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Microbiological dynamics of red complex bacteria following full-mouth air polishing in periodontally healthy subjects—a randomized clinical pilot study

  • Belinda Reinhardt
  • Astrid Klocke
  • Sarah H. Neering
  • Sabine Selbach
  • Ulrike Peters
  • Thomas F. Flemmig
  • Thomas BeiklerEmail author
Original Article
  • 4 Downloads

Abstract

Objectives

Suppression of periodontal pathogens in the oral cavity of periodontally healthy individuals may lower the risk for periodontal or periimplant diseases. Therefore, the present study aimed to analyze the effect of supragingival debridement (SD) with adjunctive full mouth glycine powder air polishing (FM-GPAP) on the prevalence of periodontal pathogens in periodontally healthy individuals.

Materials and Methods

Eighty-seven systemically and periodontally healthy intraoral carriers of red complex bacteria, i.e., Porphyromonas gingivalis, Tannerella forsythia, and Treponema denticola or other periodontal pathogens including Aggregatibacter actinomycetemcomitans, Prevotella intermedia, and Eikenella corrodens were enrolled into the study and randomly assigned to receive SD with adjunctive FM-GPAP (test, n = 42) or SD alone (control, n = 45). In the first observation period, microbiological samples were obtained prior to, and 2, 5, and 9 days following intervention. If one of these periodontal pathogens could still not be identified, additional microbial sampling was performed after 6 and 12 weeks.

Results

The prevalence of red complex bacteria was significantly reduced in the test compared to the control group following treatment (p = 0.004) and at day 9 (p = 0.031). Intragroup comparison showed a significant (test, p < 0.001; control, p ≤ 0.01) reduction in the mean prevalence in both groups from BL through day 9 with an additional significant intergroup difference (p = 0.048) at day 9. However, the initial strong reduction returned to baseline values after 6 and 12 weeks.

Conclusion

In periodontally healthy carriers of periodontal pathogens, FM-GPAP as an adjunct to SD transiently enhances the suppression of red complex bacteria.

Clinical relevance

Whether the enhanced suppression of red complex bacteria by adjunctive FM-GPAP prevents the development of periodontitis in periodontally healthy carriers requires further investigations.

Keywords

Red complex bacteria Non-surgical periodontal therapy Full-mouth Glycine powder air polishing Periodontal health Prevention 

Notes

Funding

The follow-up was funded by the authors own departments.

Compliance with ethical standards

Conflict of interest

Thomas Flemmig is an inventor with patents covering the fine-grain, low-abrasive glycine powder used in the present study. To safeguard against the conduct and outcomes of the clinical trial being influenced by a potential conflict of interest, Thomas Flemmig refrained from any sensitive elements of the clinical trial, including patient consent, direct data scoring, statistical analysis of data, and adverse event evaluation and reporting.

No other investigators had any conflicts of interest related to this study.

Ethical approval

All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional review board of the Heinrich-Heine-University, Germany (protocol number 3519).

