PHYTOCHEMICAL ANALYSIS AND EFFECTIVENESS OF STINGLESS BEES PROPOLIS (GENIOTRIGONA THORACICA) ON MATRIX METALLOPROTEINASE-8 LEVELS IN PERIODONTAL THERAPY

Authors

  • PITU WULANDARI Department of Periodontics, Faculty of Dentistry, Universitas Sumatera Utara, Medan, Indonesia https://orcid.org/0000-0001-8337-2691
  • FELIX ZULHENDRI Kebun Efi, Kabanjahe, Sumatera Utara, Indonesia
  • OLIVIA AVRIYANTI HANAFIAH Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Universitas Sumatera Utara, Medan, Indonesia
  • IRMA ERVINA Department of Periodontics, Faculty of Dentistry, Universitas Sumatera Utara, Medan, Indonesia https://orcid.org/0000-0002-8705-4022
  • NURDIANA epartment of Oral Medicine, Faculty of Dentistry, Universitas Sumatera Utara, Medan, Indonesia https://orcid.org/0000-0002-7212-952X
  • JULIA MAHARANI Magister Student, Faculty of Dentistry, Universitas Sumatera Utara, Medan, Indonesia
  • JAYNE MARY SIMANUNGKALIT Undergraduate Student, Faculty of Dentistry, Universitas Sumatera Utara, Medan, Indonesia
  • DATIN ZAHIRA AULINA Undergraduate Student, Faculty of Dentistry, Universitas Sumatera Utara, Medan, Indonesia
  • RONNY LESMANA Physiology Division, Department of Biomedical Sciences, Faculty of Medicine, Universitas Padjadjaran, Indonesia

DOI:

https://doi.org/10.22159/ijap.2024.v16s2.06

Keywords:

Stingless bees, Geniotrigona thoracica

Abstract

Objective: Propolis is a beehive-derived natural substance containing plant secondary metabolites and can potentially be used for periodontal therapy. This study aims to analyze the phytochemicals of Indonesian stingless bee propolis and its efficacy of propolis extract gel as an adjunctive periodontal therapy. Methods: The qualitative and quantitative phytochemical analysis measured the total phenolic and flavonoid content. The gallic acid equivalent was used to measure phenolics, and the Quercetin equivalent was used to measure the flavonoids of the extract. The Kirby-Bauer method was used to analyze the antimicrobial activity. The study used periodontitis-induced Wistar rats and were treated by applying propolis gel with concentrations of 50%, 60%, and 70%. Matrix Metalloproteinase-8 (MMP-8) level was measured with the Enzyme-Linked Immunosorbent Assay (ELISA). Results: The qualitative and quantitative phytochemical analysis of the propolis extract detected the presence of phenol, flavonoid, alkaloid, triterpenoid, saponins, glycosides, and tannins. The Kirby-Bauer method showed that propolis gel with a concentration of 50%, 60%, and 70% had a significant difference in inhibition between treatment groups against Porphyromonas gingivalis (p<0.05). The 70% propolis gel appeared effective in inducing the expression of MMP-8 (p<0.05). Conclusion: Propolis extract gel with 70% concentration could potentially be used as a supportive treatment for periodontal therapy.

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References

Bhattarai G, Poudel SB, Kook SH, Lee JC. Resveratrol prevents alveolar bone loss in an experimental rat model of periodontitis. Acta Biomater. 2016;29:398-408. doi: 10.1016/j.actbio.2015.10.031, PMID 26497626.

Fischer RG, Lira Junior R, Retamal Valdes B, Figueiredo LC, Malheiros Z, Stewart B. Periodontal disease and its impact on general health in Latin America. Section V: Treatment of periodontitis. Braz Oral Res. 2020;34Suppl11:e026. doi: 10.1590/1807-3107bor-2020.vol34.0026, PMID 32294679.

Yan Y, Zhan Y, Wang X, Hou J. Clinical evaluation of ultrasonic subgingival debridement versus ultrasonic subgingival scaling combined with manual root planing in the treatment of periodontitis: study protocol for a randomized controlled trial. Trials. 2020;21(1):113. doi: 10.1186/s13063-019-4031-y, PMID 31992331.

