Histological Evaluation of Early and Immediately Loaded Implants Retrieved from Human Jaws

  • Giovanna Iezzi
  • Adriano PiattelliEmail author
  • Antonio Scarano
  • Marco Degidi
  • Jamil Awad Shibli
  • Carlo Mangano
  • Vittoria Perrotti


The only way to evaluate the short- and long-term response of human bone tissue to the insertion of dental implants and to corroborate the results of in vitro and of animal experimental studies is to study well-integrated human-retrieved dental implants, with surrounding human bone tissue, possibly after different time periods after the insertion in the bone. Several papers report that moderately rough implant surfaces are, probably, the best in terms of mineralized tissues response at the bone-implant interface. Results from our Laboratory, in a span of 30 years, have found that immediate loading did not create adverse effects regarding the formation of mineralized tissues at the interface with dental implants and has, probably, a beneficial effect on the peri-implant bone response, producing changes in the peri-implant bone microstructure. Osseointegration is a very dynamic ongoing process with the peri-implant bone tending to become more organized over the years; these higher degrees of organization are reflected by the large quantity of remodeling areas in the mature, lamellar bone, indication of multiple remodeling cycles over the years of loading. Bone remodeling is a prerequisite for dental implants to support functional loading in the long term, and remodeling, very well-organized, mineralized, lamellar bone is found at the interface of retrieved implants even after three decades of loading. Bone-implant contact (BIC) and bone mechanical properties were found to increase over time, and the bone tissue adapted to loading conditions to increase its biomechanics. In the specimens evaluated in our Laboratory, high percentages of bone-implant contact was found in all well-integrated retrieved implants, with the presence of mineralized, mature, lamellar bone in close contact with the metal surface, around all the implant perimeter, with no epithelium migration downward or presence of fibrous, connective tissue. In the specimens evaluated in our Laboratory over several decades, the bone-implant contact percentage was found to vary from 32 to 37% to more than 90–95%. These results point to the fact that dental implants could function with different percentages of mineralized tissues at the interface, and even implants with a low bone-implant contact percentage were stable, well-integrated, and able to bear loading conditions over the years. Mineralized bone was absent at the base of the threads in unloaded implants, and, at the tip of the threads in loaded implants, osteocytes (the mechanosensors in bone) were always found in the peri-implant bone, with a significantly higher number in loaded implants than in unloaded implants. Loaded implants presented a significantly higher number and thickness of bone trabeculae.


Bone-implant contact Bone remodeling Dental implants Immediate loading Osteocytes 



Bone-implant contact


Direct laser metal sintering




Zirconium implant


  1. Abrahamsson I, Berglundh T, Linder E, Lang NP, Lindhe J. Early bone formation adjacent to rough and turned endosseous implant surfaces. An experimental study in the dog. Clin Oral Implants Res. 2004;15:381–92.CrossRefGoogle Scholar
  2. Albrektsson T. Hard tissue implant interface. Aust Dent J. 2008;53(1 Suppl):534–8.Google Scholar
