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Clinical Oral Investigations

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01-09-2021 | Original Article

Guided bone regeneration simultaneous with implant placement using bovine-derived xenograft with and without liquid platelet-rich fibrin: a randomized controlled clinical trial

Authors: Gözde Işık, Meltem Özden Yüce, Nazan Koçak-Topbaş, Tayfun Günbay

Published in: Clinical Oral Investigations | Issue 9/2021

Abstract

Objective

To assess augmentation success after guided bone regeneration (GBR) carried out simultaneously with implant placement using bovine-derived xenograft alone and in combination with liquid platelet-rich fibrin (liquid-PRF).

Methods

This randomized controlled clinical trial was conducted on patients with horizontal bone deficiency in the posterior regions of the mandible. After implant placement, GBR procedures were randomly performed using liquid-PRF-enriched bovine-derived xenograft (for the test group) and with bovine-derived xenograft alone (for the control group). To assess the change in augmentation thickness, the primary outcome of the study, cone beam computed tomography was carried out at the implant sites on completion and 6 months after surgery. The secondary outcomes were marginal bone level and implant survival rate at prosthetic delivery and at 6 months, 1 year, and 2 years follow-up after loading. The significance level was set at p<0.05 for all analysis.

Results

Twenty patients with 50 implants were analyzed for the test group and 20 patients with 48 implants for the control group. At 6 months postoperatively, the mean values of augmentation thickness were 1.63 ± 0.21 mm, 2.59 ± 0.34 mm, and 3.11 ± 0.36 mm for the test group and 1.34 ± 0.14 mm, 2.49 ± 0.24 mm, and 2.97 ± 0.24 mm for the control group at 2 mm, 4 mm, and 6 mm below to the implant shoulder (p < 0.001, p = 0.007, and p = 0.036, respectively). The mean marginal bone loss was found to be less than 1 mm for both study groups during the 2 years of follow-up after prosthetic loading. Implant survival rate was 100% for both study groups.

Conclusion

Bovine-derived xenograft alone and in combination with liquid-PRF are both successful in achieving bone augmentation around the implants and produce a small change in marginal bone level and a high implant survival rate after loading.

Clinical relevance

There is a lack of evidence in the literature regarding the augmentation success of liquid-PRF used in combination with bone graft substitutes. This study indicates that liquid-PRF could be used as a supportive material with bovine-derived xenograft in GBR procedures carried out simultaneously with implant placement.

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Wessing B, Urban I, Montero E, Zechner W, Hof M, Alandez Chamorro J, Alandez Martin N, Polizzi G, Meloni S, Sanz M (2017) A multicenter randomized controlled clinical trial using a new resorbable non-cross-linked collagen membrane for guided bone regeneration at dehisced single implant sites: interim results of a bone augmentation procedure. Clin Oral Implants Res 28:e218–e226. https://doi.org/10.1111/clr.12995CrossRefPubMed

Khzam N, Arora H, Kim P, Fisher A, Mattheos N, Ivanovski S (2015) Systematic review of soft tissue alterations and aesthetic outcomes following immediate implant placement and restoration of single implants in the anterior maxilla. J Periodontol 86:1321–1330. https://doi.org/10.1902/jop.2015.150287CrossRefPubMed

Araújo MG, Lindhe J (2005) Dimensional ridge alterations following tooth extraction. An experimental study in the dog. J Clin Periodontol 32:21–218. https://doi.org/10.1111/j.1600-051X.2005.00642.xCrossRef

Cardaropoli G, Araújo M, Lindhe J (2003) Dynamics of bone tissue formation in tooth extraction sites. An experimental study in dogs. J Clin Periodontol 30:809–818. https://doi.org/10.1034/j.1600-051x.2003.00366.xCrossRefPubMed

Rocchietta I, Fontana F, Simion M (2008) Clinical outcomes of vertical bone augmentation to enable dental implant placement: a systematic review. J Clin Periodontol 35:203–215. https://doi.org/10.1111/j.1600-051X.2008.01271.xCrossRefPubMed

Checchi V, Gasparro R, Pistilli R, Canullo L, Felice P (2019) Clinical classification of bone augmentation procedure failures in the atrophic anterior maxillae: esthetic consequences and treatment options. BioMed Res Int 3:1–16. https://doi.org/10.1155/2019/4386709CrossRef

