Skip to main content
Top
Published in: BMC Complementary Medicine and Therapies 1/2019

Open Access 01-12-2019 | Streptococci | Research article

Iranian propolis efficiently inhibits growth of oral streptococci and cancer cell lines

Authors: Fariba Asgharpour, Ali Akbar Moghadamnia, Ebrahim Zabihi, Sohrab Kazemi, Amirmorteza Ebrahimzadeh Namvar, Hemmat Gholinia, Mina Motallebnejad, Hamid Reza Nouri

Published in: BMC Complementary Medicine and Therapies | Issue 1/2019

Login to get access

Abstract

Background

Propolis is a natural bee product with a wide range of biological activities that are related to its chemical composition. The present study investigated the quantification of quercetin (Q) in Ardabil ethanol extract of propolis (AEEP), and then compared its anti-bacterial, anti- biofilm and cytotoxic effects on cancer and normal cell lines.

Method

In the present study, the chemical composition of AEEP was determined through the high-performance liquid chromatography (HPLC). The AEEP and its main component, quercetin (Q), were evaluated in vitro against 57 oral streptococci by a broth micro-dilution method. The biofilm formation was assessed through the crystal violet staining and MTT assays. The impact of AEEP and Q anti-proliferative effect were evaluated on the fibroblast as normal and cancer cell lines (KB and A431).

Results

The Q concentration in the composition of AEEP was 6.9% of all its components. The findings indicated that the AEEP and Q were efficient against the cariogenic bacteria and were able to inhibit the S.mutans biofilm adherence at a sub-MIC concentration. Moreover, electron micrographs indicated the inhibition of biofilms compared to control biofilms. In addition, the AEEP and Q indicated a dose-dependent cytotoxic effect on A431 and KB cell lines. On the contrary, they had no cytotoxic effect on fibroblast cells.

