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Basic and Clinical Research

Alveolar Ridge Preservation Using Autologous Demineralized Tooth Matrix and Platelet-Rich Fibrin Versus Platelet-Rich Fibrin Alone

A Split-Mouth Randomized Controlled Clinical Trial

Ouyyamwongs, Warisara DDS, MSc*; Leepong, Narit DDS; Suttapreyasri, Srisurang DDS, PhD

Author Information
doi: 10.1097/ID.0000000000000918
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Abstract

Buccal bone collapse after tooth extraction leading to the reduction of alveolar ridge width is a major concern for both esthetics and function for further dental treatment such as dental implant placement or orthodontic tooth movement. Resorption of the buccal bone of the alveolar ridge starts immediately after tooth extraction, and most of the alveolar ridge alterations are complete within the first 3 months.1 The reduction from 2.5 to 4.5 mm in width and 0.9 to 3.6 mm in height have been reported as the consequences after tooth extraction in a recent systemic review of randomized controlled trials.2

To maintain the alveolar ridge dimensions, various bone graft materials are used for ridge preservation. Generally, xenografts or allografts are used with good outcomes.3,4 Nonetheless, the shortcomings of xenografts and allografts are that they lack osteoinductive and osteogenic properties,5,6 have additional graft costs, and risk disease transmission. Accordingly, the development of alternative bone graft materials that are autologous, and contain osteoconduction and osteoinduction properties is required.

The tooth itself is a possible alternative substance for bone substitution. The dentin consists of inorganic and organic components. The inorganic part comprises 70% hydroxyapatite. The hydroxyapatite type is low-crystalline calcium phosphate similar to bone, which promotes bone remodeling. Unlike dentin, enamel contains a high-crystalline calcium phosphate type of hydroxyapatite,7 which is hard to be decomposed by osteoclasts, resulting in a slow resorption rate. The combination of both dentin and enamel may lead to longer retention of the socket dimension and better bone regeneration. The organic part contains various growth factors that control cellular growth, proliferation, and differentiation such as bone morphogenetic proteins (BMPs).8–11 Previous studies consistently concluded that dentin has osteoconductive and osteoinductive potential. Clinical trials using dentin as bone fillers in alveolar ridge augmentation,12–14 socket preservation,15 sinus augmentation,16–18 and guided bone regeneration19 were investigated and obtained new bone formation results. The autogenous tooth bone graft has shown its potential as a bone substitute that can help hasten bone remodeling. As the tooth is autogenous, immunogenicity is reduced, medical waste is recycled, and expense is reduced for the patient.

The autologous demineralized tooth matrix (aDTM) has been developed and used clinically for bone substitution. Our recent case report showed that aDTM is safe and can maintain a proper alveolar ridge shape before dental implant placement. aDTM is biocompatible, bioresorbable, and facilitates new bone formation as shown radiologically and histologically.20

Platelet-rich fibrin (PRF) is a platelet concentrated suspension of growth factors, which contain autologous leukocytes and cytokines in a fibrin matrix.21 PRF is a biodegradable scaffold and a reservoir of growth factors that favors the epithelial cell migration to its surface.22,23 PRF can be prepared as membrane and can be used as a sole grafting material for sinus augmentation,24 resorbable membrane for guided bone regeneration,25,26 or seal an undetected sinus membrane perforation.27

The aDTM and PRF are autogenous and contain growth factors that can stimulate both soft- and hard-tissue healing. The preparations of aDTM and PRF are noninvasive, and the cost is relatively low. The application of aDTM in combination with PRF may have the potential to be used as a treatment for alveolar ridge preservation. This study aims to assess the efficacy of aDTM in combination with PRF membrane for preserving the alveolar ridge dimension and facilitating bone healing after tooth extraction.

Materials and Methods

The prospective split-mouth randomized clinical trial was approved by the Human Research Ethics Committee of the Faculty of Dentistry, Prince of Songkla University (MOE 0521.1.03/709). Calculation of the sample size was based on the study conducted by Suttapreyasri and Leepong.28 There was a difference of 15% in the buccal bone resorption between the treated and the control socket. With an α of 0.05 and 1 − β -0.80, a sample of at least 15 teeth per experimental group was required. This study was conducted at the Oral & Maxillofacial Surgery Clinic, Faculty of Dentistry, Prince of Songkla University. All patients provided written informed consent to participate in the study.

