Skip to main content

Advertisement

SpringerLink
Log in

Influence of different carrier materials on biphasic calcium phosphate induced bone regeneration

  • Original Article
  • Published:
Clinical Oral Investigations Aims and scope Submit manuscript

Abstract

Objectives

Biphasic calcium phosphate (BCP) is a bioceramic material successfully used in alloplastic bone augmentation. Despite many advantages, a disadvantage of BCP seems to be a difficult application and position instability. The aim of this study was to determine how different carrier materials influence BCP-induced quantitative and qualitative bone regeneration.

Materials and methods

A total of 70 critical size defects were set in the frontal bone of 14 domestic pigs (5 each) and filled randomly with either BCP alone (BCP), BCP in combination with nano-hydroxyapatite (BCP + NHA), BCP embedded in native porcine type I/III collagen blocks (BCP + C), autologous bone (AB), or were left empty (ED). Specimens were harvested after 4 and 8 weeks and were evaluated histologically as well as histomorphometrically.

Results

Significantly lowest rate of new bone formation was found in ED (p = < 0.001) and BCP + NHA groups (p = 0.05). After 8 weeks, the highest percentage of new bone formation was observed in the BCP + C group. Fibrous matrix was detected highest in BCP alone. The lowest residual bone substitute material was found in BCP + C after 8 weeks.

Conclusions

BCP-induced bone regeneration is indeed affected by different carrier types. Surface morphology and bioactive characteristics influence osseointegration and new bone formation in vivo. The combination of type I/III collagen seems most suitable for qualitative and quantitative bone regeneration.

Clinical relevance

Stabilization of granular bone substitutes using type I/III collagen might be an alternative to granulates alone, indicating excellent volume stability, satisfactory plasticity, and easy application.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Clementini M, Morlupi A, Canullo L, Agrestini C, Barlattani A (2012) Success rate of dental implants inserted in horizontal and vertical guided bone regenerated areas: a systematic review. Int J Oral Maxillofac Surg 41:847–852

    Article  Google Scholar 

  2. Zouhary KJ (2010) Bone graft harvesting from distant sites: concepts and techniques. Oral Maxillofac Surg Clin N Am 22:301–316. https://doi.org/10.1016/j.coms.2010.04.007

    Article  Google Scholar 

  3. Schorn L, Sproll C, Ommerborn M, Naujoks C, Kubler NR, Depprich R (2017) Vertical bone regeneration using rhBMP-2 and VEGF. Head Face Med 13:11. https://doi.org/10.1186/s13005-017-0146-0

    Article  PubMed  PubMed Central  Google Scholar 

  4. Hulbert S et al (1987) In: Vincenzini P (ed) High tech ceramics

    Google Scholar 

  5. Hench LL (1991) Bioceramics: from concept to clinic. J Am Ceram Soc 74. https://doi.org/10.1111/j.1151-2916.1991.tb07132.x

  6. Jeong J, Kim JH, Shim JH, Hwang NS, Heo CY (2019) Bioactive calcium phosphate materials and applications in bone regeneration. Biomat Res 23:4. https://doi.org/10.1186/s40824-018-0149-3

    Article  Google Scholar 

  7. Kanazawa T, Umegaki T, Monma H (1975) Apatites, new inorganic materials. Ceramics Japan 10

  8. Frank O (2002) Real-time quantitative RT-PCR analysis of human bone marrow stromal cells during osteogenic differentiation in vitro. J Cell Biochem 85. https://doi.org/10.1002/jcb.10174

  9. Orimo H (2010) The mechanism of mineralization and the role of alkaline phosphatase in health and disease. J Nippon Med Sch 77. https://doi.org/10.1272/jnms.77.4

  10. Shea JE, Miller SC (2005) Skeletal function and structure: implications for tissue-targeted therapeutics. Adv Drug Deliv Rev 57. https://doi.org/10.1016/j.addr.2004.12.017

