The Effect of Probiotic Administration on the Modulation of Subgingival Bacteria in Patients with Gingivitis
Keywords:
Probiotic, Sub gingival bacteria, Gingivitis, plaque index, gingival index
Abstract
Aim: To evaluate the efficacy of a probiotic consumption on gingivitis and to assess its impact on the subgingival microbiota.
Material and Methods: the study is a randomized clinical trial that conducted on 30 subjects divided two groups: 15 patients test group suffered from gingivitis who administered probiotic two oral tablets per day containing different probiotic bacterial strains for 20 days and 15 individual control group administered a placebo tab that resemble the probiotic tab. Clinical and microbiological examinations were carried out for 20 days at three stages: (0 day 10 days and 20 days). clinical examination included measurement of gingival (GI) &plaque (PI) indices microbiological examination by counting sub-gingival bacteria at the three stages follow up, the study was approved by the Research Ethics Committee of College of Dentistry University of Mosul with the reference number UoM. Dent/H.OM.61/22. Subjects attending the Faculty of periodontal disease, University of Mosul, College of Dentistry (Mosul, Iraq), from February to November 2022 were screened.
Result: Fredmans showed that there was no significant difference between the mean plaque & gingival indices (0.557, 0.078) respectively for control group conversely for test group who received probiotic supplement showed significant difference between the mean plaque & gingival indices (0.000, 0.000) after the follow up stages.
References
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7. Botero JE, Rosing CK, Duque A, Jaramillo A, Contreras A. Periodontal disease in children and adolescents of Latin America. Periodontology 2000. 2015;67(1):34–57
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9. Chandran, Anju, et al. "Effectiveness of Probiotic Yogurt in Moderate Gingivitis: A Randomized Clinical Trial." Research Journal of Pharmacy and Technology 16.1 (2023): 241-244.
10. Chapple, Iain LC, et al. "Primary prevention of periodontitis: managing gingivitis." Journal of clinical periodontology 42 (2015): S71-S76.
11. de Almeida Silva Levi, Yara Loyanne, et al. "Effects of oral administration of Bifidobacterium animalis subsp. lactis HN019 on the treatment of plaque-induced generalized gingivitis." Clinical Oral Investigations 27.1 (2023): 387-398.
12. Fan, Weihua, et al. "Epidemiology and associated factors of gingivitis in adolescents in Guangdong Province, Southern China: a cross-sectional study." BMC Oral Health 21.1 (2021): 1-9.
13. Fijan S. Microorganisms with claimed probiotic properties: an overview of recent literature. Int J Environ Res Public Health. (2014) 11:4745–67. doi: 10.3390/ijerph110504745
14. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. (2011) 469:543–7. doi: 10.1038/nature09646
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16. Geraldo BMC, Batalha MN, Milhan NVM, Rossoni RD, Scorzoni L, Anbinder AL. Heat-killed Lactobacillus reuteri and cell-free culture supernatant have similar effects to viable probiotics during interaction with Porphyromonas gingivalis. J Periodontal Res. (2020) 55:215–20. doi: 10.1111/jre.12704
17. Gönczi, N. N., Strang, O., Bagi, Z., Rákhely, G., & Kovács, K. L. (2021). Interactions between probiotic and oral pathogenic strains. Biologia Futura, 72(4), 461-471.
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19. Laleman I, Yilmaz E, Ozcelik O, Haytac C, Pauwels M, Herrero ER, et al. The effect of a streptococci containing probiotic in periodontal therapy: a randomized controlled trial. J Clin Periodontol. 2015;42(11):1032-4126-
20. Lloyd-Price etal,(2016) Lloyd-Price J, Abu-Ali G, Huttenhower C. The healthy human microbiome. Genome Med. (2016) 8:51. doi: 10.1186/s13073-016-0307-y
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22. Mkhoyan, G. R., et al. "The use of an Ozone Generator that Produces Ozone Using Ultraviolet Radiation for Ozonize the Contact Medium in the Treatment of Gingivitis of Young People." Journal of International Dental and Medical Research 15.1 (2022): 250-254.
23. Monteagudo-Mera A, Rastall RA, Gibson GR et al (2019) Adhesion mechanisms mediated by probiotics and prebiotics and their potential impact on human health. Appl Microbiol Biotechnol 103:6463–6472.
24. Montero, Eduardo, et al. "Clinical and microbiological effects of the adjunctive use of probiotics in the treatment of gingivitis: A randomized controlled clinical trial." Journal of clinical periodontology 44.7 (2017): 708-716.
