Comparison of matrix metalloproteinase levels in periodontal pockets treated with chlorhexidine and propolis
Year 2024,
Volume: 11 Issue: 4, 729 - 739, 03.11.2024
Ali Batuhan Bayırlı
,
İbrahim Kıvrak
,
Ercan Saruhan
,
Fulden Cantaş Türkiş
Abstract
Natural antimicrobial products are attracting interest in the treatment of periodontal diseases due to their minimal or nonexistent side effects. Propolis, a complex resin content produced by bees, has drawn particular interest for its antibacterial effects, including inhibitory effects on periodontopathogenic bacterial species. This study compared the effects of propolis, a natural product, and chlorhexidine, the gold standard antimicrobial agent, on MMP-1 and MMP-9 levels in gingival crevicular fluid (GCF). Subgingival irrigations of chlorhexidine and propolis solutions were performed in selected deep periodontal pockets of periodontitis patients along with scaling and root planing. The treatment protocol was administered three times at one-month intervals starting from the initial day of the study. GCF MMP-1 and MMP-9 levels, along with clinical periodontal parameters, were evaluated before and after treatment. The study results showed that a statistically significant decrease in clinical periodontal parameters in both groups (p<0.001). Biochemical analysis revealed a statistically significant decrease in levels of GCF MMP-1 and MMP-9 in both groups (p<0.005). Additionally, the decrease in GCF MMP-1 levels was found to be significantly greater in the propolis group compared to the chlorhexidine group (p<0.001).
Ethical Statement
Muğla Sıtkı Koçman University, Clinical Research Ethics Committee, E-72855364-050.01.04-616130.
Thanks
We would like to acknowledge the Department of Chemistry and Chemical Treatment Technologies, Muğla Vocational School, Muğla Sıtkı Koçman University, for providing the propolis extracts used in this research, as well as for their infrastructure, chemicals, and continuous support throughout the research process.
References
- Addy, M. (1995). Evaluation of clinical trials of agents and procedures to prevent caries and periodontal disease: choosing products and recommending procedures. International Dental Journal, 45(3), 185–196.
- Azmak, N., Atilla, G., Luoto, H., & Sorsa, T. (2002). The effect of subgingival controlled-release delivery of chlorhexidine chip on clinical parameters and matrix metalloproteinase-8 levels in gingival crevicular fluid. Journal of Periodontology, 73(6), 608–615. https://doi.org/10.1902/jop.2002.73.6.608
- Bankova, V., Trusheva, B., & Popova, M. (2021). Propolis extraction methods: A review. Journal of Apicultural Research, 60(5), 734 743. https://doi.org/10.1080/00218839.2021.1901426
- Bush, K., Courvalin, P., Dantas, G., Davies, J., Eisenstein, B., Huovinen, … Zgurskaya, H.I. (2011). Tackling antibiotic resistance. Nature reviews. Microbiology, 9(12), 894–896. https://doi.org/10.1038/nrmicro2693
- Coutinho A. (2012). Honeybee propolis extract in periodontal treatment: a clinical and microbiological study of propolis in periodontal treatment. Indian Journal of Dental Research: Official Publication of Indian Society for Dental Research, 23(2), 294. https://doi.org/10.4103/0970-9290.100449
- de Morais, E.F., Pinheiro, J.C., Leite, R.B., Santos, P.P.A., Barboza, C.A.G., & Freitas, R.A. (2018). Matrix metalloproteinase-8 levels in periodontal disease patients: A systematic review. Journal of Periodontal Research, 53(2), 156–163. https://doi.org/10.1111/jre.12495