Cucchi A, Vignudelli E, Napolitano A, Corinaldesi G (2017) Evaluation of complication rates and vertical bone gain after guided bone regeneration with non-resorbable membranes versus titanium meshes and resorbable membranes. A randomized clinical trial. Clin Implant Dent Relat Res 19:821–832. https://doi.org/10.1111/cid.12520CrossRefPubMedPubMedCentral

Fontana F, Maschera E, Rocchietta I, Simion M (2011) Clinical classification of complications in guided bone regeneration procedures by means of a nonresorbable membrane. Int J Periodontics Restorative Dent 31:265–273PubMed

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. https://doi.org/10.1016/j.ijom.2012.03.016CrossRefPubMed

10.

Chiapasco M, Zaniboni M (2009) Clinical outcomes of GBR procedures to correct peri-implant dehiscences and fenestrations: a systematic review. Clin Oral Implants Res 20:113–123. https://doi.org/10.1111/j.1600-0501.2009.01781.xCrossRefPubMed

11.

Hämmerle CH, Jung RE, Feloutzis A (2002) A systematic review of the survival of implants in bone sites augmented with barrier membranes (guided bone regeneration) in partially edentulous patients. J Clin Periodontol 29:226–231. https://doi.org/10.1034/j.1600-051x.29.s3.14.xCrossRefPubMed

12.

Arunjaroensuk S, Panmekiate S, Pimkhaokham A (2018) The stability of augmented bone between two different membranes used for guided bone regeneration simultaneous with dental implant placement in the esthetic zone. Int J Oral Maxillofac Implants 33:206–216. https://doi.org/10.11607/jomi.5492CrossRefPubMed

13.

Jung RE, Herzog M, Wolleb K, Ramel CF, Thoma DS, Hammerle CHF (2017) A randomized controlled clinical trial comparing small buccal dehiscence defects around dental implants treated with guided bone regeneration or left for spontaneous healing. Clin Oral Implants Res 28:348–354. https://doi.org/10.1111/clr.12806CrossRefPubMed

14.

ArRejaie A, Al-Harbi F, Alagl A, Hassan K (2016) Platelet-rich plasma gel combined with bovine-derived xenograft for the treatment of dehiscence around immediately placed conventionally loaded dental implants in humans: cone beam computed tomography and three-dimensional image evaluation. Int J Oral Maxillofac Implants 31:431–438. https://doi.org/10.11607/jomi.3859CrossRefPubMed

15.

Temmerman A, Cortellini S, Van Dessel J, De Greef A, Jacobs R, Dhondt R (2020) Bovine-derived xenograft in combination with autogenous bone chips versus xenograft alone for the augmentation of bony dehiscences around oral implants: a randomized, controlled, split-mouth clinical trial. J Clin Periodontol 47:110–119CrossRef

16.

Papageorgiou SN, Papageorgiou PN, Deschner J, Götz W (2016) Comparative effectiveness of natural and synthetic bone grafts in oral and maxillofacial surgery prior to insertion of dental implants: systematic review and network meta-analysis of parallel and cluster randomized controlled trials. J Dent 48:1–8. https://doi.org/10.1016/j.jdent.2016.03.010CrossRefPubMed

17.

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 Craniomaxillofac Surg 44:1618–1629. https://doi.org/10.1016/j.jcms.2016.07.028CrossRefPubMed

18.

Dohan DM, Choukroun J, Diss A, Dohan SL, Dohan AJ, Mouhyi J, Gogly B (2006) Platelet-rich fibrin (prf): a second-generation platelet concentrate. Part II: platelet-related biologic features. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 101:e45–e50. https://doi.org/10.1016/j.tripleo.2005.07.009CrossRefPubMed

19.

Choukroun J, Diss A, Simonpieri A, Girard MO, Schoeffler C, Dohan SL, Dohan AJ, Mouhyi J, Dohan DM (2006) Platelet-rich fibrin (prf): a second-generation platelet concentrate. Part IV: clinical effects on tissue healing. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 101:e56–e60. https://doi.org/10.1016/j.tripleo.2005.07.011CrossRefPubMed

20.