25. Morales, A., Gandolfo, A., Bravo, J., Carvajal, P., Silva, N., Godoy, C., et al. (2018). Microbiological and Clinical Effects of Probiotics and Antibiotics on Nonsurgical Treatment of Chronic Periodontitis: a Randomized Placebo- Controlled Trial with 9-month Follow-Up. J. Appl. Oral Sci. 26, e20170075. doi:10.1590/1678-7757-2017-0075
26. Murakami S, Mealey BL, Mariotti A, Chapple ILC. Dental plaque-induced gingival conditions. J Periodontol. 2018;89(Suppl 1):S17–27
27. Nadkerny, Purnima Vidyesh, et al. "A comparative evaluation of the efficacy of probiotic and chlorhexidine mouthrinses on clinical inflammatory parameters of gingivitis: A randomized controlled clinical study." Journal of Indian Society of Periodontology 19.6 (2015): 633.
28. Nazir , M .; Al - Ansari , A .; Al - Khalifa , K .; Alhareky , M .; Gaffar , B .; Almas , K. Global Prevalence of Periodontal Disease and Lack of Its Surveillance . Sci . World J. 2020 , 2020 , 2146160.
29. Olczak-Kowalczyk D, Gozdowski D, Kaczmarek U. Oral health in polish ffteen-year-old adolescents. Oral Health Prev Dent. 2019;17(2):139–46
30. Pangsomboon, Kanokporn. Biosynthetic substance (s) from lactobacillus paracasei HL32 for porphyromonas gingivalis control in periodontal diseases. Diss. Prince of Songkla University, 2007.
31. Paone P, Cani PD. Mucus barrier, mucins and gut microbiota: the expected slimy partners? Gut. (2020) 69:2232–43. doi: 10.1136/gutjnl-2020-322260
32. Papapanou , P.N .; Sanz , M .; Buduneli , N .; Dietrich , T .; Feres , M .; Fine , D.H .; Flemmig , T.F .; Garcia , R .; Giannobile , W.V .; Graziani , F .; et al . Periodontitis : Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri - Implant Diseases and Conditions . J. Periodontol . 2018 , 89 ( Suppl . S1 ) , S173 - S182 . [ CrossRef ]
33. Pera , P .; Menini , M .; Pesce , P .; Bevilacqua , M .; Pera , F .; Tealdo , T. Immediate Versus Delayed Loading of Dental Implants Supporting Fixed Full - Arch Maxillary Prostheses : A 10 - year Follow - up Report . Int . J. Prosthodont . 2019 , 32 , 27-31 .
34. Ranjith, Ambili, Niyas Bin Nazimudeen, and Kamalasanan Vijayakumary Baiju. "Probiotic mouthwash as an adjunct to mechanical therapy in the treatment of stage II periodontitis: A randomized controlled clinical trial." International Journal of Dental Hygiene 20.2 (2022): 415-421.
35. Rosier BT, Moya-Gonzalvez EM, Corell-Escuin P, Mira A. Isolation and characterization of nitrate-reducing bacteria as potential probiotics for oral and systemic health. Front Microbiol. (2020) 11:555465. doi: 10.3389/fmicb.2020.555465
36. Salzberg SL. Open questions: How many genes do we have? BMC Biol. (2018) 16:94. doi: 10.1186/s12915-018-0564-x
37. Sanz M, Herrera D, Kebschull M, Chapple I, Jepsen S, Beglundh T, et al. Treatment of stage I-III periodontitis-The EFP S3 level clinical practice guideline. J Clin Periodontol. (2020) 47:4–60. doi: 10.1111/jcpe.13290
38. Schwendicke F, Splieth CH, Bottenberg P, Breschi L, Campus G, Domejean S, et al. How to intervene in the caries process in adults: proximal and secondary caries? An EFCD-ORCA-DGZ expert Delphi consensus statement. Clin Oral Investig. (2020) 24:3315–21. doi: 10.1007/s00784-020-03431-0
39. Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. (2016) 14:e1002533. doi: 10.1371/journal.pbio.1002533
40. Serrano, J., Escribano, M., Roldan, S., Martin, C. & Herrera, D. (2015) Efficacy of adjunctive chemical plaque control in managing gingivitis. A systematic review and meta-analysis. J Clin Periodontol 2015; 42 (Suppl. 16): S106–S138.
41. Singh AK, Hertzberger RY, Knaus UG. Hydrogen peroxide production by lactobacilli promotes epithelial restitution during colitis. Redox Biol. (2018) 16:11–20. doi: 10.1016/j.redox.2018.02.003
42. Sutula, J., Coulthwaite, L. A., Thomas, L. V., & Verran, J. (2013). The effect of a commercial probiotic drink containing Lactobacillus casei strain Shirota on oral health in healthy dentate people. Microbial ecology in health and disease, 24(1), 21003.
