Brazilian red propolis reduces orange-complex periodontopathogens growing in multispecies biofilms

References

• Alencar SM, Oldoni TL, Castro ML, Cabral IS, Costa-Neto CM, Cury JA, Rosalen PL, Ikegaki M. 2007. Chemical composition and biological activity of a new type of Brazilian propolis: red propolis. J Ethnopharmacol. 113:278–283. doi:10.1016/j.jep.2007.06.005
   PubMed Web of Science ®Google Scholar
• Arbia L, Chikhi-Chorfi N, Betatache I, Pham-Huy C, Zenia S, Mameri N, Drouiche N, Lounici H. 2017. Antimicrobial activity of aqueous extracts from four plants on bacterial isolates from periodontitis patients. Environ Sci Pollut Res Int. 24:13394–13404. doi:10.1007/s11356-017-8942-4
   PubMed Web of Science ®Google Scholar
• Ardila CM, Granada MI, Guzman IC. 2010. Antibiotic resistance of subgingival species in chronic periodontitis patients. J Periodont Res. 45:557–563.
   PubMed Web of Science ®Google Scholar
• Arif M, Dong QJ, Raja MA, Zeenat S, Chi Z, Liu CG. 2018. Development of novel pH-sensitive thiolated chitosan/PMLA nanoparticles for amoxicillin delivery to treat Helicobacter pylori. Mater Sci Eng C Mater Biol Appl. 83:17–24. doi:10.1016/j.msec.2017.08.038
   PubMed Web of Science ®Google Scholar
• Balta MG, Loos BG, Nicu EA. 2017. Emerging concepts in the resolution of periodontal inflammation: a role for Resolvin E1. Front Immunol. 8:1682. doi:10.3389/fimmu.2017.01682
   PubMed Web of Science ®Google Scholar
• Barbosa Bezerra G, de Menezes de Souza L, Dos Santos AS, de Almeida GK, Souza MT, Santos SL, Aparecido Camargo E, Dos Santos Lima B, de Souza Araujo AA, Cardoso JC, et al. 2017. Hydroalcoholic extract of Brazilian red propolis exerts protective effects on acetic acid-induced ulcerative colitis in a rodent model. Biomed Pharmacother. 85:687–696. doi:10.1016/j.biopha.2016.11.080
   PubMed Web of Science ®Google Scholar
• Batchelor P. 2014. Is periodontal disease a public health problem? Br Dent J. 217:405–409. doi:10.1038/sj.bdj.2014.912
   PubMed Web of Science ®Google Scholar
• Bueno-Silva B, Alencar SM, Koo H, Ikegaki M, Silva GV, Napimoga MH, Rosalen PL. 2013. Anti-inflammatory and antimicrobial evaluation of neovestitol and vestitol isolated from Brazilian red propolis. J Agric Food Chem. 61:4546–4550. doi:10.1021/jf305468f
   PubMed Web of Science ®Google Scholar
• Bueno-Silva B, Franchin M, Alves CF, Denny C, Colon DF, Cunha TM, Alencar SM, Napimoga MH, Rosalen PL. 2016. Main pathways of action of Brazilian red propolis on the modulation of neutrophils migration in the inflammatory process. Phytomedicine. 23:1583–1590. doi:10.1016/j.phymed.2016.09.009
   PubMed Web of Science ®Google Scholar
• Bueno-Silva B, Kawamoto D, Ando-Suguimoto ES, Alencar SM, Rosalen PL, Mayer MP. 2015. Brazilian red propolis attenuates inflammatory signaling cascade in LPS-activated macrophages. Plos One. 10:e0144954. doi:10.1371/journal.pone.0144954
