Bone formation in mono cortical mandibular critical size defects after augmentation with two synthetic nanostructured and one xenogenous hydroxyapatite bone substitute – in vivo animal study
Michael Dau
Department of Oral and Maxillofacial Surgery, University of Rostock, Rostock, Germany
Department of Oral and Maxillofacial Surgery, Federal Army Hospital Hamburg-Wandsbek, Hamburg, Germany
Both authors contributed equally.
Search for more papers by this authorCorresponding Author
Peer W. Kämmerer
Department of Oral and Maxillofacial Surgery, University of Rostock, Rostock, Germany
Department of Oral and Maxillofacial Surgery, Federal Army Hospital Hamburg-Wandsbek, Hamburg, Germany
Both authors contributed equally.
Corresponding author:
Peer W. Kämmerer
Department of Oral and Maxillofacial Surgery, University of Rostock, Germany. Schillingallee 35, 18057 Rostock, Germany
Tel.: 0381-4946088
Fax: 0381-4946698
e-mail: [email protected]
Search for more papers by this authorKai-Olaf Henkel
Department of Oral and Maxillofacial Surgery, Federal Army Hospital Hamburg-Wandsbek, Hamburg, Germany
Search for more papers by this authorThomas Gerber
Department of Physics, Faculty of Mathematics and Natural Sciences, Rostock University, Rostock, Germany
Search for more papers by this authorBernhard Frerich
Department of Oral and Maxillofacial Surgery, University of Rostock, Rostock, Germany
Department of Oral and Maxillofacial Surgery, Federal Army Hospital Hamburg-Wandsbek, Hamburg, Germany
Search for more papers by this authorKarsten K. H. Gundlach
Department of Oral and Maxillofacial Surgery, University of Rostock, Rostock, Germany
Department of Oral and Maxillofacial Surgery, Federal Army Hospital Hamburg-Wandsbek, Hamburg, Germany
Search for more papers by this authorMichael Dau
Department of Oral and Maxillofacial Surgery, University of Rostock, Rostock, Germany
Department of Oral and Maxillofacial Surgery, Federal Army Hospital Hamburg-Wandsbek, Hamburg, Germany
Both authors contributed equally.
Search for more papers by this authorCorresponding Author
Peer W. Kämmerer
Department of Oral and Maxillofacial Surgery, University of Rostock, Rostock, Germany
Department of Oral and Maxillofacial Surgery, Federal Army Hospital Hamburg-Wandsbek, Hamburg, Germany
Both authors contributed equally.
Corresponding author:
Peer W. Kämmerer
Department of Oral and Maxillofacial Surgery, University of Rostock, Germany. Schillingallee 35, 18057 Rostock, Germany
Tel.: 0381-4946088
Fax: 0381-4946698
e-mail: [email protected]
Search for more papers by this authorKai-Olaf Henkel
Department of Oral and Maxillofacial Surgery, Federal Army Hospital Hamburg-Wandsbek, Hamburg, Germany
Search for more papers by this authorThomas Gerber
Department of Physics, Faculty of Mathematics and Natural Sciences, Rostock University, Rostock, Germany
Search for more papers by this authorBernhard Frerich
Department of Oral and Maxillofacial Surgery, University of Rostock, Rostock, Germany
Department of Oral and Maxillofacial Surgery, Federal Army Hospital Hamburg-Wandsbek, Hamburg, Germany
Search for more papers by this authorKarsten K. H. Gundlach
Department of Oral and Maxillofacial Surgery, University of Rostock, Rostock, Germany
Department of Oral and Maxillofacial Surgery, Federal Army Hospital Hamburg-Wandsbek, Hamburg, Germany
Search for more papers by this authorAbstract
Objectives
Healing characteristics as well as level of tissue integration and degradation of two different nanostructured hydroxyapatite bone substitute materials (BSM) in comparison with a deproteinized hydroxyapatite bovine BSM were evaluated in an in vivo animal experiment.
Material and methods
In the posterior mandible of 18 minipigs, bilateral mono cortical critical size bone defects were created. Randomized augmentation procedures with NanoBone® (NHA1), Ostim® (NHA2) or Bio-Oss® (DBBM) were conducted (each material n = 12). Samples were analyzed after five (each material n = 6) and 8 months (each material n = 6). Defect healing, formation of soft tissue and bone as well as the amount of remaining respective BSM were quantified both macro- and microscopically.
