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Tissue reactions after simultaneous alveolar ridge augmentation with biphasic calcium phosphate and implant insertion—histological and immunohistochemical evaluation in humans

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Abstract

Objectives

Simultaneous lateral augmentation and implant placement is considered as standard procedure in deficient edentulous ridges in oral implantology. Histological studies monitoring osteogenesis after application of alloplastic bone substitutes in humans are scarce. Bone formation upon simultaneous augmentation with biphasic calcium phosphate (BCP) and implantation was histologically investigated after 6 months in situ. The results of this secondary analysis are reported tempting to ascribe specific observations to uneventful submerged healing or compromised healing of soft tissues including occurrence of dehiscences and premature graft exposure.

Materials and methods

Histology of biopsies from lateral, crestal bone augmentations using alloplastic BCP comprising seven sites with compromised, prematurely exposed healing and six sites with uneventful submerged healing was investigated for expression of osteogenic, osteoclastogenic, and angiogenic differentiation markers.

Results

Histology revealed alkaline phosphatase (ALP)-positive osteoblasts and immunoreactivity for osteogenic markers osteocalcin and collagen type I in biopsies with submerged healing, while inflammatory infiltrates and accumulations of multinucleated giant cells around BCP granules were observed in compromised sites. All specimens presented adequate vessel density. Multinucleated giant cells showed inconsistent staining for the osteoclast marker tartrate-resistant acid phosphatase (TRAP).

Conclusions

The histological findings of this study indicate an osteoconductive nature of the BCP applied. Premature exposure of the bone substitute reduced new bone formation and may bear a risk for inflammatory and foreign body reactions.

Clinical relevance

A predictable appositional bone formation in simultaneously augmented sites using BCP is linked to an uneventful healing process.

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References

  1. Jensen SS, Terheyden H (2009) Bone augmentation procedures in localized defects in the alveolar ridge: clinical results with different bone grafts and bone-substitute materials. Int J Oral Maxillofac Implants 24(Suppl):218–236

    PubMed  Google Scholar 

  2. Donos N, Mardas N, Chadha V (2008) Clinical outcomes of implants following lateral bone augmentation: systematic assessment of available options (barrier membranes, bone grafts, split osteotomy). J Clin Periodontol 35:173–202

    Article  PubMed  Google Scholar 

  3. Retzepi M, Donos N (2010) Guided bone regeneration: biological principle and therapeutic applications. Clin Oral Implants Res 21:567–576

    Article  PubMed  Google Scholar 

  4. Kolk A, Handschel J, Drescher W, Rothamel D, Kloss F, Blessmann M, Heiland M, Wolff KD, Smeets R (2012) Current trends and future perspectives of bone substitute materials—from space holders to innovative biomaterials. J Craniomaxillofac Surg 40:706–718

    Article  PubMed  Google Scholar 

  5. Tal H, Artzi Z, Kolerman R, Beitlitum I, Goshen G (2012) Augmentation and preservation of the alveolar process and alveolar ridge of bone. Bone Regeneration, InTech Rijeka, pp 139–184

    Google Scholar 

  6. Cordaro L, Bosshardt DD, Palattella P, Rao W, Serino G, Chiapasco M (2008) Maxillary sinus grafting with Bio-Oss or Straumann Bone Ceramic: histomorphometric results from a randomized controlled multicenter clinical trial. Clin Oral Implants Res 19:796–803

    Article  PubMed  Google Scholar 

  7. Artzi Z, Kozlovsky A, Nemcovsky CE, 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. J Clin Periodontol 32:193–199

    Article  PubMed  Google Scholar 

  8. Schmitt CM, Doering H, Schmidt T, Lutz R, Neukam FW, Schlegel KA (2013) Histological results after maxillary sinus augmentation with Straumann®, BoneCeramic, Bio-Oss®, Puros®, and autologous bone. A randomized controlled clinical trial. Clin Oral Implants Res 24:576–585