  11. Whited BM (2006) Osteoblast response to zirconia-hybridized pyrophosphate-stabilized amorphous calcium phosphate. J Biomed Mater Res A 76. https://doi.org/10.1002/jbm.a.30573

  12. Liu D (2008) Activation of extracellular-signal regulated kinase (ERK1/2) by fluid shear is Ca2 + −and ATP-dependent in MC3T3-E1 osteoblasts. Bone 42. https://doi.org/10.1016/j.bone.2007.09.058

  13. Danciu TE (2003) Calcium regulates the PI3K-Akt pathway in stretched osteoblasts. FEBS Lett 536. https://doi.org/10.1016/S0014-5793(03)00055-3

  14. Khoshniat S (2011) The emergence of phosphate as a specific signaling molecule in bone and other cell types in mammals. Cell Mol Life Sci 68. https://doi.org/10.1007/s00018-010-0527-z

  15. Julien M (2009) Phosphate-dependent regulation of MGP in osteoblasts: role of ERK1/2 and Fra-1. J Bone Miner Res 24. https://doi.org/10.1359/jbmr.090508

  16. Mozar A (2008) High extracellular inorganic phosphate concentration inhibits RANK–RANKL signaling in osteoclast-like cells. J Cell Physiol 215. https://doi.org/10.1002/jcp.21283

  17. Ambard AJ, Mueninghoff L (2006) Calcium phosphate cement: review of mechanical and biological properties. J Prosthodont 15. https://doi.org/10.1111/j.1532-849X.2006.00129.x.

  18. Samavedi S, Whittington AR, Goldstein AS (2013) Calcium phosphate ceramics in bone tissue engineering: a review of properties and their influence on cell behavior. Acta Biomater 9. https://doi.org/10.1016/j.actbio.2013.06.014

  19. Arinzeh TL (2005) A comparative study of biphasic calcium phosphate ceramics for human mesenchymal stem-cell-induced bone formation. Biomaterials 26. https://doi.org/10.1016/j.biomaterials.2004.09.035

  20. He F (2016) Comparative study on in vivo response of porous calcium carbonate composite ceramic and biphasic calcium phosphate ceramic. Mater Sci Eng C 64. https://doi.org/10.1016/j.msec.2016.03.085

  21. Le Nihouannen D, Duval L, Lecomte A, Julien M, Guicheux J, Daculsi G, Layrolle P (2007) Interactions of total bone marrow cells with increasing quantities of macroporous calcium phosphate ceramic granules. J Mater Sci Mater Med 18:1983–1990. https://doi.org/10.1007/s10856-007-3098-2

    Article  PubMed  Google Scholar 

  22. Schwartz C, Liss P, Jacquemaire B, Lecestre P, Frayssinet P (1999) Biphasic synthetic bone substitute use in orthopaedic and trauma surgery: clinical, radiological and histological results. J Mater Sci Mater Med 10:821–825

    Article  Google Scholar 

  23. Schmitz JP, Hollinger JO (1986) The critical size defect as an experimental model for craniomandibulofacial nonunions. Clin Orthop Relat Res:299–308

  24. Fienitz T, Moses O, Klemm C, Happe A, Ferrari D, Kreppel M, Ormianer Z, Gal M, Rothamel D (2016) Histological and radiological evaluation of sintered and non-sintered deproteinized bovine bone substitute materials in sinus augmentation procedures. A prospective, randomized-controlled, clinical multicenter study. Clin Oral Investig. https://doi.org/10.1007/s00784-016-1829-9

  25. Fienitz T, Moses O, Klemm C, Happe A, Ferrari D, Kreppel M, Ormianer Z, Gal M, Rothamel D (2017) Histological and radiological evaluation of sintered and non-sintered deproteinized bovine bone substitute materials in sinus augmentation procedures. A prospective, randomized-controlled, clinical multicenter study. Clin Oral Investig 21:787–794. https://doi.org/10.1007/s00784-016-1829-9