   PubMed Web of Science ®Google Scholar
• Bueno-Silva B, Kawamoto D, Ando-Suguimoto ES, Casarin RCV, Alencar SM, Rosalen PL, Mayer M. 2017. Brazilian red propolis effects on peritoneal macrophage activity: nitric oxide, cell viability, pro-inflammatory cytokines and gene expression. J Ethnopharmacol. 207:100–107. doi:10.1016/j.jep.2017.06.015
   PubMed Web of Science ®Google Scholar
• Bueno-Silva B, Koo H, Falsetta ML, Alencar SM, Ikegaki M, Rosalen PL. 2013. Effect of neovestitol-vestitol containing Brazilian red propolis on accumulation of biofilm in vitro and development of dental caries in vivo. Biofouling. 29:1233–1242. doi:10.1080/08927014.2013.834050
   PubMed Web of Science ®Google Scholar
• Bueno-Silva B, Marsola A, Ikegaki M, Alencar SM, Rosalen PL. 2017. The effect of seasons on Brazilian red propolis and its botanical source: chemical composition and antibacterial activity. Nat Prod Res. 31:1318–1324. doi:10.1080/14786419.2016.1239088
   PubMed Web of Science ®Google Scholar
• Bueno-Silva B, Rosalen PL, Alencar SM, Mayer M. 2017. Anti-inflammatory mechanisms of neovestitol from Brazilian red propolis in LPS-activated macrophages. J Funct Foods. 36:440–447. doi:10.1016/j.jff.2017.07.029
   Web of Science ®Google Scholar
• Campo Fernandez M, Cuesta-Rubio O, Rosado Perez A, Montes De Oca Porto R, Marquez Hernandez I, Piccinelli AL, Rastrelli L. 2008. GC-MS determination of isoflavonoids in seven red Cuban propolis samples. J Agric Food Chem. 56:9927–9932. doi:10.1021/jf801870f
   PubMed Web of Science ®Google Scholar
• Cavalla F, Biguetti CC, Melchiades JL, Tabanez AP, Azevedo MCS, Trombone APF, Faveri M, Feres M, Garlet GP. 2018. Genetic association with subgingival bacterial colonization in chronic periodontitis. Genes. 23:9.
   Google Scholar
• Correa FR, Schanuel FS, Moura-Nunes N, Monte-Alto-Costa A, Daleprane JB. 2017. Brazilian red propolis improves cutaneous wound healing suppressing inflammation-associated transcription factor NFκB. Biomed Pharmacother. 86:162–171. doi:10.1016/j.biopha.2016.12.018
   PubMed Web of Science ®Google Scholar
• Costa X, Laguna E, Herrera D, Serrano J, Alonso B, Sanz M. 2013. Efficacy of a new mouth rinse formulation based on 0.07% cetylpyridinium chloride in the control of plaque and gingivitis: a 6-month randomized clinical trial. J Clin Periodontol. 40:1007–1015. doi:10.1111/jcpe.12158
   PubMed Web of Science ®Google Scholar
• Dantas Silva RP, Machado BA, Barreto GA, Costa SS, Andrade LN, Amaral RG, Carvalho AA, Padilha FF, Barbosa JD, Umsza-Guez MA. 2017. Antioxidant, antimicrobial, antiparasitic, and cytotoxic properties of various Brazilian propolis extracts. Plos One. 12:e0172585. doi:10.1371/journal.pone.0172585
   PubMed Web of Science ®Google Scholar
• Dumitrescu AL. 2015. Editorial: periodontal disease: a public health problem. Frontiers in Public Health. 3:278.