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Zee KY (2009) Smoking and periodontal disease. Aust Dent J 54(Suppl 1):S44–S50.  https://doi.org/10.1111/j.1834-7819.2009.01142.x CrossRefGoogle Scholar
  2. 2.
    Genco RJ, Borgnakke WS (2013) Risk factors for periodontal disease. Periodontol 2000 62:59–94.  https://doi.org/10.1111/j.1600-0757.2012.00457.x CrossRefGoogle Scholar
  3. 3.
    Clark WB, Loe H (1993) Mechanisms of initiation and progression of periodontal disease. Periodontol 2000 2:72–82CrossRefGoogle Scholar
  4. 4.
    Darveau RP, Tanner A, Page RC (1997) The microbial challenge in periodontitis. Periodontol 2000 14:12–32CrossRefGoogle Scholar
  5. 5.
    Flemmig TF, Beikler T (2011) Control of oral biofilms. Periodontol 2000 55:9–15.  https://doi.org/10.1111/j.1600-0757.2010.00383.x CrossRefGoogle Scholar
  6. 6.
    Pozhitkov AE, Leroux BG, Randolph TW, Beikler T, Flemmig TF, Noble PA (2015) Towards microbiome transplant as a therapy for periodontitis: an exploratory study of periodontitis microbial signature contrasted by oral health, caries and edentulism. BMC Oral Health 15:125CrossRefGoogle Scholar
  7. 7.
    Rafiei M, Kiani F, Sayehmiri K, Sayehmiri F, Tavirani M, Dousti M, Sheikhi A (2018) Prevalence of anaerobic bacteria (P.gingivalis) as major microbial agent in the incidence periodontal diseases by meta-analysis. J Dent (Shiraz) 19:232–242Google Scholar
  8. 8.
    Nadkarni MA, Chhour KL, Browne GV, Byun R, Nguyen KA, Chapple CC, Jacques NA, Hunter N (2015) Age-dependent changes in Porphyromonas gingivalis and Prevotella species/phylotypes in healthy gingiva and inflamed/diseased sub-gingival sites. Clin Oral Investig 19:911–919.  https://doi.org/10.1007/s00784-014-1301-7 CrossRefGoogle Scholar
  9. 9.
    Aruni AW, Dou Y, Mishra A, Fletcher HM (2015) The Biofilm Community-Rebels with a Cause. Curr Oral Health Rep 2:48–56CrossRefGoogle Scholar
  10. 10.
    Kinane DF, Galicia JC, Gorr SU, Stathopoulou PG, Benakanakere M (2008) P. gingivalis interactions with epithelial cells. Front Biosci 13:966–984CrossRefGoogle Scholar
  11. 11.
    Lamont RJ, Hajishengallis G (2015) Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol Med 21:172–183CrossRefGoogle Scholar
  12. 12.
    Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43:5721–5732CrossRefGoogle Scholar
  13. 13.
    Duran-Pinedo AE, Baker VD, Frias-Lopez J (2014) The periodontal pathogen Porphyromonas gingivalis induces expression of transposases and cell death of Streptococcus mitis in a biofilm model. Infect Immun 82:3374–3382CrossRefGoogle Scholar
  14. 14.
    Bosshardt DD (2018) The periodontal pocket: pathogenesis, histopathology and consequences. Periodontol 2000 76:43–50.  https://doi.org/10.1111/prd.12153 CrossRefGoogle Scholar
  15. 15.
    Mineoka T, Awano S, Rikimaru T, Kurata H, Yoshida A, Ansai T, Takehara T (2008) Site-specific development of periodontal disease is associated with increased levels of Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia in subgingival plaque. J Periodontol 79:670–676.  https://doi.org/10.1902/jop.2008.070398 CrossRefGoogle Scholar
  16. 16.
    Yao ES, Lamont RJ, Leu SP, Weinberg A (1996) Interbacterial binding among strains of pathogenic and commensal oral bacterial species. Oral Microbiol Immunol 11:35–41CrossRefGoogle Scholar
  17. 17.
    Kolenbrander PE, Andersen RN (1989) Inhibition of coaggregation between Fusobacterium nucleatum and Porphyromonas (Bacteroides) gingivalis by lactose and related sugars. Infect Immun 57:3204–3209Google Scholar