Healthy adult patients (>20 years old) in need of symmetrical premolar extraction for orthodontic treatment having a thin gingival biotype or thin buccal plate and presenting 3rd molar impaction were recruited for this study. Characteristics of a thin gingival biotype29 are described as having a narrow zone of keratinized tissue with less than 1.5-mm gingival thickness and 3.5- to 5-mm gingival width, as well as presenting a pronounced scalloped soft tissue and bony architecture with slight gingival recession and thin marginal bone.

Preparation of aDTM and PRF Membrane

The aDTM was prepared from the patient's own 3rd molar teeth. Briefly, the caries-free 3rd molar teeth were extracted at least a week before the alveolar ridge preservation. Soft tissues including the periodontal ligament and pulp were removed mechanically. The cleaned teeth were pulverized into small particles by a freezer mill (6770 Freezer/Mill; SPEXSamplePrep, Metuchen, NJ). Sieves with 500- and 700-μm aperture (Endecotts, London, United Kingdom) were used to select the desired particle size. The teeth particles were defatted, demineralized, freeze-dried, and sterilized with ethylene oxide gas before usage. The particle characteristics are shown in Figure 1.

Fig. 1
Fig. 1:
This figure shows aDTM characteristics: (A) aDTM particles in a dry condition, (B) aDTM soaked with normal saline solution.

Ten milliliters of autologous whole blood were collected from a median cubital vein (forearm) and immediately centrifuged using Hettich Zentrifugen centrifuge EBA 20 (Andreas Hettich GmbH &Co., KG, Tuttlingen, Germany) for 10 minutes at 3000 revolutions/min. A PRF clot was then obtained in the middle of the tube just between the red corpuscles at the bottom and the cellular plasma at the top. The PRF was collected and gently pressed on to create a PRF membrane using a sterile perforated metal spoon.

Surgical Procedure

The extraction sites were anesthetized with a local anesthesia. Extraction of the tooth was performed with a luxator and forceps to minimize the amount of trauma to the surrounding bone. After the tooth was removed, the buccal and lingual bone wall was carefully assessed for bone wall fracture, bone dehiscence, and bone plate loss. The sockets were assigned randomly to the aDTM/PRF or control group. In the aDTM/PRF group, the extraction sockets were filled with aDTM in layers until the extraction sockets were filled up to 1 mm below the marginal bone and covered with PRF membrane. In the control group, the sockets were sealed with PRF membrane. In both groups, figure-of-eight sutures, with resorbable suture material (Vicryl 4-0; Ethicon, Norderstedt, Germany), were used to secure the PRF membrane over the socket during the early healing period. Postoperatively, the patients were prescribed antibiotics (amoxicillin 500 mg, every 8 hours for 5 days) and anti-inflammatory drugs (ibuprofen 400 mg every 8 hours for 5 days). Sutures were removed 2 weeks after the operation.

Study Parameters

Clinical and radiographic examinations of the extraction sites were performed immediately after tooth extraction at baseline (T0), 2 (T2), 4 (T4), 6 (T6), and 8 (T8) weeks after tooth extraction. Tissue biocompatibility was performed by assessing the signs of acute and chronic infection at the extraction site, texture and color of the soft tissue covering the extraction site, and the existence of graft particle migration outside of the socket.

Changes of the alveolar ridge dimensions were assessed on a dental cast. Briefly, the cast of each time point was scanned with model scanners (3Shape D700, 3Shape A/S, Copenhagen, Denmark), and the casts at the follow-up period (T2, T4, T6, and T8) were superimposed with that of T0 using Ortho Analyzer software (3Shape). The alveolar ridge width alterations (buccal and lingual resorption) were measured from the horizontal line located 3 mm apically to the reference line, which connects the most apical point of the gingival marginal scallop of the adjacent teeth on the T0 cast (Fig. 2, A and B).

Fig. 2
Fig. 2:
A, cast at T0 (yellow) and T4 (green) captured by Ortho AnalyzerTM software. B, Measurement of alveolar ridge dimensional change from superimposed cast. The alveolar ridge width alterations (buccal and lingual resorption) were measured from the horizontal line located 3 mm apically to the reference line, which connects the most apical point of the gingival marginal scallop of the adjacent teeth on the T0 cast.

