A Human Clinical, Histological, Histomorphometrical, and Radiographical Study on Biphasic HA-Beta-TCP 30/70 in Maxillary Sinus Augmentation
Carlo Mangano MD, DDS
Specialist in anesthesiology, assistant professor and head of oral surgery
Department of Morphological and Surgical Science, University of Insubria, Varese, Italy
Search for more papers by this authorBruna Sinjari DDS
Research fellow
Department of Medical, Oral and Biotechnological Sciences, University of Chieti-Pescara, Chieti, Italy
Search for more papers by this authorJamil A. Shibli DDS, MS, PhD
Professor of oral surgery
Dental Research Division, Guarulhos University, SP, Guarulhos, Brazil
Search for more papers by this authorFrancesco Mangano DDS
Oral surgeon
Department of Morphological and Surgical Science, University of Insubria, Varese, Italy
Search for more papers by this authorAdriano Piattelli MD, DDS
Professor of oral pathology and medicine
Department of Medical, Oral and Biotechnological Sciences, University of Chieti-Pescara, Chieti, Italy
Search for more papers by this authorVittoria Perrotti DDS, PhD
Research fellow
Department of Medical, Oral and Biotechnological Sciences, University of Chieti-Pescara, Chieti, Italy
Search for more papers by this authorCorresponding Author
Giovanna Iezzi DDS, PhD
Researcher
Department of Medical, Oral and Biotechnological Sciences, University of Chieti-Pescara, Chieti, Italy
Reprint requests: Prof. Giovanna Iezzi, Department of Medical, Oral and Biotechnological Sciences, University of Chieti-Pescara, Via dei Vestini 31, Chieti 66100, Italy; e-mail: [email protected]Search for more papers by this authorCarlo Mangano MD, DDS
Specialist in anesthesiology, assistant professor and head of oral surgery
Department of Morphological and Surgical Science, University of Insubria, Varese, Italy
Search for more papers by this authorBruna Sinjari DDS
Research fellow
Department of Medical, Oral and Biotechnological Sciences, University of Chieti-Pescara, Chieti, Italy
Search for more papers by this authorJamil A. Shibli DDS, MS, PhD
Professor of oral surgery
Dental Research Division, Guarulhos University, SP, Guarulhos, Brazil
Search for more papers by this authorFrancesco Mangano DDS
Oral surgeon
Department of Morphological and Surgical Science, University of Insubria, Varese, Italy
Search for more papers by this authorAdriano Piattelli MD, DDS
Professor of oral pathology and medicine
Department of Medical, Oral and Biotechnological Sciences, University of Chieti-Pescara, Chieti, Italy
Search for more papers by this authorVittoria Perrotti DDS, PhD
Research fellow
Department of Medical, Oral and Biotechnological Sciences, University of Chieti-Pescara, Chieti, Italy
Search for more papers by this authorCorresponding Author
Giovanna Iezzi DDS, PhD
Researcher
Department of Medical, Oral and Biotechnological Sciences, University of Chieti-Pescara, Chieti, Italy
Reprint requests: Prof. Giovanna Iezzi, Department of Medical, Oral and Biotechnological Sciences, University of Chieti-Pescara, Via dei Vestini 31, Chieti 66100, Italy; e-mail: [email protected]Search for more papers by this authorAbstract
Background
By mixing hydroxyapatite (HA) and tricalcium phosphate (TCP), biphasic calcium phosphate ceramics can be obtained, and by varying their ratio it is possible to tailor the characteristics of the biomaterial.
Purpose
The aim of the present human study was to evaluate the histological and radiographical aspects of bone formation in maxillary sinus augmentation using a 30/70 HA-beta-TCP with a reticular structure.
Materials and Methods
A total of 12 patients, undergoing two-stage sinus augmentation procedure using HA-beta-TCP at a ratio of 30/70, were included in the present study. After a 6-month healing period, during implant insertion, radiographical analysis was performed, and then the bone core biopsies were harvested and processed for histology.
