Inscrição na biblioteca: Guest
Portal Digital Begell Biblioteca digital da Begell eBooks Diários Referências e Anais Coleções de pesquisa
Journal of Long-Term Effects of Medical Implants
SJR: 0.133 SNIP: 0.491 CiteScore™: 0.89

ISSN Imprimir: 1050-6934
ISSN On-line: 1940-4379

Journal of Long-Term Effects of Medical Implants

DOI: 10.1615/JLongTermEffMedImplants.2019031828
pages 135-140

Histological Analysis of an Implant Retrieved from a β-Tricalcium Phosphate Graft after 4 Years: A Case Study

Shadi Daher
Clinical Assistant Professor, Department of Oral and Maxillofacial Surgery, Boston University Henry M. Goldman School of Dental Medicine, Boston, MA
Joseph Leary
Periodontist, Implant Dentistry Centre, Boston, MA
Rolf Ewers
Professor Emeritus, Department of Oral, Maxillary, and Facial Surgery, Medical University of Vienna; Head, CMF Institute Vienna, Vienna, Austria
Paulo G. Coelho
Department of Biomaterials, Hansjörg Wyss Department of Plastic Surgery, Mechanical and Aerospace Engineering, New York University, New York, NY
Estevam Augusto Bonfante
Unigranrio University, School of Heath Sciences, Duque De Caxias, Rio De Janeiro; Department of Prosthodontics and Periodontology, University of Sao Paulo Bauru School of Dentistry, Bauru, SP, Brazil, 17.012-901


We describe the retrieval of a dental implant device that had been successfully osseointegrated for more than 4 years. After obtaining an informed patient consent, the device was retrieved for retreatment purposes from its position in a β-tricalcium phosphate (β-TCP) grafted sinus floor. The sinus floor augmentation, using β-TCP, had been performed in conjunction with the original implant placement, which in turn enabled the histological evaluation of specific regions of interest that were comprised of either grafted or native bone. Radiographs documented the rehabilitated area before and after grafting. The osteogenic events that occurred during the 4-yr-period depict the interplay of implant, synthetic graft material, and native bone in a dynamic process of osteogenesis, ongoing bone maturation, and remodeling that led to the development of haversian-like bone morphology. Two distinct areas were observed histologically, wherein osteointegration occurred uneventfully in both native bone and areas of grafted bone. Of particular interest was the presence of multiple remodeling sites of lamellar bone that could be seen between the plateaus−healing chambers−in which bone eventually evolved into a haversian cortical-like configuration.


  1. Jarcho M. Calcium phosphate ceramics as hard tissue prosthetics. Clin Orthop Relat Res. 1981(157):259-78.

  2. Kumar P, Vinitha B, Fathima G. Bone grafts in dentistry. J Pharm Bioallied Sci. 2013;5(Suppl 1):S125-7.

  3. Ducheyne P, Qiu Q. Bioactive ceramics: The effect of surface reactivity on bone formation and bone cell function. Biomaterials. 1999;20(23-24):2287-303.

  4. Sheikh Z, Hamdan N, Ikeda Y, Grynpas M, Ganss B, Glogauer M. Natural graft tissues and synthetic biomaterials for periodontal and alveolar bone reconstructive applications: A review. Biomater Res. 2017;21:9.

  5. Rogers GF, Greene AK. Autogenous bone graft: Basic science and clinical implications. J Craniofac Surg. 2012;23(1):323-7.

  6. Bauer TW, Muschler GF. Bone graft materials. An overview of the basic science. Clin Orthop Relat Res. 2000(371):10-27.

  7. Ivanov S, Mukhametshin R, Muraev A, Solodkaya D. Synthetic materials used for the substitution of bone defects. Annals Oral Maxillofacial Surg. 2013;1(1):1-4.

  8. Sakkas A, Wilde F, Heufelder M, Winter K, Schramm A. Autogenous bone grafts in oral implantology-Is it still a ''gold standard''? A consecutive review of279 patients with 456 clinical procedures. Int J Implant Dent. 2017;3(1):23.

  9. Ewers R. Maxilla sinus grafting with marine algae derived bone forming material: A clinical report of long-term results. J Oral Maxillofac Surg. 2005;63(12):1712-23.

  10. Clarke B. Normal bone anatomy and physiology. Clin J Am Soc Nephrol. 2008;3(Suppl 3):S131-9.

  11. Tovar N, Witek L, Atria P, Sobieraj M, Bowers M, Lopez CD, Cronstein BN, Coelho PG. Form and functional repair of long bone using 3D-printed bioactive scaffolds. J Tissue Eng Regen Med. 2018;12(9):1986-99.

  12. Witek L, Alifarag AM, Tovar N, Lopez CD, Cronstein BN, Rodriguez ED, Coelho PG. Repair of critical-sized long bone defects using dipyridamole-augmented 3D-printed bioactive ceramic scaffolds. J Orthop Res. 2019. doi: 10.1002/jor.24424.

  13. Lopez CD, Witek L, Torroni A, Flores RL, Demissie DB, Young S, Cronstein BN, Coelho PG. The role of 3D printing in treating craniomaxillofacial congenital anomalies. Birth Defects Res. 2018;110(13):1055-64.