- Ertugrul, A.S., Dursun, R., Dundar, N., Avunduk, M.C., & Hakki, S.S. (2013). MMP-1, MMP-9, and TIMP-1 levels in oral lichen planus patients with gingivitis or periodontitis. Archives of Oral Biology, 58(7), 843–852. https://doi.org/10.1016/j.archoralbio.2013.01.015
- Eslami, H., Pouralibaba, F., Falsafi, P., Bohluli, S., Najati, B., Negahdari, R., & Ghanizadeh, M. (2016). Efficacy of Hypozalix spray and propolis mouthwash for prevention of chemotherapy-induced oral mucositis in leukemic patients: A double-blind randomized clinical trial. Journal of Dental Research, Dental Clinics, Dental Prospects, 10(4), 226–233. https://doi.org/10.15171/joddd.2016.036
- Jenkins, S., Addy, M., & Wade, W. (1988). The mechanism of action of chlorhexidine. A study of plaque growth on enamel inserts in vivo. Journal of Clinical Periodontology, 15(7), 415–424. https://doi.org/10.1111/j.1600-051x.1988.tb01595.x
- Jones C.G. (1997). Chlorhexidine: is it still the gold standard?. Periodontology 2000, 15, 55–62. https://doi.org/10.1111/j.1600-0757.1997.tb00105.x
- Kale, Y., Yadav, S., Dadpe, M., Dahake, P., & Kendre, S. (2022). Bioinductive and anti-inflammatory properties of Propolis and Biodentine on SHED. The Saudi Dental Journal, 34(7), 544–552. https://doi.org/10.1016/j.sdentj.2022.08.009
- Khurshid, Z., Naseem, M., Zafar, M.S., Najeeb, S., & Zohaib, S. (2017). Propolis: A natural biomaterial for dental and oral healthcare. Journal of Dental Research, Dental Clinics, Dental Prospects, 11(4), 265–274. https://doi.org/10.15171/joddd.2017.046
- Kolahi, J., & Soolari, A. (2006). Rinsing with chlorhexidine gluconate solution after brushing and flossing teeth: a systematic review of effectiveness. Quintessence International (Berlin, Germany: 1985), 37(8), 605–612.
- Kosalec, I., Pepeljnjak, S., Bakmaz, M., & Vladimir-Knezević, S. (2005). Flavonoid analysis and antimicrobial activity of commercially available propolis products. Acta pharmaceutica (Zagreb, Croatia), 55(4), 423–430.
- Kubota, T., Itagaki, M., Hoshino, C., Nagata, M., Morozumi, T., Kobayashi, T., Takagi, R., & Yoshie, H. (2008). Altered gene expression levels of matrix metalloproteinases and their inhibitors in periodontitis-affected gingival tissue. Journal of Periodontology, 79(1), 166–173. https://doi.org/10.1902/jop.2008.070159
- Kujumgiev, A., Tsvetkova, I., Serkedjieva, Y., Bankova, V., Christov, R., & Popov, S. (1999). Antibacterial, antifungal and antiviral activity of propolis of different geographic origin. Journal of Ethnopharmacology, 64(3), 235–240. https://doi.org/10.1016/s0378-8741(98)00131-7
- Kuo, Y.Y., Jim, W.T., Su, L.C., Chung, C.J., Lin, C.Y., Huo, C., … Chuu, C.P. (2015). Caffeic Acid phenethyl ester is a potential therapeutic agent for oral cancer. International Journal of Molecular Sciences, 16(5), 10748–10766. https://doi.org/10.3390/ijms160510748
- Liberio, S.A., Pereira, A.L., Dutra, R.P., Reis, A.S., Araújo, M.J., Mattar, N.S., … Monteiro-Neto, V. (2011). Antimicrobial activity against oral pathogens and immunomodulatory effects and toxicity of geopropolis produced by the stingless bee Melipona fasciculata Smith. BMC Complementary and Alternative Medicine, 11, 108. https://doi.org/10.1186/1472-6882-11-108
- Mariotti, A.J., & Rumpf, D.A. (1999). Chlorhexidine-induced changes to human gingival fibroblast collagen and non-collagen protein production. Journal of Periodontology, 70(12), 1443–1448. https://doi.org/10.1902/jop.1999.70.12.1443
- Nakao, R., Senpuku, H., Ohnishi, M., Takai, H., & Ogata, Y. (2020). Effect of topical administration of propolis in chronic periodontitis. Odontology, 108(4), 704–714. https://doi.org/10.1007/s10266-020-00500-4
