The success of implant dentistry has been largely related to the advent of bone augmentation techniques that allow for the regeneration of atrophic alveolar ridges into an ideal ridge form for placement of implants in an ideal functional and esthetic position. Horizontal resorption of the alveolar ridge and subsequent lack of adequate width for optimal implant placement are frequent conditions after extraction of teeth. Other factors that may result in alveolar deficiencies include physiologic bone resorption, trauma, congenitally missing teeth, periodontal disease, etc. The literature reflects a variety of techniques and combinations of materials in an attempt by clinicians to find the most effective and predictable means of ridge augmentation.1–10
A number of surgical procedures have been documented to reconstruct the lost ridge width. These include bone grafting with different grafting materials (autograft, allograft, alloplast, and xenograft), ridge split osteotomy technique, distraction osteogenesis, and GBR alone or with combination of other grafting materials or growth factors.1–10 The gold standard for ridge augmentation is considered to be autogenous block graft.2 It is considered ideal material for grafting because of its inherent osteogenic, osteoinductive, and osteoconductive properties. The disadvantage of using autogenous graft harvesting is complications associated with a second surgical site and graft resorption. Allografts, on the other hand, have shown good results and are not associated with donor site morbidity and are available in many forms (blocks, particulate, or putty).9,10 Some have advocated mixing autogenous bone with the various bone substitutes to combine the osteoinductive growth factors of autogenous bone with the osteoconductive properties of an allograft.11,12
Optecure-CCC (Exactech, Inc., Gainesville, FL) is a demineralized bone matrix (DBM) allograft that has verified osteoinductive properties in athymic mice.13,14 This DBM is a second-generation matrix graft and contains about 2X higher concentration of bone morphogenetic proteins than the first-generation DBM product (Regenaform; Exactech, Inc.) which also had lot verified osteoinductive properties. DBM is in a putty form, and the matrix is mixed with corticocancellous chips. DBM provides osteoinductive potential while the corticocancellous particles add stability and volume to the graft. The main advantage of using DBM over autogenous bone particles is to avoid a second surgical site and to prevent donor site morbidity.
Guided bone regeneration is based on the principle of selective cell repopulation and epithelial and connective tissue exclusion. Various resorbable and nonresorbable membranes have been used as barriers to provide ideal environment for bone regeneration by soft-tissue exclusion, clot stabilization, and space maintenance for the bone substitute graft.4–8,10–12,23,25,26 Nonresorbable membranes are associated with complications such as membrane exposure and higher need for additional grafting procedures compared with resorbable membranes.8 Acellular dermal matrix (ADMG) is a donor dermis membrane that is treated to remove all cellular components leaving only the extracellular matrix. It heals by incorporating into host tissue. The acellular dermal matrix - GBR membrane is designed for GBR. It is the thinner version of membrane which is used for root coverage procedures.
The primary aim of this randomized, controlled, blinded clinical trial was to compare a mix of particulate allograft and autogenous particles (70:30) to an osteoinductive DBM allograft to determine whether autogenous harvesting would provide any osteoinductive advantage over the bone morphogenetic proteins contained in a DBM allograft putty.
Materials and Methods
A total of 16 patients were included in this 4-month study of ridge augmentation of horizontally deficient ridges that were treatment planned to receive a dental implant. The positive control (DBM) had 7 patients who were randomly selected, using a coin toss, to receive a DBM allograft with cortical cancellous chips (Optecure-CCC; Exactech) secured with a bone screw (Salvin Dental Specialities, Inc., Charlotte, NC). The test group (Autogenous) had 7 test patients who received corticocancellous allograft (MinerOss; BioHorizon, Birmingham, AL) mixed with particulate autogenous bone chips in a 70:30 ratio. The autogenous bone chips were harvested from sites adjacent to the deficient ridge using a Safescraper TWIST—curved version (Osteogenics Biomedical, Lubbock, TX). Corticocancellous particulate allograft was used as the buccal overlay graft for both groups and then covered with an ADMG membrane (AlloDerm GBR RTM; BioHorizon). ADMG transitions into the patient's own tissue. After 4 months of healing, the site was re-entered and clinical measurements taken. A trephine core was removed from the osteotomy site for histological evaluation, and the site was prepared for implant placement. All measurements were performed by a blinded examiner (A.R.), who was unaware of the treatment assignment at all time points. All patients signed an informed consent approved by the University of Louisville Institutional Review Board in July 2015. This study was conducted in accordance with the Helsinki Declaration of 1975, as revised in 2000. The study was conducted between August 2015 and May 2016 in the Graduate Periodontics clinic at the University of Louisville.
