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Table of Contents
Year : 2019  |  Volume : 2  |  Issue : 3  |  Page : 45-51

Autologous tooth graft for maxillary sinus augmentation: A multicenter clinical study

1 Visiting Professor University of Bari “Aldo Moro”, Bari; Private Practice, Milan, Italy
2 Visiting Professor University of Bari “Aldo Moro”, Bari; Associate Professor in implant Dentistry, College of Medicine and Dentistry Birmingham, England; Private Practice, Lecce, Trieste, Italy
3 Private Practice, Trieste, Italy
4 Private Practice, Seriate, Turin, Italy
5 Private Practice, Milan, Italy
6 Visiting Professor University of Genoa; Private Practice, Turin, Italy
7 Visiting Professor Olomouc University; Private Practice Hradec Kralove, Czech Republic, Pescara, Italy
8 Biomaterial Clinical and Histological Research Association; Private Practice, Pescara, Italy

Date of Web Publication20-Dec-2019

Correspondence Address:
Dr. Elio Minetti
Viale Pisa 10, 20146 Milano
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/GFSC.GFSC_13_19

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Aim: The aim of this pilot study was to assess the performance of autologous tooth matrix, used as a graft material for maxillary sinus augmentation, after at least 1-year of follow-up. Settings and Design: The patients included in this prospective case series study were treated in four clinical centers using standardized clinical procedures. Materials and Methods: Patients with atrophic posterior maxilla in need of sinus augmentation before rehabilitation with implant-supported prostheses, and with compromised teeth to be extracted, were included. The extracted tooth was cleaned and processed by a recently introduced automated device, which allows fragmentation and partial demineralization of the tooth matrix, and used as a graft material for sinus augmentation. A covering membrane was used to protect the graft. Implants were placed after 6 months of healing. Five bone biopsies of the grafted sites were taken at the time of implant surgery, for histological analysis. Implants were followed for at least 1 year after placement. Cone-beam computed tomography and/or standardized periapical radiographs were used to assess the ridge height before and after grafting, up to 1-year postimplantation. Statistical Analysis: Descriptive statistics were used to synthesize the results, using mean values and standard deviations. Results: Twenty-three patients (9 males, mean age at surgery 57.1 ± 9.4 years) were treated and 40 implants were placed in grafted sites. Residual ridge height was 5.22 ± 2.04 mm and increased to 14.72 ± 2.83 mm after grafting. One implant failed during healing phase. Cumulative implant survival rate was 97.5% after 19.1 ± 8.0 months of follow-up (range 12.3–44.1 months). After 6 months of healing, the graft height appeared stable. No signs of sinus infection were present. The histologic analysis revealed neither inflammatory nor infective reaction against tooth graft. Granules appeared surrounded by newly formed bone and partially resorbed, indicating ongoing remodeling.
Conclusion: Autologous human tooth matrix can be successfully used as graft material in sinus augmentation procedure.

Keywords: Bone regeneration, dentin graft, dentin matrix, oral implantology, sinus lift, tooth graft

How to cite this article:
Minetti E, Palermo A, Contessi M, Gambardella U, Schmitz JH, Giacometti E, Celko M, Trisi P. Autologous tooth graft for maxillary sinus augmentation: A multicenter clinical study. Int J Growth Factors Stem Cells Dent 2019;2:45-51

How to cite this URL:
Minetti E, Palermo A, Contessi M, Gambardella U, Schmitz JH, Giacometti E, Celko M, Trisi P. Autologous tooth graft for maxillary sinus augmentation: A multicenter clinical study. Int J Growth Factors Stem Cells Dent [serial online] 2019 [cited 2024 Mar 2];2:45-51. Available from: https://www.cellsindentistry.org/text.asp?2019/2/3/45/273690