- Papapanou, P.N., Sanz, M., Buduneli, N., Dietrich, T., Feres, M., Fine, D.H., … Tonetti, M.S. (2018). Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. Journal of Periodontology, 89 Suppl 1, S173–S182. https://doi.org/10.1002/JPER.17-0721
- Paraskevas S. (2005). Randomized controlled clinical trials on agents used for chemical plaque control. International Journal of Dental Hygiene, 3(4), 162 178. https://doi.org/10.1111/j.1601-5037.2005.00145.x
- Poppolo Deus, F., & Ouanounou, A. (2022). Chlorhexidine in Dentistry: Pharmacology, Uses, and Adverse Effects. International Dental Journal, 72(3), 269277. https://doi.org/10.1016/j.identj.2022.01.005
- Romano, F., Arduino, P.G., Maggiora, M., Curmei, E., Manavella, V., Broccoletti, R., & Aimetti, M. (2019). Effect of a structured plaque control on MMP-1 and MMP-9 crevicular levels in patients with desquamative gingivitis associated with oral lichen planus. Clinical Oral Investigations, 23(6), 2651–2658. https://doi.org/10.1007/s00784-018-2704-7
- Rufatto, L.C., Luchtenberg, P., Garcia, C., Thomassigny, C., Bouttier, S., Henriques, J.A.P., Roesch-Ely, M., Dumas, F., & Moura, S. (2018). Brazilian red propolis: Chemical composition and antibacterial activity determined using bioguided fractionation. Microbiological Research, 214, 74–82. https://doi.org/10.1016/j.micres.2018.05.003
- Sajjan, P., Laxminarayan, N., Kar, P.P., & Sajjanar, M. (2016). Chlorhexidine as an antimicrobial agent in dentistry–a review. Oral Health Dent Manag, 15(2), 93-100.
- Sanghani, N.N., Bm, S., & S.S. (2014). Health from the hive: propolis as an adjuvant in the treatment of chronic periodontitis - a clinicomicrobiologic study. Journal of Clinical and Diagnostic Research: JCDR, 8(9), ZC41 ZC44. https://doi.org/10.7860/JCDR/2014/8817.4856
- Séguier, S., Gogly, B., Bodineau, A., Godeau, G., & Brousse, N. (2001). Is collagen breakdown during periodontitis linked to inflammatory cells and expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human gingival tissue?. Journal of Periodontology, 72(10), 1398 1406. https://doi.org/10.1902/jop.2001.72.10.1398
- Sekhon, B.S. (2010). Matrix metalloproteinases–an overview. Research and Reports in Biology, 1-20.
- Seth, T.A., Kale, T.A., Lendhey, S.S., & Bhalerao, P.V. (2022). Comparative evaluation of subgingival irrigation with propolis extract versus chlorhexidine as an adjunct to scaling and root planing for the treatment of chronic periodontitis: A randomized controlled trial. Journal of Indian Society of Periodontology, 26(2), 151 156. https://doi.org/10.4103/jisp.jisp_613_20
- Shrivastava, D., Natoli, V., Srivastava, K.C., Alzoubi, I.A., Nagy, A.I., Hamza, M.O., Al-Johani, K., Alam, M.K., & Khurshid, Z. (2021). Novel Approach to Dental Biofilm Management through Guided Biofilm Therapy (GBT): A Review. Microorganisms, 9(9), 1966. https://doi.org/10.3390/microorganisms9091966
- Teles, R., Moss, K., Preisser, J.S., Genco, R., Giannobile, W.V., Corby, P., … Cugini, M. (2018). Patterns of periodontal disease progression based on linear mixed models of clinical attachment loss. Journal of Clinical Periodontology, 45(1), 15 25. https://doi.org/10.1111/jcpe.12827
- Tonetti, M.S., Greenwell, H., & Kornman, K.S. (2018). Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. Journal of Periodontology, 89 Suppl 1, S159–S172. https://doi.org/10.1002/JPER.18-0006
- van Winkelhoff, A.J., Herrera Gonzales, D., Winkel, E.G., Dellemijn-Kippuw, N., Vandenbroucke-Grauls, C.M., & Sanz, M. (2000). Antimicrobial resistance in the subgingival microflora in patients with adult periodontitis. A comparison between The Netherlands and Spain. Journal of Clinical Periodontology, 27(2), 79 86. https://doi.org/10.1034/j.1600-051x.2000.027002079.x
