Clinical Oral Investigations

, Volume 19, Issue 6, pp 1353–1362

Comparative assessment of the interfacial soft and hard tissues investing implants and natural teeth in the macaque mandible

  • Chong Huat Siar
  • Chooi Gait Toh
  • Georgios E Romanos
  • Kok Han Ng
Original Article



The aim of this study was to conduct a comparative qualitative and quantitative assessment of the interfacial soft and hard tissues investing implants and natural teeth.

Materials and methods

The test sample consisted of six adult healthy male Macaca fascicularis with three-unit splinted crowns, each crown supported by an Ankylos screw-shaped titanium implant. These implants were placed in the mandibular premolar-second molar region, one side by an immediate-loading (IL) and the other by delayed-loading (DL) protocol. The animals were sacrificed after 3 months of functional loading. Another two monkeys with natural dentition served as controls. Nondecalcified sections were prepared for assessment of optical intensities (OI) under a confocal laser scanning microscope.


In both the test (IL and DL) and control, the soft tissue complexes demonstrated a highly fluorescent keratinized layer and diminished cytoplasmic and enhanced membranous fluorescence in the remaining epithelium. Peri-implant mucosa was further characterized by an intense fluorescence at the junctional epithelium-implant interface and in the stromal mononuclear infiltrate. Connective tissue contact and periodontal ligament were weakly fluorescent. In hard tissues, a high fluorescence was observed in peri-implant woven bone and along the implant-bone interface. Mean OI was significantly higher in peri-implant woven bone than around teeth (P < 0.05). In the remaining soft and hard tissue complexes, no significant differences in mean OI between the test and control were observed (P > 0.05).


Present findings suggest that peri-implant woven bone is highly mineralized, while the peri-implant and gingival mucosa share structural similarities.

Clinical relevance

Optical intensities of interfacial tissues investing implants and teeth are related to their biological properties.