Results
At radiographic evaluation, the bone gain was on average 6.85 ± 0.60 mm. HA-beta-TCP 30/70 appeared to be lined by newly formed bone, with no gaps at the interface. The histomorphometric analysis revealed 26 ± 2% of residual grafted biomaterial, 29 ± 3% of newly formed bone, and 45 ± 2% of marrow spaces.
Conclusions
The present results indicate histologically the high biocompatibility and osteoconductivity of HA-beta-TCP 30/70, and clinically its successful use for sinus augmentation procedures.
References
- 1 Tatum OH. Maxillary and sinus implant reconstruction. Dent Clin North Am 1986; 30: 207–229.
- 2 Bauer TW, Muschler GF. Bone graft materials. An overview of the basic science. Clin Orthop Relat Res 2000; 371: 10–27.
- 3 Wang M. Developing bioactive composite materials for tissue replacement. Biomaterials 2003; 24: 2133–2151.
- 4 Van der Bergh JP, ten Bruggenkate CM, Krekeler G, Tuinzing DB. Sinus floor elevation and grafting with autogenous iliac crest bone. Clin Oral Implants Res 1998; 9: 429–435.
- 5 Lindgren C, Sennerby L, Mordenfeld A, Hallman M. Clinical histology of microimplants placed in two different biomaterials. Int J Oral Maxillofac Implants 2009; 24: 1093–1100.
- 6 Mangano C, Scarano A, Perrotti V, Iezzi G, Piattelli A. Maxillary sinus augmentation with a porous synthetic hydroxyapatite and bovine derived hydroxyapatite: comparative clinical and histological study. Int J Oral Maxillofac Implants 2007; 22: 980–986.
- 7 Becker W, Schenk R, Higuchi K, Lekholm U, Becker BE. Variations in bone regeneration adjacent to implants augmented with barrier membranes alone or with demineralized freeze-dried bone or autologous grafts in dogs. Int J Oral Maxillofac Implants 1995; 10: 143–154.
- 8 Piattelli A, Scarano A, Corigliano M, Piattelli M. Comparison of bone regeneration with the use of mineralized and demineralized freeze-dried bone allografts: a histological and histochemical study in man. Biomaterials 1996; 17: 1127–1131.
- 9 Nystrom C. Plugging of bone cavities with rivanol-plasterporridge. Acta Chir Scand 1928; 63: 296.
- 10 Edberg E. Some experiences of filling osseous cavities with plaster. Acta Chir Scand 1930; 67: 313–319.
- 11 Wallace SS, Froum SJ. Effect of maxillary sinus augmentation on the survival of endosseous dental implants. A systematic review. Ann Periodontol 2003; 8: 328–343.
- 12 Jensen SS, Broggini N, Hjørting-Hansen E, Sclenk R, Buser D. Bone healing and graft resorption of autograft, anorganic bovine bone and β-tricalcium phosphate. A histologic and histomorphometric study in the mandibles of minipigs. Clin Oral Implants Res 2006; 17: 237–243.
- 13 Pietrzak WS, Ronk R. Calcium sulphate bone void filler: a review and a look ahead. J Craniofac Surg 2000; 11: 327–333. (Discussion 334. Review).
- 14 De Leonardis D, Pecora GE. Prospective study on the augmentation of the maxillary sinus with calcium sulfate: histological results. J Periodontol 2000; 71: 940–947.
- 15 Sottosanti J. Calcium sulfate: a biodegradable and biocompatible barrier for guided tissue regeneration. Compendium 1992; 13: 226–228. 230, 232–4. Review.
- 16
Dorozhkin S, Epple M. Biological and medical significance of calcium phosphates. Angew Chem Int Ed Engl 2002; 41: 3130–3146.
10.1002/1521-3773(20020902)41:17<3130::AID-ANIE3130>3.0.CO;2-1 CAS PubMed Web of Science® Google Scholar
- 17 Daculsi G, Passuti N. Bioactive ceramics, fundamental properties and clinical applications: the osseo-coalescence process. Bioceramics 1989; 2: 3–10.