A periapical radiograph was taken digitally using a digital sensor, size 0 (BPD-I; BEMEMS Co. Ltd., Seoul, South Korea), with a standardized custom-lead step wedge attached to the sensor holder (XCP-DS, Rinn; Dentsply, Chicago, IL). The vertical resorption of marginal bones at the extraction site was determined using image analysis software (Apixia Digital Imaging Software 3.0; Masterlink, LLC., Glendale, CA) in the following ways (Fig. 3, A). A horizontal line was drawn to connect the cemento-enamel junction of the adjacent teeth. Then, the vertical lines perpendicular to the reference line were drawn and measured from the most coronal prominent point, mesially (M), distally (D), and from the center (C) of the sockets. The density of the extraction site was measured from a 2 × 2-mm area located at the end of the 5-mm line drawn perpendicularly from the reference line to the middle of the socket (E) (Fig. 3, B).

Fig. 3
Fig. 3:
A, The marginal bone resorption at the extraction site. Horizontal line is the radiographic cemento-enamel junction line. C is the bone resorption distance at the center of the socket orifice. D is the bone resorption distance at the distal side. M is the bone resorption distance at the mesial side. B, The density measurement area (E).

Data Analysis

All data were presented in mean values and SDs. One-way analysis of variance and a post hoc test with the Scheffé test was applied to detect differences among groups, when appropriate. The paired T Test was used to analyze the differences between the 2 groups. The statistical analysis was performed using SPSS (version 13, SPSS, Chicago, IL). P < 0.05 was considered statistically significant.

Results

A total of 40 extraction sites (24 maxillary premolars and 16 mandibular premolars) from 12 subjects (10 women, 2 men) aged 20 to 22 years (means, 20.5 ± 0.80 years) were included in the study.

All extraction sites healed uneventfully and similarly in both groups (Fig. 4). After tooth removal, the socket was carefully investigated. Three incomplete buccal plate fractures were found (2 sites in the aDTM/PRF group and 1 site in the control group). However, neither bone dehiscence nor buccal bone plate loss was observed in either group. No infection or complication of any kind was found after the operation. Soft tissue that covered the extraction site was normal in terms of texture and color, and the gingival tissues around the extraction site and at adjacent teeth seemed to be clinically healthy. There was no graft particle migration outside of the socket.

Fig. 4
Fig. 4:
The buccal and lingual contour reduction in dimension at the extraction sites. The 2 graphs show the mean reductions at week 2 to 8 of both control and test group. Asterisk (*) indicates that the differences are statistically significant at P < 0.05.

The dimensional changes at the buccal side and lingual/palatal side were shown in Figure 4. At baseline, no statistically significant differences between the aDTM/PRF and control group were found for any of the parameters assessed (P > 0.05). In both groups, the buccal contours reduction was more pronounced than the lingual side. The buccal contraction in the aDTM/PRF group (T2: 0.39 ± 0.11, T4: 0.65 ± 0.24, T6: 0.89 ± 0.37, and T8: 1.04 ± 0.40 mm) was significantly less than the control group (T2: 0.53 ± 0.17, T4: 0.86 ± 0.29, T6: 1.14 ± 0.28, and T8: 1.34 ± 0.37 mm) at every time point. The lingual resorption in the aDTM/PRF group was also less than the control group; however, no statistically significant differences were found among the groups for all time frames.

Radiologically, the socket in the aDTM/PRF group revealed the radiopaque granules of aDTM fully saturating the entire socket. The sequential radiographic demonstrated the aDTM particles were gradually resorbed but still visible at 8 weeks after the operation (Fig. 5). The vertical resorption distances of marginal bone on the mesial side, distal side, and at the center of the sockets in the aDTM/PRF group (0.67 ± 0.47, 0.93 ± 0.39, 0.79 ± 0.47 mm) were not significantly different from those of the control group (0.86 ± 0.31, 0.81 ± 0.42, 0.70 ± 0.28 mm). No statistically significant differences were detected between the groups throughout all time frames at 2, 4, 6, and 8 weeks after extraction (P > 0.05) (Fig. 6).