Dental implant Interfacial tissues Natural teeth Optical intensity 

Supplementary material

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  1. 1.
    Berglundh T, Abrahamsson I, Welander M, Lang NP, Lindhe J (2007) Morphogenesis of the peri-implant mucosa: an experimental study in dogs. Clin Oral Implants Res 18:1–8PubMedCrossRefGoogle Scholar
  2. 2.
    Hermann JS, Buser D, Schenk RK, Higginbottom FL, Cochran DL (2000) Biologic width around titanium implants. A physiologically formed and stable dimension over time. Clin Oral Implants Res 11:1–11PubMedCrossRefGoogle Scholar
  3. 3.
    Yeung SCH (2008) Biological basis for soft tissue management in implant dentistry. Aust Dent J 53(Suppl 1):S39–S42PubMedCrossRefGoogle Scholar
  4. 4.
    Abrahamsson I, Berglundh T, Glantz T, Lindhe J (1998) The mucosal attachment at different abutments. An experimental study in dogs. J Clin Periodontol 25:721–727PubMedCrossRefGoogle Scholar
  5. 5.
    Abrahamsson I, Berglundh T, Moon IS, Lindhe J (1999) Peri-implant tissues at submerged and non-submerged titanium implants. J Clin Periodontol 26:600–607PubMedCrossRefGoogle Scholar
  6. 6.
    Abrahamsson I, Zitzmann NU, Berglundh T, Linder E, Wennerberg A, Lindhe J (2002) The mucosal attachment to titanium implants with different surface characteristics: an experimental study in dog. J Clin Periodontol 29:448–455PubMedCrossRefGoogle Scholar
  7. 7.
    Albrektsson T (2008) Hard tissue implant interface. Aust Dent J 53(Suppl 1):S34–S38PubMedCrossRefGoogle Scholar
  8. 8.
    Marco F, Giavaresi G, Vittoria O (2005) Peri-implant osteogenesis in health and osteoporosis. Micron 36:630–644PubMedCrossRefGoogle Scholar
  9. 9.
    Chang P-C, Lang NP, Giannobile WV (2010) Evaluation of functional dynamics during osseointegration and regeneration associated with oral implants. Clin Oral Implants Res 21:1–12PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Rozé J, Babu S, Safarzadah A, Gayet-Delacroix M, Hoornaert A, Layrolle P (2009) Correlating implant stability to bone structure. Clin Oral Implants Res 20:1140–1145PubMedCrossRefGoogle Scholar
  11. 11.
    O’ Sullivan D, Sennerby L, Meredith N (2004) Influence of implant taper on primary and secondary stability of osseointegrated titanium implants. Clin Oral Implants Res 15:474–480CrossRefGoogle Scholar
  12. 12.
    Bacchelli B, Giavaresi G, Franchi M, Martini D, De Pasquale V, Trirè A, Fini M, Giardino R, Ruggeri A (2009) Influence of a zirconia sandblasting treated surface on peri-implant bone healing: An experimental study in sheep. Acta Biomater 5:2246–2257PubMedCrossRefGoogle Scholar
  13. 13.
    Scarano A, Orsini G, Pecora G, Iezzi G, Perrotti V, Piattelli A (2007) Peri-implant bone regeneration with calcium sulfate: a light and transmission electron microscopy case report. Implant Dent 16:195–203PubMedCrossRefGoogle Scholar
  14. 14.
    Liu S, Broucek J, Virdi AS, Sumner DR (2012) Limitations of using micro-computer tomography to predict bone-implant contact and mechanistic fixation. J Microsc 245:34–42PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Bahat O, Sullivan RM (2010) Parameters for successful implant integration revisited part II: Algorithm for immediately loading diagnostic factors. Clin Implant Dent Relat Res 12(Suppl 1):e13–22PubMedGoogle Scholar
  16. 16.
    Baschong W, Suetterlin R, Hefti A, Schiel H (2001) Confocal laser scanning microscopy and scanning electron microscopy of tissue Ti-implant interfaces. Micron 32:33–41PubMedCrossRefGoogle Scholar
  17. 17.
    Al-Nawas B, Götz H (2003) Three-dimensional topographic and metrologic evaluation of dental implants by confocal laser scanning microscopy. Clin Implant Dent Relat Res 5:176–183PubMedCrossRefGoogle Scholar
  18. 18.
    Traini T, Degidi M, Murmura G, Piatelli A, Caputi S (2007) Bone microstructure evaluation near unloaded dental implants combining confocal scanning laser microscopy, circularly polarized light microscopy, and SEM backscattered electrons imaging. Int J Immunopathol Pharmacol 20(1 Suppl 1):37–41PubMedGoogle Scholar
  19. 19.
    Nishikawa T, Masuno K, Mori M, Tajime Y, Kakudo K, Tanaka A (2006) Calcification at the interface between titanium implants and bone: Observation with confocal laser scanning microscopy. J Oral Implantol 32:211–217PubMedCrossRefGoogle Scholar
  20. 20.
    Traini T, Degidi M, Iezzi G, Artese L, Piattelli A (2007) Comparative evaluation of the peri-implant bone tissue mineral density around unloaded titanium dental implants. J Dent 35:84–92PubMedCrossRefGoogle Scholar
  21. 21.
    Piatelli A, Trisi P, Passi P, Piatelli M, Cordioli GP (1994) Histochemical and confocal laser scanning microscopy study of the bone-titanium interface: an experimental study in rabbits. Biomaterials 15:194–200CrossRefGoogle Scholar
  22. 22.
    Lan J, Wang ZF, Shi B, Xia HB, Cheng R (2007) The influence of recombinant human BMP-2 on bone-implant osseointegration: biomechanical testing and histomorphometric analysis. Int J Oral Maxillofac Surg 36:345–349PubMedCrossRefGoogle Scholar
  23. 23.
