Sufficient bone volume and quality have been described as major determinants of success in rehabilitation with dental implants. The posterior maxillary region has frequently shown insufficient bone volume to guarantee a predictable long-term result. Many studies have described the problem of bone deficiency in this region, and numerous techniques for maxillary sinus floor augmentation have been presented 1.
In the posterior maxilla, standard implant placement is often restricted because of generally reduced amount of bone 2–4. During the last decades, surgical procedures have been developed to increase the local bone volume to permit restoration of the posterior maxilla by placement of dental implants 4–6. In cases of enlarged maxillary sinus, the sinus floor elevation has been advocated to allow for implant placement 3–6. Autogenous bone, xenogenic bone, or a mixture of both may be used for sinus augmentation 4,7–9. The amount of bone height determines the number of stages of implant (1 or 2) (i.e. being greater or less than 5 mm) for achieving primary stability of the inserted implants 5–7,10–13.
Lekovic et al. 14,15 have reported on the effects of nonabsorbable and absorbable membranes in the preservation of the alveolar process after tooth extraction by using a surgical technique based on the principles of guided bone regeneration. In both trials, buccal flaps were advanced to achieve primary closure of the surgical wound. The results showed better alveolar bone preservation compared with the control group.
An alveolar process preservation technique that does not involve the buccal flap would make the ridge preservation simpler and less traumatic than the earlier method 16.
The problem lies in resorption of the alveolar process and/or enlargement of the maxillary air sinus in the posterior region of the maxilla. Implant installation in this region requires elevation of the sinus floor (sinus lift) and condensation of the bone graft under mucosal lining of the sinus floor for augmentation of that posterior region.
The purpose of this study was to evaluate the effectiveness of β-tricalcium phosphate (β-TCP) mixed with platelet-rich fibrin (PRF) used to augment the sinus floor as well as stability of implant installation 4 months after bone grafting (augmentation).
Patients and methods
A total of 15 patients (5 men and 10 women) were included in this study. Three patients were smokers. Presurgical clinical and radiographic examinations (panoramic radiographs) revealed the length of the remaining alveolar ridge as well as the condition of the maxillary sinuses. Sinus lift was considered when the subantral bone was less than or equal to 5 mm as measured on a panoramic radiograph (Fig. 1).
All patients were operated upon under local anesthesia (2% xylocaine dental with epinephrine 1 : 50 000) (Dentsply Pharmaceutical, York, Pennsylvania, USA). The posterior maxillary edentulous area and the maxillary sinus wall were exposed by means of a crestal incision, and a buccal mucoperiosteal flap was raised. Osteotomy was performed with a fissure bur in nearly round shape 5–6 mm cranial to the intended implant site. With small sharp elevators, the cortical bony window was dissected free from the underlying sinus membrane (Fig. 2). The cut-out bone piece was put aside and stored in sterile saline. With angulated elevators of various dimensions, sinus lift was performed in all directions. After sinus membrane elevation, β-TCP mixed with PRF was packed below the elevated membrane (Fig. 3) (β-TCP is granular, granule size 1000–2000 µm, and is a new synthetic pure-phase β-TCP). This material is unique because of its interconnective open multiporosity and polygonal granule structure. PRF is prepared as follows: blood is taken without an anticoagulant in a 10 ml tube and then centrifuged directly using moderate forces (400g). In the middle of the tube, a fibrin (PRF) clot is formed (Fig. 4); this clot contains most of the platelets and leukocytes in the tube. This clot is cut into small pieces and mixed with β-TCP granules 17–19.
The cortical cut-out bone piece was thereafter repositioned and the incision closed with sutures.
Analgesics were prescribed with paracetamol and codeine for 1–2 weeks following the surgery. Antibiotic treatment was continued for 7 days postoperatively with 1 g phenoxymethylpenicillin two times daily. Patients were instructed not to blow their nose and to use nasal spray saline for 10 days after surgery. Sutures were taken out after 7–10 days. No infections were recorded.
Four months later, the dental implants were installed in the previously grafted regions. Firm primary stability was achieved at all implant sites.
Clinical and radiographic follow-up
Prosthetic rehabilitation was carried out 4 months after implant installation for most the patients. Clinical and radiographic follow-up were performed (a) immediately after surgery, (b) 4 months after surgery, (c) immediately after implantation, and (d) half-annually up to 1 year after implantation.
