Federal University of Paraná, Curitiba, Brazil.
Michel F. Otuki
Department of Pharmaceutical Sciences, State University of Ponta Grossa, Ponta Grossa, Brazil.
Marilis D. Miguel
Department of Pharmacy, Federal University of Paraná, Curitiba, Brazil.
Paulo V. Farago
Department of Pharmaceutical Sciences, State University of Ponta Grossa, Ponta Grossa, Brazil.
Obdulio G. Miguel
Department of Pharmacy, Federal University of Paraná, Curitiba, Brazil.

Notes

Address correspondence to: Paulo Vitor Farago, PhD, Department of Pharmaceutical Sciences, State University of Ponta Grossa, 4748, Carlos Cavalcanti Ave., Uvaranas, 84030-900, Ponta Grossa, Paraná, Brazil, E-mail: [email protected]

Author Disclosure Statement

No competing financial interests exist.

Metrics & Citations

Metrics

Citations

Export citation

Select the format you want to export the citations of this publication.

View Options

Access content

To read the fulltext, please use one of the options below to sign in or purchase access.

Society Access

If you are a member of a society that has access to this content please log in via your society website and then return to this publication.

Restore your content access

Enter your email address to restore your content access:

Note: This functionality works only for purchases done as a guest. If you already have an account, log in to access the content to which you are entitled.

View options

PDF/EPUB

View PDF/EPUB

Full Text

View Full Text

Figures

Tables

Media

Share

Share

Copy the content Link

Share on social media

Back to Top