Conclusion

The results indicated that the synergistic impact of main components of AEEP was related to the inhibition of the cancer cell proliferation, cariogenic bacteria and oral biofilm formation. It may play a promising role in the complementary medicine and, it is suggested to be used as food additives.
Literature
1.
go back to reference Özan F, Sümer Z, Polat ZA, Er K, Özan Ü, Deḡer O. Effect of Mouthrinse containing Propolis on Oral microorganisms and human gingival fibroblasts. Eur J Dent. 2007;1:195–201.CrossRef Özan F, Sümer Z, Polat ZA, Er K, Özan Ü, Deḡer O. Effect of Mouthrinse containing Propolis on Oral microorganisms and human gingival fibroblasts. Eur J Dent. 2007;1:195–201.CrossRef
2.
go back to reference VK S. Propolis in dentistry and oral cancer management. N Am J Med Sci. 2014;6:250–9. VK S. Propolis in dentistry and oral cancer management. N Am J Med Sci. 2014;6:250–9.
3.
go back to reference Wagh VD. Propolis: a wonder bees product and its pharmacological potentials. Adv Pharmacol Sci. 2013;2013:11. Wagh VD. Propolis: a wonder bees product and its pharmacological potentials. Adv Pharmacol Sci. 2013;2013:11.
4.
go back to reference 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;52:7286–92.CrossRef 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;52:7286–92.CrossRef
5.
go back to reference Bonamigo T, Campos JF, Alfredo TM, Balestieri JB, Cardoso CA, Paredes-Gamero EJ, et al. Antioxidant, cytotoxic, and toxic activities of Propolis from two native bees in Brazil: Scaptotrigona depilis and Melipona quadrifasciata anthidioides. Oxidative Med Cell Longev. 2017;2017:1038153.CrossRef Bonamigo T, Campos JF, Alfredo TM, Balestieri JB, Cardoso CA, Paredes-Gamero EJ, et al. Antioxidant, cytotoxic, and toxic activities of Propolis from two native bees in Brazil: Scaptotrigona depilis and Melipona quadrifasciata anthidioides. Oxidative Med Cell Longev. 2017;2017:1038153.CrossRef
6.
go back to reference Elnakady YA, Rushdi AI, Franke R, Abutaha N, Ebaid H, Baabbad M, et al. Characteristics, chemical compositions and biological activities of propolis from Al-Bahah, Saudi Arabia. Sci Rep. 2017;7:41453.CrossRef Elnakady YA, Rushdi AI, Franke R, Abutaha N, Ebaid H, Baabbad M, et al. Characteristics, chemical compositions and biological activities of propolis from Al-Bahah, Saudi Arabia. Sci Rep. 2017;7:41453.CrossRef
7.
go back to reference Cavalcante DRR, Oliveira PSD, Góis SM, Soares AF, Cardoso JC, Padilha FF, et al. Effect of green propolis on oral epithelial dysplasia in rats. Braz J Otorhinolaryngol. 2011;77:278–84.CrossRef Cavalcante DRR, Oliveira PSD, Góis SM, Soares AF, Cardoso JC, Padilha FF, et al. Effect of green propolis on oral epithelial dysplasia in rats. Braz J Otorhinolaryngol. 2011;77:278–84.CrossRef
8.
go back to reference Wassel MO, Khattab MA. Antibacterial activity against Streptococcus mutans and inhibition of bacterial induced enamel demineralization of propolis, miswak, and chitosan nanoparticles based dental varnishes. J Adv Res. 2017;8:387–92.CrossRef Wassel MO, Khattab MA. Antibacterial activity against Streptococcus mutans and inhibition of bacterial induced enamel demineralization of propolis, miswak, and chitosan nanoparticles based dental varnishes. J Adv Res. 2017;8:387–92.CrossRef
9.
go back to reference Veloz JJ, Saavedra N, Lillo A, Alvear M, Barrientos L, Salazar LA. Antibiofilm activity of Chilean Propolis on Streptococcus mutans is influenced by the year of collection. Biomed Res Int. 2015;2015:6.CrossRef Veloz JJ, Saavedra N, Lillo A, Alvear M, Barrientos L, Salazar LA. Antibiofilm activity of Chilean Propolis on Streptococcus mutans is influenced by the year of collection. Biomed Res Int. 2015;2015:6.CrossRef
10.
go back to reference Gibbons RJ, Houte JV. Bacterial adherence in oral microbial ecology. Annu Rev Microbiol. 1975;29:19–44.CrossRef Gibbons RJ, Houte JV. Bacterial adherence in oral microbial ecology. Annu Rev Microbiol. 1975;29:19–44.CrossRef
11.
go back to reference Cunha MG, Franchin M, de Carvalho Galvao LC, de Ruiz AL, de Carvalho JE, Ikegaki M, et al. Antimicrobial and antiproliferative activities of stingless bee Melipona scutellaris geopropolis. BMC Complement Altern Med. 2013;13:23.CrossRef Cunha MG, Franchin M, de Carvalho Galvao LC, de Ruiz AL, de Carvalho JE, Ikegaki M, et al. Antimicrobial and antiproliferative activities of stingless bee Melipona scutellaris geopropolis. BMC Complement Altern Med. 2013;13:23.CrossRef