Bian Y, Liu C, Fu Z. Application value of combination therapy of periodontal curettage and root planing on moderate-to-severe chronic periodontitis in patients with type 2 diabetes. Head Face Med. 2021;17(1):12. doi: 10.1186/s13005-020-00253-z, PMID 33832490.

Kapoor A, Malhotra R, Grover V, Grover D. Systemic antibiotic therapy in periodontics. Dent Res J (Isfahan). 2012;9(5):505-15. doi: 10.4103/1735-3327.104866, PMID 23559912.

Huang S, Zhang CP, Wang K, Li GQ, Hu FL. Recent advances in the chemical composition of propolis. Molecules. 2014;19(12):19610-32. doi: 10.3390/molecules191219610, PMID 25432012.

Salatino A, Salatino MLF. Scientific note: often quoted, but not factual data about propolis composition. Apidologie. 2021;52(2):312-4. doi: 10.1007/s13592-020-00821-x.

Zulhendri F, Chandrasekaran K, Kowacz M, Ravalia M, Kripal K, Fearnley J. Antiviral, antibacterial, antifungal, and antiparasitic properties of propolis: a review. Foods. 2021;10(6). doi: 10.3390/foods10061360, PMID 34208334.

Zulhendri F, Ravalia M, Kripal K, Chandrasekaran K, Fearnley J, Perera CO. Propolis in metabolic syndrome and its associated chronic diseases: a narrative review. Antioxidants (Basel). 2021;10(3):348. doi: 10.3390/antiox10030348, PMID 33652692.

Räisänen IT, Umeizudike KA, Parnanen P, Heikkila P, Tervahartiala T, Nwhator SO. Periodontal disease and targeted prevention using aMMP-8 point-of-care oral fluid analytics in the COVID-19 era. Med Hypotheses. 2020;144:110276. doi: 10.1016/j.mehy.2020.110276, PMID 33254580.

Thierbach R, Maier K, Sorsa T, Mantyla P. Peri-Implant Sulcus Fluid (PISF) Matrix Metalloproteinase (MMP) -8 levels in peri-implantitis. J Clin Diagn Res. 2016;10(5):ZC34-8. doi: 10.7860/JCDR/2016/16105.7749, PMID 27437357.

Zhang L, Li X, Yan H, Huang L. Salivary matrix metalloproteinase (MMP)-8 as a biomarker for periodontitis: a PRISMA-compliant systematic review and meta-analysis. Med (Baltim). 2018;97(3):e9642. doi: 10.1097/MD.0000000000009642, PMID 29504999.

Ingman T, Tervahartiala T, Ding Y, Tschesche H, Haerian A, Kinane DF. Matrix metalloproteinases and their inhibitors in gingival crevicular fluid and saliva of periodontitis patients. J Clin Periodontol. 1996;23(12):1127-32. doi: 10.1111/j.1600-051x.1996.tb01814.x, PMID 8997658.

Akbari G, Prabhuji ML, Karthikeyan BV, Raghunatha K, Narayanan R. Analysis of matrix metalloproteinase-8 levels in gingival crevicular fluid and whole mouth fluid among smokers and nonsmokers using enzyme-linked immune-sorbent assay and a novel chair-side test. J Indian Soc Periodontol. 2015;19(5):525-30. doi: 10.4103/0972-124X.162201, PMID 26644719.

Luchian I, Goriuc A, Sandu D, Covasa M. The role of matrix metalloproteinases (MMP-8, MMP-9, MMP-13) in periodontal and peri-implant pathological processes. Int J Mol Sci. 2022;23(3). doi: 10.3390/ijms23031806, PMID 35163727.

Yakob M, Kari K, Tervahartiala T, Sorsa T, Soder PO, Meurman JH. Associations of periodontal microorganisms with salivary proteins and MMP-8 in gingival crevicular fluid. J Clin Periodontol. 2012;39(3):256-63. doi: 10.1111/j.1600-051X.2011.01813.x, PMID 22103335.

