New reconstructive and less invasive methods have been searched to optimize bone formation and osseointegration of dental implants in maxillary sinus augmentation.
Purpose:
The aim of the presented ovine split-mouth study was to compare bovine bone mineral (BBM) alone and in combination with mesenchymal stem cells (MSCs) regarding their potential in sinus augmentation.
Material and Methods:
Bilateral sinus floor augmentations were performed in six adult sheep. BBM and MSCs were placed into the test side and only BBM in the contra-lateral control side of each sheep. Animals were sacrificed after 8 and 16 weeks. Augmentation sites were analyzed by computed tomography, histology, and histomorphometry.
Results:
The initial volumes of both sides were similar and did not change significantly with time. A tight connection between the particles of BBM and the new bone was observed histologically. Bone formation was significantly (p = 0.027) faster by 49% in the test sides.
Conclusion:
The combination of BBM and MSCs accelerated new bone formation in this model of maxillary sinus augmentation. This could allow early placement of implants.
Get full access to this article
View all access options for this article.
References
1.
ThorwarthM., SrourS., FelszeghyE., KesslerP., Schultze-MosgauS., SchlegelK.A.Stability of autogenous bone grafts after sinus lift procedures: a comparative study between anterior and posterior aspects of the iliac crest and an intraoral donor site. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 100:278. 2005.
2.
BelotiM.M., MartinsW.Jr., XavierS.P., RosaA.L.In vitro osteogenesis induced by cells derived from sites submitted to sinus grafting with anorganic bovine bone. Clin Oral Implants Res, 19:48. 2008.
3.
FroumS.J., WallaceS.S., ChoS.C., ElianN., TarnowD.P.Histomorphometric comparison of a biphasic bone ceramic to anorganic bovine bone for sinus augmentation: 6- to 8-month postsurgical assessment of vital bone formation. A pilot study. Int J Periodontics Restorative Dent, 28:273. 2008.
4.
KirmeierR., PayerM., WehrschuetzM., JakseN., PlatzerS., LorenzoniM.Evaluation of three-dimensional changes after sinus floor augmentation with different grafting materials. Clin Oral Implants Res, 19:366. 2008.
5.
OhyaM., YamadaY., OzawaR., ItoK., TakahashiM., UedaM.Sinus floor elevation applied tissue-engineered bone. Comparative study between mesenchymal stem cells/platelet-rich plasma (PRP) and autogenous bone with PRP complexes in rabbits. Clin Oral Implants Res, 16:622. 2005.
6.
PieriF., LucarelliE., CorinaldesiG., IezziG., PiattelliA., GiardinoR., BassiM., DonatiD., MarchettiC.Mesenchymal stem cells and platelet-rich plasma enhance bone formation in sinus grafting: a histomorphometric study in minipigs. J Clin Periodontol, 35:539. 2008.
7.
UedaM., TohnaiI., NakaiH.Tissue engineering research in oral implant surgery. Artif Organs, 25:164. 2001.
8.
BoyneP.J., LillyL.C., MarxR.E., MoyP.K., NevinsM., SpagnoliD.B., TriplettR.G.De novo bone induction by recombinant human bone morphogenetic protein-2 (rhBMP-2) in maxillary sinus floor augmentation. J Oral Maxillofac Surg, 63:1693. 2005.
9.
WallaceS.S., FroumS.J.Effect of maxillary sinus augmentation on the survival of endosseous dental implants. A systematic review. Ann Periodontol, 8:328. 2003.
10.
Del FabbroM., TestoriT., FrancettiL., WeinsteinR.Systematic review of survival rates for implants placed in the grafted maxillary sinus. Int J Periodontics Restorative Dent, 24:565. 2004.
11.
AghalooT.L., MoyP.K.Which hard tissue augmentation techniques are the most successful in furnishing bony support for implant placement?Int J Oral Maxillofac Implants, 22,Suppl:49. 2007.
12.
TerheydenH., JepsenS., MollerB., TuckerM.M., RuegerD.C.Sinus floor augmentation with simultaneous placement of dental implants using a combination of deproteinized bone xenografts and recombinant human osteogenic protein-1. A histometric study in miniature pigs. Clin Oral Implants Res, 10:510. 1999.
13.
ThorwarthM., SchlegelK.A., WehrhanF., SrourS., Schultze-MosgauS.Acceleration of de novo bone formation following application of autogenous bone to particulated anorganic bovine material in vivo. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 101:309. 2006.
14.
SimunekA., KopeckaD., SomanathanR.V., PilathadkaS., BrazdaT.Deproteinized bovine bone versus beta-tricalcium phosphate in sinus augmentation surgery: a comparative histologic and histomorphometric study. Int J Oral Maxillofac Implants, 23:935. 2008.
15.
CordaroL., BosshardtD.D., PalattellaP., RaoW., SerinoG., ChiapascoM.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. 2008.
16.
ChoiK.S., KanJ.Y., BoyneP.J., GoodacreC.J., LozadaJ.L., RungcharassaengK.The effects of resorbable membrane on human maxillary sinus graft: a pilot study. Int J Oral Maxillofac Implants, 24:73. 2009.
17.
McAllisterB.S., HaghighatK., GonshorA.Histologic evaluation of a stem cell-based sinus-augmentation procedure. J Periodontol, 80:679. 2009.
18.
YamadaY., UedaM., HibiH., BabaS.A novel approach to periodontal tissue regeneration with mesenchymal stem cells and platelet-rich plasma using tissue engineering technology: a clinical case report. Int J Periodontics Restorative Dent, 26:363. 2006.
19.