  18. 18.
    Kolenbrander PE, Palmer RJ Jr, Rickard AH, Jakubovics NS, Chalmers NI, Diaz PI (2006) Bacterial interactions and successions during plaque development. Periodontol 2000 42:47–79.  https://doi.org/10.1111/j.1600-0757.2006.00187.x CrossRefGoogle Scholar
  19. 19.
    Abusleme L, Dupuy AK, Dutzan N, Silva N, Burleson JA, Strausbaugh LD, Gamonal J, Diaz PI (2013) The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J 7:1016–1025CrossRefGoogle Scholar
  20. 20.
    Riep B, Edesi-Neuss L, Claessen F, Skarabis H, Ehmke B, Flemmig TF, Bernimoulin JP, Gobel UB, Moter A (2009) Are putative periodontal pathogens reliable diagnostic markers? J Clin Microbiol 47:1705–1711CrossRefGoogle Scholar
  21. 21.
    Beikler T, Abdeen G, Schnitzer S, Salzer S, Ehmke B, Heinecke A, Flemmig TF (2004) Microbiological shifts in intra- and extraoral habitats following mechanical periodontal therapy. J Clin Periodontol 31:777–783.  https://doi.org/10.1111/j.1600-051X.2004.00557.x CrossRefGoogle Scholar
  22. 22.
    Beikler T, Schnitzer S, Abdeen G, Ehmke B, Eisenacher M, Flemmig TF (2006) Sampling strategy for intraoral detection of periodontal pathogens before and following periodontal therapy. J Periodontol 77:1323–1332.  https://doi.org/10.1902/jop.2006.050204 CrossRefGoogle Scholar
  23. 23.
    Ximenez-Fyvie LA, Haffajee AD, Socransky SS (2000) Comparison of the microbiota of supra- and subgingival plaque in health and periodontitis. J Clin Periodontol 27:648–657CrossRefGoogle Scholar
  24. 24.
    Carrouel F, Viennot S, Santamaria J, Veber P, Bourgeois D (2016) Quantitative molecular detection of 19 major pathogens in the interdental biofilm of periodontally healthy young adults. Front Microbiol 7:840CrossRefGoogle Scholar
  25. 25.
    Tallarico M, Canullo L, Caneva M, Ozcan M (2017) Microbial colonization at the implant-abutment interface and its possible influence on periimplantitis: a systematic review and meta-analysis. J Prosthodont Res 61:233–241.  https://doi.org/10.1016/j.jpor.2017.03.001 CrossRefGoogle Scholar
  26. 26.
    Jervoe-Storm PM, Jepsen S, Johren P, Mericske-Stern R, Enkling N (2015) Internal bacterial colonization of implants: association with peri-implant bone loss. Clin Oral Implants Res 26:957–963.  https://doi.org/10.1111/clr.12421 CrossRefGoogle Scholar
  27. 27.
    Keller W, Bragger U, Mombelli A (1998) Peri-implant microflora of implants with cemented and screw retained suprastructures. Clin Oral Implants Res 9:209–217CrossRefGoogle Scholar
  28. 28.
    Leonhardt A, Dahlen G, Renvert S (2003) Five-year clinical, microbiological, and radiological outcome following treatment of peri-implantitis in man. J Periodontol 74:1415–1422.  https://doi.org/10.1902/jop.2003.74.10.1415 CrossRefGoogle Scholar
  29. 29.
    Flemmig TF, Hetzel M, Topoll H, Gerss J, Haeberlein I, Petersilka G (2007) Subgingival debridement efficacy of glycine powder air polishing. J Periodontol 78:1002–1010.  https://doi.org/10.1902/jop.2007.060420 CrossRefGoogle Scholar
  30. 30.
    Pelka MA, Altmaier K, Petschelt A, Lohbauer U (2010) The effect of air-polishing abrasives on wear of direct restoration materials and sealants. J Am Dent Assoc 141:63–70CrossRefGoogle Scholar
  31. 31.
    Petersilka G, Faggion CM Jr, Stratmann U, Gerss J, Ehmke B, Haeberlein I, Flemmig TF (2008) Effect of glycine powder air-polishing on the gingiva. J Clin Periodontol 35:324–332.  https://doi.org/10.1111/j.1600-051X.2007.01195.x CrossRefGoogle Scholar
