Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
BMC Complementary Medicine and Therapies
Published in: BMC Complementary Medicine and Therapies 1/2011

Open Access 01-12-2011 | Research article

Antimicrobial activity against oral pathogens and immunomodulatory effects and toxicity of geopropolis produced by the stingless bee Melipona fasciculata Smith

Authors: Silvana A Liberio, Antônio Luís A Pereira, Richard P Dutra, Aramys S Reis, Maria José AM Araújo, Nadia S Mattar, Lucilene A Silva, Maria Nilce S Ribeiro, Flávia Raquel F Nascimento, Rosane NM Guerra, Valério Monteiro-Neto

Published in: BMC Complementary Medicine and Therapies | Issue 1/2011

Login to get access

Abstract

Background

Native bees of the tribe Meliponini produce a distinct kind of propolis called geopropolis. Although many pharmacological activities of propolis have already been demonstrated, little is known about geopropolis, particularly regarding its antimicrobial activity against oral pathogens. The present study aimed at investigating the antimicrobial activity of M. fasciculata geopropolis against oral pathogens, its effects on S. mutans biofilms, and the chemical contents of the extracts. A gel prepared with a geopropolis extract was also analyzed for its activity on S. mutans and its immunotoxicological potential.

Methods

Antimicrobial activities of three hydroalcoholic extracts (HAEs) of geopropolis, and hexane and chloroform fractions of one extract, were evaluated using the agar diffusion method and the broth dilution technique. Ethanol (70%, v/v) and chlorhexidine (0.12%, w/w) were used as negative and positive controls, respectively. Total phenol and flavonoid concentrations were assayed by spectrophotometry. Immunotoxicity was evaluated in mice by topical application in the oral cavity followed by quantification of biochemical and immunological parameters, and macro-microscopic analysis of animal organs.

Results

Two extracts, HAE-2 and HAE-3, showed inhibition zones ranging from 9 to 13 mm in diameter for S. mutans and C. albicans, but presented no activity against L. acidophilus. The MBCs for HAE-2 and HAE-3 against S. mutans were 6.25 mg/mL and 12.5 mg/mL, respectively. HAE-2 was fractionated, and its chloroform fraction had an MBC of 14.57 mg/mL. HAE-2 also exhibited bactericidal effects on S. mutans biofilms after 3 h of treatment. Significant differences (p < 0.05) in total phenol and flavonoid concentrations were observed among the samples. Signs toxic effects were not observed after application of the geopropolis-based gel, but an increase in the production of IL-4 and IL-10, anti-inflammatory cytokines, was detected.