Ghanaati S, Herrera-Vizcaino C, Al-Maawi S, Lorenz J, Miron RJ, Nelson K, Schwarz F, Choukroun J, Sader R (2018) Fifteen years of platelet rich fibrin (PRF) in dentistry and oromaxillofacial surgery: how high is the level of scientific evidence? J Oral Implantol 44:471–492. https://doi.org/10.1563/aaid-joi-D-17-00179CrossRefPubMed

21.

Strauss FJ, Nasirzade J, Kargarpoor Z, Stähli A, Gruber R (2020) Effect of platelet-rich fibrin on cell proliferation, migration, differentiation, inflammation, and osteoclastogenesis: a systematic review of in vitro studies. Clin Oral Investig 24:569–584. https://doi.org/10.1007/s00784-019-03156-9CrossRefPubMed

22.

Choukroun J, Ghanaati S (2018) Reduction of relative centrifugation force within PRF (platelet-rich-fibrin) concentrates advances patients’ own inflammatory cells and platelets: first introduction of the low speed centrifugation concept. Eur J Trauma Emerg Surg 44:87–95. https://doi.org/10.1007/s00068-017-0767-9CrossRefPubMed

23.

El-Baghdadi K, Kubesch A, Yu X, Al-Maawi S, Orlowska A, Dias A, Booms P, Dohle E, Sader R, Kirkpatrick J, Choukroun J, Ghanaati S (2019) Reduction of relative centrifugal forces increases growth factor release within solid platelet-rich-fibrin (PRF)-based matrices: a proof of concept of LSCC (low speed centrifugation concept). Eur J Trauma Emerg Surg 45:467–479. https://doi.org/10.1007/s00068-017-0785-7CrossRef

24.

Miron RJ, Fujioka-Kobayashi M, Hernandez M, Kandalam U, Zhang Y, Ghanaati S, Choukroun J (2017) Injectable platelet rich fibrin (i-prf): opportunities in regenerative dentistry? Clin Oral Investig 21:2619–2627. https://doi.org/10.1007/s00784-017-2063-9CrossRefPubMed

25.

Gülşen U, Dereci Ö (2019) Evaluation of new bone formation in sinus floor augmentation with injectable platelet-rich fibrin-soaked collagen plug: a pilot study. Implant Dent 28:220–225. https://doi.org/10.1097/ID.0000000000000883CrossRefPubMed

26.

Thanasrisuebwong P, Surarit R, Bencharit S, Ruangsawasdi N (2019) Influence of fractionation methods on physical and biological properties of injectable platelet-rich fibrin: an exploratory study. Int J Mol Sci 20:1657. https://doi.org/10.3390/ijms20071657CrossRefPubMedCentral

27.

Valladão CAA, Monteiro MF, Joly JC (2020) Guided bone regeneration in staged vertical and horizontal bone augmentation using platelet-rich fibrin associated with bone grafts: a retrospective clinical study. Int J Implant Dent 6:72. https://doi.org/10.1186/s40729-020-00266-yCrossRef

28.

Juodzbalys G, Raustia AM (2004) Accuracy of clinical and radiological classification of the jawbone anatomy for implantation--a survey of 374 patients. J Oral Implantol 30:30–39. https://doi.org/10.1563/1548-1336(2004)030<0030:AOCARC>2.0.CO;2CrossRefPubMed

29.

Chen LC, Lundgren T, Hallström H, Cherel F (2008) Comparison of different methods of assessing alveolar ridge dimensions prior to dental implant placement. J Periodontol 79:401–405. https://doi.org/10.1902/jop.2008.070021CrossRefPubMed

30.

Urban IA, Monje A, Lozada J, Wang HL (2017) Principles for vertical ridge augmentation in the atrophic posterior mandible: a technical review. Int J Periodontics Restorative Dent 37:639–645. https://doi.org/10.11607/prd.3200CrossRefPubMed

31.

Choukroun J (2014) Advanced PRF, &i-PRF : platelet concentrates or blood concentrates? J Periodont Med Clin Pract 1:3

32.

Miron RJ, Pinto NR, Quirynen M, Ghanaati S (2019) Standardization of relative centrifugal forces in studies related to platelet-rich fibrin. J Periodontol 90:817–820. https://doi.org/10.1002/JPER.18-0553CrossRefPubMed

33.