12.
go back to reference Duarte S, Koo H, Bowen WH, Hayacibara MF, Cury JA, Ikegaki M, et al. Effect of a novel type of propolis and its chemical fractions on glucosyltransferases and on growth and adherence of mutans streptococci. Biol Pharm Bull. 2003;26:527–31.CrossRef Duarte S, Koo H, Bowen WH, Hayacibara MF, Cury JA, Ikegaki M, et al. Effect of a novel type of propolis and its chemical fractions on glucosyltransferases and on growth and adherence of mutans streptococci. Biol Pharm Bull. 2003;26:527–31.CrossRef
13.
go back to reference Hegde KS, Bhat SS, Rao A, Sain S. Effect of Propolis on Streptococcus mutans counts: an in vivo study. Int J Clin Pediatr Dent. 2013;6:22–5.CrossRef Hegde KS, Bhat SS, Rao A, Sain S. Effect of Propolis on Streptococcus mutans counts: an in vivo study. Int J Clin Pediatr Dent. 2013;6:22–5.CrossRef
14.
go back to reference Jeon JG, Rosalen PL, Falsetta ML, Koo H. Natural products in caries research: current (limited) knowledge, challenges and future perspective. Caries Res. 2011;45:243–63.CrossRef Jeon JG, Rosalen PL, Falsetta ML, Koo H. Natural products in caries research: current (limited) knowledge, challenges and future perspective. Caries Res. 2011;45:243–63.CrossRef
15.
go back to reference Andrade JKS, Denadai M, de Oliveira CS, Nunes ML, Narain N. Evaluation of bioactive compounds potential and antioxidant activity of brown, green and red propolis from Brazilian northeast region. Food Res Int. 2017;101:129–38.CrossRef Andrade JKS, Denadai M, de Oliveira CS, Nunes ML, Narain N. Evaluation of bioactive compounds potential and antioxidant activity of brown, green and red propolis from Brazilian northeast region. Food Res Int. 2017;101:129–38.CrossRef
16.
go back to reference Pejin B, Ciric A, Markovic JD, Glamoclija J, Nikolic M, Stanimirovic B, et al. Quercetin potently reduces biofilm formation of the strain Pseudomonas aeruginosa PAO1 in vitro. Curr Pharm Biotechnol. 2015;16:733–7.CrossRef Pejin B, Ciric A, Markovic JD, Glamoclija J, Nikolic M, Stanimirovic B, et al. Quercetin potently reduces biofilm formation of the strain Pseudomonas aeruginosa PAO1 in vitro. Curr Pharm Biotechnol. 2015;16:733–7.CrossRef
17.
go back to reference Ouyang J, Sun F, Feng W, Sun Y, Qiu X, Xiong L, et al. Quercetin is an effective inhibitor of quorum sensing, biofilm formation and virulence factors in Pseudomonas aeruginosa. J Appl Microbiol. 2016;120:966–74.CrossRef Ouyang J, Sun F, Feng W, Sun Y, Qiu X, Xiong L, et al. Quercetin is an effective inhibitor of quorum sensing, biofilm formation and virulence factors in Pseudomonas aeruginosa. J Appl Microbiol. 2016;120:966–74.CrossRef
18.
go back to reference Lee JH, Park JH, Cho HS, Joo SW, Cho MH, Lee J. Anti-biofilm activities of quercetin and tannic acid against Staphylococcus aureus. Biofouling. 2013;29:491–9.CrossRef Lee JH, Park JH, Cho HS, Joo SW, Cho MH, Lee J. Anti-biofilm activities of quercetin and tannic acid against Staphylococcus aureus. Biofouling. 2013;29:491–9.CrossRef
19.
go back to reference Vazquez-Armenta FJ, Bernal-Mercado AT, Tapia-Rodriguez MR, Gonzalez-Aguilar GA, Lopez-Zavala AA, Martinez-Tellez MA, et al. Quercetin reduces adhesion and inhibits biofilm development by listeria monocytogenes by reducing the amount of extracellular proteins. Food Control. 2018;90:266–73.CrossRef Vazquez-Armenta FJ, Bernal-Mercado AT, Tapia-Rodriguez MR, Gonzalez-Aguilar GA, Lopez-Zavala AA, Martinez-Tellez MA, et al. Quercetin reduces adhesion and inhibits biofilm development by listeria monocytogenes by reducing the amount of extracellular proteins. Food Control. 2018;90:266–73.CrossRef
20.
go back to reference Sankari SL, Babu NA, Rani V, Priyadharsini C, Masthan KM. Flavonoids - clinical effects and applications in dentistry: a review. J Pharm Bioallied Sci. 2014;6:26–9.CrossRef Sankari SL, Babu NA, Rani V, Priyadharsini C, Masthan KM. Flavonoids - clinical effects and applications in dentistry: a review. J Pharm Bioallied Sci. 2014;6:26–9.CrossRef
21.
go back to reference Aghapour F, Moghadamnia AA, Nicolini A, Kani SNM, Barari L, Morakabati P, et al. Quercetin conjugated with silica nanoparticles inhibits tumor growth in MCF-7 breast cancer cell lines. Biochem Biophys Res Commun. 2018;500:860–5.CrossRef Aghapour F, Moghadamnia AA, Nicolini A, Kani SNM, Barari L, Morakabati P, et al. Quercetin conjugated with silica nanoparticles inhibits tumor growth in MCF-7 breast cancer cell lines. Biochem Biophys Res Commun. 2018;500:860–5.CrossRef
