Clinical Oral Investigations

, Volume 22, Issue 6, pp 2149–2160 | Cite as

Clinical and laboratory evaluation of the effects of different treatment modalities on titanium healing caps: a randomized, controlled clinical trial

  • Kristina Emily Schmidt
  • Thorsten Mathias Auschill
  • Christian Heumann
  • Roland Frankenberger
  • Sigrun Eick
  • Anton Sculean
  • Nicole Birgit Arweiler
Original Article



The objective of this study is to evaluate the effects of treatment modalities on titanium surface characteristics and surrounding tissues.

Materials and methods

Eighteen participants each had four titanium healing caps (HC) attached to four newly inserted implants. After healing, each HC was randomly assigned to either (1) titanium curettes (TC), (2) stainless steel ultrasonic tip (PS), (3) erythritol air-polishing powder (EP), or (4) only rubber cup polishing (CON). Probing depths (PD), bleeding on probing (BOP), matrix metalloproteinase 8 (MMP-8), and periopathogens were recorded before and 3 months following instrumentation. After final assessments, HCs were removed, cleaned, and subjected to (a) bacterial colonization (Streptococcus gordonii, 24 h; mixed culture, 24 h) and (b) gingival fibroblasts (5 days). HC surfaces were analyzed with a scanning electron microscope (SEM).


No significant differences between the groups were evident before or after instrumentation for PD and BOP (except TC showed a significant decrease in PD; p = 0.049). MMP-8 levels and bacterial loads were always very low. MMP-8 decreased further after instrumentation, while bacteria levels showed no change. No significant differences (p > 0.05) were evident in bacterial colonization or fibroblast attachment. A comparison of the overall mean SEM surface roughness scores showed a significant difference between all groups (p < 0.0001) with the lowest roughness after EP.


All treatments performed yielded comparable outcomes and may be implemented safely.

Clinical relevance

Clinicians may fear implant surface damage, but all instrumentation types are safe and non-damaging. They can be implemented as needed upon considering the presence of staining and soft and hard deposits.


Titanium dental implants Healing caps Instrumentation Probing depths Bleeding on probing Matrix metalloproteinase-8 Biofilm formation Attachment of fibroblasts Surface roughness Biocompatibility 



Special thanks to Dr. Ralf Rössler for inserting the dental implants.

Funding source

This study was partially supported by an unrestricted grant from the Oral Reconstruction Foundation (previously Camlog Foundation), Basel, Switzerland (Grant CF41203), who also provided the dental implants and the specially constructed titanium healing caps for the experimental investigation. The design, documentation, and analyses of this study were carried out independently.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The protocol of the study was reviewed and approved by the Medical Ethics Committee, Philipps-University Marburg in Germany (no. 159/12). The study was conducted in accordance with the International Council for Harmonisation of Technical Requirements for Pharmaceuticals for Human Use (ICH) and Good Clinical Practice guidelines as well as the Declaration of Helsinki.

Informed consent

All participants gave their informed consent prior to their inclusion in the study.