Conclusions

In summary, geopropolis produced by M. fasciculata can exert antimicrobial action against S. mutans and C. albicans, with significant inhibitory activity against S. mutans biofilms. The extract with the highest flavonoid concentration, HAE-2, presented the highest antimicrobial activity. In addition, a geopropolis-based gel is not toxic in an animal model and displays anti-inflammatory effect.
Appendix
Available only for authorised users
Literature
1.
2.
Banskota AH, Tezuka Y, Adnyana IK, Midorikawa K, Matsushige K, Message D, Huertas AA, Kadota S: Cytotoxic, hepatoprotective and free radical scavenging effects of propolis from Brazil, Peru, the Netherlands and China. J Ethnopharmacol. 2000, 72 (1-2): 239-246. 10.1016/S0378-8741(00)00252-X.CrossRefPubMed
3.
Dobrowolski JW, Vohora SB, Sharma K, Shah SA, Naqvi SA, Dandiya PC: Antibacterial, antifungal, antiamoebic, antiinflammatory and antipyretic studies on propolis bee products. J Ethnopharmacol. 1991, 35 (1): 77-82. 10.1016/0378-8741(91)90135-Z.CrossRefPubMed
4.
Sforcin JM: Propolis and the immune system: a review. J Ethnopharmacol. 2007, 113 (1): 1-14. 10.1016/j.jep.2007.05.012.CrossRefPubMed
5.
Bankova V: Chemical diversity of propolis and the problem of standardization. J Ethnopharmacol. 2005, 100 (1-2): 114-117. 10.1016/j.jep.2005.05.004.CrossRefPubMed
6.
Velikova M, Bankova V, Marcucci MC, Tsvetkova I, Kujumgiev A: Chemical composition and biological activity of propolis from Brazilian meliponinae. Z Naturforsch [C]. 2000, 55 (9-10): 785-789.
7.
Pereira AL, Bicalho B, Aquino-Neto FR: Comparison of propolis from Apis mellifera and Tetragonisca angustula. Apidologie. 2003, 34: 291-298. 10.1051/apido:2003023.CrossRef
8.
Bankova V, Popova M: Propolis of stingless bees: a promising source of biologically active compounds. Pharmacog Rev. 2007, 1 (1): 88-92.
9.
Roubik D: Ecology and Natural History of Tropical Bees. 1989, Cambridge: Cambridge Univ. PressCrossRef
10.
Kerr WE: Biologia e manejo da tiúba: a abelha do Maranhão. 1996, São Luís, MA: EDUFMA
11.
Castaldo S, Capasso F: Propolis, an old remedy used in modern medicine. Fitoterapia. 2002, 73 (Suppl 1): S1-6.CrossRefPubMed
12.
Quezada-Euan JJG, de Jesus May-Itza W, Gonzalez-Acereto JA: Meliponiculture in Mexico: problems and perspectives for development. Bee World. 2001, 82: 160-167.CrossRef
13.
Kujumgiev A, Tsvetkova I, Serkedjieva Y, Bankova V, Christov R, Popov S: Antibacterial, antifungal and antiviral activity of propolis of different geographic origin. J Ethnopharmacol. 1999, 64 (3): 235-240. 10.1016/S0378-8741(98)00131-7.CrossRefPubMed
14.
Farnesi AP, Aquino-Ferreira R, De Jong D, Bastos JK, Soares AE: Effects of stingless bee and honey bee propolis on four species of bacteria. Genet Mol Res. 2009, 8 (2): 635-640. 10.4238/vol8-2kerr023.CrossRefPubMed
15.
Uzel A, Sorkun K, Oncag O, Cogulu D, Gencay O, Salih B: Chemical compositions and antimicrobial activities of four different Anatolian propolis samples. Microbiol Res. 2005, 160 (2): 189-195. 10.1016/j.micres.2005.01.002.CrossRefPubMed
16.
Ikeno K, Ikeno T, Miyazawa C: Effects of propolis on dental caries in rats. Caries Res. 1991, 25 (5): 347-351. 10.1159/000261390.CrossRefPubMed
17.
Koo H, Gomes BP, Rosalen PL, Ambrosano GM, Park YK, Cury JA: In vitro antimicrobial activity of propolis and Arnica montana against oral pathogens. Arch Oral Biol. 2000, 45 (2): 141-148. 10.1016/S0003-9969(99)00117-X.CrossRefPubMed
18.
Liberio SA, Pereira AL, Araujo MJ, Dutra RP, Nascimento FR, Monteiro-Neto V, Ribeiro MN, Goncalves AG, Guerra RN: The potential use of propolis as a cariostatic agent and its actions on mutans group streptococci. J Ethnopharmacol. 2009, 125 (1): 1-9. 10.1016/j.jep.2009.04.047.CrossRefPubMed
19.