  3. Cesaretti G, Lang NP, Viganò P, Bengazi F, Apaza Alccayhuaman KA. Immediate and delayed loading of fixed dental prostheses supported by single or two splinted implants: a histomorphometric study in dogs. J Oral Rehabil. 2018;45(4):308–16.CrossRefGoogle Scholar
  4. Coelho PG, Marin C, Granato R, Suzuki M. Histomorphologic analysis of 30 plateau root form implants retrieved after 8 to 13 years in function. A human retrieval study. J Biomed Mater Res Part B. 2009;91B:975–9.CrossRefGoogle Scholar
  5. D’Avila S, Delfino Dos Reis L, Piattelli A, Aguiar KCS, de Faveri M, Borges FL, Iezzi G, Oliveira NTC, Cardoso LA, Shibli JA. Impact of smoking on human bone apposition at different dental implant surfaces: a histologic study in type IV bone. J Oral Implantol. 2010;36:85–90.CrossRefGoogle Scholar
  6. Degidi M, Petrone G, Iezzi G, Piattelli A. Histologic evaluation of 2 human immediately loaded and 1 submerged titanium implants inserted in the posterior mandible and retrieved after 6 months. J Oral Implantol. 2003a;29:223–9.CrossRefGoogle Scholar
  7. Degidi M, Scarano A, Petrone G, Piattelli A. Histological analysis of clinically retrieved immediately loaded implants: a report of 11 cases. Clin Impl Dent Relat Res. 2003b;5:89–94.CrossRefGoogle Scholar
  8. Degidi M, Petrone G, Iezzi G, Piattelli A. Bone contact around acid-etched implants: a histological and histomorphometrical evaluation of two human-retrieved implants. J Oral Implantol. 2003c;29:13–8.CrossRefGoogle Scholar
  9. Degidi M, Piattelli A, Iezzi G, Carinci F. Immediately loaded short implants. Analysis of a case series of 133 implants. Quintessence Int. 2007a;38:193–201.PubMedGoogle Scholar
  10. Degidi M, Piattelli A, Carinci F. Immediate loaded dental implants: comparison between fixtures inserted in postextractive and healed bone sites. J Craniofac Surg. 2007b;18:965–71.CrossRefGoogle Scholar
  11. Degidi M, Iezzi G, Scarano A, Piattelli A. Immediately loaded titanium implant with a tissue-stabilizing/maintaining design (‘beyond platform switch’) retrieved from man after 4 weeks: a histological and histomorphometrical evaluation. A case report. Clin Oral Implants Res. 2008;19:276–82.CrossRefGoogle Scholar
  12. Degidi M, Iezzi G, Perrotti V, Piattelli A. Comparative analysis of immediate functional loading and immediate non-functional loading to traditional healing periods: a five-year follow-up of 550 dental implants. Clin Impl Dent Relat Res. 2009a;11:257–66.CrossRefGoogle Scholar
  13. Degidi M, Nardi D, Piattelli A. Immediate rehabilitation of the edentulous mandible with a definitive prosthesis supported by an intra-oral welded titanium bar. Int J Oral Maxillofac Implants. 2009b;24:342–7.PubMedGoogle Scholar
  14. Degidi M, Piattelli A, Shibli JA, Perrotti V, Iezzi G. Bone formation after 4 and 8 weeks around immediately loaded and submerged dental implants with a modified sandblasted and acid-etched surface. A histologic and histomorphometric analysis in man. Int J Oral Maxillofac Implants. 2009c;24:896–901.PubMedGoogle Scholar
  15. Degidi M, Nardi D, Piattelli A. A comparison between immediate loading and immediate restoration in cases of partial posterior mandibular edentulism: a three-year randomized clinical trial. Clin Oral Impl Res. 2010a;21:682–7.CrossRefGoogle Scholar
  16. Degidi M, Perrotti V, Piattelli A, Iezzi G. Mineralized bone-implant contact and implant stability quotient in 16 human implants retrieved after early healing periods: a histologic and histomorphometric evaluation. Int J Oral Maxillofac Implants. 2010b;25:45–8.PubMedGoogle Scholar
  17. Degidi M, Daprile G, Piattelli A. Determination of primary stability: a comparison of the surgeon’s perception and objective measurements. Int J Oral Maxillofac Implants. 2010c;25:558–61.PubMedGoogle Scholar
