Ridge augmentation and maxillary sinus grafting with a biphasic calcium phosphate: histologic and histomorphometric observations
Anton Friedmann
Department of Periodontology, CharitéCenter 3, Campus Virchow-Klinikum, Charité Universitätsmedizin Berlin, Berlin, Germany
Search for more papers by this authorBernd-Michael Kleber
Department of Periodontology, CharitéCenter 3, Campus Virchow-Klinikum, Charité Universitätsmedizin Berlin, Berlin, Germany
Search for more papers by this authorJean-Pierre Bernimoulin
Department of Periodontology, CharitéCenter 3, Campus Virchow-Klinikum, Charité Universitätsmedizin Berlin, Berlin, Germany
Search for more papers by this authorDieter D. Bosshardt
Department of Oral Surgery and Stomatology, School of Dental Medicine, University of Berne, Berne, Switzerland
Department of Periodontology, School of Dental Medicine, University of Berne, Berne, Switzerland
Search for more papers by this authorAnton Friedmann
Department of Periodontology, CharitéCenter 3, Campus Virchow-Klinikum, Charité Universitätsmedizin Berlin, Berlin, Germany
Search for more papers by this authorBernd-Michael Kleber
Department of Periodontology, CharitéCenter 3, Campus Virchow-Klinikum, Charité Universitätsmedizin Berlin, Berlin, Germany
Search for more papers by this authorJean-Pierre Bernimoulin
Department of Periodontology, CharitéCenter 3, Campus Virchow-Klinikum, Charité Universitätsmedizin Berlin, Berlin, Germany
Search for more papers by this authorDieter D. Bosshardt
Department of Oral Surgery and Stomatology, School of Dental Medicine, University of Berne, Berne, Switzerland
Department of Periodontology, School of Dental Medicine, University of Berne, Berne, Switzerland
Search for more papers by this authorAbstract
Objectives: This retrospective study reports on histologic and histomorphometric observations performed on human biopsies harvested from sites augmented exclusively by biphasic calcium phosphate [BCP: hydroxyapatite (HA)/ tricalcium phosphate (TCP) 60/40] and healed for a minimum of 6 months.
Materials and methods: Five patients benefited from three augmentation regimens (i.e.: one-stage lateral augmentation; two-stage lateral augmentation; and two-stage sinus grafting). In all patients, a degradable collagen membrane served as a cell-occlusive barrier. Core biopsies were obtained from lateral as from crestal aspects 6–10 months after augmentation surgeries. For histologic and histomorphometric evaluations, the non-decalcified tissue processing was performed.
Results: The histological examination of 11 biopsies showed graft particles frequently being bridged by the new bone, and a close contact between the graft particles and newly formed bone was seen in all samples. The mean percentages of newly formed bone, soft tissue compartment, and graft material were 38.8% (±5.89%), 41.75% (±6.08%), and 19.63% (±4.85%), respectively. Regarding bone-to-graft contact values, the percentage of bone coverage of graft particles for all biopsies ranged from 27.83% to 80.17%. The mean percentage of bone coverage was 55.39% (±13.03%).
Conclusions: Data from the present study demonstrated osteoconductivity scores for the BCP material (HA/TCP 60/40) in patients resembling those previously shown for grafting materials of xenogenic and alloplastic origin.
References
- Artzi, Z., Kozlovsky, A., Nemcovsky, C.E. & Weinreb, M. (2005) The amount of newly formed bone in sinus grafting procedures depends on tissue depth as well as the type and residual amount of the grafted material. Journal of Clinical Periodontology 32: 193–199.
- Artzi, Z., Nemcovsky, C.E., Tal, H. & Dayan, D. (2001) Histopathological morphometric evaluation of 2 different hydroxyapatite-bone derivatives in sinus augmentation procedures: a comparative study in humans. Journal of Periodontology 72: 911–920.
- Artzi, Z.W.M., Carmeli, G., Dor, R.L., Dard, M. & Nemcovsky, C. (2008) Histologic and histomorphometric assessments of bone formation in sinus augmentation utilizing a combination of autogenous and hydroxyapatite/biphasic tricalcium phosphate graft materials: observations at 6 and 9 months in humans. Clinical Oral Implants Research 19: 686–692.
- Arx von, T. & Kurt, B. (1999) Implant placement and simultaneous ridge augmentation using autogenous bone and a micro titanium mesh: a prospective clinical study with 20 implants. Clinical Oral Implants Research 10: 24–33.
- Busenlechner, D., Kantor, M., Tangl, S., Tepper, G., Zechner, W., Haas, R. & Watzek, G. (2005) Alveolar ridge augmentation with a prototype trilayer membrane and various bone grafts: a histomorphometric study in baboons. Clinical Oral Implants Research 16: 220–227.
