Regenerative medicine provides different therapy alternatives alongside gold standard
autogenous grafts for the treatment of periodontal or peri-implant osseous
defects. Continuing progress in the field of alloplastic bone substitutes
has yielded promising solutions to the appropriate indications with the membrane
technique either alone or in combination with enamel matrix derivatives.
Their clinical outcomes, however, still require critical discussion

Bayerlein, T.

Bienengräber, V.

Gedrange, T.

Mack, F.

Mundt, T.

Proff, P.

English

Via Medica Journals

Folia Morphol. Vol. 65, No. 1, pp. 66–69Copyright © 2006 Via MedicaISSN 0015–5659www.fm.viamedica.plT E C H N I C A L   N O T E66Address for correspondence: Dr. T. Bayerlein, Department of Orthodontics, Ernst Moritz Arndt University Greifswald, Rotgerberstr. 8,D-17487 Greifswald, Germany, tel: 0049 3834 867110, fax: 0049 3834 867107, e-mail: thomas.bayerlein@gmx.deBone graft substitutes in periodontaland peri-implant bone regenerationT. Bayerlein1, T. Mundt2, F. Mack2, V. Bienengräber3, P. Proff1, T. Gedrange11Clinic for Orthodontics and Preventive and Paediatric Dentistry, University of Greifswald Dental School,Greifswald, Germany2Clinic for Prosthodontics, Ernst Moritz Arndt University, Greifswald, Germany3Clinic for Cranio-Maxillofacial and Plastic Surgery, University of Rostock, Germany[Received 21 December 2005; Accepted 8 February 2006]Regenerative medicine provides different therapy alternatives alongside gold stan-dard autogenous grafts for the treatment of periodontal or peri-implant os-seous defects. Continuing progress in the field of alloplastic bone substituteshas yielded promising solutions to the appropriate indications with the mem-brane technique either alone or in combination with enamel matrix derivatives.Their clinical outcomes, however, still require critical discussion.Key words: bone graft substitutes, bone regeneration,periodontology, implantologyINTRODUCTIONFor over two decades regenerative therapy hasbeen finding its way into the disciplines of period-ontology and implantology. Bone graft substitutesare used for the periodontal reconstruction of sup-portive tissue and for implantological bone augmen-tation and therapy of peri-implant lesions, thus pro-viding an alternative to autologous bone grafts,which require an intraoral or extraoral second entry,depending on the indication and quantity needed.The development of biological-alloplastic osteocon-ductive bone reconstruction materials, which prima-rily aim at bony defect regeneration not only in phys-ical but also in biological terms, has steadily gainedimportance during recent years [7, 13, 15]. Besidethese alloplastic bone substitutes, primarily used forimplant-supporting therapy, the scope of the mate-rials used in periodontal regenerative therapy hasbeen broadened by membrane systems used accord-ing to the principles of guided tissue regeneration(GTR) and the application of enamel matrix deriva-tives (EMD).REGENERATIVE TREATMENTOF PERIODONTAL DEFECTSThe objective of periodontal therapy is a signifi-cant reduction in pocket depth and a gain of clinicalattachment, with treatment mainly including mechan-ical debridement of root and tooth surfaces (Fig. 1).Large defects or unfavourable pocket configurations,where complete healing is not achieved by mechan-ical debridement, may lend themselves to defect fill-ing, not only in order to achieve physiologicalFigure 1. A. X-ray presentation of periodontal bone defect 34and 36 with loss of tooth 35; B. Periodontal bone defect with pe-riodontal testing probe.A B67T. Bayerlein et al., Bone graft substitutes in periodontal and peri-implant bone regenerationbone morphology but also to improve the healingprospects of the tooth root in the alveolus [11]. Be-side the initially exclusive application of barrier mem-branes, bone grafts or bone substitutes have beenused more often (Fig. 2).BONE GRAFTS AND BONE SUBSTITUTESLost bone may be replaced by autogenous, al-logenous or xenogenous bone grafts or, alterna-tively, treated using alloplastic bone substitutes.Good results in the treatment of periodontal boneloss have been obtained using bone grafts. Bothautogenous (formed from a