A proof-of-principle study was conducted to assess the safety and efficacy of dental putty as an alternative sinus augmentation biomaterial. Six healthy patients requiring a total of 10 sinus augmentations received sinus augmentations. All patients volunteered and signed an informed consent based on the Helsinki declaration of 1975, as revised in 2000. The sinus augmentation was performed under local anesthesia with a mucoperiosteal flap elevated to expose the buccal wall of the maxillary sinus. The space was then filled with the dental putty in several increments, and the window was covered with an absorbable collagen membrane. Biopsies were harvested from all 10 treated sinuses using a 3-mm trephine bur at the time of implant placement at either 6 or at 9 months after sinus augmentation. All patients completed the study without complications, except for 1 patient who reported fistulas at 1 and 2 months after the surgery. Clinical reentry revealed that regenerated bone on the osteotomy site was soft and immature. The ground sections of the biopsied cores revealed minimum amounts of trabeculation surrounded by an abundant array of irregular-shaped residual alloplastic particles embedded in loose connective tissue. The present study's findings revealed inadequate bone formation, although the material appears to be bioinert as there is no elicitation of inflammatory response.
This study was conducted to assess the safety and efficacy of dental putty (Novabone Products, LLC, Alachua, Fla) as an osteoconductive biomaterial for the sinus augmentation. This putty is a bioactive alloplast claiming to stimulate osteoblast differentiation and proliferation, resulting in an increased rate of bone formation.1
The maxillary sinus tends to pneumatize together with the loss of alveolar bone volume following extraction of maxillary posterior teeth. This nonnatural bone-forming area has been used to demonstrate success and efficacy of autogenous, nonautogenous, and growth factor materials.2–9 There has been a high rate of success when placing implants in augmented sinuses; however, there is a gradient of osteogenesis relative to the material selected. Although the sinus augmentation procedure has low complication rates, they do occur and can jeopardize the final implant outcome.2–6,10–12
Bone substitutes used for the sinus augmentation should possess osteoconductive potential to act as a scaffold for cellular migration and allow vital bone formation that can eventually undergo a remodeling process.2–6,10–12 Alloplasts appeared to be of considerable interest because of their abundant supply and synthetic nature.13,14 The results of proof-of-principle and evidence-based investigations should be available to clinicians before applying these bone substitutes to patient care.
Materials and Methods
Six healthy patients (4 men and 2 women between the ages of 41 and 59 years) requiring a total of 10 sinus augmentations (4 bilateral and 2 unilateral) were recruited for this study. They all required multiple dental implants to restore missing dentition. Oral and written explanations of the study including the risks, benefits, and alternative therapies were provided. All patients volunteered and signed an informed consent based on the Helsinki declaration of 1975, as revised in 2000. Preoperative periapical radiographs and computerized tomography (CT) scans revealed insufficient native alveolar bone (less than 5 mm) for implant placement in all sites. Thorough assessments were done to exclude patients with a history of sinus pathologies or treatment regimens. None of the patients admitted to recent tobacco experiences.
The sinus augmentation was performed under local anesthesia (2% lidocaine with 1:100 000 epinephrine) with a mucoperiosteal flap elevated to expose the buccal wall of the maxillary sinus. An oval osteotomy was made with piezoelectric surgery (Piezosurgery Incorporated, Columbus, Ohio), and the integrity of the Schneiderian membrane was preserved and elevated to the medial wall of the sinus to allow placement of the grafting material (Figure 1a). Decortical lining of the sinus cavity was perforated in numerous areas with the piezoelectric surgery to promote angiogenesis. The space was then filled with the dental putty (Novabone Products, LLC) in several increments, and the window was covered with an absorbable collagen membrane (Bio-Gide, Osteohealth, Shirley, New York; Figure 1b and c). This putty was a premixed composite of bioactive calcium-phopho-silicate particulate and an absorbable binder (a combination of polyethylene glycol and glycerin).1
Primary flap closure was accomplished with 3-0 silk sutures (Ethicon, Inc, Somerville, NJ). The patients received an antibiotic prophylaxis (amoxicillin 500 mg/3 times a day/5 days or clindamycin 300 mg/3 times a day/5 days) and analgesics (ibuprofen 800 mg/3 times a day/5 days). They were instructed to rinse twice daily with 0.12% chlorhexidine digluconate solution for 1 week, received written postoperative instructions, and were advised to return in 7 to 10 days for suture removal and wound assessment. They were routinely monitored for the next 6 to 9 months during the postoperative healing period.
A postoperative CT scan was taken 5 months after the sinus augmentation procedure. Biopsies were harvested from all 10 treated sinuses using a 3-mm trephine bur (Biomet 3i, Palm Beach Gardens, Fla) at the time of implant placement either 6 or at 9 months after sinus augmentation. The cores were immediately placed in 10% buffered formalin for histologic evaluation.
The fixed samples were dehydrated in a graded series of ethanol with agitation and vacuum. The cores were infiltrated with the resin (Technovit 7200 VLC, Heraeus Kulzers GmbH, Germany) and were placed into embedding molds, and polymerization was performed under ultraviolet light. The polymerized blocks were then sliced longitudinally (Exakt, Norderstedt, Germany), and the slices were reduced by microgrinding and polishing (Exakt) to an even thickness of 30–40 μm. Sections were stained with toluidine blue/pyronine G and examined using a light microscope (Leica 6000DRB light microscope, Germany).