    Article  PubMed  Google Scholar 

  9. Becker J, Al-Nawas B, Klein MO, Schliephake H, Terheyden H, Schwarz F (2009) Use of a new cross-linked collagen membrane for the treatment of dehiscence-type defects at titanium implants: a prospective, randomized-controlled double-blinded clinical multicenter study. Clin Oral Implants Res 20:742–749

    Article  PubMed  Google Scholar 

  10. Moses O, Pitaru S, Artzi Z, Nemcovsky CE (2005) Healing of dehiscence-type defects in implants placed together with different barrier membranes: a comparative clinical study. Clin Oral Implants Res 16:210–219

    Article  PubMed  Google Scholar 

  11. Schwarz F, Hegewald A, Sahm N, Becker J (2013) Long-term follow-up of simultaneous guided bone regeneration using native and cross-linked collagen membranes over 6 years. Clin Oral Implants Res. doi:10.1111/clr.12220

    Google Scholar 

  12. Friedmann A, Gissel K, Soudan M, Kleber BM, Pitaru S, Dietrich T (2011) Randomized controlled trial on lateral augmentation using two collagen membranes: morphometric results on mineralized tissue compound. J Clin Periodontol 38:677–685

    Article  PubMed  Google Scholar 

  13. Friedmann A, Dard M, Kleber BM, Bernimoulin JP, Bosshardt DD (2009) Ridge augmentation and maxillary sinus grafting with a biphasic calcium phosphate: histologic and histomorphometric observations. Clin Oral Implants Res 20:708–714

    Article  PubMed  Google Scholar 

  14. Jung RE, Windisch SI, Eggenschwiler AM, Thoma DS, Weber FE, Hammerle CH (2009) A randomized-controlled clinical trial evaluating clinical and radiological outcomes after 3 and 5 years of dental implants placed in bone regenerated by means of GBR techniques with or without the addition of BMP-2. Clin Oral Implants Res 20:660–666

    Article  PubMed  Google Scholar 

  15. Götz W, Gerber T, Michel B, Lossdörfer S, Henkel KO, Heinemann F (2008) Immunohistochemical characterization of nanocrystalline hydroxyapatite silica gel (NanoBone(r)) osteogenesis: a study on biopsies from human jaws. Clin Oral Implants Res 19:1016–1026

    Article  PubMed  Google Scholar 

  16. Frenken JW, Bouwman WF, Bravenboer N, Zijderveld SA, Schulten EA, ten Bruggenkate CM (2010) The use of Straumann Bone Ceramic in a maxillary sinus floor elevation procedure: a clinical, radiological, histological and histomorphometric evaluation with a 6-month healing period. Clin Oral Implants Res 21:201–208

    Article  PubMed  Google Scholar 

  17. Chan RC, Marino V, Bartold PM (2012) The effect of Emdogain and platelet-derived growth factor on the osteoinductive potential of hydroxyapatite tricalcium phosphate. Clin Oral Investig 16:1217–1227

    Article  PubMed  Google Scholar 

  18. Mrozik KM, Gronthos S, Menicanin D, Marino V, Bartold PM (2012) Effect of coating Straumann Bone Ceramic with Emdogain on mesenchymal stromal cell hard tissue formation. Clin Oral Investig 16:867–878

    Article  PubMed  Google Scholar 

  19. Mardas N, Chadha V, Donos N (2010) Alveolar ridge preservation with guided bone regeneration and a synthetic bone substitute or a bovine-derived xenograft: a randomized, controlled clinical trial. Clin Oral Implants Res 21:688–698

    Article  PubMed  Google Scholar 

  20. Iezzi G, Degidi M, Piattelli A, Mangano C, Scarano A, Shibli JA, Perrotti V (2012) Comparative histological results of different biomaterials used in sinus augmentation procedures: a human study at 6 months. Clin Oral Implants Res 23:1369–1376