- Vitkov, L., Muñoz, L.E., Schoen, J., Knopf, J., Schauer, C., Minnich, B., Herrmann, M., & Hannig, M. (2021). Neutrophils Orchestrate the Periodontal Pocket. Frontiers in Immunology, 12, 788766. https://doi.org/10.3389/fimmu.2021.788766
- Vitt, A., Babenka, A., Boström, E. A., Gustafsson, A., Lira Junior, R., Slizen, V., … Buhlin, K. (2020). Adjunctive Antiseptic Irrigation of Periodontal Pockets: Effects on Microbial and Cytokine Profiles. Dentistry Journal, 8(4), 124. https://doi.org/10.3390/dj8040124
- Yan, Y., Zhan, Y., Wang, X., & Hou, J. (2020). 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, 21(1), 113. https://doi.org/10.1186/s13063-019-4031-y
- 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. Journal of Dental Research, 97(8), 928–936. https://doi.org/10.1177/0022034518758034
- Yuan, Q., Wang, Y., Zeng, J., & Luan, Q. (2022). Integrated effects of ultrasonic scaling and subgingival irrigation with 0.12% chlorhexidine by a newly designed ultrasonic scaler tip in chronic periodontitis. Quintessence International (Berlin, Germany: 1985), 53(4), 298–305. https://doi.org/10.3290/j.qi.b2407777
- Zarch, R.E., Askari, M., Boostani, H., & Mirzaii-Dizgah, I. (2021). Effect of propolis extract on clinical parameters and salivary level of matrix metalloproteinase 8 in periodontitis patients: A randomized controlled clinical trial. Journal of Advanced Periodontology & Implant Dentistry, 13(2), 84–89. https://doi.org/10.34172/japid.2021.013
Comparison of matrix metalloproteinase levels in periodontal pockets treated with chlorhexidine and propolis
Year 2024,
Volume: 11 Issue: 4, 729 - 739, 03.11.2024
Ali Batuhan Bayırlı
,
İbrahim Kıvrak
,
Ercan Saruhan
,
Fulden Cantaş Türkiş
Abstract
Natural antimicrobial products are attracting interest in the treatment of periodontal diseases due to their minimal or nonexistent side effects. Propolis, a complex resin content produced by bees, has drawn particular interest for its antibacterial effects, including inhibitory effects on periodontopathogenic bacterial species. This study compared the effects of propolis, a natural product, and chlorhexidine, the gold standard antimicrobial agent, on MMP-1 and MMP-9 levels in gingival crevicular fluid (GCF). Subgingival irrigations of chlorhexidine and propolis solutions were performed in selected deep periodontal pockets of periodontitis patients along with scaling and root planing. The treatment protocol was administered three times at one-month intervals starting from the initial day of the study. GCF MMP-1 and MMP-9 levels, along with clinical periodontal parameters, were evaluated before and after treatment. The study results showed that a statistically significant decrease in clinical periodontal parameters in both groups (p<0.001). Biochemical analysis revealed a statistically significant decrease in levels of GCF MMP-1 and MMP-9 in both groups (p<0.005). Additionally, the decrease in GCF MMP-1 levels was found to be significantly greater in the propolis group compared to the chlorhexidine group (p<0.001).
Ethical Statement
Muğla Sıtkı Koçman University, Clinical Research Ethics Committee, E-72855364-050.01.04-616130.
Thanks
We would like to acknowledge the Department of Chemistry and Chemical Treatment Technologies, Muğla Vocational School, Muğla Sıtkı Koçman University, for providing the propolis extracts used in this research, as well as for their infrastructure, chemicals, and continuous support throughout the research process.