Miron R, Choukroun J, Ghanaati S (2018) Controversies related to scientific report describing g-forces from studies on platelet-rich fibrin: necessity for standardization of relative centrifugal force values. Int J Growth Factors Stem Cells Dent 1:80–89. https://doi.org/10.4103/GFSC.GFSC_23_18CrossRef

34.

Danesh-Sani SA, Tarnow D, Yip JK, Mojaver R (2017) The influence of cortical bone perforation on guided bone regeneration in humans. Int J Oral Maxillofac Surg 46:261–266. https://doi.org/10.1016/j.ijom.2016.10.017CrossRefPubMed

35.

Meloni SM, Jovanovic SA, Pisano M, De Riu G, Baldoni E, Tallarico M (2018) One-stage horizontal guided bone regeneration with autologous bone, anorganic bovine bone and collagen membranes: follow-up of a prospective study 30 months after loading. Eur J Oral Implantol 11:89–95. https://doi.org/10.1111/jcpe.13209CrossRefPubMed

36.

Basler T, Naenni N, Schneider D, Hämmerle CHF, Jung RE, Thoma DS (2018) Randomized controlled clinical study assessing two membranes for guided bone regeneration of peri-implant bone defects: 3-year results. Clin Oral Implants Res 29:499–507. https://doi.org/10.1111/clr.13147CrossRefPubMed

37.

Albrekttson T, Zarb G, Worthington P, Eriksson AR (1986) The long-term efficacy of currently used dental implants: a review and proposed criteria of success. Int J Oral Maxillofac Implants 1:11–25

38.

Hämmerle CH, Jung RE, Yaman D, Lang NP (2008) Ridge augmentation by applying bioresorbable membranes and deproteinized bovine bone mineral: a report of twelve consecutive cases. Clin Oral Implants Res 19:19–25. https://doi.org/10.1111/j.1600-0501.2007.01407.xCrossRefPubMed

39.

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. https://doi.org/10.1111/j.1600-0501.2004.01100.xCrossRefPubMed

40.

Juodzbalys G, Raustia AM, Kubilius R (2007) A 5-year follow-up study on one-stage implants inserted concomitantly with localized alveolar ridge augmentation. J Oral Rehabil 34:781–789. https://doi.org/10.1111/j.1365-2842.2006.01679.xCrossRefPubMed

41.

Mordini L, Hur Y, Ogata Y, Finkelman M, Cavani F, Steffensen B (2020) Volumetric changes following lateral guided bone regeneration. Int J Oral Maxillofac Implants 35:e77–e85. https://doi.org/10.11607/jomi.7524CrossRefPubMed

42.

Khojasteh A, Motamedian SR, Sharifzadeh N, Zadeh HH (2016) The influence of initial alveolar ridge defect morphology on the outcome of implants in augmented atrophic posterior mandible: an exploratory retrospective study. Clin Oral Implants Res 28:208–217. https://doi.org/10.1111/clr.12991CrossRef

43.

Wang X, Zhang Y, Choukroun J, Ghanaati S, Miron RJ (2017) Behavior of gingival fibroblasts on titanium implant surfaces in combination with either injectable-PRF or PRP. Int J Mol Sci 18:331. https://doi.org/10.3390/ijms18020331CrossRefPubMedCentral

44.

Miron RJ, Zucchelli G, Pikos MA, Salama M, Lee S, Guillemette V, Fujioka-Kobayashi M, Bishara M, Zhang Y, Wang HL, Chandad F, Nacopoulos C, Simonpieri A, Aalam AA, Felice P, Sammartino G, Ghanaati S, Hernandez MA, Choukroun J (2017) Use of platelet-rich fibrin in regenerative dentistry: a systematic review. Clin Oral Investig 21:1913–1927. https://doi.org/10.1007/s00784-017-2133-zCrossRefPubMed

45.

Castro AB, Meschi N, Temmerman A, Pinto N, Lambrechts P, Teughels W, Quirynen M (2017) Regenerative potential of leucocyte- and platelet-rich fibrin. Part B: sinus floor elevation, alveolar ridge preservation and implant therapy. a systematic review. J Clin Periodontol 44:225–234. https://doi.org/10.1111/jcpe.12658CrossRefPubMedPubMedCentral

46.