43. Tekce M, Ince G, Gursoy H, Dirikan Ipci S, Cakar G, Kadir T, et al. Clinical and microbiological effects of probiotic lozenges in the treatment of chronic periodontitis: a 1-year follow-up study. J Clin Periodontol. 2015;42(4):363-72
44. Tierney BT, Yang Z, Luber JM, Beaudin M, Wibowo MC, Baek C, et al. The landscape of genetic content in the gut and oral human microbiome. Cell Host Microbe. (2019) 26:283–95. doi: 10.1016/j.chom.2019.07.008
45. Tomazoni F, Vettore MV, Zanatta FB, Tuchtenhagen S, Moreira CH, Ardenghi TM. The associations of socioeconomic status and social capital with gingival bleeding among schoolchildren. J Public Health Dent. 2017;77(1):21–9.
46. Trombelli L, Farina R, Silva CO, Tatakis DN. Plaque-induced gingivitis: case defnition and diagnostic considerations. J Periodontol. 2018;89(Suppl 1):S46–73
47. Underhill DM, Gordon S, Imhof BA, Nunez G, Bousso P. Elie Metchnikoff (1845-1916): celebrating 100 years of cellular immunology and beyond. Nat Rev Immunol. (2016) 16:651–6. doi: 10.1038/nri.2016.89
48. West N, Chapple I, Claydon N, D'Aiuto F, Donos N, Ide M, et al. British society of P, implant dentistry guideline group P. BSP implementation of european s3 - level evidence-based treatment guidelines for stage i-iii periodontitis in uk clinical practice. J Dent. (2021) 106:103562. doi: 10.1016/j.jdent.2020.103562
2. Alanzi, A., Honkala, S., Honkala, E., Varghese, A., Tolvanen, M., & Söderling, E. (2018). Effect of Lactobacillus rhamnosus and Bifidobacterium lactis on gingival health, dental plaque, and periodontopathogens in adolescents: a randomised placebo-controlled clinical trial. Beneficial microbes, 9(4), 593-602.
3. Allaker, Robert P., and Abish S. Stephen. "Use of probiotics and oral health." current oral health reports 4 (2017): 309-318.
4. Araos , R .; D'Agata , E.M.C. The human microbiota and infection prevention . Infect . Control Hosp . Epidemiol . 2019 , 40 , 585-589 .
5. Borrell García, C., Ribelles Llop, M., García Esparza, M. Á., Flichy-Fernández, A. J., Marqués Martínez, L., & Izquierdo Fort, R. (2021). The use of Lactobacillus reuteri DSM 17938 and ATCC PTA 5289 on oral health indexes in a school population: A pilot randomized clinical trial. International Journal of Immunopathology and Pharmacology, 35, 20587384211031107.
6. Borrell García, Carla, et al. "The use of Lactobacillus reuteri DSM 17938 and ATCC PTA 5289 on oral health indexes in a school population: A pilot randomized clinical trial." International Journal of Immunopathology and Pharmacology 35 (2021): 20587384211031107.
7. Botero JE, Rosing CK, Duque A, Jaramillo A, Contreras A. Periodontal disease in children and adolescents of Latin America. Periodontology 2000. 2015;67(1):34–57
8. Caglar E, Topcuoglu N, Cildir SK, et al. (2009) Oral colonization by Lactobacillus reuteri ATCC 55730 after exposure to probiotics. International Journal of Paediatric Dentistry 19(5): 377–381.
9. Chandran, Anju, et al. "Effectiveness of Probiotic Yogurt in Moderate Gingivitis: A Randomized Clinical Trial." Research Journal of Pharmacy and Technology 16.1 (2023): 241-244.
10. Chapple, Iain LC, et al. "Primary prevention of periodontitis: managing gingivitis." Journal of clinical periodontology 42 (2015): S71-S76.
11. de Almeida Silva Levi, Yara Loyanne, et al. "Effects of oral administration of Bifidobacterium animalis subsp. lactis HN019 on the treatment of plaque-induced generalized gingivitis." Clinical Oral Investigations 27.1 (2023): 387-398.
12. Fan, Weihua, et al. "Epidemiology and associated factors of gingivitis in adolescents in Guangdong Province, Southern China: a cross-sectional study." BMC Oral Health 21.1 (2021): 1-9.