- Buser, D., Hoffmann, B., Bernard, J.P., Lussi, A., Mettler, D. & Schenk, R.K. (1998) Evaluation of filling materials in membrane-protected bone defects. A comparative histomorphometric study in the mandible of miniature pigs. Clinical Oral Implants Research 9: 137–150.
- Cordaro, L.B. Personal Communication, April 15, 2008.
- Cordaro, L.B., D, D., Palatella, P., Rao, W., Serino, G. & Chiapasco, M. (2008) Maxillary sinus grafting with Bio-Oss or Institute Straumann BoneCeramic: histomorphometric results from a randomized controlled multicenter clinical trial. Clinical Oral Implants Research 19: 796–803.
- Dahlin, C., Linde, A., Gottlow, J. & Nyman, S. (1988) Healing of bone defects by guided tissue regeneration. Plastic Reconstructive Surgery 81: 672–676.
- Dahlin, C., Sennerby, L., Lekholm, U., Linde, A. & Nyman, S. (1989) Generation of new bone around titanium implants using a membrane technique: an experimental study in rabbits. International Journal of Oral & Maxillofacial Implants 4: 19–25.
- Donos, N., Bosshardt, D., Lang, N., Graziani, F., Tonetti, M., Karring, T. & Kostopoulos, L. (2005) Bone formation by enamel matrix proteins and xenografts: an experimental study in the rat ramus. Clinical Oral Implants Research 16: 140–146.
- Eggli, P.S., Muller, W. & Schenk, R.K. (1988) Porous hydroxyapatite and tricalcium phosphate cylinders with two different pore size ranges implanted in the cancellous bone of rabbits. A comparative histomorphometric and histologic study of bony ingrowth and implant substitution. Clinical Orthopaedics and Related Research 232: 127–138.
- Fiorellini, J., Engebretson, S., Donath, K. & Weber, H. (1998) Guided bone regeneration utilizing expanded polytetrafluoroethylene membranes in combination with submerged and nonsubmerged dental implants in beagle dogs. Journal of Periodontology 69: 528–535.
- Fiorellini, J.P. & Nevins, M.L. (2003) Localized ridge augmentation/preservation. A systematic review. Annals of Periodontology 8: 321–327.
- Friedmann, A., Dehnhardt, J., Kleber, B.-M. & Bernimoulin, J.-P. (2008) Cytobiocompatibility of collagen and e-PTFE membranes on osteoblast-like cells in vitro. Journal of Biomedical Materials Research 86A: 935–941.
- Friedmann, A., Strietzel, F.P., Maretzki, B., Pitaru, S. & Bernimoulin, J.P. (2002) Histological assessment of augmented jaw bone utilizing a new collagen barrier membrane compared to a standard barrier membrane to protect a granular bone substitute material. Clinical Oral Implants Research 13: 587–594.
- Hammerle, C.H. & Karring, T. (1998) Guided bone regeneration at oral implant sites. Periodontology 2000 17: 151–175.
- Jensen, S.S., Bornstein, M.M., Dard, M., Bosshardt, D. & Buser, D. (2008) Comparative study of biphasic calcium phosphates with different HA/TCP ratios in mandibular bone defects. A long-term histomorphometric study in minipigs. Key Engineering Materials 361–363: 1241–1244.
- Jensen, S.S., Bornstein, M.M., Dard, M., Bosshardt, D. & Buser, D. (2009) Comparative study of biphasic calcium phosphates with different HA/TCP ratios in mandibular bone defects. A long-term histomorphometric study. Journal of Biomedical Materials Research B, E pub.
- Jensen, S.S., Broggini, N., Weibrich, G., Hjorting-Hansen, E., Schenk, R. & Buser, D. (2005) Bone regeneration in standardized bone defects with autografts or bone substitutes in combination with platelet concentrate: a histologic and histomorphometric study in the mandibles of minipigs. International Journal of Oral & Maxillofacillofacial Implants 20: 703–712.
- Jensen, S.S., Yeo, A., Dard, M., Hunziker, E., Schenk, R. & Buser, D. (2007) Evaluation of a novel biphasic calcium phosphate in standardized bone defects. A histologic and histomorphometric study in the mandibles of minipigs. Clinical Oral Implants Research 18: 752–760.
- Knabe, C., Koch, C., Rack, A. & Stiller, M. (2008) Effect of b-tricalcium phosphate particles with varying porosity on osteogenesis after sinus floor augmentation in humans. Biomaterials 29: 2249–2258 (epub ahead of print).
- Lang, N.P., Hammerle, C.H., Bragger, U., Lehmann, B. & Nyman, S.R. (1994) Guided tissue regeneration in jawbone defects prior to implant placement. Clinical Oral Implants Research 5: 92–97.