    Abuduwali N, Lossdörfer S, Winter J, Wolf M, Götz W, Jäger A (2013) Autofluorescent characteristics of human periodontal ligament cells in vitro. Ann Anat 195:449–454PubMedCrossRefGoogle Scholar
  24. 24.
    Pearce AL, Richards RG, Milz S, Schneider E, Pearce SG (2007) Animal models for implant biomaterial research in bone: a review. Eur Cells Mater 13:1–10Google Scholar
  25. 25.
    Stadlinger B, Pourmand P, Locher MC, Schulz MC (2012) Systemic review of animal models for the study of implant integration, assessing the influence of material, surface and design. J Clin Periodontol 39(Suppl 12):28–36PubMedCrossRefGoogle Scholar
  26. 26.
    Emilson CG, Bowen WH (1981) Microbial analyses of dental plaque of monkeys (Macaca fascicularis) using fluorescent antibody techniques. Scand J Dent Res 89:458–462PubMedGoogle Scholar
  27. 27.
    Siar CH, Toh CG, Romanos G, Swaminathan D, Ong AH, Yaacob H, Nentwig G-H (2003) Peri-implant soft tissues integration of immediately loaded implants in the posterior macaque mandible: a histomorphometric study. J Periodontol 74:571–578PubMedCrossRefGoogle Scholar
  28. 28.
    Romanos G, Toh GC, Siar CH, Swaminathan D, Ong AH, Yaacob H, Nentwig G-H (2001) Peri-implant bone reactions to immediately loaded implants. An experimental study in monkeys. J Periodontol 72:506–511PubMedCrossRefGoogle Scholar
  29. 29.
    Moure SP, Carrard VC, Lauxen IS, Manso PPA, Oliveira MG, Martins MD, Sant Ana Filho M (2011) Collagen and elastic fibers in odontogenic entities: analysis using light and confocal laser microscopic methods. Open Dent J 5:116–21PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Pavlova I, Williams M, El-Naggar A, Richards-Kortum R, Gillenwater A (2008) Understanding the biological basis of autofluorescence imaging for oral cancer detection: high resolution fluorescence microscopy in viable tissue. Clin Cancer Res 14:2396–2404PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Ganeles J, Listgarten MA, Evian CI (1986) Ultrastructure of durapatite-periodontal tissue interface in human intrabony defects. J Periodontol 57:133–139PubMedCrossRefGoogle Scholar
  32. 32.
    De Lange GL, Donath K (1989) Interface between bone tissue and implants of solid hydroxyapatite or hydroxyapatite-coated titanium implants. Biogeosciences 10:121–125Google Scholar
  33. 33.
    De Lange GL, de Putter C, de Wijs FLJA (1990) Histological and ultrastructural appearance of the hydroxyapatite-bone interface. J Biomed Mater Res 24:829–845PubMedCrossRefGoogle Scholar
  34. 34.
    LeGeros RZ, Orly I, Gregoire M, Daculsi G (1991) Substrate surface dissolution and interfacial biological mineralization. In: Davies J (ed) Bone Biomaterial Interface. Toronto Univ Press, Toronto, p 76Google Scholar
  35. 35.
    Palmquist A, Grandfield K, Norlindh B, Mattsson T, Brånemark R, Thomsen P (2012) Bone-titanium oxide interface in humans revealed by transmission electron microscopy and electron tomography. J R Soc Interface 9:396–400PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Favia G, Pilolli GP, Maiorano E (2009) Histologic and histomorphometric features of bisphosphonate-related osteonecrosis of the jaws: an analysis of 31 cases with confocal laser scanning microscopy. Bone 45:406–413PubMedCrossRefGoogle Scholar
  37. 37.
    Wu Y, Qu JY (2006) Combined depth- and time-resolved autofluorescence spectroscopy of epithelial tissue. Opt Lett 31:1833–1835PubMedCrossRefGoogle Scholar
  38. 38.
    Hashimoto M, Akagawa Y, Nikai H, Tsuru H (1989) Ultrastructure of the peri-implant junctional epithelium on single-crystal sapphire endosseous dental implant loaded with functional stress. J Oral Rehabil 16:261–270PubMedCrossRefGoogle Scholar
  39. 39.
    Bauman GR, Rapley JW, Hallmon WW, Mills M (1993) The peri-implant sulcus. Int J Oral Maxillofac Implants 8:273–280PubMedGoogle Scholar
  40. 40.
    Marchetti C, Farina A, Cornaglia AI (2002) Microscopic, immunocytochemical, and ultrastructural properties of peri-implant mucosa in humans. J Periodontol 73:555–563PubMedCrossRefGoogle Scholar
  41. 41.
    Moon IS, Berglundh T, Abrahamsson I, Linder E, Lindhe J (1999) The barrier between the keratinized mucosa and the dental implant. An experimental study in the dog. J Clin Periodontol 26:658–663PubMedCrossRefGoogle Scholar
  42. 42.
    Buser D, Weber HP, Donath K, Fiorellini JP, Paquette DW, Williams RC (1992) Soft tissue reactions to non-submerged unloaded titanium implants in beagle dogs. J Periodontol 63:225–235PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Chong Huat Siar
    • 1
  • Chooi Gait Toh
    • 2
  • Georgios E Romanos
    • 3
  • Kok Han Ng
    • 4
  1. 1.Department of Oro-Maxillofacial Surgical and Medical Sciences, Faculty of DentistryUniversity of MalayaKuala LumpurMalaysia
  2. 2.School of DentistryInternational Medical UniversityKuala LumpurMalaysia
  3. 3.School of Dental MedicineStony Brook UniversityStony BrookUSA
  4. 4.Cancer Research CentreInstitute for Medical ResearchKuala LumpurMalaysia

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