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Effect of topical administration of propolis in chronic periodontitis

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Abstract

To investigate the effect of topical administration of propolis (a honeybee product) or curry leaf (an herbal product) into the periodontal pockets of periodontitis patients, a double-blind controlled clinical trial was conducted with 24 subjects including one drop-out diagnosed with moderate-to-advanced chronic periodontitis who completed initial periodontal therapy. They were randomly allocated to the following treatments: placebo, propolis, curry leaf, and minocycline. Gingival crevicular fluid (GCF) samples collected before and after the intervention were analyzed to quantify the number of total bacteria and number of six major periodontopathic bacteria by real-time PCR. Periodontitis-related clinical parameters were also analyzed. Among the six propolis-treated patients whose GCF samples were P. gingivalis-positive, three patients converted to be P. gingivalis-negative after the intervention. The minocycline-treated group exhibited a decrease in probing pocket depth (PPD) with statistically significant improvement, but not gain of clinical attachment level (CAL). Both PPD and CAL have been improved in the propolis-treated group at a statistically significant level, but not the curry leaf-treated group. In conclusion, treatment with propolis significantly improved both PPD and CAL, together with a tendency towards reduced P. gingivalis burden in GCF. It is likely that a propolis-based therapy becomes an alternative treatment option for chronic periodontitis during supportive periodontal therapy.

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References

  1. Lamont RJ, Hajishengallis GN, Jenkinson HF. Oral microbiology and immunology. 2nd ed. New York: ASM Press; 2013.

    Google Scholar 

  2. Hung HC, Douglass CW. Meta-analysis of the effect of scaling and root planing, surgical treatment and antibiotic therapies on periodontal probing depth and attachment loss. J Clin Periodontol. 2002;29(11):975–86 (epub 2002/12/11).

  3. Haffajee AD, Teles RP, Socransky SS. The effect of periodontal therapy on the composition of the subgingival microbiota. Periodontol. 2000;2006(42):219–58. https://doi.org/10.1111/j.1600-0757.2006.00191.x (epub 2006/08/26).

  4. Kawashima H, Sato S, Kishida M, Ito K. A comparison of root surface instrumentation using two piezoelectric ultrasonic scalers and a hand scaler in vivo. J Periodontal Res. 2007;42(1):90–5. https://doi.org/10.1111/j.1600-0765.2006.00924.x(epub 2007/01/12).

    Article  PubMed  Google Scholar 

  5. Donos N, Calciolari E, Brusselaers N, Goldoni M, Bostanci N, Belibasakis GN. The adjunctive use of host modulators in non-surgical periodontal therapy. A systematic review of randomized, placebo-controlled clinical studies. J Clin Periodontol. 2019. https://doi.org/10.1111/jcpe.13232(epub 2019/12/14).

    Article  PubMed  Google Scholar 

  6. Matesanz-Perez P, Garcia-Gargallo M, Figuero E, Bascones-Martinez A, Sanz M, Herrera D. A systematic review on the effects of local antimicrobials as adjuncts to subgingival debridement, compared with subgingival debridement alone, in the treatment of chronic periodontitis. J Clin Periodontol. 2013;40(3):227–41. https://doi.org/10.1111/jcpe.12026(epub 2013/01/17).

    Article  PubMed  Google Scholar 

  7. Ratka-Kruger P, Schacher B, Burklin T, Boddinghaus B, Holle R, Renggli HH, et al. Non-surgical periodontal therapy with adjunctive topical doxycycline: a double-masked, randomized, controlled multicenter study II. Microbiological results. J Periodontol. 2005;76(1):66–74. https://doi.org/10.1902/jop.2005.76.1.66(epub 2005/04/16).

    Article  PubMed  Google Scholar 

  8. Machion L, Andia DC, Benatti BB, Carvalho MD, Nogueira-Filho GR, Casati MZ, et al. Locally delivered doxycycline as an adjunctive therapy to scaling and root planing in the treatment of smokers: a clinical study. J Periodontol. 2004;75(3):464–9. https://doi.org/10.1902/jop.2004.75.3.464(epub 2004/04/20).

    Article  PubMed  Google Scholar 

  9. Machion L, Andia DC, Saito D, Klein MI, Goncalves RB, Casati MZ, et al. Microbiological changes with the use of locally delivered doxycycline in the periodontal treatment of smokers. J Periodontol. 2004;75(12):1600–4. https://doi.org/10.1902/jop.2004.75.12.1600(epub 2005/03/01).

    Article  PubMed  Google Scholar 

  10. Nakao R, Takigawa S, Sugano N, Koshi R, Ito K, Watanabe H, et al. Impact of minocycline ointment for periodontal treatment of oral bacteria. Jpn J Infect Dis. 2011;64(2):156–60 (epub 2011/04/27).