  Introduction Top

One of the most popular techniques for the rehabilitation of atrophic maxilla with implant-supported restorations, when the available bone volume is insufficient to install standard dental implants, is maxillary sinus augmentation. The sinus floor elevation technique for grafting the floor of the maxillary sinus was first presented in 1977 by Tatum and first published in 1980 by Boyne and James.[1] Maxillary sinus augmentation is a predictable and well-documented method of grafting bone and bone substitutes for implant placement in the posterior maxilla.[2] The classical sinus lift procedure consists of the creation of a window in the lateral maxillary sinus bone wall.[3] This window exposes the Schneiderian membrane, which is then carefully detached from the bony wall and elevated to forming the new sinus floor. Then, the space coronal to this lifted membrane is filled with graft material. Eventually, a resorbable membrane can be placed before suturing, to protect the healing site and avoid graft displacement.[3],[4],[5],[6] Many evidence-based studies, systematic reviews, and meta-analyses demonstrated that maxillary sinus augmentation is associated with a high implant and prosthesis survival/success rate, also in the medium–long term.[7],[8],[9],[10],[11],[12],[13] The residual bone height and width, and the use of covering membranes to protect the graft, were among the factors mostly affecting the prognosis of the treatment, while no detrimental effect was demonstrated by the occurrence of Schneiderian membrane perforation.[14],[15] In addition, no clear superiority was demonstrated by any of the numerous types of graft materials that have been used over the years.[16],[17] Although autogenous bone has long been considered the “gold standard” because of its osteogenic, osteoconductive, and osteoinductive properties, it may have some drawbacks, such as donor site morbidity, limited availability, and, in some cases, high resorption rate.[18]

In the recent years, the use of dentin matrix from autologous extracted teeth has emerged as a promising alternative material to promote bone healing in intraoral defects.[19],[20],[21],[22],[23]

Indeed, the tooth grafting procedure has been introduced by Yeomans and Urist and Bang and Urist, more than 50 years ago, when they discovered the osteoinduction potential of demineralized dentin matrix.[24],[25] More recently, Bessho et al. demonstrated the presence of bone morphogenetic proteins (BMPs) in the human dentin matrix. In particular, it was observed ectopic bone formation and osteoblasts presence in the rat muscle after demineralized human dentin matrix graft.[26]

Early experimental research showed that both bone tissue and dentin matrix contained specific molecules, essential to bone regeneration, such as BMPs, and other bioactive growth factors, such as transforming growth factor-beta.[27] Some authors theorized that the demineralization process allows better bone augmentation than nondemineralized dentin, probably because the availability of these molecules increases with matrix demineralization.[28]

Moreover, the chemical composition of bone and dentin is quite similar, consisting of an inorganic portion made of hydroxyapatite and an organic one, mainly composed of collagen type 1 and other secondary proteins.[29]

The effectiveness and safety of autogenous partially demineralized tooth matrix-prepared onsite, for clinical application in bone regeneration procedures related to implant dentistry, including socket preservation, alveolar ridge augmentation, and maxillary sinus floor augmentation were recently highlighted in human studies.[30],[31]

An innovative medical device able to process extracted teeth, producing a suitable graft material, was introduced in the market. Such device ensures completely automated disinfection, grinding, and demineralizing processes avoiding human manipulation of the process.

A preliminary case series reported successful clinical outcomes and bone regeneration after autologous tooth grafting using this new device, demonstrating complete filling of the bone defects, in the absence of complications.[32]

The aim of this study was to assess the clinical, radiographic, and histological performance of autologous tooth matrix, used as a graft material for maxillary sinus augmentation.

  Materials and Methods Top

All the procedures employed in the present study were in accordance with the ethical standards embedded in the Declaration of Helsinki 1975, as revised in 2000. No ethical approval was needed as there were no experimental procedures: standard protocols were followed and all materials and devices used are currently present in the market. This report was written by following the STrengthening the Reporting of OBservational studies in Epidemiology guidelines for cohort studies.

All patients considered for inclusion in the study were examined and treated between February 2016 and October 2018 in four dental clinics located in Northern Italy and Czech Republic. Four operators with extensive experience in implant dentistry and maxillary sinus augmentation performed the surgical procedures. All patients signed written informed consent form before being included in the study.