  14. Lopez CD, Diaz-Siso JR, Witek L, Bekisz JM, Cronstein BN, Torroni A, Flores RL, Rodriguez ED, Coelho PG. Three dimensionally printed bioactive ceramic scaffold osseoconduction across critical-sized mandibular defects. J Surg Res. 2018;223:115-22.

  15. Coelho PG, Coimbra M, Ribeiro C, Fancio E, Higa O, Suzuki M, Marincola M. Physico/chemical characterization and preliminary human histology assessment of a P-TCP particulate material for bone augmentation. Mater Sci Eng C. 2009;29(7):2085-91.

  16. 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 B Appl Biomater. 2009;91(2):975-9.

  17. Gil LF, Suzuki M, Janal MN, Tovar N, Marin C, Granato R, Bonfante EA, Jimbo R, Gil JN, Coelho PG. Progressive plateau root form dental implant osseointegration: A human retrieval study. J Biomed Mater Res B Appl Biomater. 2015;103(6):1328-32.

  18. Coelho PG, Bonfante EA, Marin C, Granato R, Giro G, Suzuki M. A human retrieval study of plasma-sprayed hydroxyapatite-coated plateau root form implants after 2 months to 13 years in function. J Long Term Effects Med Implants. 2010;20(4):335-42.

  19. Baldassarri M, Bonfante E, Suzuki M, Marin C, Granato R, Tovar N, Coelho PG. Mechanical properties of human bone surrounding plateau root form implants retrieved after 0.3-24 years of function. J Biomed Mater Res B Appl Biomater. 2012;100(7):2015-21.

  20. Coelho PG, Granato R, Marin C, Bonfante EA, Janal MN, Suzuki M. Biomechanical and bone histomorphologic evaluation of four surfaces on plateau root form implants: An experimental study in dogs. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;109(5):e39-45.

  21. Coelho PG, Jimbo R. Osseointegration of metallic devices: Current trends based on implant hardware design. Arch Biochem Biophys. 2014;561:99-108.

  22. Coelho PG, Jimbo R, Tovar N, Bonfante EA. Osseointegration: Hierarchical designing encompassing the macrometer, micrometer, and nanometer length scales. Dent Mater. 2015;31(1):37-52.

  23. SynthoGraft pure phase beta-tricalcium phosphate [monograph on the Internet]. Boston: Bicon; 2010 [cited 2019 Aug 8]. Available from: thoGraft_Manual.pdf.

  24. Rosen PS, Summers R, Mellado JR, Salkin LM, Shanaman RH, Marks MH, Fugazzotto PA. The bone-added osteotome sinus floor elevation technique: Multicenter retrospective report of consecutively treated patients. Int J Oral Maxillofac Implants. 1999;14(6):853-8.

  25. Donath K, Breuner G. A method for the study of undecalcified bones and teeth with attached soft tissues. The Sage- Schliff (sawing and grinding) technique. J Oral Pathol. 1982;11(4):318-26.

  26. Granato R, Marin C, Suzuki M, Gil JN, Janal MN, Coelho PG. Biomechanical and histomorphometric evaluation of a thin ion beam bioceramic deposition on plateau root form implants: An experimental study in dogs. J Biomed Mater Res B Appl Biomater. 2009;90(1):396-403.

  27. Suzuki M, Guimaraes MV, Marin C, Granato R, Gil JN, Coelho PG. Histomorphometric evaluation of alumina- blasted/acid-etched and thin ion beam-deposited bioceramic surfaces: An experimental study in dogs. J Oral Maxillofac Surg. 2009;67(3):602-7.

  28. Coelho PG, Suzuki M, Guimaraes MV, Marin C, Granato R, Gil JN, Miller RJ. Early bone healing around different implant bulk designs and surgical techniques: A study in dogs. Clin Implant Dent Relat Res. 2010;12(3):202-8.

  29. Granato R, Marin C, Gil JN, Chuang SK, Dodson TB, Suzuki M, Coelho PG. Thin bioactive ceramic-coated alumina-blasted/acid-etched implant surface enhances biomechanical fixation of implants: An experimental study in dogs. Clin Implant Dent Relat Res. 2011;13(2):87-94.

  30. Marin C, Granato R, Suzuki M, Gil JN, Janal MN, Coelho PG. Histomorphologic and histomorphometric evaluation of various endosseous implant healing chamber configurations at early implantation times: A study in dogs. Clin Oral Implants Res. 2010;21(6):577-83.

  31. Coelho PG, Granato R, Marin C, Teixeira HS, Suzuki M, Valverde GB, Janal MN, Lilin T, Bonfante EA. The effect of different implant macrogeometries and surface treatment in early biomechanical fixation: An experimental study in dogs. J Mech Beh Biomed Mater. 2011;4(8):1974-81.

  32. Cionca N, Hashim D, Mombelli A. Zirconia dental implants: Where are we now, and where are we heading? Periodontol 2000. 2017;73(1):241-58.

  33. Nishihara H, Haro Adanez M, Att W. Current status of zirconia implants in dentistry: Preclinical tests. J Prosthodont Res. 2019;63(1):1-14.

  34. Sicilia A, Cuesta S, Coma G, Arregui I, Guisasola C, Ruiz E, Maestro A. Titanium allergy in dental implant patients: A clinical study on 1500 consecutive patients. Clin Oral Implants Res. 2008;19(8):823-35.

  35. Chen Q, Thouas GA. Metallic implant biomaterials. Mater Sci Eng R Rep. 2015;87:1-57.