    Article  PubMed  Google Scholar 

  21. Boyan BD, Bonewald LF, Paschalis EP, Lohmann CH, Rosser J, Cochran DL, Dean DD, Schwartz Z, Boskey AL (2002) Osteoblast-mediated mineral deposition in culture is dependent on surface microtopography. Calcif Tissue Int 71:519–529

    Article  PubMed  Google Scholar 

  22. Knabe C, Koch C, Rack A, Stiller M (2008) Effect of beta-tricalcium phosphate particles with varying porosity on osteogenesis after sinus floor augmentation in humans. Biomaterials 29:2249–2258

    Article  PubMed  Google Scholar 

  23. de Lange GL, Overman JR, Farré-Guasch E, Korstjens CM, Hartman B, Langenbach GE, Van Duin MA, Klein-Nulend J (2014) A histomorphometric and micro-computed tomography study of bone regeneration in the maxillary sinus comparing biphasic calcium phosphate and deproteinized cancellous bovine bone in a human split-mouth model. Oral Surg Oral Med Oral Pathol Oral Radiol 117:8–22

    Article  PubMed  Google Scholar 

  24. Koerdt S, Siebers J, Bloch W, Ristow O, Kuebler AC, Reuther T (2013) Immunohistochemial study on the expression of von Willebrand factor (vWF) after onlay autogenous iliac grafts for lateral alveolar ridge augmentation. Head Face Med 9:40

    Article  PubMed Central  PubMed  Google Scholar 

  25. Götz W, Reichert C, Canullo L, Jäger A, Heinemann F (2012) Coupling of osteogenesis and angiogenesis in bone substitute healing—a brief overview. Ann Anat 194:171–173

    Article  PubMed  Google Scholar 

  26. Hammerle CH, Lang NP (2001) Single stage surgery combining transmucosal implant placement with guided bone regeneration and bioresorbable materials. Clin Oral Implants Res 12:9–18

    Article  PubMed  Google Scholar 

  27. Anderson JM, Rodriguez A, Chang DT (2008) Foreign body reaction to biomaterials. Semin Immunol 20:86–100

    Article  PubMed Central  PubMed  Google Scholar 

  28. Chappard D, Guillaume B, Mallet R, Pascaretti-Grizon F, Baslé MF, Libouban H (2010) Sinus lift augmentation and ß-TCP: a microCT and histological analysis on human bone biopsies. Micron 41:321–326

    Article  PubMed  Google Scholar 

  29. Kucera T, Sponer P, Urban K, Kohout A (2013) Histological assessment of tissue from large human bone defects repaired with ß-tricalcium phosphate. Eur J Orthop Surg Traumatol In press.

  30. Ghanaati S, Barbeck M, Ort C, Willershausen I, Thimm BW, Hoffmann C, Rasic A, Sader RA, Unger RE, Peters F, Kirckpatrick CJ (2010) Influence of ß-tricalcium phosphate granule size and morphology on tissue reaction in vivo. Acta Biomater 6:4476–4487

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Mrs. Inka Müller-Bay for technical assistance.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Periodontology, School of Dentistry, Faculty of Health, Witten-Herdecke University, Witten, Germany

    Anton Friedmann & Kirsten Gissel

  2. Department of Orthodontics, University of Bonn, Bonn, Germany

    Anna Konermann

  3. Department of Orthodontics, Oral Biology Laboratory, University of Bonn, Bonn, Germany

    Werner Götz

Authors
  1. Anton Friedmann
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  2. Kirsten Gissel
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  3. Anna Konermann
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  4. Werner Götz
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Corresponding author

Correspondence to Anna Konermann.

Additional information

Anton Friedmann and Kirsten Gissel contributed equally to this work.

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Friedmann, A., Gissel, K., Konermann, A. et al. Tissue reactions after simultaneous alveolar ridge augmentation with biphasic calcium phosphate and implant insertion—histological and immunohistochemical evaluation in humans. Clin Oral Invest 19, 1595–1603 (2015). https://doi.org/10.1007/s00784-014-1385-0

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  • DOI: https://doi.org/10.1007/s00784-014-1385-0

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