22.
go back to reference Ren KW, Li YH, Wu G, Ren JZ, Lu HB, Li ZM, et al. Quercetin nanoparticles display antitumor activity via proliferation inhibition and apoptosis induction in liver cancer cells. Int J Oncol. 2017;50:1299–311.CrossRef Ren KW, Li YH, Wu G, Ren JZ, Lu HB, Li ZM, et al. Quercetin nanoparticles display antitumor activity via proliferation inhibition and apoptosis induction in liver cancer cells. Int J Oncol. 2017;50:1299–311.CrossRef
23.
go back to reference Falcão SI, Tomás A, Vale N, Gomes P, Freire C, Vilas-Boas M. Phenolic quantification and botanical origin of Portuguese propolis. Ind Crop Prod. 2013;49:805–12.CrossRef Falcão SI, Tomás A, Vale N, Gomes P, Freire C, Vilas-Boas M. Phenolic quantification and botanical origin of Portuguese propolis. Ind Crop Prod. 2013;49:805–12.CrossRef
24.
go back to reference CLSI. Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement; 2015. p. M100–S25. CLSI. Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement; 2015. p. M100–S25.
25.
go back to reference Kouidhi B, Zmantar T, Bakhrouf A. Anti-cariogenic and anti-biofilms activity of Tunisian propolis extract and its potential protective effect against cancer cells proliferation. Anaerobe. 2010;16:566–71.CrossRef Kouidhi B, Zmantar T, Bakhrouf A. Anti-cariogenic and anti-biofilms activity of Tunisian propolis extract and its potential protective effect against cancer cells proliferation. Anaerobe. 2010;16:566–71.CrossRef
26.
go back to reference Hasan S, Singh K, Danisuddin M, Verma PK, Khan AU. Inhibition of major virulence pathways of Streptococcus mutans by quercitrin and deoxynojirimycin: a synergistic approach of infection control. PLoS One. 2014;9:e91736.CrossRef Hasan S, Singh K, Danisuddin M, Verma PK, Khan AU. Inhibition of major virulence pathways of Streptococcus mutans by quercitrin and deoxynojirimycin: a synergistic approach of infection control. PLoS One. 2014;9:e91736.CrossRef
27.
go back to reference Pandamooz S, Hadipour A, Akhavan-Niaki H, Pourghasem M, Abedian Z, Ardekani AM, et al. Short exposure to collagenase and coculture with mouse embryonic pancreas improve human dermal fibroblast culture. Biotechnol Appl Biochem. 2012;59:254–61.CrossRef Pandamooz S, Hadipour A, Akhavan-Niaki H, Pourghasem M, Abedian Z, Ardekani AM, et al. Short exposure to collagenase and coculture with mouse embryonic pancreas improve human dermal fibroblast culture. Biotechnol Appl Biochem. 2012;59:254–61.CrossRef
28.
go back to reference Liberio SA, Pereira AL, Araujo MJ, Dutra RP, Nascimento FR, Monteiro-Neto V, et al. The potential use of propolis as a cariostatic agent and its actions on mutans group streptococci. J Ethnopharmacol. 2009;125:1–9.CrossRef Liberio SA, Pereira AL, Araujo MJ, Dutra RP, Nascimento FR, Monteiro-Neto V, et al. The potential use of propolis as a cariostatic agent and its actions on mutans group streptococci. J Ethnopharmacol. 2009;125:1–9.CrossRef
29.
go back to reference Sforcin JM, Bankova V. Propolis: is there a potential for the development of new drugs? J Ethnopharmacol. 2011;133:253–60.CrossRef Sforcin JM, Bankova V. Propolis: is there a potential for the development of new drugs? J Ethnopharmacol. 2011;133:253–60.CrossRef
30.
go back to reference Chen SF, Nien S, Wu CH, Liu CL, Chang YC, Lin YS. Reappraisal of the anticancer efficacy of quercetin in oral cancer cells. JCMA. 2013;76:146–52.PubMed Chen SF, Nien S, Wu CH, Liu CL, Chang YC, Lin YS. Reappraisal of the anticancer efficacy of quercetin in oral cancer cells. JCMA. 2013;76:146–52.PubMed
31.
go back to reference Gatto MT, Falcocchio S, Grippa E, Mazzanti G, Battinelli L, Nicolosi G, et al. Antimicrobial and anti-lipase activity of quercetin and its C2-C16 3-O-acyl-esters. Bioorg Med Chem. 2002;10:269–72.CrossRef Gatto MT, Falcocchio S, Grippa E, Mazzanti G, Battinelli L, Nicolosi G, et al. Antimicrobial and anti-lipase activity of quercetin and its C2-C16 3-O-acyl-esters. Bioorg Med Chem. 2002;10:269–72.CrossRef
32.
go back to reference Hayacibara MF, Koo H, Rosalen PL, Duarte S, Franco EM, Bowen WH, et al. In vitro and in vivo effects of isolated fractions of Brazilian propolis on caries development. J Ethnopharmacol. 2005;101:110–5.CrossRef Hayacibara MF, Koo H, Rosalen PL, Duarte S, Franco EM, Bowen WH, et al. In vitro and in vivo effects of isolated fractions of Brazilian propolis on caries development. J Ethnopharmacol. 2005;101:110–5.CrossRef