Backscatter scanning electron microscopy
Following the light microscopic evaluation, the specimens were sputter coated with 6-nm thick carbon layer (SCD050 Sputter Unit, Bal-Tec, Liechzenstein, Germany) and examined in the backscatter modus (Supra 40VP scanning electron microscope, Zeiss, Oberkochen, Germany).
Radiographic and clinical evaluations
All 6 patients requiring 10 maxillary sinus augmentations completed the study without complications, and membrane perforation was not observed during the surgery. However, 1 patient reported fistulas at 1 and 2 months after the surgery, and the infection was resolved by the use of 0.12% chlorhexidine digluconate solution and systemic antibiotic (Pen VK 500 mg). The CT scan evaluations at 5 months after surgery for remaining patients demonstrated variability in radiopacity in the sinus (Figure 2).
The Table and Figures 3a through d provide the clinical observations at the time of 6- and 9-month reopening. The surgical observation of unresolved osteotomy sites together with the soft-tissue ingrowth for 3 augmented sites (patient Nos. 1b, 2a, and 4b) at 6 months was responsible for the delay of the remaining 7 sites for the additional 3 months (Figure 3a). The fistula patient (patient No. 4) experienced complete failure on both augmented sites at 6 and 9 months postoperation and required complete removal of the grafting material in addition to systemic antibiotics. Only 1 sinus augmented site (patient No. 6) demonstrated complete buccal bone healing at the 6-month postoperative visit (Figure 3d). The clinical results of the remaining cases are found in the Table. In summary, 3 sites experienced complete failure (patient Nos. 2a, 4a, and 4b), 3 sites evidenced soft and immature bone (patient Nos. 1b, 2b, and 5), 3 sites appeared to have some resistance to the trephine (patient Nos. 1a, 3a, and 3b), and 1 site appeared to have dense buccal bone (patient No. 6). Overall, regenerated bone on the osteotomy site was soft and did not offer significant resistance to the trephine. For those patients who experienced complete failure, regrafting of the sinus using an alterative bone graft was performed.
The ground sections of the biopsied cores revealed minimum amounts of bone trabeculation surrounded by an abundant array of irregular-shaped residual alloplastic particles embedded in loose connective tissue (Figures 4a,b and 5). Newly formed vital bone adjacent to areas of augmentation materials was rare; thus, osteoconductivity was limited (Figures 6a,b and 7). There were no signs of local inflammation. Histomorphometric analysis was not performed because of insignificant trabeculation of new bone.
A clinical, radiographic, and histologic evaluation of dental putty (Novabone Products) was conducted to test its safety and effectiveness as an osteoconductive material in the maxillary sinus. The maxillary sinus is an ideal site to investigate the osteogenic behavior of bone substitute materials because it is a nonnatural bone-forming area.8,9,15,16 The goal of a sinus augmentation procedure is not only to form the vital bone in the pneumatized sinus and allow osseointegration of implants in that bone but also the long-term survival of those implants under functional load.3
In recent years, a number of nonviable osteoconductive bone substitutes have been introduced in dentistry to minimize the use of autogenous bone grafting that has long been considered to be the gold standard. However, clinicians should not expect all marketed bone substitutes to achieve the same level of bone formation as well as the gold standard in all clinical situations. The results held in comparison to the use of freeze-dried bone allograft or demineralized freeze-dried bone allograft to the use of a xenograft clearly demonstrated osteoconductive behavior of the matrix with significant bone structure to accomplish osseointegration.17 The paucity of bone formation seen from our study by osteoconduction with dental putty at 6 months was difficult to elicit and at 9 months was minimum. Histological review demonstrated particle embedded in connective tissue with little or no bone formation. A recent study using rhPDGF-BB together with xenograft resulted in significant new bone formation with minimal retention of the matrix.18 There appeared to be resorptive activity of the xenograft when combined with the recombinant protein. Recent studies performed with recombinant human bone morphogenetic protein-2 (rhBMP-2) on collagen sponge resulted in significant de novo bone formation.8
The findings of the present study unfortunately did not reveal sufficient evidence of bone formation. As a result, only 4 of 10 sites received dental implants due to soft-tissue ingrowth and inadequacy of bone trabeculation. Limited new bone formation was insufficient to support contact or distance osseointegration. Expanding the study from 6 to 9 months resulted in only 1 appropriately healed osteotomy site and did not accomplish the hopeful results.
The optimal bone substitute should conduct or induce new bone formation and eventually demonstrate time-dependent resorption and replacement by new bone. Histologic results for the 6-month and 9-month specimens revealed minimum amounts of newly formed bone tissue on the surface of irregular-shaped residual graft particles embedded in connective tissue. All analyzed specimens demonstrated minimum osteoconduction and inadequate signs of vital bone formation.
In the present study, the high graft failure associated with the alloplast cannot be associated with the patient selection because all patients were systemically healthy with no contraindications for dental surgery. An absorbable collagen barrier membrane that was used in this study has been used in dentistry for many years and has a solid safety track record for sinus augmentation.19,20
Our clinical and histologic results from the current study did not support the use of dental putty for sinus augmentation cases because of its limited osteoconductivity. There could be other areas that may be of interest for the use of dental putty with future research.
This study was sponsored by a grant from Sunstar Americas, Inc. The authors report no conflicts of interest related to this study.