  11. Naik SK, Mohanty S, Padhi A, Pati R, Sonawane A. Evaluation of antibacterial and cytotoxic activity of Artemisia nilagirica and Murraya koenigii leaf extracts against mycobacteria and macrophages. BMC Complement Altern Med. 2014;14:87. https://doi.org/10.1186/1472-6882-14-87(epub 2014/03/07).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Vats M, Singh H, Sardana S. Phytochemical screening and antimicrobial activity of roots of Murraya koenigii (Linn.) Spreng. (Rutaceae). Braz J Microbiol. 2011;42(4):1569–73. https://doi.org/10.1590/S1517-838220110004000044(epub 2011/10/01).

  13. Keluskar P, Ingle S. Ethnopharmacology guided screening of traditional Indian herbs for selective inhibition of Plasmodium specific lactate dehydrogenase. J Ethnopharmacol. 2012;144(1):201–7. https://doi.org/10.1016/j.jep.2012.09.006(epub 2012/09/18).

    Article  PubMed  Google Scholar 

  14. Burdock GA. Review of the biological properties and toxicity of bee propolis (propolis). Food Chem Toxicol. 1998;36(4):347–63.

    Article  Google Scholar 

  15. Sforcin JM. Biological properties and therapeutic applications of propolis. Phytother Res. 2016;30(6):894–905. https://doi.org/10.1002/ptr.5605.

    Article  PubMed  Google Scholar 

  16. Park YK, Alencar SM, Aguiar CL. Botanical origin and chemical composition of Brazilian propolis. J Agric Food Chem. 2002;50(9):2502–6 (epub 2002/04/18).

  17. Yoshimasu Y, Ikeda T, Sakai N, Yagi A, Hirayama S, Morinaga Y, et al. Rapid bactericidal action of propolis against Porphyromonas gingivalis. J Dent Res. 2018;97(8):928–36. https://doi.org/10.1177/0022034518758034(epub 2018/03/02).

    Article  PubMed  Google Scholar 

  18. Gebaraa EC, Pustiglioni AN, de Lima LA, Mayer MP. Propolis extract as an adjuvant to periodontal treatment. Oral Health Prev Dent. 2003;1(1):29–35 (epub 2005/01/13).

  19. Sanghani NN, Bm S. Health from the hive: propolis as an adjuvant in the treatment of chronic periodontitis—a clinicomicrobiologic study. J Clin Diagn Res. 2014;8(9):ZC41–4. https://doi.org/10.7860/JCDR/2014/8817.4856.

  20. Periodontology AAo. American Academy of Periodontology Task Force Report on the update to the 1999 classification of periodontal diseases and conditions. J Periodontol. 2015;86(7):835–8. https://doi.org/10.1902/jop.2015.157001(epub 2015/07/01).

  21. Kato A, Imai K, Ochiai K, Ogata Y. Prevalence and quantitative analysis of Epstein–Barr virus DNA and Porphyromonas gingivalis associated with Japanese chronic periodontitis patients. Clin Oral Invest. 2015;19(7):1605–10. https://doi.org/10.1007/s00784-014-1387-y(epub 2014/12/18).

    Article  Google Scholar 

  22. O'Leary TJ, Drake RB, Naylor JE. The plaque control record. J Periodontol. 1972;43(1):38. https://doi.org/10.1902/jop.1972.43.1.38(epub 1972/01/01).

    Article  PubMed  Google Scholar 

  23. Ramfjord SP, Knowles JW, Nissle RR, Burgett FG, Shick RA. Results following three modalities of periodontal therapy. J Periodontol. 1975;46(9):522–6. https://doi.org/10.1902/jop.1975.46.9.522(epub 1975/09/01).

    Article  PubMed  Google Scholar 

  24. Ramfjord SP, Knowles JW, Nissle RR, Shick RA, Burgett FG. Longitudinal study of periodontal therapy. J Periodontol. 1973;44(2):66–77. https://doi.org/10.1902/jop.1973.44.2.66(epub 1973/02/01).

    Article  PubMed  Google Scholar 

  25. Pedersen AML, Sorensen CE, Proctor GB, Carpenter GH, Ekstrom J. Salivary secretion in health and disease. J Oral Rehabil. 2018;45(9):730–46. https://doi.org/10.1111/joor.12664(epub 2018/06/08).

    Article  PubMed  Google Scholar 

  26. Coutinho A. Honeybee propolis extract in periodontal treatment: a clinical and microbiological study of propolis in periodontal treatment. Indian J Dent Res. 2012;23(2):294. https://doi.org/10.4103/0970-9290.100449.