References
- Addy, M. (1995). Evaluation of clinical trials of agents and procedures to prevent caries and periodontal disease: choosing products and recommending procedures. International Dental Journal, 45(3), 185–196.
- Azmak, N., Atilla, G., Luoto, H., & Sorsa, T. (2002). The effect of subgingival controlled-release delivery of chlorhexidine chip on clinical parameters and matrix metalloproteinase-8 levels in gingival crevicular fluid. Journal of Periodontology, 73(6), 608–615. https://doi.org/10.1902/jop.2002.73.6.608
- Bankova, V., Trusheva, B., & Popova, M. (2021). Propolis extraction methods: A review. Journal of Apicultural Research, 60(5), 734 743. https://doi.org/10.1080/00218839.2021.1901426
- Bush, K., Courvalin, P., Dantas, G., Davies, J., Eisenstein, B., Huovinen, … Zgurskaya, H.I. (2011). Tackling antibiotic resistance. Nature reviews. Microbiology, 9(12), 894–896. https://doi.org/10.1038/nrmicro2693
- Coutinho A. (2012). Honeybee propolis extract in periodontal treatment: a clinical and microbiological study of propolis in periodontal treatment. Indian Journal of Dental Research: Official Publication of Indian Society for Dental Research, 23(2), 294. https://doi.org/10.4103/0970-9290.100449
- de Morais, E.F., Pinheiro, J.C., Leite, R.B., Santos, P.P.A., Barboza, C.A.G., & Freitas, R.A. (2018). Matrix metalloproteinase-8 levels in periodontal disease patients: A systematic review. Journal of Periodontal Research, 53(2), 156–163. https://doi.org/10.1111/jre.12495
- Ertugrul, A.S., Dursun, R., Dundar, N., Avunduk, M.C., & Hakki, S.S. (2013). MMP-1, MMP-9, and TIMP-1 levels in oral lichen planus patients with gingivitis or periodontitis. Archives of Oral Biology, 58(7), 843–852. https://doi.org/10.1016/j.archoralbio.2013.01.015
- Eslami, H., Pouralibaba, F., Falsafi, P., Bohluli, S., Najati, B., Negahdari, R., & Ghanizadeh, M. (2016). Efficacy of Hypozalix spray and propolis mouthwash for prevention of chemotherapy-induced oral mucositis in leukemic patients: A double-blind randomized clinical trial. Journal of Dental Research, Dental Clinics, Dental Prospects, 10(4), 226–233. https://doi.org/10.15171/joddd.2016.036
- Jenkins, S., Addy, M., & Wade, W. (1988). The mechanism of action of chlorhexidine. A study of plaque growth on enamel inserts in vivo. Journal of Clinical Periodontology, 15(7), 415–424. https://doi.org/10.1111/j.1600-051x.1988.tb01595.x
- Jones C.G. (1997). Chlorhexidine: is it still the gold standard?. Periodontology 2000, 15, 55–62. https://doi.org/10.1111/j.1600-0757.1997.tb00105.x
- Kale, Y., Yadav, S., Dadpe, M., Dahake, P., & Kendre, S. (2022). Bioinductive and anti-inflammatory properties of Propolis and Biodentine on SHED. The Saudi Dental Journal, 34(7), 544–552. https://doi.org/10.1016/j.sdentj.2022.08.009
- Khurshid, Z., Naseem, M., Zafar, M.S., Najeeb, S., & Zohaib, S. (2017). Propolis: A natural biomaterial for dental and oral healthcare. Journal of Dental Research, Dental Clinics, Dental Prospects, 11(4), 265–274. https://doi.org/10.15171/joddd.2017.046
- Kolahi, J., & Soolari, A. (2006). Rinsing with chlorhexidine gluconate solution after brushing and flossing teeth: a systematic review of effectiveness. Quintessence International (Berlin, Germany: 1985), 37(8), 605–612.