   PubMed Web of Science ®Google Scholar
• Feres M, Figueiredo LC, Soares GM, Faveri M. 2015. Systemic antibiotics in the treatment of periodontitis. Periodontol 2000. 67:131–186. doi:10.1111/prd.12075
   PubMed Web of Science ®Google Scholar
• Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. 2016. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol. 14:563–575. doi:10.1038/nrmicro.2016.94
   PubMed Web of Science ®Google Scholar
• Franchin M, Colon DF, Castanheira FV, da Cunha MG, Bueno-Silva B, Alencar SM, Cunha TM, Rosalen PL. 2016. Vestitol isolated from Brazilian red propolis inhibits neutrophils migration in the inflammatory process: elucidation of the mechanism of action. J Nat Prod. 79:954–960. doi:10.1021/acs.jnatprod.5b00938
   PubMed Web of Science ®Google Scholar
• Franchin M, Colon DF, da Cunha MG, Castanheira FV, Saraiva AL, Bueno-Silva B, Alencar SM, Cunha TM, Rosalen PL. 2016. Neovestitol, an isoflavonoid isolated from Brazilian red propolis, reduces acute and chronic inflammation: involvement of nitric oxide and IL-6. Sci Rep. 6:36401. doi:10.1038/srep36401
   PubMed Web of Science ®Google Scholar
• Freires IA, de Alencar SM, Rosalen PL. 2016. A pharmacological perspective on the use of Brazilian red propolis and its isolated compounds against human diseases. Eur J Med Chem. 110:267–279. doi:10.1016/j.ejmech.2016.01.033
   PubMed Web of Science ®Google Scholar
• Frozza C, Santos DA, Rufatto LC, Minetto L, Scariot FJ, Echeverrigaray S, Pich CT, Moura S, Padilha FF, Borsuk S, et al. 2017. Antitumor activity of Brazilian red propolis fractions against Hep-2 cancer cell line. Biomed Pharmacother. 91:951–963. doi:10.1016/j.biopha.2017.05.027
   PubMed Web of Science ®Google Scholar
• Hajishengallis G. 2015. Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol. 15:30–44. doi:10.1038/nri3785
   PubMed Web of Science ®Google Scholar
• Hajishengallis G, Lamont RJ. 2012. Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol. 27:409–419. doi:10.1111/j.2041-1014.2012.00663.x
   PubMed Web of Science ®Google Scholar
• Inui S, Hatano A, Yoshino M, Hosoya T, Shimamura Y, Masuda S, Ahn MR, Tazawa S, Araki Y, Kumazawa S. 2014. Identification of the phenolic compounds contributing to antibacterial activity in ethanol extracts of Brazilian red propolis. Natural Product Research. 28:1293–1296. doi:10.1080/14786419.2014.898146
   PubMed Web of Science ®Google Scholar
• James P, Worthington HV, Parnell C, Harding M, Lamont T, Cheung A, Whelton H, Riley P. 2017. Chlorhexidine mouthrinse as an adjunctive treatment for gingival health. Cochrane Database Syst Rev. 3:CD008676.
   PubMed Web of Science ®Google Scholar
• Jepsen K, Jepsen S. 2016. Antibiotics/antimicrobials: systemic and local administration in the therapy of mild to moderately advanced periodontitis. Periodontol 2000. 71:82–112. doi:10.1111/prd.12121
   PubMed Web of Science ®Google Scholar
• Ji QX, Zhao QS, Deng J, Lu R. 2010. A novel injectable chlorhexidine thermosensitive hydrogel for periodontal application: preparation, antibacterial activity and toxicity evaluation. J Mater Sci Mater Med. 21:2435–2442. doi:10.1007/s10856-010-4098-1
   PubMed Web of Science ®Google Scholar
• Joaquim CR, Miranda TS, Marins LM, Silva HDP, Feres M, Figueiredo LC, Duarte PM. 2018. The combined and individual impact of diabetes and smoking on key subgingival periodontal pathogens in patients with chronic periodontitis. J Periodont Res. 53:315–323. doi:10.1111/jre.12516
   PubMed Web of Science ®Google Scholar
• Khurshid Z, Naseem M, Zafar MS, Najeeb S, Zohaib S. 2017. Propolis: a natural biomaterial for dental and oral healthcare. J Dent Res Dent Clin Dent Prospects. 11:265–274.