    Article  PubMed  Google Scholar 

  26. Rothamel D, Schwarz F, Fienitz T, Smeets R, Dreiseidler T, Ritter L, Happe A, Zoller J (2012) Biocompatibility and biodegradation of a native porcine pericardium membrane: results of in vitro and in vivo examinations. Int J Oral Maxillofac Implants 27:146–154

    PubMed  Google Scholar 

  27. 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. J Oral Pathol 11:318–326

    Article  Google Scholar 

  28. Bighetti ACC, Cestari TM, Santos PS, Arantes RVN, Paini S, Assis GF, Costa BC, de Oliveira FA, Tokuhara CK, de Oliveira RC, Taga R (2020) In vitro and in vivo assessment of CaP materials for bone regenerative therapy. The role of multinucleated giant cells/osteoclasts in bone regeneration. J Biomed Mater Res B Appl Biomater 108:282–297. https://doi.org/10.1002/jbm.b.34388.

    Article  PubMed  Google Scholar 

  29. Klein M, Al-Nawas B (2011) For which clincal indications in dental implantology is the use of bone substitute materials scientifically substantiated? Eur J Oral Implantol 4:11–29

    Google Scholar 

  30. Fahmy RA, Mahmoud N, Soliman S, Nouh SR, Cunningham L, El-Ghannam A (2015) Acceleration of alveolar ridge augmentation using a low dose of recombinant human bone morphogenetic protein-2 loaded on a resorbable bioactive ceramic. J Oral Maxillofac Surg 73:2257–2272. https://doi.org/10.1016/j.joms.2015.07.004

    Article  PubMed  Google Scholar 

  31. Felice P, Marchetti C, Piattelli A, Pellegrino G, Checchi V, Worthington H, Esposito M (2008) Vertical ridge augmentation of the atrophic posterior mandible with interpositional block grafts: bone from the iliac crest versus bovine anorganic bone. Eur J Oral Implantol 1:183–198

    PubMed  Google Scholar 

  32. Troeltzsch M, Troeltzsch M, Kauffmann P, Gruber R, Brockmeyer P, Moser N, Rau A, Schliephake H (2016) Clinical efficacy of grafting materials in alveolar ridge augmentation: A systematic review. J Cranio-maxillo-facial Surg 44:1618–1629. https://doi.org/10.1016/j.jcms.2016.07.028

    Article  Google Scholar 

  33. Rothamel D, Neugebauer J, Lingohr T, Dreiseidler T, Ritter L, Zöller J (2009) Oberflächenstruktur, Biokompatibilität und Hartgewebsregeneration. Z Oral Implant:2–9

  34. Merten HA, Wiltfang J, Grohmann U, Hoenig JF (2001) Intraindividual comparative animal study of alpha- and beta-tricalcium phosphate degradation in conjunction with simultaneous insertion of dental implants. J Craniofac Surg 12:59–68

    Article  Google Scholar 

  35. Fujita R, Yokoyama A, Kawasaki T, Kohgo T (2003) Bone augmentation osteogenesis using hydroxyapatite and beta-tricalcium phosphate blocks. J Oral Maxillofac Surg 61:1045–1053

    Article  Google Scholar 

  36. LeGeros RZ, Lin S, Rohanizadeh R, Mijares D, LeGeros JP (2003) Biphasic calcium phosphate bioceramics: preparation, properties and applications. J Mat Sci Mat Med 14:201–209

    Article  Google Scholar 

  37. Jensen SS, 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. Clin Oral Implants Res 18:752–760. https://doi.org/10.1111/j.1600-0501.2007.01417.x

    Article  PubMed  Google Scholar 

  38. Giesenhagen B (2008) Die einzeitige vertikale Augmentation mit ringförmigen Knochentransplantaten. Z Zahnärztl Impl 24:129–132

    Google Scholar 

  39. Carrel JP, Wiskott A, Moussa M, Rieder P, Scherrer S, Durual S (2016) A 3D printed TCP/HA structure as a new osteoconductive scaffold for vertical bone augmentation. Clin Oral Implants Res 27:55–62. https://doi.org/10.1111/clr.12503