  1. 1.
    Derks J, Tomasi C (2015) Peri-implant health and disease. A systematic review of current epidemiology. J Clin Periodontol 42(Suppl 16):S158–S171. PubMedCrossRefGoogle Scholar
  2. 2.
    Renvert S, Roos-Jansåker A-M, Claffey N (2008) Non-surgical treatment of peri-implant mucositis and peri-implantitis: a literature review. J Clin Periodontol 35(8 Suppl):305–315. PubMedCrossRefGoogle Scholar
  3. 3.
    Armitage GC, Xenoudi P (2016) Post-treatment supportive care for the natural dentition and dental implants. Periodontol 71(1):164–184. CrossRefGoogle Scholar
  4. 4.
    Louropoulou A, Slot DE, Van der Weijden FA (2012) Titanium surface alterations following the use of different mechanical instruments: a systematic review. Clin Oral Implants Res 23(6):643–658. PubMedCrossRefGoogle Scholar
  5. 5.
    Louropoulou A, Slot DE, Van der Weijden FA (2015) Influence of mechanical instruments on the biocompatibility of titanium dental implants surfaces: a systematic review. Clin Oral Implants Res 26(7):841–850. PubMedCrossRefGoogle Scholar
  6. 6.
    Quirynen M, Bollen CM (1995) The influence of surface roughness and surface-free energy on supra- and subgingival plaque formation in man. A review of the literature. J Clin Periodontol 22(1):1–14PubMedCrossRefGoogle Scholar
  7. 7.
    Teughels W, Van Assche N, Sliepen I, Quirynen M (2006) Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implants Res 17(S2):68–81. PubMedCrossRefGoogle Scholar
  8. 8.
    Duarte PM, Reis AF, de Freitas PM, Ota-Tsuzuki C (2009) Bacterial adhesion on smooth and rough titanium surfaces after treatment with different instruments. J Periodontol 80(11):1824–1832. PubMedCrossRefGoogle Scholar
  9. 9.
    Bollen CM, Papaioanno W, Van Eldere J, Schepers E, Quirynen M, van Steenberghe D (1996) The influence of abutment surface roughness on plaque accumulation and peri-implant mucositis. Clin Oral Implants Res 7(3):201–211. PubMedCrossRefGoogle Scholar
  10. 10.
    Marín-Pareja N, Salvagni E, Guillem-Marti J, Aparicio C, Ginebra MP (2014) Collagen-functionalised titanium surfaces for biological sealing of dental implants: effect of immobilisation process on fibroblasts response. Colloids Surf B Biointerface 122:601–610. CrossRefGoogle Scholar
  11. 11.
    Zhao B, van der Mei HC, Subbiahdoss G, de Vries J, Rustema-Abbing M, Kuijer R, Busscher HJ, Ren Y (2014) Soft tissue integration versus early biofilm formation on different dental implant materials. Dent Mater 30(7):716–727. PubMedCrossRefGoogle Scholar
  12. 12.
    Guillem-Marti J, Delgado L, Godoy-Gallardo M, Pegueroles M, Herrero M, Gil FJ (2013) Fibroblast adhesion and activation onto micro-machined titanium surfaces. Clin Oral Implants Res 24(7):770–780. PubMedCrossRefGoogle Scholar
  13. 13.
    Figuero E, Graziani F, Sanz I, Herrera D, Sanz M (2014) Management of peri-implant mucositis and peri-implantitis. Periodontol 66(1):255–273. CrossRefGoogle Scholar
  14. 14.
    Schwarz F, Schmucker A, Becker J (2015) Efficacy of alternative or adjunctive measures to conventional treatment of peri-implant mucositis and peri-implantitis: a systematic review and meta-analysis. Int J Implant Dent 1(1):22. PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Schmidt KE, Auschill TM, Heumann C, Frankenberger R, Eick S, Sculean A, Arweiler NB (2017) Influence of different instrumentation modalities on the surface characteristics and biofilm formation on dental implant neck, in vitro. Clin Oral Implants Res 28(4):483–490. PubMedCrossRefGoogle Scholar
  16. 16.
    Eick S, Bender P, Flury S, Lussi A, Sculean A (2013) In vitro evaluation of surface roughness, adhesion of periodontal ligament fibroblasts, and Streptococcus gordonii following root instrumentation with Gracey curettes and subsequent polishing with diamond-coated curettes. Clin Oral Investig 17(2):397–404. PubMedCrossRefGoogle Scholar
  17. 17.
    Bain CA (1998) An in vitro and in vivo evaluation of various implant-cleaning instruments. Quintessence Int 29(7):423–427PubMedGoogle Scholar
  18. 18.
    Pontoriero R, Tonelli MP, Carnevale G, Mombelli A, Nyman SR, Lang NP (1994) Experimentally induced peri-implant mucositis. A clinical study in humans. Clin Oral Implants Res 5(4):254–259. PubMedCrossRefGoogle Scholar
  19. 19.
    Salvi GE, Aglietta M, Eick S, Sculean A, Lang NP (2012) Reversibility of experimental peri-implant mucositis compared with experimental gingivitis in humans. Clin Oral Implants Res 23(2):182–190. PubMedCrossRefGoogle Scholar
  20. 20.
    Máximo MB, de Mendonça AC, Renata Santos V, Figueiredo LC, Feres M, Duarte PM (2009) Short-term clinical and microbiological evaluations of peri-implant diseases before and after mechanical anti-infective therapies. Clin Oral Implants Res 20(1):99–108. PubMedCrossRefGoogle Scholar