  18. Di Stefano D, Iezzi G, Scarano A, Perrotti V, Piattelli A. Immediately loaded blade implant retrieved from man after a 20 years loading period: a histological and histomorphometrical case report. J Oral Implantol. 2006;32:171–6.CrossRefGoogle Scholar
  19. Eccellente T, Piombino M, Piattelli A, Perrotti V, Iezzi G. A new treatment concept for the immediate loading of implants inserted in the edentulous mandible. Quintessence Int. 2010;41:489–95.PubMedGoogle Scholar
  20. Erkapers M, Ekstrand K, Baer RA, Toljanic JA, Thor A. Patient satisfaction following dental implant treatment with immediate loading in the edentulous atrophic maxilla. Int J Oral Maxillofac Implants. 2011;26:356–64.PubMedGoogle Scholar
  21. Gandolfi MG, Taddei P, Siboni F, Perrotti V, Iezzi G, Piattelli A, Prati C. Micro-topography and reactivity of implant surfaces: an in vitro study in simulated body fluid (SBF). Microsc Microanal. 2015;21:190–203.CrossRefGoogle Scholar
  22. Gapski R, Wang HL, Mascarenhas P, Lang NP. Critical review of immediate implant loading. Clin Oral Impl Res. 2003;14:515–27.CrossRefGoogle Scholar
  23. Han JY, Hou JX, Zhou G, Wang C, Fan YB. A histological and biomechanical study of bone stress and bone remodeling around immediately loaded implants. Sci China Life Sci. 2014;57:618–26.CrossRefGoogle Scholar
  24. Iezzi G, Fiera E, Scarano A, Pecora G, Piattelli A. Histologic evaluation of a provisional implant retrieved from man 7 months after placement in a sinus augmented with calcium sulphate: a case report. J Oral Implantol. 2007;33:89–95.CrossRefGoogle Scholar
  25. Iezzi G, Orlandi S, Pecora G, Piattelli A. Histologic and histomorphometric evaluation of the bone response around a hydroxyapatite-coated implant retrieved after 15 years. Int J Periodontics Restorative Dent. 2009a;29:99–105.PubMedGoogle Scholar
  26. Iezzi G, Pecora G, Scarano A, Perrotti V, Piattelli A. Immediately loaded screw implant retrieved after a 12-year loading period: a histologic and histomorphometric case report. J Osseointegr. 2009b;1:54–9.Google Scholar
  27. Iezzi G, Vantaggiato G, Shibli JA, Fiera E, Falco A, Piattelli A, Perrotti V. Machined and sandblasted human dental implants retrieved after 5 years: a histologic and histomorphometric analysis of three cases. Quintessence Int. 2012;43:287–92.PubMedGoogle Scholar
  28. Iezzi G, Piattelli A, Mangano C, Degidi M, Testori T, Vantaggiato G, Fiera E, Frosecchi M, Floris P, Perroni R, Ravera L, Moreno GG, De Martinis E, Perrotti V. Periimplant bone response in human-retrieved, clinically stable, successful, and functioning dental implants after a long-term loading period: a report of 17 cases from 4 to 20 years. Implant Dent. 2016;25:380–6.CrossRefGoogle Scholar
  29. Kuroshima S, Yasutake M, Tsuiki K, Nakano T, Sawase T. Structural and qualitative bone remodeling around repetitive loaded implants in rabbits. Clin Impl Dent Relat Res. 2015;17(Suppl 2):699–710.CrossRefGoogle Scholar
  30. Linkow LI, Miller RJ. Immediate loading of endosseous implants is not new. J Oral Implantol. 2004;30:314–7.CrossRefGoogle Scholar
  31. Mangano C, Raspanti M, Traini T, Sammons R, Piattelli A. Stereo-imaging and cytocompatibility of a model dental implant formed by direct laser fabrication. J Biomed Mater Res A. 2009;88:823–31.CrossRefGoogle Scholar
  32. Mangano C, Piattelli A, Mortellaro C, Mangano F, Perrotti V, Iezzi G. Evaluation of peri-implant bone response in implants retrieved for fracture after more than 20 years of loading: a case series. J Oral Implantol. 2015;41:414–8.CrossRefGoogle Scholar