The procedure was well tolerated by the patients under local anesthesia, most without preoperative sedation. Packing of the β-TCP mixed with PRF proved to be easy and reliable throughout the procedure. Twelve of the 15 patients in the study developed a noninflammatory reaction at the operative site. None of them developed infections or showed poor wound healing, and the sutures were removed after 7–10 days with the wound clean and nonirritated. Only in three patients had some of the graft materials escaped through the mucosa (at the line of the incision) during early postoperative follow-up. However, this did not require revision. Those three patients showed delayed wound healing postoperatively and needed the antibiotics to be extended for five more days. There was, however, no need to remove the bone graft. Clinically, the implants showed good stability during their installation. At 6 months after installation, there were no signs of looseness or instability. The same situation was noticed at 1 year after installation with more implant stability. The radiograph showed that, at the sites where bone was minimal at grafting time, new bone was generated 4 months after grafting. Most implants showed a stable marginal situation on the radiograph at ∼8 months from grafting time. The radiograph revealed complete or near-complete degradation of the β-TCP ceramic granules with concurrent bone substitution in the majority of cases (Figs 5–7).
The implants were firmly fixed to the bone at the end of follow-up.
The sinus lift procedure is an internal augmentation of the maxillary sinus. The purpose of this procedure is to increase the bone volume in that part of the maxillary bone to allow for dental implantation. Sinus augmentation procedures are widely used and have resulted in the highest success rates of all augmentation procedures 20–22.
Bone substitutes and bone regenerating materials are in high demand in oral and maxillofacial surgery. Otherwise, autogenous bone grafts are used. However, the additional surgical procedure for bone harvesting as well as the potential donor site morbidity will result in patient insult. Accordingly, a variety of bone substitutes are available as alternatives. The synthetic pure-phase β-TCP granules used in this study have multiporosity and a polygonal granule structure. This almost matches some properties of autogenous bone. The high porosity of these granules is seen in about 65% of them, which helps in angiogenesis and forms the basis for cell nutrition and resorption from within the granules. Good bone healing without irritation, ease of material handling, and regular timed resorption (depending on the patient’s physiologic condition) with simultaneous formation of new bone represent the advantages of β-TCP granules. Use of PRF mixed with β-TCP allows the formation of a biological bonding with granules of β-TCP, and the fibrin matrix leads to improved vascularization of these granules 17–19,23. In addition, mixing PRF with β-TCP favors neoangiogenesis and capture of stem cells, and induces the migration of osteoprogenitor cells to the center of the graft, which subsequently leads to the formation of osteoblast cells inside the mixture (graft material) and finally the formation of new bone (regeneration) at a faster rate compared with the use of β-TCP without PRF 24, 25. Use of this mixture allows for implant placement after 4 months, which is an interval also needed by normal bone for new bone formation and regeneration but without donor site morbidity.
Use of this mixture showed good solubility and biocompatibility, which was seen by the nearly complete bone regeneration after 12 months of grafting without inflammatory reactions. This favorable biodegradation property is due to the pure-phase (99%) β-TCP ceramic composition with open macroporosity and microporosity and newly formed angiogenesis due to the presence of PRF. Therefore, it is recommended that dental implants should not be installed until ceramic degradation has shown considerable progress with bone regeneration. This requires a period of at least 4 months for implant installation 26,27.
Use of this mixture (graft) for sinus floor elevation showed consistent biodegradation and new bone formation at a faster rate compared with autogenous bone grafting, as well as reduced risk of autogenous bone graft harvesting (donor site morbidity).
Conflicts of interest
There are no conflicts of interest.
1. Coulthard P, Esposito M, Jokstad A, Worthington HV. Interventions for replacing missing teeth: bone augmentation techniques for dental implant treatment. Cochrane Database Syst Rev 2003; 3:CD003607.
2. Van den Bergh JP, ten Bruggenkate CM, Disch FJ, Tuinzing DB. Anatomical aspects of sinus floor elevations. Clin Oral Implants Res 2000; 11:256–265.
3. Garg AK. Augmentation grafting of the maxillary sinus for placement of dental implants: anatomy, physiology, and procedures. Implant Dent 1999; 8:36–46.
4. Boyne PJ, James RA. Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surg 1980; 38:613–616.
5. Wallace SS, Froum SJ. Effect of maxillary sinus augmentation on the survival of endosseous dental implants. A systematic review. Ann Periodontol 2003; 8:328–343.
6. Chanavaz M. Sinus grafting related to implantology. Statistical analysis of 15 years of surgical experience (1979–1994). J Oral Implantol 1996; 22:119–130.
7. Hallman M, Nordin T. Sinus floor augmentation with bovine hydroxyapatite mixed with fibrin glue and later placement of nonsubmerged implants: a retrospective study in 50 patients. Int J Oral Maxillofac Implants 2004; 19:222–227.
8. Valentini P, Abensur DJ. Maxillary sinus grafting with an organic bovine bone: a clinical report of long-term results. Int J Oral Maxillofac Implants 2003; 18:556–560.