13. Fijan S. Microorganisms with claimed probiotic properties: an overview of recent literature. Int J Environ Res Public Health. (2014) 11:4745–67. doi: 10.3390/ijerph110504745
14. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. (2011) 469:543–7. doi: 10.1038/nature09646
15. Funieru C, Klinger A, Baicus C, Funieru E, Dumitriu HT, Dumitriu A. Epidemiology of gingivitis in schoolchildren in Bucharest, Romania: a cross-sectional study. J Periodontal Res. 2017;52(2):225–32.
16. Geraldo BMC, Batalha MN, Milhan NVM, Rossoni RD, Scorzoni L, Anbinder AL. Heat-killed Lactobacillus reuteri and cell-free culture supernatant have similar effects to viable probiotics during interaction with Porphyromonas gingivalis. J Periodontal Res. (2020) 55:215–20. doi: 10.1111/jre.12704
17. Gönczi, N. N., Strang, O., Bagi, Z., Rákhely, G., & Kovács, K. L. (2021). Interactions between probiotic and oral pathogenic strains. Biologia Futura, 72(4), 461-471.
18. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. (2014) 11:506–14. doi: 10.1038/nrgastro.2014.66
19. Laleman I, Yilmaz E, Ozcelik O, Haytac C, Pauwels M, Herrero ER, et al. The effect of a streptococci containing probiotic in periodontal therapy: a randomized controlled trial. J Clin Periodontol. 2015;42(11):1032-4126-
20. Lloyd-Price etal,(2016) Lloyd-Price J, Abu-Ali G, Huttenhower C. The healthy human microbiome. Genome Med. (2016) 8:51. doi: 10.1186/s13073-016-0307-y
21. Mann, Soyon, et al. "Isolation, characterization and biosafety evaluation of Lactobacillus fermentum OK with potential oral probiotic properties." Probiotics and Antimicrobial Proteins 13 (2021): 1363-1386.
22. Mkhoyan, G. R., et al. "The use of an Ozone Generator that Produces Ozone Using Ultraviolet Radiation for Ozonize the Contact Medium in the Treatment of Gingivitis of Young People." Journal of International Dental and Medical Research 15.1 (2022): 250-254.
23. Monteagudo-Mera A, Rastall RA, Gibson GR et al (2019) Adhesion mechanisms mediated by probiotics and prebiotics and their potential impact on human health. Appl Microbiol Biotechnol 103:6463–6472.
24. Montero, Eduardo, et al. "Clinical and microbiological effects of the adjunctive use of probiotics in the treatment of gingivitis: A randomized controlled clinical trial." Journal of clinical periodontology 44.7 (2017): 708-716.
25. Morales, A., Gandolfo, A., Bravo, J., Carvajal, P., Silva, N., Godoy, C., et al. (2018). Microbiological and Clinical Effects of Probiotics and Antibiotics on Nonsurgical Treatment of Chronic Periodontitis: a Randomized Placebo- Controlled Trial with 9-month Follow-Up. J. Appl. Oral Sci. 26, e20170075. doi:10.1590/1678-7757-2017-0075
26. Murakami S, Mealey BL, Mariotti A, Chapple ILC. Dental plaque-induced gingival conditions. J Periodontol. 2018;89(Suppl 1):S17–27
27. Nadkerny, Purnima Vidyesh, et al. "A comparative evaluation of the efficacy of probiotic and chlorhexidine mouthrinses on clinical inflammatory parameters of gingivitis: A randomized controlled clinical study." Journal of Indian Society of Periodontology 19.6 (2015): 633.
28. Nazir , M .; Al - Ansari , A .; Al - Khalifa , K .; Alhareky , M .; Gaffar , B .; Almas , K. Global Prevalence of Periodontal Disease and Lack of Its Surveillance . Sci . World J. 2020 , 2020 , 2146160.
29. Olczak-Kowalczyk D, Gozdowski D, Kaczmarek U. Oral health in polish ffteen-year-old adolescents. Oral Health Prev Dent. 2019;17(2):139–46
30. Pangsomboon, Kanokporn. Biosynthetic substance (s) from lactobacillus paracasei HL32 for porphyromonas gingivalis control in periodontal diseases. Diss. Prince of Songkla University, 2007.
31. Paone P, Cani PD. Mucus barrier, mucins and gut microbiota: the expected slimy partners? Gut. (2020) 69:2232–43. doi: 10.1136/gutjnl-2020-322260
32. Papapanou , P.N .; Sanz , M .; Buduneli , N .; Dietrich , T .; Feres , M .; Fine , D.H .; Flemmig , T.F .; Garcia , R .; Giannobile , W.V .; Graziani , F .; et al . Periodontitis : Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri - Implant Diseases and Conditions . J. Periodontol . 2018 , 89 ( Suppl . S1 ) , S173 - S182 . [ CrossRef ]
33. Pera , P .; Menini , M .; Pesce , P .; Bevilacqua , M .; Pera , F .; Tealdo , T. Immediate Versus Delayed Loading of Dental Implants Supporting Fixed Full - Arch Maxillary Prostheses : A 10 - year Follow - up Report . Int . J. Prosthodont . 2019 , 32 , 27-31 .