Júnior UPS, Cabrera SP, Silva TMGd, Silva EMSd, Camara CA, Silva TMS. Geopropolis gel for the adjuvant treatment of candidiasis-formulation and in vitro release assay. Revista Brasileira de Farmacognosia. 2019;29(3):278-86. doi: 10.1016/j.bjp.2019.02.010.

Zulhendri F, Perera CO, Chandrasekaran K, Ghosh A, Tandean S, Abdulah R. Propolis of stingless bees for the development of novel functional food and nutraceutical ingredients: a systematic scoping review of the experimental evidence. J Funct Foods. 2022;88:1-20. doi: 10.1016/j.jff.2021.104902.

Linares A, Sanz Sanchez I, Dopico J, Molina A, Blanco J, Montero E. Efficacy of adjunctive measures in the non-surgical treatment of peri-implantitis: a systematic review. J Clinic Periodontology. 2023;50Suppl 26:224-43. doi: 10.1111/jcpe.13821.

Hienz SA, Paliwal S, Ivanovski S. Mechanisms of bone resorption in periodontitis. J Immunol Res. 2015;2015:615486. doi: 10.1155/2015/615486, PMID 26065002.

Frederic LJ, Michel B, Selena T. Oral microbes, biofilms and their role in periodontal and peri-implant diseases. Materials. 2018;11(10). doi: 10.3390/ma11101802.

Almadi EM, Almohaimede AA. Natural products in endodontics. Saudi Med J. 2018;39(2):124-30. doi: 10.15537/smj.2018.2.21038, PMID 29436559.

Chinsembu KC. Plants and other natural products used in the management of oral infections and improvement of oral health. Acta Trop. 2016;154:6-18. doi: 10.1016/j.actatropica.2015.10.019, PMID 26522671.

Martinello M, Mutinelli F. Antioxidant activity in bee products: a review. Antioxidants (Basel, Switzerland). 2021;10(1):1-42. doi: 10.3390/antiox10010071, PMID 33430511.

Przybyłek I, Karpinski TM. Antibacterial properties of propolis. Molecules. 2019;24(11). doi: 10.3390/molecules24112047, PMID 31146392.

Şenel E, Demir E. Bibliometric analysis of apitherapy in complementary medicine literature between 1980 and 2016. Complement Ther Clin Pract. 2018;31:47-52. doi: 10.1016/j.ctcp.2018.02.003, PMID 29705479.

Bankova VS, De Castro SL, Marcucci MC. Propolis: recent advances in chemistry and plant origin. Apidologie. 2000;31(1):3-15. doi: 10.1051/apido:2000102.

Marcucci MC, Ferreres F, Garcia Viguera C, Bankova VS, De Castro SL, Dantas AP. Phenolic compounds from Brazilian propolis with pharmacological activities. J Ethnopharmacol. 2001;74(2):105-12. doi: 10.1016/s0378-8741(00)00326-3, PMID 11167028.

Almuhayawi MS. Propolis as a novel antibacterial agent. Saudi J Biol Sci. 2020;27(11):3079-86. doi: 10.1016/j.sjbs.2020.09.016, PMID 33100868.

Pasupuleti VR, Sammugam L, Ramesh N, Gan SH. Honey, propolis, and royal jelly: a comprehensive review of their biological actions and health benefits. Oxid Med Cell Longev. 2017;2017:1259510. doi: 10.1155/2017/1259510, PMID 28814983.

De Souza Ferreira SB, de Assis Dias BR, Obregon CS, Gomes CC, de Araujo Pereira RR, Ribeiro Godoy JS. Microparticles containing propolis and metronidazole: in vitro characterization, release study and antimicrobial activity against periodontal pathogens. Pharm Dev Technol. 2014;19(2):173-80. doi: 10.3109/10837450.2013.763262, PMID 23356908.

Balata GF, Abdelhady MIS, Mahmoud GM, Matar MA, Abd El-Latif AN. Formulation of Saudi propolis into biodegradable chitosan chips for vital pulpotomy. Curr Drug Deliv. 2018;15(1):97-109. doi: 10.2174/1567201814666170125121735, PMID 28124615.