Eskan MA, Greenwell H, Hill M, Morton D, Vidal R, Shumway B, Girouard ME (2014) Platelet-rich plasma-assisted guided bone regeneration for ridge augmentation: a randomized, controlled clinical trial. J Periodontol 85:661–668. https://doi.org/10.1902/jop.2013.130260CrossRefPubMed

47.

Miron RJ, Dham A, Dham U, Zhang Y, Pikos MA, Sculean A (2019) The effect of age, gender, and time between blood draw and start of centrifugation on the size outcomes of platelet-rich fibrin (PRF) membranes. Clin Oral Investig 23:2179–2185. https://doi.org/10.1007/s00784-018-2673-xCrossRefPubMed

48.

Lourenço ES, Mourão CFAB, Leite PEC, Granjeiro JM, Calasans-Maia MD, Alves GG (2018) The in vitro release of cytokines and growth factors from fibrin membranes produced through horizontal centrifugation. J Biomed Mater Res A 106:1373–1380. https://doi.org/10.1002/jbm.a.36346CrossRefPubMed

49.

Miron RJ, Chai J, Sculean A, Zhang Y (2019) A novel method for evaluating and quantifying cell types in platelet rich fibrin and an introduction to horizontal centrifugation. J Biomed Mater Res A 107:2257–2271. https://doi.org/10.1002/jbm.a.36734CrossRefPubMed

50.

Fujioka-Kobayashi M, Kono M, Katagiri H, Schaller B, Zhang Y, Schulean A, Miron RJ (2021) Histological comparison of platelet rich fibrin clots prepared by fixed-angle versus horizontal centrifugation. Platelets. 32:413–419. https://doi.org/10.1080/09537104.2020.1754382CrossRefPubMed

51.

Benic GI, Eisner BM, Jung RE, Basler T, Schneider D, Hämmerle CHF (2019) Hard tissue change after guided bone regeneration after peri-implant defects comparing block versus particulate bone substitutes: 6 months results of randomized controlled trial. Clin Oral Implants Res 30:1016–1026. https://doi.org/10.1111/clr.13515CrossRefPubMed

52.

Elnayef B, Porta C, Suárez-López Del Amo F, Mordini L, Gargallo-Albiol J, Hernández-Alfaro F (2018) The fate of lateral ridge augmentation: a systematic review and meta-analysis. Int J Oral Maxillofac Implants 33:622–635. https://doi.org/10.11607/jomi.6290CrossRefPubMed

53.

Nizam N, Eren G, Akçalı A, Donos N (2018) Maxillary sinus augmentation with leukocyte and platelet-rich fibrin and deproteinized bovine bone mineral: a split-mouth histological and histomorphometric study. Clin Oral Implants Res 29:67–75. https://doi.org/10.1111/clr.13044CrossRefPubMed

54.

Scarano A, Inchingolo F, Murmura G, Traini T, Piattelli A, Lorusso F (2018) Three-dimensional architecture and mechanical properties of bovine bone mixed with autologous platelet liquid, blood, or physiological water: an in vitro study. Int J Mol Sci 19:1230. https://doi.org/10.3390/ijms19041230CrossRefPubMedCentral

55.

Koller CD, Pereira-Cenci T, Boscato N (2016) Parameters associated with marginal bone loss around implant after prosthetic loading. Braz Dent J 27:292–297. https://doi.org/10.1590/0103-6440201600874CrossRefPubMed

Title: Guided bone regeneration simultaneous with implant placement using bovine-derived xenograft with and without liquid platelet-rich fibrin: a randomized controlled clinical trial
Authors: Gözde Işık
Meltem Özden Yüce
Nazan Koçak-Topbaş
Tayfun Günbay
Publication date: 01-09-2021
Publisher: Springer Berlin Heidelberg
Published in: Clinical Oral Investigations / Issue 9/2021
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI: https://doi.org/10.1007/s00784-021-03987-5

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Guided bone regeneration simultaneous with implant placement using bovine-derived xenograft with and without liquid platelet-rich fibrin: a randomized controlled clinical trial

Abstract

Objective

Methods

Results

Conclusion

Clinical relevance

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objective

Methods

Results

Conclusion

Clinical relevance

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