Inclusion criteria

General inclusion criteria were those commonly adopted in the four clinics: patients aged at least 18 years, with a good general health condition, and able to undergo surgical and restorative procedures (ASA-1 and ASA-2). Specific criteria were patients with edentulous posterior maxilla, and residual ridge insufficient for the placement of standard dental implants (at least 10-mm long); patients with residual ridge height at the intended implantation site no greater than 8 mm; and patients with one or more compromised teeth to be extracted before or simultaneously to sinus augmentation procedure. The reason for extraction had to be periodontal disease or caries. In case of caries, it had to involve less than one-third of the tooth.

Exclusion criteria

Subjects were excluded if they were current heavy smokers (more than 10 cigarettes/day) or if they had uncontrolled systemic conditions causing healing impairment, i.e., diabetes mellitus, cancer, AIDS, bone metabolic diseases, patients taking systemic corticosteroids, immunosuppressive agents, radiation therapy, and/or chemotherapy within the past 6 months. Subjects taking intramuscular or intravenous bisphosphonates or who had allergies or sensitivity to alginate, latex, collagen, or acrylic were also excluded, as were pregnant, lactating, or intending to become pregnant women, or those participating in other clinical intervention studies. Patients unwilling or unavailable to attend the standard scheduled follow-ups were excluded. Teeth that underwent root canal treatment, as well as teeth with caries involving more than one-third of the tooth, could not be processed to obtaining graft material.

Presurgical procedures

A preliminary clinical and radiographic examination was made before the surgical procedures. All patients underwent a session of professional oral hygiene 2 weeks before surgery. In addition, patients were instructed about standard oral hygiene procedures and were prescribed with chlorhexidine 0.2% mouthrinse, twice a day for 2 weeks for plaque control.

A complete diagnostic radiographic examination with cone-beam computed tomography (CBCT) scans and conventional periapical or panoramic radiographs was performed, to assess the width and height of the residual alveolar process and the maxillary sinus dimension.

Surgical procedures and follow-up

Antibiotic prophylaxis (amoxicillin and clavulanic acid 1 g) was administered 1 hour before intervention. Extraction of the compromised tooth/teeth was performed before sinus surgery, and teeth were processed using a specific device (Tooth Transformer [TT] S.r.l., Milan, Italy) to produce dentin matrix graft. After local anesthesia with articaine 4% + adrenaline 1:100,000, a mucoperiosteal full-thickness buccal flap was elevated to expose the lateral maxillary sinus wall. The extension of the sinus was determined referring to the CBCT scans. A lateral window was created using an ultrasonic device. The Schneiderian membrane was carefully detached starting from the mesial wall and elevated using appropriate membrane elevators. The absence of membrane perforations was assessed.

The sinus was filled with particulate dentin matrix grafts obtained with the TT.

The cortical osteotomy was then covered with absorbable membranes. The covering membrane extended 2–3 mm beyond window margins. Afterward, the flap was repositioned to stabilize soft tissue and was sutured. Amoxicillin (1000 mg b.i.d. for 6 days), or clindamycin (300 mg q.i.d. for 6–7 days) for subjects with penicillin allergies, was prescribed. At 1-week postsurgery, the sutures were removed.

Procedure to obtaining tooth graft

The whole procedure to obtaining tooth graft was described previously.[29] Briefly, the extracted tooth was first cleaned from residual calculus using a piezoelectric instrument. The root surface was polished using diamond burs under abundant irrigation in order to carefully remove any filling materials (e.g., gutta-percha, composite) from the tooth. The tooth was then cut in small pieces, which were inserted into the mill. A box containing disposable solutions was placed in the device in a specific position. These solutions ensure dentin and enamel demineralization with release of BMP-2 and collagen, as well as thorough decontamination. After 25 min, demineralized tooth graft was ready to be used in the patient's mouth.