Simu MR, Pall E, Radu T, Miclaus M, Culic B, Mesaros AS. Development of a novel biomaterial with an important osteoinductive capacity for hard tissue engineering. Tissue Cell. 2018;52:101-7. doi: 10.1016/j.tice.2018.04.004, PMID 29857818.

Ahi ZB, Renkler NZ, Gul Seker M, Tuzlakoglu K. Biodegradable polymer films with a natural antibacterial extract as novel periodontal barrier membranes. Int J Biomater. 2019;2019:7932470. doi: 10.1155/2019/7932470, PMID 31485230.

Ideguchi H, Yamashiro K, Yamamoto T, Shimoe M, Hongo S, Kochi S. Molecular imaging assessment of periodontitis lesions in an experimental mouse model. Clin Oral Investig. 2019;23(2):821-7. doi: 10.1007/s00784-018-2510-2, PMID 29876665.

Ishida N, Ishihara Y, Ishida K, Tada H, Funaki Kato Y, Hagiwara M. Periodontitis induced by bacterial infection exacerbates features of Alzheimer’s disease in transgenic mice. NPJ Aging Mech Dis. 2017;3:15. doi: 10.1038/s41514-017-0015-x, PMID 29134111.

Bostanci N, Mitsakakis K, Afacan B, Bao K, Johannsen B, Baumgartner D. Validation and verification of predictive salivary biomarkers for oral health. Sci Rep. 2021;11(1):6406. doi: 10.1038/s41598-021-85120-w, PMID 33742017.

Enersen M, Nakano K, Amano A. Porphyromonas gingivalis fimbriae. J Oral Microbiol. 2013;5. doi: 10.3402/jom.v5i0.20265, PMID 23667717.

Figueiredo LC, Freitas Figueiredo N, da Cruz DF, Baccelli GT, Sarachini GE, Bueno MR. Propolis, aloe vera, green tea, cranberry, calendula, myrrha and salvia properties against periodontal microorganisms. Microorganisms. 2022;10(11). doi: 10.3390/microorganisms10112172, PMID 36363764.

Yoshimasu Y, Ikeda T, Sakai N, Yagi A, Hirayama S, Morinaga Y. Rapid bactericidal action of propolis against Porphyromonas gingivalis. J Dent Res. 2018;97(8):928-36. doi: 10.1177/0022034518758034, PMID 29494308.

Nakao R, Senpuku H, Ohnishi M, Takai H, Ogata Y. Effect of topical administration of propolis in chronic periodontitis. Odontology. 2020;108(4):704-14. doi: 10.1007/s10266-020-00500-4, PMID 32112365.

Veloz JJ, Alvear M, Salazar LA. Antimicrobial and antibiofilm activity against Streptococcus mutans of individual and mixtures of the main polyphenolic compounds found in Chilean propolis. BioMed Res Int. 2019;2019:7602343. doi: 10.1155/2019/7602343, PMID 30719447.

Nazir NH, SWNSS. Chemical constituents of Malaysian Geniotrigona thoracica propolis. Pertanika J Trop Agric. 2018;41:955-62.

Wang CY, Chen YW, Hou CY. Antioxidant and antibacterial activity of seven predominant terpenoids. International Journal of Food Properties. 2019;22(1):230-8. doi: 10.1080/10942912.2019.1582541.

Rajoo M. The role of propolis in inflammation and orofacial pain: a review. Annu Res Rev Biol. 2014;4(4):651-64. doi: 10.9734/ARRB/2014/6111.

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):1302-9. doi: 10.1128/AAC.46.5.1302-1309.2002, PMID 11959560.

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. doi: 10.4103/0970-9290.100449, PMID 22945731.

Skaba D, Morawiec T, Tanasiewicz M, Mertas A, Bobela E, Szliszka E. Influence of the toothpaste with Brazilian ethanol extract propolis on the oral cavity health. Evid Based Complement Alternat Med. 2013;2013:215391. doi: 10.1155/2013/215391, PMID 23861699.