  32. 32.
    Petersilka GJ (2011) Subgingival air-polishing in the treatment of periodontal biofilm infections. Periodontol 2000 55:124–142.  https://doi.org/10.1111/j.1600-0757.2010.00342.x CrossRefGoogle Scholar
  33. 33.
    Charles CJ, Charles AH (1994) Periodontal screening and recording. J Calif Dent Assoc 22:43–46Google Scholar
  34. 34.
    Ainamo J, Barmes D, Beagrie G, Cutress T, Martin J, Sardo-Infirri J (1982) Development of the World Health Organization (WHO) community periodontal index of treatment needs (CPITN). Int Dent J 32:281–291Google Scholar
  35. 35.
    Saxer UPM, R H (1975) Motivation and education. SSO Schweiz Monatsschr Zahnheilkd 85:905–919Google Scholar
  36. 36.
    Lange DEP, C H, Eenboom A, Promesberger A (1977) Clinical methods for the objective evaluation of oral hygiene. Dtsch Zahnarztl Z 32:44–47Google Scholar
  37. 37.
    Ashimoto A, Chen C, Bakker I, Slots J (1996) Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol 11:266–273CrossRefGoogle Scholar
  38. 38.
    Stubbs SL, Brazier JS, O'Neill GL, Duerden BI (1999) PCR targeted to the 16S-23S rRNA gene intergenic spacer region of Clostridium difficile and construction of a library consisting of 116 different PCR ribotypes. J Clin Microbiol 37:461–463Google Scholar
  39. 39.
    Quirynen M, De Soete M, Dierickx K, van Steenberghe D (2001) The intra-oral translocation of periodontopathogens jeopardises the outcome of periodontal therapy. A review of the literature. J Clin Periodontol 28:499–507CrossRefGoogle Scholar
  40. 40.
    Leblebicioglu B, Kulekci G, Ciftci S, Keskin F, Badur S (2009) Salivary detection of periodontopathic bacteria and periodontal health status in dental students. Anaerobe 15:82–86.  https://doi.org/10.1016/j.anaerobe.2008.12.005 CrossRefGoogle Scholar
  41. 41.
    Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144CrossRefGoogle Scholar
  42. 42.
    Tan KH, Seers CA, Dashper SG, Mitchell HL, Pyke JS, Meuric V, Slakeski N, Cleal SM, Chambers JL, McConville MJ, Reynolds EC (2014) Porphyromonas gingivalis and Treponema denticola exhibit metabolic symbioses. PLoS Pathog 10:e1003955CrossRefGoogle Scholar
  43. 43.
    Tanner A, Maiden MF, Macuch PJ, Murray LL, Kent RL Jr (1998) Microbiota of health, gingivitis, and initial periodontitis. J Clin Periodontol 25:85–98CrossRefGoogle Scholar
  44. 44.
    Thurnheer T, Belibasakis GN, Bostanci N (2014) Colonisation of gingival epithelia by subgingival biofilms in vitro: role of “red complex” bacteria. Arch Oral Biol 59:977–986.  https://doi.org/10.1016/j.archoralbio.2014.05.023 CrossRefGoogle Scholar
  45. 45.
    Hajishengallis G, Liang S, Payne MA, Hashim A, Jotwani R, Eskan MA, McIntosh ML, Alsam A, Kirkwood KL, Lambris JD, Darveau RP, Curtis MA (2011) Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 10:497–506CrossRefGoogle Scholar
  46. 46.
    Nussbaum G, Shapira L (2011) How has neutrophil research improved our understanding of periodontal pathogenesis? J Clin Periodontol 38(Suppl 11):49–59.  https://doi.org/10.1111/j.1600-051X.2010.01678.x CrossRefGoogle Scholar
  47. 47.
    van Winkelhoff AJ, Rams TE, Slots J (1996) Systemic antibiotic therapy in periodontics. Periodontol 2000 10:45–78CrossRefGoogle Scholar
  48. 48.
    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.  https://doi.org/10.1111/prd.12121 CrossRefGoogle Scholar
  49. 49.