- Kosalec, I., Pepeljnjak, S., Bakmaz, M., & Vladimir-Knezević, S. (2005). Flavonoid analysis and antimicrobial activity of commercially available propolis products. Acta pharmaceutica (Zagreb, Croatia), 55(4), 423–430.
- Kubota, T., Itagaki, M., Hoshino, C., Nagata, M., Morozumi, T., Kobayashi, T., Takagi, R., & Yoshie, H. (2008). Altered gene expression levels of matrix metalloproteinases and their inhibitors in periodontitis-affected gingival tissue. Journal of Periodontology, 79(1), 166–173. https://doi.org/10.1902/jop.2008.070159
- Kujumgiev, A., Tsvetkova, I., Serkedjieva, Y., Bankova, V., Christov, R., & Popov, S. (1999). Antibacterial, antifungal and antiviral activity of propolis of different geographic origin. Journal of Ethnopharmacology, 64(3), 235–240. https://doi.org/10.1016/s0378-8741(98)00131-7
- Kuo, Y.Y., Jim, W.T., Su, L.C., Chung, C.J., Lin, C.Y., Huo, C., … Chuu, C.P. (2015). Caffeic Acid phenethyl ester is a potential therapeutic agent for oral cancer. International Journal of Molecular Sciences, 16(5), 10748–10766. https://doi.org/10.3390/ijms160510748
- Liberio, S.A., Pereira, A.L., Dutra, R.P., Reis, A.S., Araújo, M.J., Mattar, N.S., … Monteiro-Neto, V. (2011). Antimicrobial activity against oral pathogens and immunomodulatory effects and toxicity of geopropolis produced by the stingless bee Melipona fasciculata Smith. BMC Complementary and Alternative Medicine, 11, 108. https://doi.org/10.1186/1472-6882-11-108
- Mariotti, A.J., & Rumpf, D.A. (1999). Chlorhexidine-induced changes to human gingival fibroblast collagen and non-collagen protein production. Journal of Periodontology, 70(12), 1443–1448. https://doi.org/10.1902/jop.1999.70.12.1443
- Nakao, R., Senpuku, H., Ohnishi, M., Takai, H., & Ogata, Y. (2020). Effect of topical administration of propolis in chronic periodontitis. Odontology, 108(4), 704–714. https://doi.org/10.1007/s10266-020-00500-4
- Papapanou, P.N., Sanz, M., Buduneli, N., Dietrich, T., Feres, M., Fine, D.H., … Tonetti, M.S. (2018). Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. Journal of Periodontology, 89 Suppl 1, S173–S182. https://doi.org/10.1002/JPER.17-0721
- Paraskevas S. (2005). Randomized controlled clinical trials on agents used for chemical plaque control. International Journal of Dental Hygiene, 3(4), 162 178. https://doi.org/10.1111/j.1601-5037.2005.00145.x
- Poppolo Deus, F., & Ouanounou, A. (2022). Chlorhexidine in Dentistry: Pharmacology, Uses, and Adverse Effects. International Dental Journal, 72(3), 269277. https://doi.org/10.1016/j.identj.2022.01.005
- Romano, F., Arduino, P.G., Maggiora, M., Curmei, E., Manavella, V., Broccoletti, R., & Aimetti, M. (2019). Effect of a structured plaque control on MMP-1 and MMP-9 crevicular levels in patients with desquamative gingivitis associated with oral lichen planus. Clinical Oral Investigations, 23(6), 2651–2658. https://doi.org/10.1007/s00784-018-2704-7
- Rufatto, L.C., Luchtenberg, P., Garcia, C., Thomassigny, C., Bouttier, S., Henriques, J.A.P., Roesch-Ely, M., Dumas, F., & Moura, S. (2018). Brazilian red propolis: Chemical composition and antibacterial activity determined using bioguided fractionation. Microbiological Research, 214, 74–82. https://doi.org/10.1016/j.micres.2018.05.003
- Sajjan, P., Laxminarayan, N., Kar, P.P., & Sajjanar, M. (2016). Chlorhexidine as an antimicrobial agent in dentistry–a review. Oral Health Dent Manag, 15(2), 93-100.