The primary outcome variable was horizontal ridge width at the crest, and the power analysis was based on this variable. Other variables evaluated included: vertical ridge dimension change and histologic assessment of vital bone, nonvital bone, and trabecular space.
Subjects were enrolled in the study if they met the following inclusion criteria: (1) at least a 1 tooth area with a ridge defect and treatment planned to receive a dental implant. The site must be bordered by at least 1 tooth. Ridge defect should be classified as Seibert class I or III,15 (2) healthy person who is at least 18 years old, and (3) patient who understands and signs informed consent approved by the University of Louisville Human Studies Committee.
(1) Debilitating systemic diseases, or diseases that have a clinically significant effect on the periodontium; (2) previous head and neck radiation or chemotherapy within the previous 12 months; (3) known allergy to any material or medication used in the study; (4) smokers; (5) require antibiotic prophylaxis; (6) history of intravenous bisphosphonate use or oral bisphosphonate use for more than 3 years; (7) long-term steroid therapy; (8) pregnancy; (9) failure to sign informed consent approved by the Human Studies Committee; and (10) patients were excluded after treatment if they failed to follow the post-treatment protocol, loss of graft or membrane, or any unanticipated healing complications that adversely affect treatment results.
Clinical and Radiographic Parameters
At the initial visit, each patient received a diagnostic work-up that included a full periodontal examination, standardized periapical radiographs using a stent, diagnostic study casts, plaque and gingival indices, bleeding on probing, adjacent tooth mobility, keratinized tissue width, and a full periodontal examination.16–18 For each patient, study casts were used to fabricate acrylic occlusal stents to record vertical hard tissue measurements from a fixed reference guide.
Horizontal ridge width was measured with a modified digital caliper to the nearest 10−2 mm at the midridge crestal level and then 5 mm apically. Vertical distance from the acrylic stent to the alveolar crest was measured using a UNC-15 periodontal probe. A size 30 endodontic file with rubber stopper was used to record soft-tissue thickness at crest, 5 mm apical to crest and to the midocclusal of the deficient ridge.
These clinical and radiographic measurements were repeated at re-entry after 4 months of healing.
The surgical procedure consisted of sulcular incisions around teeth with mesial and distal vertical releasing incisions. A superficial split-thickness flap was reflected on the buccal, and a full thickness flap was reflected on the lingual to expose the residual alveolar ridge. This technique gives tension-free primary closure (Figure 5).19 Multiple cortical perforations were performed with a 1/2 round bur to increase angiogenesis and supply of growth factors in all defect areas (A).20 A titanium bone screw was placed to achieve 8 to 10 mm of total horizontal ridge width and to aid in graft stability. The graft was extended at least 10 to 12 mm in the apicocoronal direction. Both the groups received a buccal overlay with a corticocancellous particulate allograft. For the test group, the autogenous bone chips were harvested from adjacent sites near the exposed ridge, hence avoiding the need for a second surgical site (Figure 6). The grafted site was covered with ADMG membrane. Tension-free primary flap closure was achieved and sutured using a 4-0 polytetrafluoroethylene suture (Cytoplast; Osteogenics Biomedical, Lubbock, TX). Prescriptions were given for a Medrol dose pack, amoxicillin 500 mg three times a day for 7 days, and narcotic analgesics, as needed. Sutures were removed in 2 to 4 weeks. Patients were seen approximately every 2 weeks until at least 12 weeks healing had occurred. Thereafter, they were seen monthly until the 4-month re-entry for implant placement. No appliances were allowed for any sites.