Park YK, Koo MH, Abreu JA, Ikegaki M, Cury JA, Rosalen PL: Antimicrobial activity of propolis on oral microorganisms. Curr Microbiol. 1998, 36 (1): 24-28. 10.1007/s002849900274.CrossRefPubMed
20.
Sawaya ACHF, Souza KS, Marcucci MC, Cunha IBS, Shimizu MT: Analysis of the composition of Brazilian propolis extracts by chromatography and evaluation of their in vitro activity against gram-positive bacteria. Braz J Microbiol. 2004, 35 (1-2): 104-109. 10.1590/S1517-83822004000100017.CrossRef
21.
Burdock GA: Review of the biological properties and toxicity of bee propolis (propolis). Food Chem Toxicol. 1998, 36 (4): 347-363. 10.1016/S0278-6915(97)00145-2.CrossRefPubMed
22.
Jasprica I, Mornar A, Debeljak Z, Smolcic-Bubalo A, Medic-Saric M, Mayer L, Romic Z, Bucan K, Balog T, Sobocanec S: In vivo study of propolis supplementation effects on antioxidative status and red blood cells. J Ethnopharmacol. 2007, 110 (3): 548-554. 10.1016/j.jep.2006.10.023.CrossRefPubMed
23.
Mani F, Damasceno HCR, Novelli ELB, Martins EAM, Sforcin JM: Propolis: Effect of different concentrations, extracts and intake period on seric biochemical variables. J Ethnopharmacol. 2006, 105: 95-98. 10.1016/j.jep.2005.10.011.CrossRefPubMed
24.
Mohammadzadeh S, Shariatpanahi M, Hamedi M, Ahmadkhaniha R, Samadi N, Ostad SN: Chemical composition, oral toxicity and antimicrobial activity of Iranian propolis. Food Chem. 2007, 103: 1097-1103. 10.1016/j.foodchem.2006.10.006.CrossRef
25.
Moreno MIN, Zampini IC, Ordóñez RM, Jaime GS, Vattuone MA, Isla MI: Evaluation of the cytotoxicity, genotoxicity, mutagenicity, and antimutagenicity of propolis from Tucuman, Argentina. J Agric Food Chem. 2005, 53: 8957-8962. 10.1021/jf0513359.CrossRef
26.
Ahuja A, (ed.): Handbook of Bioseparations. 2000, New York: Academic Press
27.
Ferro VA, Bradbury F, Cameron P, Shakir E, Rahman SR, Stimson WH: In vitro susceptibilities of Shigella flexneri and Streptococcus pyogenes to inner gel of Aloe barbadensis Miller. Antimicrob Agents Chemother. 2003, 47 (3): 1137-1139. 10.1128/AAC.47.3.1137-1139.2003.CrossRefPubMedPubMedCentral
28.
Koo H, Rosalen PL, Cury JA, Ambrosano GM, Murata RM, Yatsuda R, Ikegaki M, Alencar SM, Park YK: Effect of a new variety of Apis mellifera propolis on mutans Streptococci. Curr Microbiol. 2000, 41 (3): 192-196. 10.1007/s0028400101170.CrossRefPubMed
29.
Curran TM, Ma Y, Rutherford GC, Marquis RE: Turning on and turning off the arginine deiminase system in oral streptococci. Can J Microbiol. 1998, 44: 1078-1085. 10.1139/w98-106.CrossRefPubMed
30.
Koo H, Pearson SK, Scott-Anne K, Abranches J, Cury JA, Rosalen PL, Park YK, Marquis RE, Bowen WH: Effects of apigenin and tt-farnesol on glucosyltransferase activity, biofilm viability and caries development in rats. Oral Microbiol Immunol. 2002, 17 (6): 337-343. 10.1034/j.1399-302X.2002.170602.x.CrossRefPubMed
31.
Koo H, Rosalen PL, Cury JA, Park YK, Bowen WH: Effects of compounds found in propolis on Streptococcus mutans growth and on glucosyltransferase activity. Antimicrob Agents Chemother. 2002, 46 (5): 1302-1309. 10.1128/AAC.46.5.1302-1309.2002.CrossRefPubMedPubMedCentral
32.
Enríquez A, Prieto E, De Los Ríos E, Ruiz S: Estudio farmacognóstico y fitoquímico del rizoma de Zingiber officinale Roscoe "Jengibre" de la ciudad de Chanchamayo - Región Junín. Perú. Rev Med Vallejiana. 2008, 5 (1): 50-64.
33.
Woisky RGR, Salatino A: Analysis of propolis: some parameters and procedures for chemical quality control. J Apic Res. 1998, 37: 99-105.CrossRef
34.
Matos FJA: Introdução à Fitoquímica Experimental. 2009, Fortaleza: UFC, 3
35.
Brazil: Instrução Normativa n°3, de 19 de janeiro de 2001. Aprova os regulamentos Técnicos de Identidade e Qualidade de Apitoxina, Cera de Abelha, Geléia Real, Geléia Real Liofilizada, Pólen Apícola, Própolis e Extrato de Própolis, conforme consta dos Anexos desta Instrução Normativa. Edited by: Ministério da Agricultura PedA. 2001, Brasília DF: Diário Oficial da União, 18-