- Sanghani, N.N., Bm, S., & S.S. (2014). Health from the hive: propolis as an adjuvant in the treatment of chronic periodontitis - a clinicomicrobiologic study. Journal of Clinical and Diagnostic Research: JCDR, 8(9), ZC41 ZC44. https://doi.org/10.7860/JCDR/2014/8817.4856
- Séguier, S., Gogly, B., Bodineau, A., Godeau, G., & Brousse, N. (2001). Is collagen breakdown during periodontitis linked to inflammatory cells and expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human gingival tissue?. Journal of Periodontology, 72(10), 1398 1406. https://doi.org/10.1902/jop.2001.72.10.1398
- Sekhon, B.S. (2010). Matrix metalloproteinases–an overview. Research and Reports in Biology, 1-20.
- Seth, T.A., Kale, T.A., Lendhey, S.S., & Bhalerao, P.V. (2022). Comparative evaluation of subgingival irrigation with propolis extract versus chlorhexidine as an adjunct to scaling and root planing for the treatment of chronic periodontitis: A randomized controlled trial. Journal of Indian Society of Periodontology, 26(2), 151 156. https://doi.org/10.4103/jisp.jisp_613_20
- Shrivastava, D., Natoli, V., Srivastava, K.C., Alzoubi, I.A., Nagy, A.I., Hamza, M.O., Al-Johani, K., Alam, M.K., & Khurshid, Z. (2021). Novel Approach to Dental Biofilm Management through Guided Biofilm Therapy (GBT): A Review. Microorganisms, 9(9), 1966. https://doi.org/10.3390/microorganisms9091966
- Teles, R., Moss, K., Preisser, J.S., Genco, R., Giannobile, W.V., Corby, P., … Cugini, M. (2018). Patterns of periodontal disease progression based on linear mixed models of clinical attachment loss. Journal of Clinical Periodontology, 45(1), 15 25. https://doi.org/10.1111/jcpe.12827
- Tonetti, M.S., Greenwell, H., & Kornman, K.S. (2018). Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. Journal of Periodontology, 89 Suppl 1, S159–S172. https://doi.org/10.1002/JPER.18-0006
- van Winkelhoff, A.J., Herrera Gonzales, D., Winkel, E.G., Dellemijn-Kippuw, N., Vandenbroucke-Grauls, C.M., & Sanz, M. (2000). Antimicrobial resistance in the subgingival microflora in patients with adult periodontitis. A comparison between The Netherlands and Spain. Journal of Clinical Periodontology, 27(2), 79 86. https://doi.org/10.1034/j.1600-051x.2000.027002079.x
- Vitkov, L., Muñoz, L.E., Schoen, J., Knopf, J., Schauer, C., Minnich, B., Herrmann, M., & Hannig, M. (2021). Neutrophils Orchestrate the Periodontal Pocket. Frontiers in Immunology, 12, 788766. https://doi.org/10.3389/fimmu.2021.788766
- Vitt, A., Babenka, A., Boström, E. A., Gustafsson, A., Lira Junior, R., Slizen, V., … Buhlin, K. (2020). Adjunctive Antiseptic Irrigation of Periodontal Pockets: Effects on Microbial and Cytokine Profiles. Dentistry Journal, 8(4), 124. https://doi.org/10.3390/dj8040124
- Yan, Y., Zhan, Y., Wang, X., & Hou, J. (2020). 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, 21(1), 113. https://doi.org/10.1186/s13063-019-4031-y
- 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. Journal of Dental Research, 97(8), 928–936. https://doi.org/10.1177/0022034518758034
- Yuan, Q., Wang, Y., Zeng, J., & Luan, Q. (2022). Integrated effects of ultrasonic scaling and subgingival irrigation with 0.12% chlorhexidine by a newly designed ultrasonic scaler tip in chronic periodontitis. Quintessence International (Berlin, Germany: 1985), 53(4), 298–305. https://doi.org/10.3290/j.qi.b2407777
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