- LeGeros, R.Z., Lin, S., Rohanizadeh, R., Mijares, D. & LeGeros, J.P. (2003) Biphasic calcium phosphate bioceramics: preparation, properties and applications. Journal of Material Science. Materials in Medicine 14: 201–209.
- McAllister, B.S. & Haghighat, K. (2007) Bone augmentation techniques. Journal of Periodontology 78: 377–396.
- Moradian-Oldak, J., Wen, H.B., Schneider, G.B. & Stanford, C.M. (2006) Tissue engineering strategies for the future generation of dental implants. Periodontology 2000 41: 157–176.
- Moses, O., Pitaru, S., Artzi, Z. & Nemcovsky, C.E. (2005) Healing of dehiscence-type defects in implants placed together with different barrier membranes: a comparative clinical study. Clinical Oral Implants Research 16: 210–219.
- Nemcovsky, C.E. & Artzi, Z. (2002) Comparative study of buccal dehiscence defects in immediate, delayed, and late maxillary implant placement with collagen membranes: clinical healing between placement and second-stage surgery. Journal of Periodontology 73: 754–761.
- Proussaefs, P. & Lozada, J. (2006) Use of titanium mesh for staged localized alveolar ridge augmentation: clinical and histologic-histomorphometric evaluation. Journal of Oral Implantology 32: 237–247.
- Rothamel, D., Schwarz, F., Sager, M., Herten, M., Sculean, A. & Becker, J. (2005) Biodegradation of differently cross-linked collagen membranes: an experimental study in the rat. Clinical Oral Implants Research 16: 369–378.
- Rothamel, D., Schwarz, F., Sculean, A., Herten, M., Scherbaum, W. & Becker, J. (2004) Biocompatibility of various collagen membranes in cultures of human PDL fibroblasts and human osteoblast-like cells. Clinical Oral Implants Research 15: 443–449.
- Schenk, R.K., Olah, A.J. & Herrmann, W. (1984) Preparation of calcified tissues for light microscopy. In: G.R. Dickson, ed. Methods of Calcified Tissue Preparation, 1–56. Amsterdam: Elsevier.
- Schwarz, F., Rothamel, D., Herten, M., Sager, M. & Becker, J. (2006) Angiogenesis pattern of native and cross-linked collagen membranes: an immunohistochemical study in the rat. Clinical Oral Implants Research 17: 403–409.
- Valentini, P., Abensur, D., Wenz, B., Peetz, M. & Schenk, R. (2000) Sinus grafting with porous bone mineral (Bio-Oss) for implant placement: a 5-year study on 15 patients. International Journal of Periodontics and Restorative Dentistry 20: 245–253.
- Von Arx, T., Cochran, D.L., Hermann, J.S., Schenk, R.K., Higginbottom, F.L. & Buser, D. (2001) Lateral ridge augmentation and implant placement: an experimental study evaluating implant osseointegration in different augmentation materials in the canine mandible. International Journal of Oral & Maxillofacial Implants 16: 343–354.
- Weibel, E.R. (1979) Practical methods for biological morphometry. In: E.R. Weibel, ed. Stereological Methods, Vol. 1, 1st edition, 1–415. New York: Academic Press.
- Zerbo, I.R., Bronckers, A.L., De Lange, G. & Burger, E.H. (2005) Localisation of osteogenic and osteoclastic cells in porous beta-tricalcium phosphate particles used for human maxillary sinus floor elevation. Biomaterials 26: 1445–1451.
- Zerbo, I.R., De Lange, G.L., Joldersma, M., Bronckers, A.L. & Burger, E.H. (2003) Fate of monocortical bone blocks grafted in the human maxilla: a histological and histomorphometric study. Clinical Oral Implants Research 14: 759–766.
- Zerbo, I.R., Zijderveld, S.A., De Boer, A., Bronckers, A.L., De Lange, G., Ten Bruggenkate, C.M. & Burger, E.H. (2004) Histomorphometry of human sinus floor augmentation using a porous beta-tricalcium phosphate: a prospective study. Clinical Oral Implants Research 15: 724–732.
- Zijderveld, S.A., Zerbo, I.R., Van Den Bergh, J.P., Schulten, E.A. & Ten Bruggenkate, C.M. (2005) Maxillary sinus floor augmentation using a beta-tricalcium phosphate (Cerasorb) alone compared to autogenous bone grafts. International Journal of Oral & Maxillofacial Implants 20: 432–440.
- Zitzmann, N.U., Naef, R. & Schärer, P. (1997) Resorbable versus nonresorbable membranes in combination with bio-oss for guided bone regeneration. International Journal of Oral & Maxillofacial Implants 12: 844–852.
- Zitzmann, N.U., Rateitschak-Pluss, E. & Marinello, C.P. (2003) Treatment of angular bone defects with a composite bone grafting material in combination with a collagen membrane. Journal of Periodontology 74: 687–694.