Results
For NHA2, the residual bone defect after 5 weeks was significantly less compared to NHA1 or DBBM. There was no difference in residual BSM between NHA1 and DBBM, but the amount in NHA2 was significantly lower. NHA2 also showed the least amount of soft tissue and the highest amount of new bone after 5 weeks. Eight months after implantation, no significant differences in the amount of residual bone defects, in soft tissue or in bone formation were detected between the groups. Again, NHA2 showed significant less residual material than NHA1 and DBBM.
Discussion
We observed non-significant differences in the biological hard tissue response of NHA1 and DBBM. The water-soluble NHA2 initially induced an increased amount of new bone but was highly compressed which may have a negative effect in less stable augmentations of the jaw.
References
- Baldini, N., De Sanctis, M. & Ferrari, M. (2011) Deproteinized bovine bone in periodontal and implant surgery. Dental Materials 27: 61–70.
- Bauer, T.W. & Muschler, G.F. (2000) Bone graft materials. An overview of the basic science. Clinical Orthopedics and Related Research 371: 10–27.
- Behnia, H., Khojasteh, A., Kiani, M.T., Khoshzaban, A., Mashhadi Abbas, F., Bashtar, M. & Dashti, S.G. (2013) Bone regeneration with a combination of nanocrystalline hydroxyapatite silica gel, platelet-rich growth factor, and mesenchymal stem cells: A histologic study in rabbit calvaria. Oral Surgery Oral Medicine Oral Pathology and Oral Radiology 115: e7–e15.
- Berglundh, T. & Lindhe, J. (1997) Healing around implants placed in bone defects treated with Bio-Oss. An experimental study in the dog. Clinical Oral Implants Research 8: 117–124.
- Bosch, C., Melsen, B. & Vargervik, K. (1998) Importance of the critical-size bone defect in testing bone-regenerating materials. The Journal of Craniofacial Surgery 9: 310–316.
- Busenlechner, D., Tangl, S., Mair, B., Fugger, G., Gruber, R., Redl, H. & Watzek, G. (2008) Simultaneous in vivo comparison of bone substitutes in a guided bone regeneration model. Biomaterials 29: 3195–3200.
- Canuto, R.A., Pol, R., Martinasso, G., Muzio, G., Gallesio, G. & Mozzati, M. (2013) Hydroxyapatite paste Ostim, without elevation of full-thickness flaps, improves alveolar healing stimulating BMP- and VEGF-mediated signal pathways: An experimental study in humans. Clinical Oral Implants Research 24 (Suppl. A100): 42–48.
- Carmagnola, D., Abati, S., Celestino, S., Chiapasco, M., Bosshardt, D. & Lang, N.P. (2008) Oral implants placed in bone defects treated with Bio-Oss, Ostim-Paste or PerioGlas: An experimental study in the rabbit tibiae. Clinical Oral Implants Research 19: 1246–1253.
- Chiapasco, M., Casentini, P. & Zaniboni, M. (2009) Bone augmentation procedures in implant dentistry. The International Journal of Oral & Maxillofacial Implants 24(Suppl): 237–259.
- Chris Arts, J.J., Verdonschot, N., Schreurs, B.W. & Buma, P. (2006) The use of a bioresorbable nano-crystalline hydroxyapatite paste in acetabular bone impaction grafting. Biomaterials 27: 1110–1118.
- Donath, K. & Breuner, G. (1982) A method for the study of undecalcified bones and teeth with attached soft tissues. The Sage-Schliff (sawing and grinding) technique. Journal of Oral Pathology 11: 318–326.
- Duda, M. & Pajak, J. (2004) The issue of bioresorption of the Bio-Oss xenogeneic bone substitute in bone defects. Annalis Universitatis Mariae Curie Sklodowska. Sectio D: Medicina 59: 269–277.
- Finkemeier, C.G. (2002) Bone-grafting and bone-graft substitutes. The Journal of Bone and Joint Surgery. American Volume 84-A: 454–464.
- Gauthier, O., Bouler, J.M., Aguado, E., Pilet, P. & Daculsi, G. (1998) Macroporous biphasic calcium phosphate ceramics: Influence of macropore diameter and macroporosity percentage on bone ingrowth. Biomaterials 19: 133–139.
- Gazdag, A.R., Lane, J.M., Glaser, D. & Forster, R.A. (1995) Alternatives to autogenous bone graft: efficacy and indications. The Journal of the American Academy of Orthopedic Surgeons 3: 1–8.