    Article  PubMed  Google Scholar 

  40. Cardaropoli G, Araujo M, Hayacibara R, Sukekava F, Lindhe J (2005) Healing of extraction sockets and surgically produced - augmented and non-augmented - defects in the alveolar ridge. An experimental study in the dog. J Clin Periodontol 32:435–440. https://doi.org/10.1111/j.1600-051X.2005.00692.x

    Article  PubMed  Google Scholar 

  41. Meyer U, Meyer T, Handschel J, Wiesmann HP (2009) Fundamentals of Tissue Engineering and Regenerative Medicine. Springer-Verlag, Heidelberg

    Book  Google Scholar 

  42. Mygind T (2007) Mesenchymal stem cell ingrowth and differentiation on coralline hydroxyapatite scaffolds. Biomaterials 28. https://doi.org/10.1016/j.biomaterials.2006.10.003

  43. Webster TJ et al (2000) Specific proteins mediate enhanced osteoblast adhesion on nanophase ceramics. J Biomed Mater Res: an official journal of the Society for Biomaterials, the Japanese Society for Biomaterials, and the Australian Society for Biomaterials and the Korean society for. Biomaterials 51:475–483

    Google Scholar 

  44. Deligianni DD (2000) Effect of surface roughness of hydroxyapatite on human bone marrow cell adhesion, proliferation, differentiation and detachment strength. Biomaterials 22. https://doi.org/10.1016/S0142-9612(00)00174-5

  45. Fellah BH, Gauthier O, Weiss P, Chappard D, Layrolle P (2008) Osteogenicity of biphasic calcium phosphate ceramics and bone autograft in a goat model. Biomaterials 29:1177–1188. https://doi.org/10.1016/j.biomaterials.2007.11.034

    Article  PubMed  Google Scholar 

  46. Chapman MW, Bucholz R, Cornell C (1997) Treatment of acute fractures with a collagen-calcium phosphate graft material. A randomized clinical trial. J Bone Joint Surg Am 79:495–502

    Article  Google Scholar 

  47. Thorwarth M, Schultze-Mosgau S, Kessler P, Wiltfang J, Schlegel KA (2005) Bone regeneration in osseous defects using a resorbable nanoparticular hydroxyapatite. J Oral Maxillofac Surg 63:1626–1633. https://doi.org/10.1016/j.joms.2005.06.010

    Article  PubMed  Google Scholar 

  48. Hu J, Zhou Y, Huang L, Liu J, Lu H (2014) Effect of nano-hydroxyapatite coating on the osteoinductivity of porous biphasic calcium phosphate ceramics. BMC Musculoskelet Disord 15:114. https://doi.org/10.1186/1471-2474-15-114

    Article  PubMed  PubMed Central  Google Scholar 

  49. 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. Clin Oral Investig 13:149–155. https://doi.org/10.1007/s00784-008-0214-8

    Article  PubMed  Google Scholar 

  50. Rothamel D, Schwarz F, Herten M, Berndsen K, Steigmann M, Neugebauer J, Becker J (2008) Vertical augmentation of the mandible using cortico-spongious xenoblocks. A histomorphometrical study in dogs. Schweiz Monatsschr Zahnmed 118:1162–1169

    PubMed  Google Scholar 

  51. Aloise AC, Pelegrine AA, Zimmermann A, de Mello EOR, Ferreira LM (2015) Repair of critical-size bone defects using bone marrow stem cells or autogenous bone with or without collagen membrane: a histomorphometric study in rabbit calvaria. Int J Oral Maxillofac Implants 30:208–215. https://doi.org/10.11607/jomi.4010

    Article  PubMed  Google Scholar 

  52. Paknejad M, Rokn AR, Yaghobee S, Moradinejad P, Heidari M, Mehrfard A (2014) Effects of two types of anorganic bovine bone on bone regeneration: a histological and histomorphometric study of rabbit calvaria. J Dentist (Tehran, Iran) 11:687–695

    Google Scholar 

  53. Hermansen K, Pedersen LE, Olesen HO (1986) The analgesic effect of buprenorphine, etorphine and pethidine in the pig: a randomized double blind cross-over study. Acta Pharmacol Toxicol (Copenh) 59:27–35. https://doi.org/10.1111/j.1600-0773.1986.tb00130.x.