  33. Mangano FG, Iezzi G, Shibli JA, Pires JT, Luongo G, Piattelli A, Mangano C. Early bone formation around immediately loaded implants with nanostructured calcium-incorporated and machined surface: a randomized, controlled histologic and histomorphometric study in the human posterior maxilla. Clin Oral Invest. 2017a;21:2603–11.CrossRefGoogle Scholar
  34. Mangano FG, Pires JT, Shibli JA, Mijiritsky E, Iezzi G, Piattelli A, Mangano C. Early bone response to dual acid-etched and machined dental implants placed in the posterior maxilla: a histologic and Histomorphometric human study. Implant Dent. 2017b;26:24–9.CrossRefGoogle Scholar
  35. Paolantonio M, Dolci M, Scarano A, d’Archivio D, di Placido G, Tumini V, Piattelli A. Immediate implantation in fresh extraction sockets. A controlled clinical and histological study in man. J Periodontol. 2001;72:1560–71.CrossRefGoogle Scholar
  36. Piattelli A, Corigliano M, Scarano A, Costigliola G, Paolantonio M. Immediate loading of titanium plasma-sprayed implants: an histologic analysis in monkeys. J Periodontol. 1998;69:321–7.CrossRefGoogle Scholar
  37. Piattelli M, Scarano A, Paolantonio M, Iezzi G, Petrone G, Piattelli A. Bone response to machined and resorbable blast material titanium implants: an experimental study in rabbits. J Oral Implantol. 2002;28:2–8.CrossRefGoogle Scholar
  38. Piattelli A, Degidi M, Paolantonio M, Mangano C, Scarano A. Residual aluminum oxide on the surface of titanium implants has no effect on osseointegration. Biomaterials. 2003;24:4081–9.CrossRefGoogle Scholar
  39. Piattelli A, Artese L, Penitente E, Iaculli F, Degidi M, Mangano C, Shibli JA, Coelho PG, Perrotti V, Iezzi G. Osteocyte density in the peri-implant bone of implants retrieved after different time periods (4 weeks to 27 years). J Biomed Mater Res B Appl Biomater. 2014;102:239–43.CrossRefGoogle Scholar
  40. Proussaefs P, Lozada J. Evaluation of two vitallium blade-form implants retrieved after 13 and 21 years of function: a clinical report. J Prosthet Dent. 2002;87:412–5.CrossRefGoogle Scholar
  41. Proussaefs P, Lozada J. Immediate loading of hydroxyapatite-coated implants in the maxillary premolar area: three-year results of a pilot study. J Prosthet Dent. 2004;91:228–33.CrossRefGoogle Scholar
  42. Quaranta A, Piattelli A, Scarano A, Quaranta M, Pompa G, Iezzi G. Light microscopic evaluation of the dimensions of peri-implant mucosa around immediately loaded and submerged titanium implants in monkeys. J Periodontol. 2008;79:1697–703.CrossRefGoogle Scholar
  43. Rocci A, Martignoni M, Miranda Burgos P, Gottlow J, Sennerby L. Histology of retrieved immediately and early loaded oxidized implants: light microscopic observations after 5 to 9 months of loading in the posterior mandible. Clin Impl Dent Relat Res. 2003;5(Suppl.1):88–98.CrossRefGoogle Scholar
  44. Romanos GE. Present status of immediate loading of oral implants. J Oral Implantol. 2004;30:189–97.CrossRefGoogle Scholar
  45. Romanos G, Degidi M, Testori T, Piattelli A. Histological and histomorphometrical findings from human retrieved immediately functional loaded implants. J Periodontol. 2005;76:1823–32.CrossRefGoogle Scholar
  46. Romanos GE. Wound healing in immediately loaded implants. Periodontol 2000. 2015;68:153–67.CrossRefGoogle Scholar
  47. Sagirkaya E, Kucukekenci AS, Karasoy D, Akca K, Eckert S, Cehreli MC. Comparative assessments, meta-analysis, and recommended guidelines for reporting studies on histomorphometric bone-implant contact in humans. Int J Oral Maxillofac Implants. 2013;28:1243–58.CrossRefGoogle Scholar