Fig. 5
Fig. 5:
The radiographs of the socket sites after extraction (T0), at the 4th week (T4), and at the 8th week (T8) of both control and test group.
Fig. 6
Fig. 6:
The marginal bone resorption at the extraction sites measured from radiographs. Each graph shows the resorptions of both control and test group at mesial side, lingual side, and at the central of socket bone. None of the differences is statistically significant at P < 0.05.

Throughout the 8-week period, bone healing density in the aDTM/PRF group (T0: 37.17 ± 7.21, T2: 38.91 ± 6.00, T4: 45.22 ± 13.27, T6: 48.03 ± 8.95, and T8: 44.84 ± 9.12) was higher than in the control group (T0: 23.39 ± 7.62, T2: 23.02 ± 6.74, T4: 31.32 ± 14.50, T6: 31.28 ± 13.42, and T8: 35.85 ± 15.15). However, the results were only statistically significant during the first 6 weeks (P < 0.05) (Fig. 7).

Fig. 7
Fig. 7:
The radiographic density at extraction sites. Asterisk (*) indicates that the differences is statistically significant at P < 0.05.

Discussion

This study evaluated whether the use of aDTM with PRF, which contain autologous biomaterials, could minimize the alveolar ridge resorption after tooth extraction on the basis of clinical parameters and radiographs. The results indicated that the aDTM in combination with PRF membrane significantly decreases the buccal ridge collapse and promotes bone healing, and could be used effectively for alveolar ridge preservation after tooth extraction.

After the tooth was removed, consequent bone remodeling began and remained intact for years. The thickness of the buccal and lingual cortical bone as well as the height of the interproximal bone influenced the dimensional change of the remaining alveolar ridge.30 Previous animal and clinical studies demonstrate a greater amount of bone loss for the buccal side when compared with the lingual side.1,28,31,32 This may be attributed to the higher proportion of resorption-prone bundle bone of the buccal plate, which in normal extraction procedure may show some degree of bone defect. Therefore, this study included all extraction sockets to represent the real situation.

aDTM was previously reported as a bone graft substitution before implant placement.20 After a 4-month period, the alveolar ridge filled with aDTM and was covered with a free palatal gingival graft showing good ridge architecture and no sign of graft rejection. The histologic examination demonstrated that aDTM was incorporated into the new bone with the evidence of osteoid formation around the particles. Graft resorption was marked by the resorption rim.20 aDTM, constituting autologous biomaterials, may be a good alternative for bone substitution because it is osteoconductive and osteoinductive as it contains various growth factors essential for bone regeneration such as BMPs, Transforming growth factor–beta (TGF-β), and insulin-like growth factor–1 and insulin-like growth factor–2 (IGF-1 and IGF-2).28 In addition, aDTM is prepared from the patient's own teeth, and the cost of grafting is cheaper than commercial allografts or xenograft bone substitution.

Usage of the resorbable membrane and other socket covering material has been actively investigated, but no consensus has been reached. The shortcomings of using a resorbable membrane in socket preservation have been reported.33,34 It tends to expose the membranes, stimulate inflammatory cell response, require longer surgical time, and incur higher treatment costs. To avoid these complications, this study did not use occlusive membranes, and a PRF membrane closure of the socket was applied instead. Regarding PRF membrane influence, a study by Suttapreyasri and Leepong28 found that PRF has no part in maintaining alveolar ridge shape; however, it hastened soft-tissue healing. Therefore, in this study, the PRF was used as the sealing material in both the DTM and the control group but only to retain auto-DTM particles within the sockets and help the orifices. As PRF has no effect on ridge preservation, the phenomenon found in this study is derived from auto-DTM alone.

Concerning the use of autologous teeth as a bone graft substitution, many studies have stated that they found success when using teeth as bone grafting material for alveolar ridge preservation. Gomes et al35 reported the healing process of the third molar socket filled with autogenous demineralized dentin matrix (ADDM) and covered with polytetrafluoroethylene (PTFE) membrane for 90 days. The result showed that the healing process was faster in the ADDM + PTFE group than the empty socket and the PTFE alone groups. The radiographic bone density of the socket filled with ADDM was similar to that of the surrounding normal bone on the 90 day. A similar outcome was also reported by Valdec et al36 who used autologous dentin particles and free palatal gingival grafts for alveolar ridge preservation. After 4 months, a subsequent implant was successful both functionally and aesthetically. Kim et al15 reported on a preserved extraction socket with autogenous tooth bone graft powder and blocks in 2 patients. After the healing period of 3 to 3.5 months, good healing progress was achieved, and the subsequent implant treatment was performed successfully. In agreement with this study, an autogenous tooth matrix has the potential and is safe to be used as a bone graft substitution. To the best of our knowledge, no previous study regarding a randomized controlled clinical trial using an autogenous tooth matrix has been performed. Because the aDTM and PRF are autogenous biomaterials containing growth factors related to soft tissue and bone healing, the application of these biomaterials as grafting materials for alveolar ridge preservation may be the choice of treatment.