Lisbona Gonzalez MJ, Munoz Soto E, Lisbona Gonzalez C, Vallecillo Rivas M, Diaz Castro J, Moreno Fernandez J. Effect of propolis paste and mouthwash formulation on healing after teeth extraction in periodontal disease. Plants (Basel, Switzerland). 2021;10(8). doi: 10.3390/plants10081603, PMID 34451647.

Nilminie R. Salivary matrix metalloproteinase-8 and-9 and myeloperoxidase in relation to coronary heart and periodontal diseases: a subgroup report from the parokrank study (Periodontitis and its relation to coronary artery disease). PLOS ONE. 2015;10(7):e0126370. doi: 10.1371/journal.pone.0126370

Sorsa T, Mantyla P, Tervahartiala T, Pussinen PJ, Gamonal J, Hernandez M. MMP activation in diagnostics of periodontitis and systemic inflammation. J Clin Periodontol. 2011;38(9):817-9. doi: 10.1111/j.1600-051X.2011.01753.x, PMID 21707693.

Eghbali Zarch R, Askari M, boostani H, Mirzaii Dizgah I. Effect of propolis extract on clinical parameters and salivary level of matrix metalloproteinase 8 in periodontitis patients: a randomized controlled clinical trial. J Adv Periodontol Implant Dent. 2021;13(2):84-9. doi: 10.34172/japid.2021.013, PMID 35919679.

Franco C, Patricia HR, Timo S, Claudia B, Marcela H. Matrix metalloproteinases as regulators of periodontal inflammation. Int J Mol Sci. 2017;18(2). doi: 10.3390/ijms18020440, PMID 28218665.

Al-Majid A, Alassiri S, Rathnayake N, Tervahartiala T, Gieselmann DR, Sorsa T. Matrix metalloproteinase-8 as an inflammatory and prevention biomarker in periodontal and peri-implant diseases. Int J Dent. 2018;2018:7891323. doi: 10.1155/2018/7891323, PMID 30305812.

Sorsa T, Gursoy UK, Nwhator S, Hernandez M, Tervahartiala T, Leppilahti J. Analysis of matrix metalloproteinases, especially MMP-8, in gingival creviclular fluid, mouth rinse and saliva for monitoring periodontal diseases. Periodontol 2000. 2016;70(1):142-63. doi: 10.1111/prd.12101, PMID 26662488.

Lopez Valverde N, Pardal Pelaez B, Lopez Valverde A, Flores Fraile J, Herrero Hernandez S, Macedo-de-Sousa B. Effectiveness of propolis in the treatment of periodontal disease: updated systematic review with meta-analysis. Antioxidants (Basel, Switzerland). 2021;10(2):1-14. doi: 10.3390/antiox10020269, PMID 33578659.

de Morais EF, Pinheiro JC, Leite RB, Santos PPA, Barboza CAG, Freitas RA. Matrix metalloproteinase-8 levels in periodontal disease patients: a systematic review. J Periodont Res. 2018;53(2):156-63. doi: 10.1111/jre.12495.

Kraft Neumarker M, Lorenz K, Koch R, Hoffmann T, Mantyla P, Sorsa T. Full-mouth profile of active MMP-8 in periodontitis patients. J Periodontal Res. 2012;47(1):121-8. doi: 10.1111/j.1600-0765.2011.01416.x, PMID 21958332.

Tonetti MS, Freiburghaus K, Lang NP, Bickel M. Detection of interleukin-8 and matrix metalloproteinases transcripts in healthy and diseased gingival biopsies by RNA/PCR. J Periodontal Res. 1993;28:511-3. doi: 10.1111/j.1600-0765.1993.tb02114.x, PMID 8263721.

Gupta N, Gupta ND, Gupta A, Khan S, Bansal N. Role of salivary matrix metalloproteinase-8 (MMP-8) in chronic periodontitis diagnosis. Front Med. 2015;9(1):72-6. doi: 10.1007/s11684-014-0347-x, PMID 25098434.