natural part of thebody) or allogenous (foreign to the body) graftsare of human origin by definition. Normally the chinarea, the tuber region and the toothless jaw seg-ments serve as donor regions. In the treatment ofperiodontal osseous defects such intraoral bonetransplantation, leading to formation of new ce-mentum, periodontal ligament and alveolar boneis, therefore, superior to extraoral transplantation(e.g. iliac crest) with the increased risk of ankylosisand root resorption. However, the quantity of avail-able bone is per se limited, which makes extraoralbone harvesting inevitable in severe, albeit rare,cases of bone loss. Generally, autogenous bonegrafting in intrabony alveolar defects yields a clini-cal defect filling of 25 to 50% [3].Allogenous bone is produced from long tubularbones of multi-organ donors. In contrast to autoge-nous bone grafts, the demineralised freeze-driedbone allografts (DFDBA) are harvested without theburden of a second surgical entry and are availablein an unlimited quantity. A disadvantage is the po-tential danger of a virus infection, although the risk ofdisease transmission is estimated at only 1:1 million to1:8 million, depending on the tissue preparation [11].Xenogenous bone grafts (e.g. Bio-Oss®) have longbeen used in the treatment of periodontal bone de-fects. These materials are produced from animal boneand cannot be used until they have undergone suf-ficient sterilisation and deproteinisation. Thermical-ly (> 1.200 degrees) and chemically treated bovinebone has elastic modules similar to intact bone andis available in huge quantities. However, problemsremain regarding the immunological situation, theresidual infection risk and patient acceptance.Many animal experiments and patient studiesshow that periodontal regeneration occurs after xe-nogenous bone grafting [2, 9]. Regenerative resultswere enhanced by improved wound management(application of collagen membranes) [8] (Fig. 3).New-generation alloplastic bone substitutes onthe basis of anorganic bone mineral-related calci-um phosphate ceramics (a-tricalcium phosphate,b-tricalcium phosphate and hydroxyapatite) showthe best osteoconductive properties with respectto the desired bone reconstructive function. Theyare used for critical defect filling with increasingclinical success.The outcome of periodontal supportive tissuereconstruction depends upon defect configurationas much as upon the material applied. Narrow three-walled pockets represent the best conditions for vi-tal preservation and substitution with least risk ofinfection [11]. a- and b-tricalcium phosphate (TCP)are produced similarly to the synthetic hydroxyap-atite ceramics (HA ceramics), although they displaydifferent resorption properties. Within the bodya-TCP partially or completely hydrolyses to hy-droxyapatite and is, therefore, hardly degradablelike the latter. The novel nanoporous hydroxyapa-tites, however, promise a distinctly improved resorp-tion behaviour supposed to correspond to that ofb-tricalcium phosphates (e.g. Cerasorb®, Curasan-Pharma GmbH, Kleinostheim, Germany) which aredegraded almost completely. However, the use ofb-tricalcium phosphate in the treatment of perio-dontal bony defects has been critically discussed inthe literature [12].Figure 2. A. Periodontal bone loss (sketch); B. Periodontal boneloss with application of bone substitute.BAFigure 3. A. Periodontal bone loss with pronounced bone defect;B. Bone defect filled up with bone substitute.BA68Folia Morphol., 2006, Vol. 65, No. 1Since 1989 coralline calcium carbonate (e.g. Bio-coral®, Inoteb, B.P. Saint-Gonnery, France) as a pro-tein-free and sterilised natural coral skeleton has beenapproved for application in humans. Mainly afterimplantation of this material in the mandible, thezygomatic bone and the frontal calvarium, healingproceeds without problems [14]. The absence ofspecific proteins minimises the risk of immunologi-cal reactions. In the treatment of periodontal bonydefects, however, the use of coralline bone substi-tutes does not yield the desired outcome.MEMBRANE APPLICATIONAnother treatment approach for periodontal os-seous defects utilises the self-healing effect of bone.This method aims to restore the lost