- Gerber, T., Holzhüter, G., Knoblich, B., DÖrfling, P., Bienengräber, V. & Henkel, K.-O.H. (2000) Development of bioactive Sol-Gel material template for in vitro and in vivo synthesis of bone material. Journal of Sol-Gel Science and Technology 19: 441–445.
- Ghanaati, S., Barbeck, M., Willershausen, I., Thimm, B., Stuebinger, S., Korzinskas, T., Obreja, K., Landes, C., Kirkpatrick, C.J. & Sader, R.A. (2013a) Nanocrystalline hydroxyapatite bone substitute leads to sufficient bone tissue formation already after 3 months: Histological and histomorphometrical analysis 3 and 6 months following human sinus cavity augmentation. Clinical Implant Dentistry and Related Research 15: 883–892.
- Ghanaati, S., Udeabor, S.E., Barbeck, M., Willershausen, I., Kuenzel, O., Sader, R.A. & Kirkpatrick, C.J. (2013b) Implantation of silicon dioxide-based nanocrystalline hydroxyapatite and pure phase beta-tricalciumphosphate bone substitute granules in caprine muscle tissue does not induce new bone formation. Head & Face Medicine 9: 1.
- Hegedus, Z. (1923) The rebuilding of the alveolar process by bone transplantation. Dental Cosmos 65: 736.
- Heinemann, F., Mundt, T., Biffar, R., Gedrange, T. & Goetz, W. (2009) A 3-year clinical and radiographic study of implants placed simultaneously with maxillary sinus floor augmentations using a new nanocrystalline hydroxyapatite. Journal of Physiology and Pharmacology 60(Suppl. 8): 91–97.
- Henkel, K.O., Gerber, T., Dietrich, W. & Bienengraeber, V. (2004) Novel calcium phosphate formula for filling bone defects. Initial in vivo long-term results. Mund-, Kiefer- und Gesichtschirugie 8: 277–281.
- Henkel, K.O., Gerber, T., Lenz, S., Gundlach, K.K.H. & Bienengraeber, V. (2006) Macroscopical, histological, and morphometric studies of porous bone-replacement materials in minipigs 8 months after implantation. Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endontology 102: 606–613.
- Herten, M., Rothamel, D., Schwarz, F., Friesen, K., Koegler, G. & Becker, J. (2009) Surface- and nonsurface-dependent in vitro effects of bone substitutes on cell viability. Clinical Oral Investigations 13: 149–155.
- Huh, J.Y., Choi, B.H., Kim, B.Y., Lee, S.H., Zhu, S.J. & Jung, J.H. (2005) Critical size defect in the canine mandible. Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endontology 100: 296–301.
- Jensen, S.S., Aaboe, M., Pinholt, E.M., Hjorting-Hansen, E., Melsen, F. & Ruyter, I.E. (1996) Tissue reaction and material characteristics of four bone substitutes. The International Journal of Oral & Maxillofacial Implants 11: 55–66.
- Kämmerer, P.W., Palarie, V., Schiegnitz, E., Nacu, V., Draenert, F.G. & Al-Nawas, B. (2013) Influence of a collagen membrane and recombinant platelet-derived growth factor on vertical bone augmentation in implant-fixed deproteinized bovine bone - animal pilot study. Clinical Oral Implants Research 24: 1222–1230.
- Khan, S.N., Cammisa, F.P., Jr, Sandhu, H.S., Diwan, A.D., Girardi, F.P. & Lane, J.M. (2005) The biology of bone grafting. The Journal of the American Academy of Orthopedic Surgeons 13: 77–86.
- Klein, M.O. & Al-Nawas, B. (2011) For which clinical indications in dental implantology is the use of bone substitute materials scientifically substantiated? Systematic review, consensus statement and recommendations of the 1st DGI Consensus Conference in September 2010, Aerzen, Germany. European Journal of Oral Implantology 4: 11–29.
- Klein, M.O., Kämmerer, P.W., Götz, H., Duschner, H. & Wagner, W. (2013) Long-term bony integration and resorption kinetics of a xenogeneic bone substitute after sinus floor augmentation: Histomorphometric analyses of human biopsy specimens. The International Journal of Periodontics & Restorative Dentistry 33: e101–e110.
- Klein, M.O., Kämmerer, P.W., Scholz, T., Moergel, M., Kirchmaier, C.M. & Al-Nawas, B. (2010) Modulation of platelet activation and initial cytokine release by alloplastic bone substitute materials. Clinical Oral Implants Research 21: 336–345.