The bone cores were decalcified, and step serial sections were taken from the center of each longitudinally sectioned core. The sections were stained with hematoxylin and eosin. Six randomly selected fields, 1 per section if possible, were used to obtain percent vital bone, nonvital bone, and trabecular space using an American Optics light microscope at 150× with a 10× objective and 15× reticle eyepieces.
Mean values and SDs were calculated for all parameters. The data were analyzed using a paired t test to determine the statistical significance of the differences between initial and final data. An unpaired t test was used to evaluate statistical differences between the test and control groups. The sample size of 7 gave statistical power of 81% to detect a difference of 1-mm ridge width between the groups. The mean and SD used for the power calculation were based on data from a previous study.
A total of 16 patients were included in the study. Two patients failed to follow the study protocol and were excluded from the study, leaving 14 for data analysis. For the Autogenous group, there were 6 women and 1 man, with a mean age of 49 ± 16, ranging from 21 to 69 years, whereas for the DBM group, there were 4 women and 3 men, with a mean age of 48 ± 9, ranging from 36 to 62 years. Specific tooth sites are noted in Table 2.
Clinical Indices and Probing Measurements
The changes between initial to final data for plaque index, gingival index, bleeding on probing, probing depth, recession, and mobility values were minimal and not statistically significant, and there were no significant differences between groups (P > 0.05). Keratinized tissue decreased from 2.9 ± 2.3 to 2.7 ± 2.0 mm for the Autogenous group and from 2.5 ± 1.6 to 2.1 ± 1.3 mm for the DBM group, which was not statistically significant between or within groups (P > 0.05).
Alveolar Ridge Width Changes at Crest
There was a significant gain in crestal ridge width in both the groups from initial to final measurements (P < 0.05). For the Autogenous group, the mean crestal width increased from 3.2 ± 0.7 mm to 6.7 ± 1.7 mm for a gain of 3.5 ± 1.4 mm (P < 0.05), and for the DBM group, the mean crestal width increased from 3.0 ± 0.6 mm to 6.8 ± 1.9 mm for a gain of 3.8 ± 1.6 mm (P < 0.05). There were no statistically significant differences between groups (P > 0.05, Table 1) (Figures 1–4, 7–9).
Alveolar Ridge Width Changes 5 mm Apical to the Crest
The mean width for the Autogenous group increased from 6.0 ± 1.7 to 8.5 ± 2.0 mm for a gain of 2.5 ± 1.4 mm (P < 0.05), whereas for the DBM group, the mean width increased from 5.8 ± 1.1 to 8.8 ± 1.0 mm for a gain of 3.0 ± 0.9 mm (P < 0.05). There were no statistical significant differences between groups (P > 0.05).
Alveolar Ridge Height Changes Relative to a Stent
The alveolar midridge height change from the initial to the 4-month re-entry for the Autogenous group was 0.0 ± 0.8 mm, whereas for the DBM group, there was a vertical loss of −0.3 ± 0.6 mm (P > 0.05). The difference between groups, however, was not statistically significant (P > 0.05).
The predictability of achieving a ≥ 6-mm ridge width was 57% for the Autogenous group and 86% for the DBM group (Table 1). The frequency of achieving placement of the planned implant size was 29% for both the Autogenous and the DBM groups (Table 2). The frequency of achieving placement of implant was 71% for both the groups (Table 2).
Loss of Augmented Ridge Width at the Crest
The Autogenous group lost 2.9 ± 1.9 mm or 30% of the augmented width (P < 0.05). The DBM group lost 2.3 ± 1.9 mm or 25% of its augmented width (P < 0.05). There were no statistically significant differences between groups (P > 0.05).
Change in Soft-Tissue Thickness
For the Autogenous group, initial soft-tissue thickness at the crest was 2.1 ± 0.6 mm, which increased to 2.5 ± 0.3 mm for a gain of 0.4 ± 0.7 mm (P > 0.05). For the DBM group, initial soft-tissue thickness at the crest was 2.0 ± 0.9 mm, which increased to 2.9 ± 0.5 mm for a gain of 0.9 ± 0.8 mm (P < 0.05). There were no statistically significant differences between groups (P > 0.05).