    Article  Google Scholar 

  54. Papich MG (2008) An update on nonsteroidal anti-inflammatory drugs (NSAIDs) in small animals. Vet Clin North Am Small Anim Pract 38(1243-1266):vi. https://doi.org/10.1016/j.cvsm.2008.09.002

    Article  Google Scholar 

  55. Boshra V (2011) Evaluation of osteoporosis risk associated with chronic use of morphine, fentanyl and tramadol in adult female rats. Curr Drug Saf 6:159–163. https://doi.org/10.2174/157488611797579267

    Article  PubMed  Google Scholar 

  56. Coluzzi F, Pergolizzi J, Raffa RB, Mattia C (2015) The unsolved case of “bone-impairing analgesics”: the endocrine effects of opioids on bone metabolism. Ther Clin Risk Manag 11:515–523. https://doi.org/10.2147/TCRM.S79409.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Xu H, Shimizu Y, Asai S, Ooya K (2003) Experimental sinus grafting with the use of deproteinized bone particles of different sizes. Clin Oral Implants Res 14:548–555

    Article  Google Scholar 

Download references

Funding

The study was financially supported by Bego Implant Systems, Bremen, Germany.

Author information

Authors and Affiliations

  1. Department of Oral-, Maxillofacial and Facial Plastic Surgery, University Hospital Düsseldorf, Moorenstr. 5, Düsseldorf, Germany

    Lara Schorn, Julian Lommen & Daniel Rothamel

  2. Department of Oral-, Maxillofacial and Facial Plastic Surgery, Evangelisches Krankenhaus Bethesda, Ludwig-Weber-Straße 15, 41061, Mönchengladbach, Germany

    Tim Fienitz, Henrik Holtmann & Daniel Rothamel

  3. Department of Oral-, Maxillofacial and Facial Plastic Surgery, University Hospital of Cologne, Kerpener Str. 64, 50937, Cologne, Germany

    Maximilian F. Gerstenberg

  4. Center for Experimental Medicine, Faculty of Medicine and University Hospital Cologne, University of Cologne, Kerpener Str. 64, 50937, Cologne, Germany

    Anja Sterner-Kock & Alexandra C. Maul

Authors
  1. Lara Schorn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tim Fienitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maximilian F. Gerstenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anja Sterner-Kock
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexandra C. Maul
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Julian Lommen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Henrik Holtmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Daniel Rothamel
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

L.S. wrote the manuscript; T.F., M.G, A. S-K., and A. M. supervised and conducted the experiments and collected the data; J.L. and H.H. revised the manuscript critically; R. D. initiated the research and had the idea to publish this paper.

Corresponding author

Correspondence to Tim Fienitz.

Ethics declarations

Conflict of interest

The authors claim that Prof. Daniel Rothamel is a founder and shareholder of Botiss Biomaterials, Berlin, Germany, the manufacturer of biomaterials used in this study.

Ethical statements

This study has been approved by the state office for nature, environment, and consumer protection of North-Rhine Westphalia, Germany (LANUV NRW AZ 84-02.04.2011.A148). It complies with the ARRIVE guidelines for animal research.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(PDF 96 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schorn, L., Fienitz, T., Gerstenberg, M.F. et al. Influence of different carrier materials on biphasic calcium phosphate induced bone regeneration. Clin Oral Invest 25, 3729–3737 (2021). https://doi.org/10.1007/s00784-020-03700-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00784-020-03700-y

Keywords

Search

Navigation