36.
Alencar SM, Oldoni TL, Castro ML, Cabral IS, Costa-Neto CM, Cury JA, Rosalen PL, Ikegaki M: Chemical composition and biological activity of a new type of Brazilian propolis: red propolis. J Ethnopharmacol. 2007, 113 (2): 278-283. 10.1016/j.jep.2007.06.005.CrossRefPubMed
37.
Steinberg D, Kaine G, Gedalia I: Antibacterial effect of propolis and honey on oral bacteria. Am J Dent. 1996, 9 (6): 236-239.PubMed
38.
Koru O, Toksoy F, Acikel CH, Tunca YM, Baysallar M, Uskudar Guclu A, Akca E, Ozkok Tuylu A, Sorkun K, Tanyuksel M: In vitro antimicrobial activity of propolis samples from different geographical origins against certain oral pathogens. Anaerobe. 2007, 13 (3-4): 140-145. 10.1016/j.anaerobe.2007.02.001.CrossRefPubMed
39.
40.
Marsh PD: Microbiologic aspects of dental plaque and dental caries. Dent Clin North Am. 1999, 43 (4): 599-614.PubMed
41.
van Houte J: Role of micro-organisms in caries etiology. J Dent Res. 1994, 73 (3): 672-681.PubMed
42.
Duailibe SA, Goncalves AG, Ahid FJ: Effect of a propolis extract on Streptococcus mutans counts in vivo. J Appl Oral Sci. 2007, 15 (5): 420-423. 10.1590/S1678-77572007000500009.CrossRefPubMedPubMedCentral
43.
Duarte S, Rosalen PL, Hayacibara MF, Cury JA, Bowen WH, Marquis RE, Rehder VL, Sartoratto A, Ikegaki M, Koo H: The influence of a novel propolis on mutans streptococci biofilms and caries development in rats. Arch Oral Biol. 2006, 51 (1): 15-22. 10.1016/j.archoralbio.2005.06.002.CrossRefPubMed
44.
Twetman S: Antimicrobials in future caries control? A review with special reference to chlorhexidine treatment. Caries Res. 2004, 38 (3): 223-229. 10.1159/000077758.CrossRefPubMed
45.
Apkan A, Morgan R: Oral candidiasis. J Postgrad Med. 2002, 78: 455-459. 10.1136/pmj.78.922.455.CrossRef
46.
Samaranayake LP: Oral candidosis: an old disease in new guises. Dent Update. 1990, 17 (1): 36-38.PubMed
47.
Freitas MO, Ponte FAF, Lima MAS, Silveira ER: Flavonoids and Triterpenes from the Nest of the Stingless Bee Trigona spinipes. J Braz Chem Soc. 2008, 19 (3): 532-535. 10.1590/S0103-50532008000300022.CrossRef
48.
Katircioglu H, Mercan N: Antimicrobial activity and chemical compositions of Turkish propolis from different regions. Afr J Biotechnol. 2006, 5: 1151-1153.
49.
Russo A, Longo R, Vanella A: Antioxidant activity of propolis: role of caffeic acid phenethyl ester and galangin. Fitoterapia. 2002, 73 (Suppl 1): S21-29.CrossRefPubMed
50.
Cushnie TPT, Lamb AJ: Antimicrobial activity of flavonoids. Int J Antimicrob Agents. 2005, 26 (5): 343-356. 10.1016/j.ijantimicag.2005.09.002.CrossRefPubMed
51.
Callejo A, Armentia A, Lombardero M, Asensio T: Propolis, a new bee-related allergen. Allergy. 2001, 56 (6): 579-10.1034/j.1398-9995.2001.056006579.x.CrossRefPubMed
52.
Walgrave SE, Warshaw EM, Glesne LA: Allergic contact dermatitis from propolis. Dermatitis. 2005, 16: 209-215. 10.2310/6620.2005.05019.PubMed
53.
Bhadauria M, Nirala SK, Shukla S: Multiple treatment of propolis extract ameliorates carbon tetrachloride induced liver injury in rats. Food Chem Toxicol. 2008, 46: 2703-2712. 10.1016/j.fct.2008.04.025.CrossRefPubMed
54.
Ozen S, Akyol O, Iraz M, Sogut S, Ozugurlu F, Ozyurt H, Odaci E, Yildirim Z: Role of caffeic acid phenethyl ester, an active component of propolis, against cisplatin-induced nephrotoxicity in rats. J Appl Toxicol. 2004, 24: 27-35. 10.1002/jat.941.CrossRefPubMed
55.
Almeida AS, Faleiros ACG, Teixeira DNS, Cota UA, Chica JEL: Reference values for blood-based biochemical parameters in BALB/c and C57BL/6 wild-type mice. Jornal Brasileiro Patol Med Lab. 2008, 44 (6): 429-432. 10.1590/S1676-24442008000600006.CrossRef
56.