periodontalstructures by a differentiated tissue response and isreferred to as “guided tissue regeneration” (GTR)using resorbable or non-resorbable membranes. Thisprinciple implies the creation of a secluded hollowspace, in which bone tissue regenerates but gingivalconnective tissue is prevented from growing. Thehollow space is filled with bone, bone reconstructivematerial or a mixture of both. Subsequently, a slowlyresorbable membrane is inserted as a physical barri-er. In consequence, desmodontal cells are the firstto form on the root surface of the tooth. These newdesmodontal structures then coalesce with the gin-gival connective tissue, thus leading to eliminationof the periodontal pocket.The use of resorbable membranes involves vari-ous polylactides and copolymers of polylactides/polyglycolides, while filter membranes and polytet-rafluorethylene (Teflon) have been successfully usedas non-resorbable materials. We have to consider,however, that a surgical re-entry is required for theremoval of non-resorbable membranes. The use ofmembranes permits combination with bone graftsor bone substitute materials.ENAMEL MATRIX DERIVATIVESStudies on tooth development conducted byHammarström in 1997 [5] showed that acellular ce-mentum is formed as soon as dental follicle cellscome into contact with an endogenous or exoge-nous enamel matrix. On the basis of these findingsattempts have been made to integrate enamel ma-trix proteins into periodontal regenerative therapyas a possible treatment alternative. The applicationof EMDOGAIN® (BIORA AB, Malmö, Sweden), a hy-drophobe mixture of enamel matrix proteins pro-duced from the tooth germs of young pigs, to thedebrided root surface aims to mimic the cell-matrixinteraction of embryogenesis with the associatedformation of acellular cementum, which plays a keyrole in the periodontal regeneration of intrabonydefects and, therefore, is supposed to improve thelatter (Fig. 4).Numerous studies, such as that by Heijl et al. [6],who applied EMDOGAIN® to infra-alveolar bonepockets and subsequently observed the formationof new cementum, periodontal ligament, and a 66%defect filling with new bone after 36 months, ap-pear to prove the effectiveness of this therapy con-cept.However, the use of EMDOGAIN®, which is com-posed of purified amelogenins, has the disadvan-tages that it can be used only in existing periodontalbone defects and not in implantology and that itseffects are not fully predictable [13].PERI-IMPLANT BONE REGENERATIONIn the field of implantology a deficient bone sup-ply in the implantation area on the one hand anda loss of peri-implant bone as a result of peri-im-plantitis on the other hand are often a great chal-lenge to the dental practitioner. Numerous augmen-tative procedures with their respective advantagesand disadvantages as mentioned above with respectto periodontal regenerative therapy are also utilisedfor peri-implant bone regeneration. Research and fur-ther development of bioceramic bone substitutematerials on a calcium phosphate basis from a merely“bridging” to a “bone-reconstructive” function turnsthose materials into an applicable alternative for therespective indications.Particularly in elderly prosthodontic patients, theclinician faces a reduced bone supply as a result ofFigure 4. A. Intrabony defect before treatment; B. Periodontalregeneration of intrabony defect after treatment with EnamelMatrix Derivatives.A B69T. Bayerlein et al., Bone graft substitutes in periodontal and peri-implant bone regenerationprogressive atrophy of the alveolar ridge. As an ex-ample, Tiolox implants (Tiolox, Implants GmbH, Den-taurum Company) are demonstrated in regions 43,44, 46, and 47 with vestibular bone deficit after im-plantation. The defects have been covered using bonegrafts, which were harvested during preparation ofthe implant bed.Additionally, Biogran (Fa. 3i) was applied in thetwo distal implants. The relatively large augmenta-tion areas were covered by a titan mesh, Tiomesh(Tiolox Implants GmbH, Dentaurum Company, Isprin-gen) for material fixation. The titan mesh was fixedto the implant by means of the cover screw (Fig. 5).In the regenerative therapy of multi-factorial fun-nel-shaped and slit-shaped