Implant placement

The dental implants were placed after 6 months of healing according to the standardized surgical procedures, as indicated by the implant manufacturers.

Histological and histomorphometric analysis

At the time of implant placement, biopsies were taken in five cases, in the region of the augmented sites, for histological analysis. The samples were taken crestally before implant insertion, using graduated trephine drills (3–6 mm external diameter), under copious sterile saline irrigation. Biopsy sampling was done in correspondence with the implant site preparation and should not be considered additional surgical maneuver respect to the standard therapy.

Biopsies were carefully washed and fixed in 10% buffered formalin for 48 h at room temperature. Then, the samples were sent to the laboratory.

Each sample was dehydrated by a series of solutions with increasing alcohol concentration, up to pure alcohol and then infiltrated into methacrylic resin. After the light-curing of the resin, the sample was processed to obtain nondecalcified sections, using a disk abrasion system (LS2-Remet, Bologna) and a diamond disk cutting system (Micromet-Remet, Bologna).

In the first phase, the inclusion in resin is abraded to eliminate the resin component that covers the sample and the area of the biopsy to be observed was thus brought to the surface. Then, the surface was glued to a showcase with cyanoacrylate-based adhesives. Subsequently, cutting with high speed and cooling diamond blade is performed, to obtain a sample of about 200 μ thick, which was then thinned by abrasion. Each sample is then abraded reducing the thickness down to about 40–50 μ. At this point, the slide was polished with polishing papers and colored with basic fuchsin and blue toluidine for the final observation under light and polarized light microscopy.

For histomorphometric measurements, the histological images obtained from the transmitted light microscope were digitized through a digital camera and analyzed by means of an image analysis software IAS 2000. For each sample were calculated: BV% = Percentage of residual bone volume with the exclusion of medullary tissues; Graft% = Percentage of the remaining graft, excluding bone and marrow; VB% = Percentage of vital bone with exclusion of the bone marrow and the residual graft.

Prosthesis delivery and follow-up

The prosthetic phase occurred after 5–6 months of implant placement, following the standard procedures adopted in each clinical center. Patients were recalled at 6 and 12 months after prosthesis delivery for standard clinical and radiographic controls.

The outcome variables were:

  1. Implant survival, evaluated based on the following criteria: presence of the implant in the patient's mouth, absence of peri-implant radiolucency, no recurrence or persistent peri-implant infection and no complaint of pain and of neuropathies or paresthesia
  2. Prosthesis success, defined by the presence of functional prosthesis in patient's mouth with no mechanical complications
  3. Histomorphometric parameters from biopsies analysis.

Statistical analysis

Patients' data were collected and stored on a specific datasheet (Microsoft Excel, Microsoft Corp., Redmond, WA, USA). Simple descriptive statistics were used, presenting the sample characteristics and the outcomes using mean values and standard deviations.

  Results Top

Twenty-three subjects (9 men and 14 women) with a mean age at surgery of 57.1 ± 9.4 years (range 40–76 years) were enrolled and treated following the described protocol. Four patients were smokers. One had a previous history of breast cancer.

The average dimension of the sinus was vertical 9.47 ± 3.45 mm (range 6–18 mm), buccopalatal 10.00 ± 2.22 mm (range 8–14 mm), and mesiodistal 11.69 ± 5.29 mm (range 6–25 mm).

The mean residual ridge height at the intended implantation site was 5.22 ± 2.04 mm (range 2.1–8.0 mm).

Twenty-three teeth, accounting for 52 roots (on the average 2.26 roots per each patient), were extracted and used for preparing the tooth graft. Nineteen teeth were nonvital and four were vital. Nine teeth were sound and 14 infected. In 13 cases, only root dentin was used, and in 10 cases also, enamel was processed.