Amin A, Hamza AA: Hepatoprotective effects of Hibiscus, Rosmarinus and Salvia on azathioprine-induced toxicity in rats. Life Sciences. 2005, 77: 266-278. 10.1016/j.lfs.2004.09.048.CrossRefPubMed
57.
Suja SR, Latha PG, Pushpangandan P, Rajasekharan S: Evaluation of hepatoprotective effects of Helminthostachys zeylanica (L) Hook against carbon tetrachloride induced liver damage in Wistar rats. J Ethnopharmacol. 2004, 92: 61-66. 10.1016/j.jep.2004.01.019.CrossRefPubMed
58.
Pascual C, Gonzalez R, Torricella R: Scavenging action of propolis extract against oxygen radicals. J Ethnopharmacol. 1994, 41: 9-13. 10.1016/0378-8741(94)90052-3.CrossRefPubMed
59.
Wan YY, Flavell RA: The roles for cytokines in the generation and maintenance of regulatory T cells. Immunol Rev. 2006, 212: 114-130. 10.1111/j.0105-2896.2006.00407.x.CrossRefPubMed
60.
Khayyal MT, El-Ghazaly MA, El-Khatib AS, Hatem AM, De Vries PJF, El-Shafei S, Khattab MM: A clinical pharmacological study of the potential beneficial effects of a propolis food product as an adjuvant in asthmatic patients. Fund Clin Pharmacol. 2003, 17: 93-102. 10.1046/j.1472-8206.2003.00117.x.CrossRef
61.
Orsatti CL, Missima F, Pagliarone AC, Bachiega TC, Búfalo MC, Araújo JP, Sforcin JM: Propolis immunomodulatory action in vivo on Toll-Like receptors 2 and 4 expression and on pro-inflammatory cytokines production in mice. Phytother Res. 2010, 24 (8): 1141-1146.PubMed
62.
Orsi RO, Funari SR, Soares AMVC, Calvi SA, Oliveira SL, Sforcin JM, Bankova V: Immunomodulatory action of propolis on macrophage activation. J Venom AnimToxins. 2000, 6 (2): 205-219. 10.1590/S0104-79302000000200006.CrossRef
63.
Sforcin JM, Orsi RO, Bankova V: Effect of propolis, some isolated compounds and its source plant on antibody production. J Ethnopharmacol. 2005, 98 (3): 301-305. 10.1016/j.jep.2005.01.042.CrossRefPubMed
64.
Ahn MR, Kumazawa S, Hamasaka T, Bang KS, Nakayama T: Antioxidant activity and constituents of propolis collected in various areas of Korea. J Agric Food Chem. 2004, 52 (24): 7286-7292. 10.1021/jf048726s.CrossRefPubMed
65.
Orsolic N, Basic I: Antitumor, hematostimulative and radioprotective action of water-soluble derivative of propolis (WSDP). Biomed Pharmacother. 2005, 59 (10): 561-570. 10.1016/j.biopha.2005.03.013.CrossRefPubMed
Metadata
Title
Antimicrobial activity against oral pathogens and immunomodulatory effects and toxicity of geopropolis produced by the stingless bee Melipona fasciculata Smith
Authors
Silvana A Liberio
Antônio Luís A Pereira
Richard P Dutra
Aramys S Reis
Maria José AM Araújo
Nadia S Mattar
Lucilene A Silva
Maria Nilce S Ribeiro
Flávia Raquel F Nascimento
Rosane NM Guerra
Valério Monteiro-Neto
Publication date
01-12-2011
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2011
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/1472-6882-11-108

Other articles of this Issue 1/2011

BMC Complementary Medicine and Therapies 1/2011 Go to the issue

Research article

Antiproliferative effect of methanolic extraction of tualang honey on human keloid fibroblasts

Research article

Attenuating effect of Acorus calamus extract in chronic constriction injury induced neuropathic pain in rats: an evidence of anti-oxidative, anti-inflammatory, neuroprotective and calcium inhibitory effects

Research article

Developing a patient-centered outcome measure for complementary and alternative medicine therapies I: defining content and format

Research article

Nurses' experiences, expectations, and preferences for mind-body practices to reduce stress

Research article

Inhibitory activity of a standardized elderberry liquid extract against clinically-relevant human respiratory bacterial pathogens and influenza A and B viruses

Research article

In vivo activity of Sapindus saponaria against azole-susceptible and -resistant human vaginal Candida species