    Article  PubMed  Google Scholar 

  27. Sparabombe S, Monterubbianesi R, Tosco V, Orilisi G, Hosein A, Ferrante L, et al. Efficacy of an all-natural polyherbal mouthwash in patients with periodontitis: a single-blind randomized controlled trial. Front Physiol. 2019;10:632. https://doi.org/10.3389/fphys.2019.00632(epub 2019/06/14).

  28. Deas DE, Pasquali LA, Yuan CH, Kornman KS. The relationship between probing attachment loss and computerized radiographic analysis in monitoring progression of periodontitis. J Periodontol. 1991;62(2):135–41. https://doi.org/10.1902/jop.1991.62.2.135(epub 1991/02/01).

    Article  PubMed  Google Scholar 

  29. Hajishengallis G. Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol. 2015;15(1):30–44. https://doi.org/10.1038/nri3785.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol. 2012;10(10):717–25. https://doi.org/10.1038/nrmicro2873.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Maekawa T, Krauss JL, Abe T, Jotwani R, Triantafilou M, Triantafilou K, et al. Porphyromonas gingivalis manipulates complement and TLR signaling to uncouple bacterial clearance from inflammation and promote dysbiosis. Cell Host Microbe. 2014;15(6):768–78. https://doi.org/10.1016/j.chom.2014.05.012.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Zaric S, Shelburne C, Darveau R, Quinn DJ, Weldon S, Taggart CC, et al. Impaired immune tolerance to Porphyromonas gingivalis lipopolysaccharide promotes neutrophil migration and decreased apoptosis. Infect Immun. 2010;78(10):4151–6. https://doi.org/10.1128/IAI.00600-10(epub 2010/08/04).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998;25(2):134–44.

    Article  Google Scholar 

  34. Henderson B, Ward JM, Ready D. Aggregatibacter (Actinobacillus) actinomycetemcomitans: a triple A* periodontopathogen? Periodontol 2000. 2010;54(1):78–105. https://doi.org/10.1111/j.1600-0757.2009.00331.x(epub 2010/08/18).

  35. Ulger Toprak N, Veloo ACM, Urban E, Wybo I, Justesen US, Jean-Pierre H, et al. A multicenter survey of antimicrobial susceptibility of Prevotella species as determined by Etest methodology. Anaerobe. 2018;52:9–15. https://doi.org/10.1016/j.anaerobe.2018.05.005(epub 2018/06/04).

    Article  PubMed  Google Scholar 

  36. Harvey AL, Edrada-Ebel R, Quinn RJ. The re-emergence of natural products for drug discovery in the genomics era. Nat Rev Drug Discov. 2015;14(2):111–29. https://doi.org/10.1038/nrd4510(epub 2015/01/24).

    Article  Google Scholar 

  37. Huang S, Zhang CP, Wang K, Li GQ, Hu FL. Recent advances in the chemical composition of propolis. Molecules. 2014;19(12):19610–32. https://doi.org/10.3390/molecules191219610.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Paulino N, Abreu SR, Uto Y, Koyama D, Nagasawa H, Hori H, et al. Anti-inflammatory effects of a bioavailable compound, Artepillin C, in Brazilian propolis. Eur J Pharmacol. 2008;587(1–3):296–301. https://doi.org/10.1016/j.ejphar.2008.02.067(epub 2008/05/14).

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank Yoshiko Obara, Yuri Yoshimasu, Naomi Nojiri, and Junko Sugita for technical assistance. The authors thank all members affiliated with the Department of Periodontology, Nihon University Hospital at Matsudo for great support in data collection for the clinical study.

Funding

This work was supported by a grant from the Japan Society for the Promotion of Science KAKENHI (JP26462866), the Urakami Foundation for Food and Food Culture Promotion, and a Yamada Research Grant (0163, 0186).

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Authors and Affiliations

  1. Department of Bacteriology I, National Institute of Infectious Diseases, 1-23-1 Toyama, Shinjuku-ku, Tokyo, 162-8640, Japan

    Ryoma Nakao, Hidenobu Senpuku & Makoto Ohnishi

  2. Department of Periodontology, Nihon University School of Dentistry at Matsudo, Chiba, Japan

    Hideki Takai & Yorimasa Ogata

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  1. Ryoma Nakao
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  2. Hidenobu Senpuku
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Correspondence to Ryoma Nakao.

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Nakao, R., Senpuku, H., Ohnishi, M. et al. Effect of topical administration of propolis in chronic periodontitis. Odontology 108, 704–714 (2020). https://doi.org/10.1007/s10266-020-00500-4

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