The graft was covered with absorbable collagen membranes in 18 cases (Bego Collagen Membrane [porcine pericardium], Bego, Implant Systems, Bremen, Germany, in 16 cases; Biogide®, Geistlich Pharma, Wolhusen, Switzerland, in two cases). In the remaining cases, the graft was covered with a membrane made of a plasma rich in growth factors (PRGF®-Endoret, BTI Biotechnology Institute, Vitoria, Alava, Spain; 3 cases) or platelet-rich fibrin (A-PRF™, PRF Process, Nice, France; 2 cases). After grafting, the mean bone height was 14.72 ± 2.83 mm (range 9.5–20.65 mm). The mean increase respect to baseline was 9.50 ± 2.70 mm (range 5.0–15.14 mm). A total of 40 implants were placed. Four implant types of four different companies were used: Visio® One (CEA MEDICAL SA, Geneva, Switzerland; n = 30), External Hex (Biomet 3i, Palm Beach Gardens, FL, USA; n = 5), BTI Interna (BTI Biotechnology Institute, Vitoria, Alava, Spain; n = 4), SLActive RN Tissue Level (Straumann Holding AG, Basel, Switzerland; n = 1).

The mean follow-up after implant placement was 19.1 ± 8.0 months (range 12.3–44.1 months). The follow-up for the graft was 6 months longer. Throughout the healing period, hard and soft tissues were stable. The healing of soft tissues after grafting procedures was free of complications. [Figure 1] and [Figure 2] are panoramic radiographs of a case before grafting and at 6 months of healing, soon after implant placement.
Figure 1: Panoramic view from cone-beam computed tomography scan taken after extraction of the first upper left molar and before sinus lift procedure. The residual height at the intended implantation site was 5.37 mm

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Figure 2: Panoramic view from cone-beam computed tomography scan taken 6 months after sinus augmentation procedure, soon after implant placement. The margin of biopsy is visible around the apical portion of the implant

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During the follow-up, one implant was lost. It showed suppuration after 3 months of placement. The implant was replaced without compromising prosthesis function. Implant and prosthesis survival after 1 year were 97.5% and 100%. After 1 year from implant placement, peri-implant bone levels and graft height were stable.

The results of the histomorphometric analysis of the graft biopsies showed that the mean BV% was 36.28% ± 9.77%, the mean residual graft% was 14.61% ± 9.37% and the VB% was 21.51% ± 8.61% [Figure 3], [Figure 4], [Figure 5]. No inflammatory reactions around dentin granules were observed. The graft appeared to be subjected to physiological bone remodeling, demonstrating an excellent integration with the host tissues. No difference was found, either from a clinical or a histological standpoint, between originally infected and noninfected teeth, and between vital and nonvital teeth.
Figure 3: Overview of a biopsy at low magnification: Dentin matrix granules (darker stain) and newly formed bone were visible (Toluidine Blue, ×8)

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Figure 4: Newly formed bone trabeculae (N) and dentin matrix graft particles (D) were observed. On the left side, a granule is almost completely surrounded by new bone (Toluidine Blue, ×25)

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Figure 5: Dentin matrix graft granules (D) appeared well integrated into the new bone (N). The dentin granules showed numerous characteristic dots that correspond to dentinal tubules (Toluidine Blue, ×50)

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This study evaluated hard and soft tissue healing and implant survival rate after maxillary sinus augmentation performed using an autologous graft made of demineralized dentin/enamel matrix. This graft derives from the extracted patient's tooth and is produced by processing the tooth itself with a recently introduced device, able to shred and decontaminate dental elements and transform them into a grafting material usable for the treatment of different types of bone defects in oral surgery procedures. The results of this study suggested that autologous tooth matrix is a feasible grafting material for sinus augmentation, being the clinical and histomorphometric outcomes in line with the current literature.[7],[8],[9],[10],[11],[12],[13],[16],[17],[33] This study has several limitations that should be taken into account. First, the number of patients, as well as the follow-up duration, is relatively limited. However, also, other studies presenting histologic and histomorphometric results of graft materials had similar sample size.[34],[35],[36],[37] Second, the study was not comparative. This was a preliminary study, aiming at evaluating the feasibility and safety of the tooth graft as a sinus grafting material. Since the results were satisfactory, the authors will plan to perform evidence-based comparative studies in the near future, to confirm the outcomes obtained using the TT device.