- 18 Daculsi G, Laboux O, Malard O, Weiss P. Current state of the art of biphasic calcium phosphate bioceramics. J Mater Sci Mater Med 2003; 14: 195–200.
- 19 Ripamonti U, Richter PW, Nilen RW, Renton L. The induction of bone formation by smart biphasic hydroxyapatite tricalcium phosphate biomimetic matrices in the non-human primate Papio ursinus. J Cell Mol Med 2008; 12(6B): 2609–2621.
- 20 Ripamonti U. Osteoinduction in porous hydroxyapatite implanted in heteropic sites of different animal models. Biomaterials 1996; 17: 31–35. 63–7.
- 21 Hattori H, Matsuoka H, Yamamoto K. Radiological and histological analysis of synthetic bone grafts in recurring giant cell tumour of bone: a retrospective study. Radiological and histological analysis of synthetic bone grafts in recurring giant cell tumour of bone: a retrospective study. J Orthop Surg (Hong Kong) 2010; 18: 63–67.
- 22 Cheng L, Ye F, Yang R, et al. Osteoinduction of hydroxyapatite/b-tricalcium phosphate bioceramics in mice with a fractured fibula. Acta Biomater 2010; 6: 1569–1574.
- 23 Mayr H, Schlufter S, Detsch R, Ziegler G. Influence of phase composition on degradation and resorption of biphasic calcium phosphate ceramics. Key Eng Mat 2008; 361–363:1043–1046.
- 24 Kim CK, Chai JK, Cho KS, et al. Periodontal repair in intrabony defects treated with a calcium sulfate implant and calcium sulfate barrier. J Periodontol 1998; 69: 1317–1324.
- 25 Pecora GE, De Leonardis D, Della Rocca C, Cornelini R, Cortesini C. Short-term healing following the use of calcium sulfate as a grafting material for sinus augmentation: a clinical report. Int J Oral Maxillofac Implants 1998; 13: 866–873.
- 26 Raynaud S, Champion E, Lafon JP, Bernache-Assolant D. Calcium phosphate apatites with variable Ca/P atomic ratio III. Mechanical properties and degradation in solution of hot pressed ceramics. Biomaterials 2002; 23: 1081–1089.
- 27 Jones JR, Atwood RC, Poologasundarampillai G, Yue S, Lee PD. Quantifying the 3D macrostructure of tissue scaffolds. J Mater Sci Mater Med 2009; 20: 463–471.
- 28 Sanzana ES, Navarro M, Ginebra MP, Planell JA, Ojeda AC, Montecinos HA. Role of porosity and pore architecture in the in vivo bone regeneration capacity of biodegradable glass scaffolds. J Biomed Mater Res A 2013. DOI: 10.1002/jbm.a.34845
- 29 Lindgren C, Hallman M, Sennerby L, Sammons R. Back-scattered electron imaging and elemental analysis of retrieved bone tissue following sinus augmentation with deproteinized bovine bone or biphasic calcium phosphate. Clin Oral Implants Res 2010; 21: 924–930.
- 30 Lindgren C, Mordenfeld A, Hallman M. A prospective 1-year clinical and radiographic study of implants placed after maxillary sinus floor augmentation with synthetic biphasic calcium phosphate or deproteinized bovine bone. Clin Implant Dent Relat Res 2012; 14: 41–50.
- 31 Hallman M, Thor A. Bone substitutes and growth factors as an alternative/complement to autogenous bone for grafting in implant dentistry. Periodontol 2000 2008; 47: 172–192.
- 32 Deisinger U, Hamisch S, Schumacher M, Uhl F, Detsch R, Ziegler G. Fabrication of tailored hydroxyapatite scaffolds: comparison between a direct and an indirect rapid prototyping technique. Key Eng Mater 2008; 361–363:915–918.
- 33 Piattelli A, Scarano A, Quaranta M. High-precision, cost-effective cutting system for producing thin sections of oral tissues containing dental implants. Biomaterials 1997; 18: 577–579.