    Badersten A, Nilveus R, Egelberg J (1981) Effect of nonsurgical periodontal therapy. I. Moderately advanced periodontitis. J Clin Periodontol 8:57–72CrossRefGoogle Scholar
  50. 50.
    Wilder-Smith P, Arrastia AM, Schell MJ, Liaw LH, Grill G, Berns MW (1995) Effect of ND:YAG laser irradiation and root planing on the root surface: structural and thermal effects. J Periodontol 66:1032–1039.  https://doi.org/10.1902/jop.1995.66.12.1032 CrossRefGoogle Scholar
  51. 51.
    Flemmig TF, Arushanov D, Daubert D, Rothen M, Mueller G, Leroux BG (2012) Randomized controlled trial assessing efficacy and safety of glycine powder air polishing in moderate-to-deep periodontal pockets. J Periodontol 83:444–452.  https://doi.org/10.1902/jop.2011.110367 CrossRefGoogle Scholar
  52. 52.
    Mussano F, Rovasio S, Schierano G, Baldi I, Carossa S (2013) The effect of glycine-powder airflow and hand instrumentation on peri-implant soft tissues: a split-mouth pilot study. Int J Prosthodont 26:42–44CrossRefGoogle Scholar
  53. 53.
    Eick S, Pfister W (2004) Efficacy of antibiotics against periodontopathogenic bacteria within epithelial cells: an in vitro study. J Periodontol 75:1327–1334.  https://doi.org/10.1902/jop.2004.75.10.1327 CrossRefGoogle Scholar
  54. 54.
    Matsunaga T, Nakayuki A, Saito Y, Kato A, Noiri Y, Ebisu S, Azakami H (2011) Genomic recombination through plasmid-encoded recombinase enhances hemolytic activity and adherence to epithelial cells in the periodontopathogenic bacterium Eikenella corrodens. Biosci Biotechnol Biochem 75:748–751.  https://doi.org/10.1271/bbb.100866 CrossRefGoogle Scholar
  55. 55.
    Longo PL, Nunes AC, Umeda JE, Mayer MP (2013) Gene expression and phenotypic traits of Aggregatibacter actinomycetemcomitans in response to environmental changes. J Periodontal Res 48:766–772.  https://doi.org/10.1111/jre.12067 Google Scholar
  56. 56.
    Ebersole JL, Dawson DR 3rd, Morford LA, Peyyala R, Miller CS, Gonzalez OA (2013) Periodontal disease immunology: ‘double indemnity’ in protecting the host. Periodontol 2000 62:163–202CrossRefGoogle Scholar
  57. 57.
    Periasamy S, Kolenbrander PE (2009) Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early, and late colonizers of enamel. J Bacteriol 191:6804–6811CrossRefGoogle Scholar
  58. 58.
    Bollen CM, Quirynen M (1996) Microbiological response to mechanical treatment in combination with adjunctive therapy: a review of the literature. J Periodontol 67:1143–1158.  https://doi.org/10.1902/jop.1996.67.11.1143 CrossRefGoogle Scholar
  59. 59.
    Fang H, Han M, Li QL, Cao CY, Xia R, Zhang ZH (2016) Comparison of full-mouth disinfection and quadrant-wise scaling in the treatment of adult chronic periodontitis: a systematic review and meta-analysis. J Periodontal Res 51:417–430.  https://doi.org/10.1111/jre.12326 CrossRefGoogle Scholar
  60. 60.
    Eberhard J, Jepsen S, Jervoe-Storm PM, Needleman I, Worthington HV (2015) Full-mouth treatment modalities (within 24 hours) for chronic periodontitis in adults. Cochrane Database Syst Rev:CD004622.  https://doi.org/10.1002/14651858.CD004622.pub3

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.DüsseldorfGermany
  2. 2.MelbourneAustralia
  3. 3.Department of Periodontics, Preventive and Restorative DentistryUniversity Medical Center of Hamburg-Eppendorf (UKE)HamburgGermany
  4. 4.University of Hong KongHong KongPeople’s Republic of China

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