The use of tooth derivatives such as dentin and/or enamel as potential graft materials for the treatment of bone defects have emerged in the last decades. The strong points in favor of using such material are as follows: it is totally autogenous; it does not require an additional surgical site for harvesting bone graft; the dentin structure and composition is very similar to that of bone; it has been shown to contain BMP-2, that is made available by the demineralization procedure, giving to the material osteoinductive properties (in addition to the osteoconductive features, provided by the porous three-dimensional matrix). Furthermore, the idea of recycling compromised teeth that need to be extracted, instead of discarding them, thereby avoiding the use of expensive heterologous or synthetic bone substitutes, is expected to be well-accepted by patients.

Several studies pointed out that the demineralization process is highly critical to determine tooth graft properties.[29],[30],[31] This process is required to expose and make available the growth and differentiation factors embedded in the hydroxyapatite crystals, especially the BMPs, which have osteoinductive properties.[24],[25],[26] In fact, different exposure times, combinations and concentrations of the strong acids used for demineralization, may produce grafts with different biological activity, as suggested by previous in vivo studies on ectopic[38],[39],[40],[41],[42] and orthotopic models.[43],[44],[45] In a recent review, Kim et al. concluded that the osteoinductive properties of dentin graft might depend on different acid treatment protocols, underlying the importance of this process.[46]

The physical-chemical and biochemical features of dentin and enamel matrix obtained after processing teeth derivatives with the TT device have been described in a recent in vitro study.[47] That study found that the biocompatibility of demineralized dentin is even higher than the more popular anorganic bovine bone, and that demineralization increases BMP-2 and collagen type I bioavailability as compared with nondemineralized tooth derivatives. The tooth graft also proved to have high wettability that allows easy handling and positioning on the defect site. In addition, the study found that the sterilization process accomplished by the TT device is highly effective as no microbial contamination was detected on the processed samples. The study concluded that demineralized tooth matrix represents a suitable biomaterial for bone regeneration and replacement.[47]

In a previous clinical study, the same device was used in a series of 15 patients, mostly for postextraction alveolar socket preservation, reporting favorable clinical and radiographic results, in the absence of complications and adverse events.[32]

As there is a wide availability of teeth that every day are extracted and discarded in dental offices, this new device may represent an advanced system in the area of tissue engineering, with a strong potential to produce suitable substrates for bone regeneration procedures.

In recent years, two systematic reviews of the literature were published, assessing the reliability of autogenous tooth graft material applied to bone augmentation procedures for alveolar ridge reconstruction.[27],[48] Both reviews identified only six studies that used autogenous teeth for bone grafting of alveolar deficiencies. The studies had different design, from randomized to retrospective, and collectively showed limited available evidence on the efficacy of such material.

In one of these reviews, the authors reported an implant survival rate of 97.7% (of a total of 182 implants analyzed), in line with the results of the present study, and also, histological results were very similar to those herein reported.

In spite of the limited number of studies, sample size, and evidence level, all these investigations showed very promising results, suggesting that autogenous tooth matrix can be considered a feasible alternative to more popular biomaterials. The results of these reviews are encouraging and underline the need for performing further investigations to estimate the true effect of using processed tooth as bone graft material.

  Conclusion Top

Demineralized autogenous teeth represent a feasible and safe substrate for grafting the maxillary sinus, due to osteoconductive and osteoinductive properties.

Future studies with long follow-up period are needed to get more insight on the potential of demineralized tooth autografts.

Elio Minetti acts as consultant for TT Tooth Transformer SRL (Via Washington, 59 – Milan, Italy).

Financial support and sponsorship


Conflicts of interest

Elio Minetti acts as consultant for TT Tooth Transformer SRL (Via Washington, 59 – Milan, Italy).

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