33.
go back to reference Woznicka E, Kuzniar A, Nowak D, Nykiel E, Kopacz M, Gruszecka J, et al. Comparative study on the antibacterial activity of some flavonoids and their sulfonic derivatives. Acta Pol Pharm. 2013;70:567–71.PubMed Woznicka E, Kuzniar A, Nowak D, Nykiel E, Kopacz M, Gruszecka J, et al. Comparative study on the antibacterial activity of some flavonoids and their sulfonic derivatives. Acta Pol Pharm. 2013;70:567–71.PubMed
34.
go back to reference Baker CN, Thornsberry C. Antimicrobial susceptibility of Streptococcus mutans isolated from patients with endocarditis. Antimicrob Agents Chemother. 1974;5:268–71.CrossRef Baker CN, Thornsberry C. Antimicrobial susceptibility of Streptococcus mutans isolated from patients with endocarditis. Antimicrob Agents Chemother. 1974;5:268–71.CrossRef
35.
go back to reference Machado CS, Mokochinski JB, de Lira TO, de Oliveira Fde C, Cardoso MV, Ferreira RG, et al. Comparative study of chemical composition and biological activity of yellow, green, Brown, and red Brazilian Propolis. eCAM. 2016;2016:6057650.PubMed Machado CS, Mokochinski JB, de Lira TO, de Oliveira Fde C, Cardoso MV, Ferreira RG, et al. Comparative study of chemical composition and biological activity of yellow, green, Brown, and red Brazilian Propolis. eCAM. 2016;2016:6057650.PubMed
36.
go back to reference Alizadeh AM, Afrouzan H, Dinparast-Djadid N, Sawaya AC, Azizian S, Hemmati HR, et al. Chemoprotection of MNNG-initiated gastric cancer in rats using Iranian propolis. Arch Iran Med. 2015;18:18–23.PubMed Alizadeh AM, Afrouzan H, Dinparast-Djadid N, Sawaya AC, Azizian S, Hemmati HR, et al. Chemoprotection of MNNG-initiated gastric cancer in rats using Iranian propolis. Arch Iran Med. 2015;18:18–23.PubMed
37.
go back to reference Najafi MF, Vahedy F, Seyyedin M, Jomehzadeh HR, Bozary K. Effect of the water extracts of propolis on stimulation and inhibition of different cells. Cytotechnology. 2007;54:49–56.CrossRef Najafi MF, Vahedy F, Seyyedin M, Jomehzadeh HR, Bozary K. Effect of the water extracts of propolis on stimulation and inhibition of different cells. Cytotechnology. 2007;54:49–56.CrossRef
38.
go back to reference Afrouzan H, Zakeri S, Abouie Mehrizi A, Molasalehi S, Tahghighi A, Shokrgozar MA, et al. Anti-Plasmodial assessment of four different Iranian Propolis extracts. Arch Iran Med. 2017;20:270–81.PubMed Afrouzan H, Zakeri S, Abouie Mehrizi A, Molasalehi S, Tahghighi A, Shokrgozar MA, et al. Anti-Plasmodial assessment of four different Iranian Propolis extracts. Arch Iran Med. 2017;20:270–81.PubMed
39.
go back to reference Tsai YC, Wang YH, Liou CC, Lin YC, Huang H, Liu YC. Induction of oxidative DNA damage by flavonoids of propolis: its mechanism and implication about antioxidant capacity. Chem Res Toxicol. 2012;25:191–6.CrossRef Tsai YC, Wang YH, Liou CC, Lin YC, Huang H, Liu YC. Induction of oxidative DNA damage by flavonoids of propolis: its mechanism and implication about antioxidant capacity. Chem Res Toxicol. 2012;25:191–6.CrossRef
40.
go back to reference Asgharpour F, Moghadamnia AA, Kazemi S, Nouri HR, Pouramir M, Mousavi SN, Motallebnejad M. Chemical composition analysis and In Vitro investigation of cytotoxic and Antioxidative activities of Iranian Propolis against breast Cancer cell line, MCF-7. ChemistrySelect. 2018;3:10857–63.CrossRef Asgharpour F, Moghadamnia AA, Kazemi S, Nouri HR, Pouramir M, Mousavi SN, Motallebnejad M. Chemical composition analysis and In Vitro investigation of cytotoxic and Antioxidative activities of Iranian Propolis against breast Cancer cell line, MCF-7. ChemistrySelect. 2018;3:10857–63.CrossRef
Metadata
Title
Iranian propolis efficiently inhibits growth of oral streptococci and cancer cell lines
Authors
Fariba Asgharpour
Ali Akbar Moghadamnia
Ebrahim Zabihi
Sohrab Kazemi
Amirmorteza Ebrahimzadeh Namvar
Hemmat Gholinia
Mina Motallebnejad
Hamid Reza Nouri
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Streptococci
Published in
BMC Complementary Medicine and Therapies / Issue 1/2019
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-019-2677-3

Other articles of this Issue 1/2019

BMC Complementary Medicine and Therapies 1/2019 Go to the issue