Luo KW, Wei Chen, Lung WY, Wei XY, Cheng BH, Cai ZM. EGCG inhibited bladder cancer SW780 cell proliferation and migration both in vitro and in vivo via down-regulation of NF-κB and MMP-9. J Nutr Biochem. 2017;41:56-64. doi: 10.1016/j.jnutbio.2016.12.004, PMID 28040581.

Verstappen J, Von den Hoff JW. Tissue Inhibitors of Metalloproteinases (TIMPs): their biological functions and involvement in oral disease. J Dent Res. 2006;85(12):1074-84. doi: 10.1177/154405910608501202.

Miller CS, Ding X, Dawson DR, Ebersole JL. Salivary biomarkers for discriminating periodontitis in the presence of diabetes. J Clin Periodontol. 2021;48(2):216-25. doi: 10.1111/jcpe.13393, PMID 33098098.

Miller CS, King CP, Langub MC, Kryscio RJ, Thomas MV. Salivary biomarkers of existing periodontal disease: a cross-sectional study. J Am Dent Assoc. 2006;137(3):322-9. doi: 10.14219/jada.archive.2006.0181, PMID 16570465.

Ebersole JL, Nagarajan R, Akers D, Miller CS. Targeted salivary biomarkers for discrimination of periodontal health and disease(s). Front Cell Infect Microbiol. 2015;5:62. doi: 10.3389/fcimb.2015.00062, PMID 26347856.

Arakawa H, Uehara J, Hara ES, Sonoyama W, Kimura A, Kanyama M. Matrix metalloproteinase-8 is the major potential collagenase in active peri-implantitis. J Prosthodont Res. 2012;56(4):249-55. doi: 10.1016/j.jpor.2012.07.002, PMID 23083963.

Sorsa T, Alassiri S, Grigoriadis A, Raisanen IT, Parnanen P, Nwhator SO. Active MMP-8 (aMMP-8) as a grading and staging biomarker in the periodontitis classification. Diagnostics (Basel, Switzerland). 2020;10(2). doi: 10.3390/diagnostics10020061, PMID 31979091.

Sbardella D, Fasciglione GF, Gioia M, Ciaccio C, Tundo GR, Marini S. Human matrix metalloproteinases: an ubiquitarian class of enzymes involved in several pathological processes. Mol Aspects Med. 2012;33(2):119-208. doi: 10.1016/j.mam.2011.10.015, PMID 22100792.

Li G, Yue Y, Tian Y, Li JL, Wang M, Liang H. Association of matrix metalloproteinase (MMP)-1, 3, 9, interleukin (IL)-2, 8 and cyclooxygenase (COX)-2 gene polymorphisms with chronic periodontitis in a Chinese population. Cytokine. 2012;60(2):552-60. doi: 10.1016/j.cyto.2012.06.239, PMID 22819245.

Araujo MG, Lindhe J. Peri-implant health. J Periodontol. 2018;89Suppl 1:S249-56. doi: 10.1002/JPER.16-0424, PMID 29926949.

Konopka L, Pietrzak A, Brzezinska Błaszczyk E. Effect of scaling and root planing on interleukin-1β, interleukin-8 and MMP-8 levels in gingival crevicular fluid from chronic periodontitis patients. J Periodontal Res. 2012;47(6):681-8. doi: 10.1111/j.1600-0765.2012.01480.x, PMID 22510045.

Published

27-05-2024

How to Cite

WULANDARI, P., ZULHENDRI, F., HANAFIAH, O. A., ERVINA, I., NURDIANA, MAHARANI, J., SIMANUNGKALIT, J. M., AULINA, D. Z., & LESMANA, R. (2024). PHYTOCHEMICAL ANALYSIS AND EFFECTIVENESS OF STINGLESS BEES PROPOLIS (GENIOTRIGONA THORACICA) ON MATRIX METALLOPROTEINASE-8 LEVELS IN PERIODONTAL THERAPY. International Journal of Applied Pharmaceutics, 16(2), 22–28. https://doi.org/10.22159/ijap.2024.v16s2.06

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