9. Stricker A, Voss PJ, Gutwald R, Schramm A, Schmelzeisen R. Maxillary sinus floor augmentation with autogenous bone grafts to enable placement of SLA-surfaced implants: preliminary results after 15–40 months. Clin Oral Implants Res 2003; 14:207–212.
10. Zitzmann NU, Schärer P. Sinus elevation procedures in the resorbed posterior maxilla. Comparison of the crestal and lateral approaches. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998; 85:8–17.
11. Summers RB. A new concept in maxillary implant surgery: the osteotome technique. Compendium 1994; 15:152154-6, 158 passim; quiz 162.
12. Toffler M. Osteotome-mediated sinus floor elevation: a clinical report. Int J Oral Maxillofac Implants 2004; 19:266–273.
13. Rodoni LR, Glauser R, Feloutzis A, Hämmerle CH. Implants in the posterior maxilla: a comparative clinical and radiologic study. Int J Oral Maxillofac Implants 2005; 20:231–237.
14. Lekovic V, Kenney EB, Weinlaender M, Han T, Klokkevold P, Nedic M, Orsini M. A bone regenerative approach to alveolar ridge maintenance following tooth extraction. Report of 10 cases. J Periodontol 1997; 68:563–570.
15. Lekovic V, Camargo PM, Klokkevold PR, Weinlaender M, Kenney EB, Dimitrijevic B, Nedic M. Preservation of alveolar bone in extraction sockets using bioabsorbable membranes. J Periodontol 1998; 69:1044–1049.
16. Camargo PM, Lekovic V, Weinlaender M, Klokkevold PR, Kenney EB, Dimitrijevic B, et al.. Influence of bioactive glass on changes in alveolar process dimensions after exodontia. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000; 90:581–586.
17. Choukroun J, Diss A, Simonpieri A, Girard MO, Schoeffler C, Dohan SL, et al.. 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 2006; 101:e56–e60.
18. Choukroun J, Diss A, Simonpieri A, Girard MO, Schoeffler C, Dohan SL, et al.. 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 2006; 101:299–303.
19. Choukroun JI, Braccini F, Diss A, Giordano G, Doglioli P, Dohan DM. Influence of platelet rich fibrin (PRF) on proliferation of human preadipocytes and tympanic keratinocytes: a new opportunity in facial lipostructure (Coleman’s technique) and tympanoplasty? [in French]. Rev Laryngol Otol Rhinol (Bord) 2007; 128:27–32.
20. Wiltfang J, Schultze-Mosgau S, Nkenke E, Thorwarth M, Neukam FW, Schlegel KA. Onlay augmentation versus sinus lift procedure in the treatment of the severely resorbed maxilla: a 5-year comparative longitudinal study. Int J Oral Maxillofac Surg 2005; 34:885–889.
21. Schliephake H, Neukam FW, Wichmann M. Survival analysis of endosseous implants in bone grafts used for the treatment of severe alveolar ridge atrophy. J Oral Maxillofac Surg 1997; 55:1227–1233discussion 1233-4.
22. Valentini P, Abensur D, Wenz B, Peetz M, Schenk R. Sinus grafting with porous bone mineral (Bio-Oss) for implant placement: a 5-year study on 15 patients. Int J Periodontics Restorative Dent 2000; 20:245–253.
23. Braccini F, Dohan DM. The relevance of Choukroun’s platelet rich fibrin (PRF) during facial aesthetic lipostructure (Coleman’s technique): preliminary results [in French]. Rev Laryngol Otol Rhinol (Bord) 2007; 128:255–260.
24. Vence BS, Mandelaris GA, Forbes DP. Management of dentoalveolar ridge defects for implant site development: an interdisciplinary approach. Compend Contin Educ Dent 2009; 30:250–252254, 256 passim; quiz 262, 278.
25. Hamdan AA, Loty S, Isaac J, Bouchard P, Berdal A, Sautier JM. Platelet-poor plasma stimulates the proliferation but inhibits the differentiation of rat osteoblastic cells in vitro. Clin Oral Implants Res 2009; 20:616–623.
26. Merten HA, Wiltfang J, Hönig JF, Funke M, Luhr HG. Intra-individual comparison of alpha- and beta-TCP ceramics in an animal experiment [in German]. Mund Kiefer Gesichtschir 2000; 4Suppl 2S509–S515.
27. Szabó G, Huys L, Coulthard P, Maiorana C, Garagiola U, Barabás J, et al.. A prospective multicenter randomized clinical trial of autogenous bone versus beta-tricalcium phosphate graft alone for bilateral sinus elevation: histologic and histomorphometric evaluation. Int J Oral Maxillofac Implants 2005; 20:371–381.