The total horizontal ridge change at 8 weeks after extraction in the aDTM/PRF group was 1.84 ± 0.48 mm, which is comparable with previous studies using various graft materials. Aimtti et al37 reported 2 mm of horizontal bone resorption after 3 weeks of preserving the ridge with calcium sulfate. Kesmas et al38 used biphasic calcium phosphate (HA/b-TCP: 60/40) in combination with collagen membrane and demonstrated 2 mm of horizontal ridge change at 16 weeks postoperatively. In addition, Brownfield and Weltman39 used the demineralized bone matrix with cancelous bone chips as a graft material and demonstrated 1.60 ± 0.80 mm of total horizontal ridge change at 10 to 12 weeks postoperatively. However, the greater horizontal ridge contraction in this study resulted from the inclusion of subjects with thin gingival biotypes or thin buccal plates, and some of the extraction sites presented incomplete buccal bone fractures, which was more prone for buccal plate resorption.

In this study, the vertical mesial and distal bone resorption as well as the bone center of socket reduction was examined using periapical radiographs. However, there was no significant difference between the 2 groups. As the examined ridge was situated between adjacent teeth, the Shapey's fiber of the adjacent teeth could anchor the periosteum and maintain the mesial and distal marginal bone level. Regarding limitations in the plain radiographs, they revealed only 2 dimensions of the true 3-dimension anatomy because the level of bone height, which was the average of the buccal and lingual12 bone wall, was difficult to identify. A Cone-beam computed tomography (CBCT)CT, if available, is recommended for the measurement of delicate images.

The previous study showed that even with various ridge preservation techniques, there will eventually be some loss of bone.40 Regarding the results of our study, the use of aDTM and PRF could, to some extent, maintain the ridge dimensions after extraction, but it would eventually be subject to some loss as mentioned in previous studies.

The design of this study was to inherently reduce bias selection through a randomized process that allowed the researcher to determine the influence of the intervention when compared with the control group. The split-mouth design used in this study also had the advantage of removing intersubject variability. However, the limitation of the study is that the patients, who were receiving orthodontic treatments, required scheduled orthodontic force within 8 weeks. This limited the study to conclude within an 8-week period, and the researcher could not harvest the bone sample to analyze bone quality at the socket preservation sites. Further clinical trial studies should be performed on patients who are planning to restore edentulous areas with a dental implant, so that the researcher can determine the bone histomorphometry and graft degradation characters.

aDTM can be categorized as a short-term ridge preservation material from the radiographic evidence as it gradually resorbed and integrated with the surrounding bone within the period of 8 weeks. The degradation property of the aDTM came from the demineralizing process that resulted in lower mineral components and crystallinity. The demineralization process also increased the bioavailability from the organic component resulting in improved new bone formation.12

Conclusion

In conclusion, application of aDTM with PRF membrane is useful for alveolar ridge preservation by reducing horizontal alveolar ridge collapse and promoting bone healing for up to 8 weeks as shown clinically and radiographically.

Disclosure

The authors claim to have no financial interest, either directly or indirectly, in the products or information listed in the article.

Approval

The prospective split-mouth randomized clinical trial was approved by the Human Research Ethics Committee of the Faculty of Dentistry, Prince of Songkla University (MOE 0521.1.03/709).

Roles/Contributions by Authors

W. Ouyyamwongs: performing the experiment, data analysis, and drafting the research paper. N. Leepong: design the experiment and supervise the experiments. S. Suttapreyasri: conception and design the experiment, revising, and approval the final version of the publication.

Acknowledgments

Graduate School Research Support Funding for the fiscal year 2015, Graduate School, Prince of Songkla University, Songkhla, 90112, Thailand.

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Keywords:

autogenous tooth; bone graft material; socket dimension

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