  21. 21.
    Cochis A, Fini M, Carrassi A, Migliario M, Visai L, Rimondini L (2013) Effect of air polishing with glycine powder on titanium abutment surfaces. Clin Oral Implants Res 24(8):904–909. PubMedCrossRefGoogle Scholar
  22. 22.
    Brägger U, Bürgin WB, Hämmerle CH, Lang NP (1997) Associations between clinical parameters assessed around implants and teeth. Clin Oral Implants Res 8(5):412–421. PubMedCrossRefGoogle Scholar
  23. 23.
    Papaioannou W, Quirynen M, Van Steenberghe D (1996) The influence of periodontitis on the subgingival flora around implants in partially edentulous patients. Clin Oral Implants Res 7(4):405–409. PubMedCrossRefGoogle Scholar
  24. 24.
    Quirynen M, Papaioannou W, van Steenberghe D (1996) Intraoral transmission and the colonization of oral hard surfaces. J Periodontol 67(10):986–993. PubMedCrossRefGoogle Scholar
  25. 25.
    Quirynen M, Vogels R, Peeters W, van Steenberghe D, Naert I, Haffajee A (2006) Dynamics of initial subgingival colonization of ‘pristine’ peri-implant pockets. Clin Oral Implants Res 17(1):25–37. PubMedCrossRefGoogle Scholar
  26. 26.
    Porras R, Anderson GB, Caffesse R, Narendran S, Trejo PM (2002) Clinical response to 2 different therapeutic regimens to treat peri-implant mucositis. J Periodontol 73(10):1118–1125. PubMedCrossRefGoogle Scholar
  27. 27.
    Trejo PM, Bonaventura G, Weng D, Caffesse RG, Bragger U, Lang NP (2006) Effect of mechanical and antiseptic therapy on peri-implant mucositis: an experimental study in monkeys. Clin Oral Implants Res 17(3):294–304. PubMedCrossRefGoogle Scholar
  28. 28.
    Gonçalves PF, Huang H, McAninley S, Alfant B, Harrison P, Aukhil I, Walker C, Shaddox LM (2013) Periodontal treatment reduces matrix metalloproteinase levels in localized aggressive periodontitis. J Periodontol 84(12):1801–1808. PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Gupta N, Gupta ND, Gupta A, Khan S, Bansal N (2015) Role of salivary matrix metalloproteinase-8 (MMP-8) in chronic periodontitis diagnosis. Front Med 9(1):72–76. PubMedCrossRefGoogle Scholar
  30. 30.
    Chen HY, Cox SW, Eley BM, Mäntylä P, Rönkä H, Sorsa T (2000) Matrix metalloproteinase-8 levels and elastase activities in gingival crevicular fluid from chronic adult periodontitis patients. J Clin Periodontol 27(5):366–369. PubMedCrossRefGoogle Scholar
  31. 31.
    Sorsa T, Gursoy UK, Nwhator S, Hernandez M, Tervahartiala T, Leppilahti J, Gursoy M, Könönen E, Emingil G, Pussinen PJ, Mäntylä P (2016) Analysis of matrix metalloproteinases, especially MMP-8, in gingival creviclular fluid, mouthrinse and saliva for monitoring periodontal diseases. Periodontol 70(1):142–163. CrossRefGoogle Scholar
  32. 32.
    Rickard AH, Gilbert P, High NJ, Kolenbrander PE, Handley PS (2003) Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol 11(2):94–100. PubMedCrossRefGoogle Scholar
  33. 33.
    Subramani K, Jung RE, Molenberg A, Hammerle CH (2009) Biofilm on dental implants: a review of the literature. Int J Oral Maxillofac Implants 24(4):616–626PubMedGoogle Scholar
  34. 34.
    Quirynen M, Marechal M, Busscher HJ, Weerkamp AH, Darius PL, van Steenberghe D (1990) The influence of surface free energy and surface roughness on early plaque formation. An in vivo study in man. J Clin Periodontol 17(3):138–144. PubMedCrossRefGoogle Scholar
  35. 35.
    Dmytryk JJ, Fox SC, Moriarty JD (1990) The effects of scaling titanium implant surfaces with metal and plastic instruments on cell attachment. J Periodontol 61(8):491–496. PubMedCrossRefGoogle Scholar
  36. 36.
    Schwarz F, Rothamel D, Sculean A, Georg T, Scherbaum W, Becker J (2003) Effects of an Er:YAG laser and the Vector ultrasonic system on the biocompatibility of titanium implants in cultures of human osteoblast-like cells. Clin Oral Implants Res 14(6):784–792. PubMedCrossRefGoogle Scholar
  37. 37.
    Arweiler NB, Auschill TM, Sculean A (2017) Patient self-care of periodontal pocket infections. Periodontol 2000 76(1):164–179.

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Kristina Emily Schmidt
    • 1
  • Thorsten Mathias Auschill
    • 1
  • Christian Heumann
    • 2
  • Roland Frankenberger
    • 3
  • Sigrun Eick
    • 4
  • Anton Sculean
    • 4
  • Nicole Birgit Arweiler
    • 1
  1. 1.Department of PeriodontologyPhilipps-University MarburgMarburgGermany
  2. 2.Department of StatisticsLudwig-Maximilian UniversityMunichGermany
  3. 3.Department of Operative Dentistry and EndodontologyPhilipps-UniversityMarburgGermany
  4. 4.Department of PeriodontologyUniversity of BerneBerneSwitzerland

Personalised recommendations