peri-implant defects withprogressive bone resorption both the membranetechnique associated with frequent premature mem-brane exposure [4] and the use of bone substitutes [10]are a subject of controversy. In contrast, defect fill-ing using autogenous bone grafts without mem-brane coverage yields far better results [1].PROSPECTSAs well as the integration of enamel matrix de-rivatives into surgical periodontal therapy as a novelregenerative technique the application of “tissueengineering” from patient cells also permits theproduction of very well tolerated tissue transplants.3D cultivation of human mesenchymal stem cells andosteogenous differentiation for bone tissue produc-tion are already performed in many laboratories.However, a large-scale clinical application of “tissueengineering” in the treatment of periodontal bonedefects is not yet possible.In the near future industrially manufactured bio-materials are likely to be applied in combination withlaboratory-grown cells.REFERENCES1. Behneke A, Behneke N, d’Hoedt B (2000) Treatmentof peri-implantitis defects with autogenous bonegrafts: six-month to 3-year results of a prospectivestudy in 17 patients. Int J Oral Maxillofac Implants,15: 125–138.2. Camelo M, Nevins ML, Schenk RK, Simion M, Rasperini G,Lynch SE, Nevins M (1998) Clinical, radiographic, andhistologic evaluation of human periodontal defectstreated with Bio-Oss and Bio-Gide. Int J PeriodonticsRestorative Dent, 18: 321–331.3. Ehmke B, Flemmig TF (1999) Knochen und Knochen-ersatzmaterialien zur parodontalen Regenrationen.Wissenschaftliche Stehlungsnahme der Deutsche Ge-sellschaft für Zahn-, Mund und Kieferheilkunde.4. Haas R, Baron M, Dortbudak O, Watzek G (2000) Le-thal photosensitization, autogenous bone, and e-PTFEmembrane for the treatment of peri-implantitis: pre-liminary results. Int J Oral Maxillofac Implants, 15:374–382.5. Hammerström L (1997) Enamel matrix, cementumdevelopment and regeneration. J Clin Periodontol, 24:658–668.6. Heijl L, Helden G, Svardstrom G, Ostgren A (1997)Enamel matrix derivate (EMDOGAIN®) in the treatmentof intrabony periodontal defects. J Clin Periodontol,24: 705–714.7. Horch HH, Sader R, Kolk A (2004) Synthetische, phasen-reine Beta-Trikalziumphosphat-Keramik (Cerasorb) zurKnochenregeneration bei der rekonstruktiven Chirugieder Kiefer-Eine klinische Langzeitstudie mit Litera-turübersicht. Deutsche Zahnärztliche Zeitschrift, 59:680–686.8. Mellonig JT (2000) Human histologic evaluation ofa bovine-derived bone xenograft in the treatment ofperiodontal osseous defects. Int J Periodontics Resto-rative Dent, 20: 19–29.9. Nevins ML, Camelo M, Rebaudi A, Lynch SE, Nevins M(2005) Three-dimensional micro-computed tomo-graphic evaluation of periodontal regeneration: a hu-man report of intrabony defects treated with Bio-Oss collagen. Int J Periodontics Restorative Dent, 25:365–373.10. Nociti FH Jr, Machado MA, Stefani CM, Sallum EA(2001) Absorbable versus nonabsorbable mem-branes and bone grafts in the treatment of ligature--induced peri-implantitis defects in dogs: a histomet-ric investigation. Int J Oral Maxillofac Implants, 5:646–652.11. Schwenzer N, Ehrenfeld M (2000) Zahn-Mund-Kiefer-Heilkunde. Lehrbuch zur Aus- und Weiterbildung Bd.1-3, 3. Aufl. G. Thieme Verlag, New York.12. Sculean A, Willershausen B (2004) Regenerative paro-dontaltherapie. Qintessenz, 55: 491–499.13. Siervo S, Coraini C, Siervo P, Giardini R (2001) Cer-sorb® und PRP in der regenerativen parodontalen undimplantatunterstützten Therapie. Implantologie J, 6:49–58.14. Soost F (1996) Biocoral — an alternative bone substi-tute. Chirurg, 67: 1193–1196.15. Wolff KD, Swaid S, Nolte D, Bockmann RA, Holzle F,Muller-Mai C (2004) Degradable injectable bone cementin maxillofacial surgery: indications and clinical experi-ence in 27 patients. J Cranio-Maxillofac Surg, 32: 71–79.Figure 5. Bone deficit after implantation. Application of a bonechipping/bone substitute mix in the defect region covered bya titan mesh.

Bone graft substitutes in periodontal and peri-implant bone regeneration

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Bone graft substitutes in periodontal and peri-implant bone regeneration

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