PittengerM.F., MackayA.M., BeckS.C., JaiswalR.K., DouglasR., MoscaJ.D., MoormanM.A., SimonettiD.W., CraigS., MarshakD.R.Multilineage potential of adult human mesenchymal stem cells. Science, 284:143. 1999.
20.
HaasR., MailathG., DortbudakO., WatzekG.Bovine hydroxyapatite for maxillary sinus augmentation: analysis of interfacial bond strength of dental implants using pull-out tests. Clin Oral Implants Res, 9:117. 1998.
21.
PinheiroJ.C., BatesD.M.Mixed-Effects Models in S and S-PLUS. New York: Springer-Verlag, 2000.
22.
BatesD., ChambersJ.R: A Language and Environment for Statistical Computing. Vienna, Austria: R_Foundation_for_Statistical_Computing, 2009.
23.
RaghoebarG.M., BrouwerT.J., ReintsemaH., Van OortR.P.Augmentation of the maxillary sinus floor with autogenous bone for the placement of endosseous implants: a preliminary report. J Oral Maxillofac Surg, 51:1198. 1993discussion 203.
24.
BoyneP.J., JamesR.A.Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surg, 38:613. 1980.
25.
DamienC.J., ParsonsJ.R.Bone graft and bone graft substitutes: a review of current technology and applications. J Appl Biomater, 2:187. 1991.
26.
ChoukrounJ., SimonpieriA., Del CorsoM., MazorZ., SammartinoG., Dohan EhrenfestD.M.Controlling systematic perioperative anaerobic contamination during sinus-lift procedures by using metronidazole: an innovative approach. Implant Dent, 17:257. 2008.
27.
VelichN., NemethZ., TothC., SzaboG.Long-term results with different bone substitutes used for sinus floor elevation. J Craniofac Surg, 15:38. 2004.
28.
YoungerE.M., ChapmanM.W.Morbidity at bone graft donor sites. J Orthop Trauma, 3:192. 1989.
29.
SilvaF.M., CortezA.L., MoreiraR.W., MazzonettoR.Complications of intraoral donor site for bone grafting prior to implant placement. Implant Dent, 15:420. 2006.
30.
CricchioG., LundgrenS.Donor site morbidity in two different approaches to anterior iliac crest bone harvesting. Clin Implant Dent Relat Res, 5:161. 2003.
31.
ArringtonE.D., SmithW.J., ChambersH.G., BucknellA.L., DavinoN.A.Complications of iliac crest bone graft harvesting. Clin Orthop Relat Res, 329:300. 1996.
32.
LundgrenS., CricchioG., PalmaV.C., SalataL.A., SennerbyL.Sinus membrane elevation and simultaneous insertion of dental implants: a new surgical technique in maxillary sinus floor augmentation. Periodontol 2000, 47:193. 2008.
33.
SroujiS., KizhnerT., Ben DavidD., RiminucciM., BiancoP., LivneE.The Schneiderian membrane contains osteoprogenitor cells: in vivo and in vitro study. Calcif Tissue Int, 84:138. 2009.
34.
StevensonS., CunninghamN., TothJ., DavyD., ReddiA.H.The effect of osteogenin (a bone morphogenetic protein) on the formation of bone in orthotopic segmental defects in rats. J Bone Joint Surg Am, 76:1676. 1994.
35.
PlachokovaA.S., NikolidakisD., MulderJ., JansenJ.A., CreugersN.H.Effect of platelet-rich plasma on bone regeneration in dentistry: a systematic review. Clin Oral Implants Res, 19:539. 2008.
36.
ChoukrounJ., DissA., SimonpieriA., GirardM.O., SchoefflerC., DohanS.L., DohaneA.J.J., MouhyiJ., DohanD.M.Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part V: histologic evaluations of PRF effects on bone allograft maturation in sinus lift. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 101:299. 2006.
37.
KhojastehA., EslaminejadM.B., NazarianH.Mesenchymal stem cells enhance bone regeneration in rat calvarial critical size defects more than platelete-rich plasma. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 106:356. 2008discussion 63.
38.
YamadaY., BooJ.S., OzawaR., NagasakaT., OkazakiY., HataK., UedaM.Bone regeneration following injection of mesenchymal stem cells and fibrin glue with a biodegradable scaffold. J Craniomaxillofac Surg, 31:27. 2003.
39.
UedaM., YamadaY., KagamiH., HibiH.Injectable bone applied for ridge augmentation and dental implant placement: human progress study. Implant Dent, 17:82. 2008.
40.
KastenP., BeyenI., EgermannM., SudaA.J., MoghaddamA.A., ZimmermannG., LuginbühlR.Instant stem cell therapy: characterization and concentration of human mesenchymal stem cells in vitro. Eur Cell Mater, 16:47. 2008.
41.
SauerbierS., StrickerA., KuschnierzJ., BuehlerF., OshimaT., XavierS.P., SchmelzeisenR., GutwaldR.In vivo comparison of hard tissue regeneration with human mesenchymal stem cells processed with either the FICOLL- or the BMAC-Method. Tissue Eng Part C Methods, 2009[Epub ahead of print.]
42.
Hernandez-AlfaroF.M.C., OrozcoL., MarinosoM.L., RodriguezL., TorricoC., VidalP.O.B.G., HornbergerM., ArmstrongR.D., HockJ.M.Clinical feasibility study: the use of cultured autologous bone marrow–derived tissue repair cells (TRC) for maxillary sinus floor augmentation in edentulous humans. [database on the Internet]SEC, 2005[cited 21.12.2005].2005.http://shareholder.api.edgaronline.com/efx_dll/edgarpro.dll?FetchFilingRTF1?sessionid=A4rUHtxcOBEyN_d&ID=4085460&PageBreakStyleID=2