- Kokubo, T., Kim, H.M. & Kawashita, M. (2003) Novel bioactive materials with different mechanical properties. Biomaterials 24: 2161–2175.
- Kruse, A., Jung, R.E., Nicholls, F., Zwahlen, R.A., Hammerle, C.H. & Weber, F.E. (2011) Bone regeneration in the presence of a synthetic hydroxyapatite/silica oxide-based and a xenogenic hydroxyapatite-based bone substitute material. Clinical Oral Implants Research 22: 506–511.
- Liu, Q., Douglas, T., Zamponi, C., Becker, S.T., Sherry, E., Sivananthan, S., Warnke, F., Wiltfang, J. & Warnke, P.H. (2011) Comparison of in vitro biocompatibility of NanoBone((R)) and BioOss((R)) for human osteoblasts. Clinical Oral Implants Research 22: 1259–1264.
- Ma, J.L., Pan, J.L., Tan, B.S. & Cui, F.Z. (2009) Determination of critical size defect of minipig mandible. Journal of Tissue Engineering and Regenerative Medicine 3: 615–622.
- Moller, B., Acil, Y., Birkenfeld, F., Behrens, E., Terheyden, H. & Wiltfang, J. (2014) Highly porous hydroxyapatite with and without local harvested bone in sinus floor augmentation: A histometric study in pigs. Clinical Oral Implants Research 25: 871–878.
- Orsini, G., Scarano, A., Degidi, M., Caputi, S., Iezzi, G. & Piattelli, A. (2007) Histological and ultrastructural evaluation of bone around Bio-Oss particles in sinus augmentation. Oral Diseases 13: 586–593.
- Peetz, M. (1997) Characterization of xenogeneic bone material. P.J. Boyne (ed) Osseous reconstruction of the maxilla and the mandible. Quintessence International 87-100.
- Punke, C., Zehlicke, T., Boltze, C. & Pau, H.W. (2008) Experimental studies on a new highly porous hydroxyapatite matrix for obliterating open mastoid cavities. Otology & Neurotology 29: 807–811.
- Punke, C., Zehlicke, T., Boltze, C. & Pau, H.W. (2009) Investigation of a new highly porous hydroxyapatite matrix for obliterating open mastoid cavities - application in guinea pigs bulla. Laryngo-Rhino-Otologie 88: 241–246.
- Ruehe, B., Niehues, S., Heberer, S. & Nelson, K. (2009) Miniature pigs as an animal model for implant research: Bone regeneration in critical-size defects. Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endontology 108: 699–706.
- Sartori, S., Silvestri, M., Forni, F., Icaro Cornaglia, A., Tesei, P. & Cattaneo, V. (2003) Ten-year follow-up in a maxillary sinus augmentation using anorganic bovine bone (Bio-Oss). A case report with histomorphometric evaluation. Clinical Oral Implants Research 14: 369–372.
- Schlegel, A.K. & Donath, K. (1998) BIO-OSS–a resorbable bone substitute? Journal of Long-Term Effects of Medical Implants 8: 201–209.
- Schlegel, K.A., Lang, F.J., Donath, K., Kulow, J.T. & Wiltfang, J. (2006) The monocortical critical size bone defect as an alternative experimental model in testing bone substitute materials. Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endontology 102: 7–13.
- Sen, M.K. & Miclau, T. (2007) Autologous iliac crest bone graft: Should it still be the gold standard for treating nonunions? Injury 38(Suppl. 1): S75–S80.
- Shakibaie, M.B. (2013) Comparison of the effectiveness of two different bone substitute materials for socket preservation after tooth extraction: A controlled clinical study. The International Journal of Periodontics & Restorative Dentistry 33: 223–228.
- Strietzel, F.P., Reichart, P.A. & Graf, H.L. (2007) Lateral alveolar ridge augmentation using a synthetic nano-crystalline hydroxyapatite bone substitution material (Ostim): Preliminary clinical and histological results. Clinical Oral Implants Research 18: 743–751.
- Tadic, D. & Epple, M. (2004) A thorough physicochemical characterisation of 14 calcium phosphate-based bone substitution materials in comparison to natural bone. Biomaterials 25: 987–994.
- Walter, P.V. (1821) Wiedereinheilung der bei der Trepanation ausgebohrten Knochenscheibe. Journal der Chirurgischen Augenheilkunde 2: 571.
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