- 34 Yildirim M, Spiekermann H, Biesterfeld S, Edelhoff D. Maxillary sinus augmentation using xenogenic bone substitute material Bio-Oss in combination with venous blood. A histologic and histomorphometric study in humans. Clin Oral Implants Res 2000; 11: 217–229.
- 35 Simunek A, Kopecka D, Somanathan RV, Pilathadka S, Brazda T. Deproteinized bovine bone versus beta-tricalcium phosphate in sinus augmentation surgery: a comparative histologic and histomorphometric study. Int J Oral Maxillofac Implants 2008; 23: 935–942.
- 36 Frenken JWFH, Bowmann WF, Braven-Boer N, Zijderveld SA, Sculten EAJM, Ten Bruggenkate CM. The use of Straumann® BoneCeramic in a maxillary sinus floor elevation procedure: a clinical, radiological, histological and histomorphometric evaluation with a 6 month healing period. Clin Oral Implants Res 2010; 21: 201–208.
- 37 Schopper C, Ziya-Ghazvini F, Goriwoda W, et al. HA/TCP compounding of a porous CaP biomaterial improves bone formation and scaffold degradation. A long term histological study. J Biomed Mater Res B Appl Biomater 2005; 74: 458–467.
- 38 Michna S, Wu W, Lewis J. Concentrated hydroxyapatite inks for direct-write assembly of 3-D periodic scaffolds. Biomaterials 2005; 26: 5632–5639.
- 39 Detsch R, Schaefer S, Deisinger U, Ziegler G, Seitz H, Leukers B. In vitro: osteoclastic activity studies on surfaces of 3D printed calcium phosphate scaffolds. J Biomater Appl 2011; 26: 359–380.
- 40 Vorndran E, Klamer M, Klammert U, et al. 3D powder printing of b-tricalcium phosphate ceramics using different strategies. Adv Eng Mater 2009; 10: B67–B71.
- 41 Deisinger U, Leiderer M, Detsch R, Hamisch S, Ziegler G. Extrusion freeform fabrication technique for tailoring hydroxyapatite scaffolds for bone tissue engineering applications. Cytotherapy 2006; S2: 15.
- 42 Simon JL, Michna S, Lewis JA, et al. In vivo bone response to 3D periodic hydroxyapatite scaffolds assembled by direct ink writing. J Biomed Mater Res A 2007; 83: 747–758.
- 43 Schumacher M, Deisinger U, Detsch R, Ziegler G. Indirect rapid prototyping of biphasic calcium phosphate scaffolds as bone substitutes: influence of phase composition, macroporosity and pore geometry on mechanical properties. J Mater Sci Mater Med 2010; 21: 3119–3127.
- 44 Yuan HP, Van den Doel M, Li SH, Van Blitterswijk CA, De Groot K, De Bruijn JD. A comparison of the osteoinductive potential of two calcium phosphate ceramics implanted intramuscularly in goats. J Mater Sci Mater Med 2002; 13: 1271–1275.
- 45 Rumpler M, Woesz A, Dunlop JW, van Dongen JT, Fratzl P. The effect of geometry on three-dimensional tissue growth. J R Soc Interface 2008; 5: 1173–1180.
- 46 Hulbert SF, Young FA, Mathews RS, Klawitter JJ, Talbert CD, Stelling FH. Potential of ceramic materials as permanently implantable skeletal prostheses. J Biomed Mater Res 1970; 4: 433–456.
- 47 Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 2005; 27: 5474–5491.
- 48 Mangano C, Perrotti V, Shibli JA, et al. Maxillary sinus grafting with biphasic calcium phosphate ceramics: clinical and histologic evaluation in man. Int J Oral Maxillofac Implants 2013; 28: 51–56.
- 49 Artzi Z, Weinreb M, Carmeli G, Lev-Dor R, Dard M, Nemcovsky CE. Histomorphometric assessment of bone formation in sinus augmentation utilizing a combination of autogenous and hydroxyapatite/biphasic tricalcium phosphate graft materials: at 6 and 9 months in humans. Clin Oral Implants Res 2008; 19: 686–692.