   PubMedGoogle Scholar
• Kouidhi B, Al Qurashi YM, Chaieb K. 2015. Drug resistance of bacterial dental biofilm and the potential use of natural compounds as alternative for prevention and treatment. Microb Pathog. 80:39–49. doi:10.1016/j.micpath.2015.02.007
   PubMed Web of Science ®Google Scholar
• Lazar V, Saviuc CM, Chifiriuc MC. 2016. Periodontitis and periodontal disease - innovative strategies for reversing the chronic infectious and inflammatory condition by natural products. CPD. 22:230–237.
   Web of Science ®Google Scholar
• Lee J, Nho YH, Yun SK, Hwang YS. 2017. Use of ethanol extracts of Terminalia chebula to prevent periodontal disease induced by dental plaque bacteria. BMC Complement Altern Med. 17:113. doi:10.1186/s12906-017-1619-1
   PubMed Web of Science ®Google Scholar
• Lima Cavendish R, de Souza Santos J, Belo Neto R, Oliveira Paixao A, Valeria Oliveira J, Divino de Araujo E, Berretta E, Maria Thomazzi S, Cordeiro Cardoso J, Zanardo Gomes M. 2015. Antinociceptive and anti-inflammatory effects of Brazilian red propolis extract and formononetin in rodents. J Ethnopharmacol. 173:127–133. doi:10.1016/j.jep.2015.07.022
   PubMed Web of Science ®Google Scholar
• Lin JH, Feng F, Yu MC, Wang CH, Chang PC. 2018. Modulation of periodontitis progression using pH-responsive nanosphere encapsulating metronidazole or N-phenacylthialzolium bromide. J Periodont Res. 53:22–28. doi:10.1111/jre.12481
   PubMed Web of Science ®Google Scholar
• Lotti C, Campo Fernandez M, Piccinelli AL, Cuesta-Rubio O, Marquez Hernandez I, Rastrelli L. 2010. Chemical constituents of red Mexican propolis. J Agric Food Chem. 58:2209–2213. doi:10.1021/jf100070w
   PubMed Web of Science ®Google Scholar
• Maciel SS, Feres M, Goncalves TE, Zimmermann GS, da Silva HD, Figueiredo LC, Duarte PM. 2016. Does obesity influence the subgingival microbiota composition in periodontal health and disease?. J Clin Periodontol. 43:1003–1012. doi:10.1111/jcpe.12634
   PubMed Web of Science ®Google Scholar
• Omar RM, Igoli J, Gray AI, Ebiloma GU, Clements C, Fearnley J, Ebel RA, Zhang T, De Koning HP, Watson DG. 2016. Chemical characterisation of Nigerian red propolis and its biological activity against Trypanosoma brucei. Phytochem Anal. 27:107–115. doi:10.1002/pca.2605
   PubMed Web of Science ®Google Scholar
• Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, Flemmig TF, Garcia R, Giannobile WV, Graziani F, et al. 2018. Periodontitis: consensus report of workgroup 2 of the 2017 world workshop on the classification of periodontal and peri-implant diseases and conditions. J Periodontol. 89:S173–S182.
   PubMed Web of Science ®Google Scholar
• Piccinelli AL, Lotti C, Campone L, Cuesta-Rubio O, Campo Fernandez M, Rastrelli L. 2011. Cuban and Brazilian red propolis: botanical origin and comparative analysis by high-performance liquid chromatography-photodiode array detection/electrospray ionization tandem mass spectrometry. J Agric Food Chem. 59:6484–6491. doi:10.1021/jf201280z
   PubMed Web of Science ®Google Scholar
• Preshaw PM. 2018. Host modulation therapy with anti-inflammatory agents. Periodontol 2000. 76:131–149. doi:10.1111/prd.12148
   PubMed Web of Science ®Google Scholar
• Prueksakorn A, Puasiri S, Ruangsri S, Makeudom A, Sastraruji T, Krisanaprakornkit S, Chailertvanitkul P. 2016. The preservative effect of Thai propolis extract on the viability of human periodontal ligament cells. Dent Traumatol. 32:495–501. doi:10.1111/edt.12292
   PubMed Web of Science ®Google Scholar
• Rams TE, Degener JE, van Winkelhoff AJ. 2014. Antibiotic resistance in human chronic periodontitis microbiota. J Periodontol. 85:160–169. doi:10.1902/jop.2013.130142
   PubMed Web of Science ®Google Scholar
• Retamal-Valdes B, Soares GM, Stewart B, Figueiredo LC, Faveri M, Miller S, Zhang YP, Feres M. 2017. Effectiveness of a pre-procedural mouthwash in reducing bacteria in dental aerosols: randomized clinical trial. Braz Oral Res. 31:e21.