34. Ranjith, Ambili, Niyas Bin Nazimudeen, and Kamalasanan Vijayakumary Baiju. "Probiotic mouthwash as an adjunct to mechanical therapy in the treatment of stage II periodontitis: A randomized controlled clinical trial." International Journal of Dental Hygiene 20.2 (2022): 415-421.
35. Rosier BT, Moya-Gonzalvez EM, Corell-Escuin P, Mira A. Isolation and characterization of nitrate-reducing bacteria as potential probiotics for oral and systemic health. Front Microbiol. (2020) 11:555465. doi: 10.3389/fmicb.2020.555465
36. Salzberg SL. Open questions: How many genes do we have? BMC Biol. (2018) 16:94. doi: 10.1186/s12915-018-0564-x
37. Sanz M, Herrera D, Kebschull M, Chapple I, Jepsen S, Beglundh T, et al. Treatment of stage I-III periodontitis-The EFP S3 level clinical practice guideline. J Clin Periodontol. (2020) 47:4–60. doi: 10.1111/jcpe.13290
38. Schwendicke F, Splieth CH, Bottenberg P, Breschi L, Campus G, Domejean S, et al. How to intervene in the caries process in adults: proximal and secondary caries? An EFCD-ORCA-DGZ expert Delphi consensus statement. Clin Oral Investig. (2020) 24:3315–21. doi: 10.1007/s00784-020-03431-0
39. Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. (2016) 14:e1002533. doi: 10.1371/journal.pbio.1002533
40. Serrano, J., Escribano, M., Roldan, S., Martin, C. & Herrera, D. (2015) Efficacy of adjunctive chemical plaque control in managing gingivitis. A systematic review and meta-analysis. J Clin Periodontol 2015; 42 (Suppl. 16): S106–S138.
41. Singh AK, Hertzberger RY, Knaus UG. Hydrogen peroxide production by lactobacilli promotes epithelial restitution during colitis. Redox Biol. (2018) 16:11–20. doi: 10.1016/j.redox.2018.02.003
42. Sutula, J., Coulthwaite, L. A., Thomas, L. V., & Verran, J. (2013). The effect of a commercial probiotic drink containing Lactobacillus casei strain Shirota on oral health in healthy dentate people. Microbial ecology in health and disease, 24(1), 21003.
43. Tekce M, Ince G, Gursoy H, Dirikan Ipci S, Cakar G, Kadir T, et al. Clinical and microbiological effects of probiotic lozenges in the treatment of chronic periodontitis: a 1-year follow-up study. J Clin Periodontol. 2015;42(4):363-72
44. Tierney BT, Yang Z, Luber JM, Beaudin M, Wibowo MC, Baek C, et al. The landscape of genetic content in the gut and oral human microbiome. Cell Host Microbe. (2019) 26:283–95. doi: 10.1016/j.chom.2019.07.008
45. Tomazoni F, Vettore MV, Zanatta FB, Tuchtenhagen S, Moreira CH, Ardenghi TM. The associations of socioeconomic status and social capital with gingival bleeding among schoolchildren. J Public Health Dent. 2017;77(1):21–9.
46. Trombelli L, Farina R, Silva CO, Tatakis DN. Plaque-induced gingivitis: case defnition and diagnostic considerations. J Periodontol. 2018;89(Suppl 1):S46–73
47. Underhill DM, Gordon S, Imhof BA, Nunez G, Bousso P. Elie Metchnikoff (1845-1916): celebrating 100 years of cellular immunology and beyond. Nat Rev Immunol. (2016) 16:651–6. doi: 10.1038/nri.2016.89
48. West N, Chapple I, Claydon N, D'Aiuto F, Donos N, Ide M, et al. British society of P, implant dentistry guideline group P. BSP implementation of european s3 - level evidence-based treatment guidelines for stage i-iii periodontitis in uk clinical practice. J Dent. (2021) 106:103562. doi: 10.1016/j.jdent.2020.103562
Published
2023-06-08
How to Cite
Ula Samir Salim, & Dr. Suhad Mwaffaq Hamdoon. (2023). The Effect of Probiotic Administration on the Modulation of Subgingival Bacteria in Patients with Gingivitis. Central Asian Journal of Medical and Natural Science, 4(3), 533-547. https://doi.org/10.17605/cajmns.v4i3.1563
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