  48. Salvi GE, Gallini G, Lang NP. Early loading (2 or 6 weeks) of sandblasted and acid-etched (SLA) ITI implants in the posterior mandible. A 1-year randomized controlled clinical trial. Clin Oral Implants Res. 2004;15:142–9.CrossRefGoogle Scholar
  49. Scarano A, Di Carlo F, Quaranta M, Piattelli A. Bone response to zirconia ceramic implants: an experimental study in rabbits. J Oral Implantol. 2003;29:8–12.CrossRefGoogle Scholar
  50. Scarano A, Piattelli M, Caputi S, Favero GA, Piattelli A. Bacterial adhesion on commercially pure titanium and zirconium oxide disks: an in vivo human study. J Periodontol. 2004;75:292–6.CrossRefGoogle Scholar
  51. Scarano A, Degidi M, Iezzi G, Petrone G, Piattelli A. Correlation between implant stability quotient and bone-implant contact: a retrospective histological and histomorphometrical study of seven titanium implants retrieved from humans. Clin Implant Dent Relat Res. 2006;8:218–22.CrossRefGoogle Scholar
  52. Shah FA, Nilson B, Branemark R, Thomsen P, Palmquist A. The bone implant interface-nanoscale analysis of clinically retrieved dental implants. Nanomedicine. 2014;10:1729–37.CrossRefGoogle Scholar
  53. Shibli JA, Aguiar KC, Melo L, d’Avila S, Zenóbio EG, Faveri M, Iezzi G, Piattelli A. Histological comparison between implants retrieved from patients with and without osteoporosis. Int J Oral Maxillofac Surg. 2008;37:321–7.CrossRefGoogle Scholar
  54. Steigenga J, Al-Shammari K, Misch C, Nociti FH, Wang HL. Effects of implant thread geometry on percentage of osseointegration and resistance to reverse torque in the tibia of rabbits. J Periodontol. 2004;75:1233–41.CrossRefGoogle Scholar
  55. Traini T, Mangano C, Perrotti V, Caputi S, Coelho P, Piattelli A, Iezzi G. Human bone reactions around implants with adverse interfacial bone strain over 20 years. J Biomed Mater Res B Appl Biomater. 2014;102:1342–52.CrossRefGoogle Scholar
  56. Uehara T, Takaoka K, Ito K. Histological evidence of osseointegration in human retrieved fractured hydroxyapatite-coated screw-type implants: a case report. Clin Oral Impl Res. 2004;15:540–5.CrossRefGoogle Scholar
  57. Vandamme K, Naert I, Geris L, Vander Sloten J, Puers R, Duyck J. Histodynamics of bone tissue formation around immediately loaded cylindrical implants in the rabbit. Clin Oral Impl Res. 2007;18:471–80.CrossRefGoogle Scholar
  58. Vandamme K, Naert I, Vander Sloten J, Puers R, Duyck J. Effect of implant surface roughness and loading on peri-implant bone formation. J Periodontol. 2008;79:150–7.CrossRefGoogle Scholar
  59. Yamamoto M, Ogawa T, Yokohama M, Koyama S, Sasaki K. Influence of immediate and early loading on bone metabolic activity around dental implants in rat tibiae. Clin Oral Implants Res. 2014;25:1084–90.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Giovanna Iezzi
    • 1
  • Adriano Piattelli
    • 1
    • 2
    • 3
    Email author
  • Antonio Scarano
    • 1
  • Marco Degidi
    • 4
  • Jamil Awad Shibli
    • 5
  • Carlo Mangano
    • 6
  • Vittoria Perrotti
    • 1
  1. 1.Department of Medical, Oral and Biotechnological SciencesUniversity of Chieti-PescaraChietiItaly
  2. 2.Biomaterials EngineeringCatholic University of San Antonio of Murcia (UCAM)MurciaSpain
  3. 3.Villa Serena Foundation for ResearchCittà S. AngelPescaraItaly
  4. 4.Private PracticeBolognaItaly
  5. 5.Department of Periodontology and Oral Implantology, Dental Research DivisionGuarulhos University (UnG)GuarulhosBrazil
  6. 6.Department of Dental Sciences, Dental School, San Raffaele UniversityMilanItaly

Personalised recommendations