   PubMed Web of Science ®Google Scholar
• Sculley DV. 2014. Periodontal disease: modulation of the inflammatory cascade by dietary n-3 polyunsaturated fatty acids. J Periodont Res. 49:277–281. doi:10.1111/jre.12116
   PubMed Web of Science ®Google Scholar
• Silva BB, Rosalen PL, Cury JA, Ikegaki M, Souza VC, Esteves A, Alencar SM. 2008. Chemical composition and botanical origin of red propolis, a new type of brazilian propolis. Evid Based Complement Alternat Med. 5:313–316. doi:10.1093/ecam/nem059
   PubMed Web of Science ®Google Scholar
• Slobodnikova L, Fialova S, Rendekova K, Kovac J, Mucaji P. 2016. Antibiofilm activity of plant polyphenols. Molecules. 13:21.
   Google Scholar
• Soares GM, Teles F, Starr JR, Feres M, Patel M, Martin L, Teles R. 2015. Effects of azithromycin, metronidazole, amoxicillin, and metronidazole plus amoxicillin on an in vitro polymicrobial subgingival biofilm model. Antimicrob Agents Chemother. 59:2791–2798. doi:10.1128/AAC.04974-14
   PubMed Web of Science ®Google Scholar
• Socransky SS, Haffajee AD, Dzink JL, Hillman JD. 1988. Associations between microbial species in subgingival plaque samples. Oral Microbiol Immunol. 3:1–7. doi:10.1111/j.1399-302X.1988.tb00596.x
   PubMedGoogle Scholar
• Trusheva B, Popova M, Naydenski H, Tsvetkova I, Gregorio Rodriguez J, Bankova V. 2004. New polyisoprenylated benzophenones from Venezuelan propolis. Fitoterapia. 75:683–689. doi:10.1016/j.fitote.2004.08.001
   PubMed Web of Science ®Google Scholar
• Van Dyke TE. 2017. Pro-resolving mediators in the regulation of periodontal disease. Mol Aspects Med. 58:21–36. doi:10.1016/j.mam.2017.04.006
   PubMed Web of Science ®Google Scholar
• van Winkelhoff AJ, Herrera D, Oteo A, Sanz M. 2005. Antimicrobial profiles of periodontal pathogens isolated from periodontitis patients in the Netherlands and Spain. J Clin Periodontol. 32:893–898. doi:10.1111/j.1600-051X.2005.00782.x
   PubMed Web of Science ®Google Scholar
• Yoshimasu Y, Ikeda T, Sakai N, Yagi A, Hirayama S, Morinaga Y, Furukawa S, Nakao R. 2018. Rapid bactericidal action of propolis against Porphyromonas gingivalis. J Dent Res. 97:928–936. doi:10.1177/0022034518758034
   PubMed Web of Science ®Google Scholar
• Yuan XJ, Wang YY, Shi BQ, Zhao YM. 2018. Effect of propolis on preserving human periodontal ligament cells and regulating pro-inflammatory cytokines. Dental Traumatol May 27.
   PubMed Web of Science ®Google Scholar
• Zhang CP, Shen XG, Chen JW, Jiang XS, Wang K, Hu FL. 2017. Artepillin C, is it a good marker for quality control of Brazilian green propolis?. Nat Prod Res. 31:2441–2444. doi:10.1080/14786419.2017.1303697
   PubMed Web of Science ®Google Scholar