The Autogenous group had a mean of 35% vital bone, 26% nonvital bone, and 39% trabecular space. The DBM group had a mean of 39% vital bone, 24% nonvital bone, and 37% trabecular space. There were no statistically significant differences between groups (P > 0.05) (Figures 10 and 11).
In this study, a mix of corticocancellous particulate allograft and autogenous bone chips in a 70:30 ratio was compared with lot verified osteoinductive DBM allograft. The Autogenous group had a mean gain in crestal ridge width of 3.5 ± 1.4 mm (112%) compared with 3.8 ± 1.6 mm (128%) obtained for the DBM group. Both groups showed a statistically significant improvement from initial ridge width (P < 0.05, Table 1). The difference between groups was not statistically significant.
The magnitude of the mean crestal ridge width change of 3.5 mm for the Autogenous group is similar and compares favorably with previous literature.21–23 Beitlitum et al compared autogenous particulate overlaid with freeze-dried bone allograft to freeze-dried bone allograft alone. He showed a ridge width gain of 3.6 mm after 6 months of healing.21 A recent study by Caldwell et al22 showed a final ridge width of 6.9 mm with a gain of 3.1 mm using a 1:1 mix of autogenous bone chips and corticocancellous particulate allograft. By contrast, this study showed a final ridge width of 6.7 mm with a gain of 3.5 mm in using a 70:30 mix of allograft and autogenous bone chips. Mordenfeld et al23 compared a mix of xenograft and autogenous particulate harvested from ramus in 2 different ratios of 90:10 and 60:40. The study showed a 2.9-mm ridge width gain for the 90:10 group and 3.5 mm gain for the 60:40 group showing higher gains in horizontal ridge width with a higher volume of autogenous bone. This study used a 70:30 ratio for corticocancellous allograft and autogenous bone chips with mean crestal width gain of 3.5 mm. This similar ridge width gain can be attributed to the osteogenic potential of the autogenous bone particles. Another point to be taken into consideration is the healing time. Mordenfeld et al had an average healing time of 8.1 months for the grafted sites while this study had 4-month healing time. Xenografts tend to take longer time to heal compared with autografts and allografts. The use of corticocancellous allograft in this study allowed the implant placement after 4 months. The results from this study are comparable with those by Beitlitum et al, Caldwell et al, and Mordenfeld et al.
The results from this study are comparable with those of a recent systematic review by Milinkovic and Cordaro.24 They reported a mean ridge width gain from particulate or DBM grafts yielded a mean gain of 3.3 mm and a final ridge width of 6.2 mm. Toscano et al25 showed horizontal ridge width gain of 3.5 mm on 73 consecutively treated cases using DBM (Regenaform, Exactech) and a resorbable membrane. Geurs et al26 showed final ridge width of 5.2 mm with a mean ridge width gain of 2.8 mm after 6 months, using a composite graft using DBM (Regenaform, Exactech) covered with a resorbable membrane. In this study, the DBM group gained 3.8 mm and a final mean ridge width of 6.8. The larger gain in our study may be due to the increased amount of lot verified osteoinductive activity which was 2X the amount in the first-generation DBM.
Very few commercially available demineralized allografts are lot tested for their osteoinductive capability. The DBM used in this study is laboratory verified and tested for its property of osteoinduction using a nude mouse model to test ectopic bone formation in muscle tissue. Schwartz et al27 reported that osteoinductive efficiency of many untested grafting materials is unreliable due to different factors, donor age being one of them. The fact that verified osteoinductive material was used may account for the slightly larger ridge width gains with the DBM treatment. Based on the crestal ridge width data, it can also be concluded that, in this study, both the autogenous and the DBM treatments were similarly successful.
Another important parameter to evaluate is the periodontal biotype. It is important to evaluate this parameter as thick periodontal biotype may be important in prevention of future recession around the implant.28–30 The soft tissue increased in thickness by a mean of 0.7 mm using the ADMG membrane. A recent study by Puisys et al29 showed a gain of 2.21 mm in soft-tissue thickness after augmentation with ADM membrane. The higher gain by Puisys et al can be attributed to the thickness of the ADM membrane. The original ADM membrane has a thickness of 0.9 to 1.6 mm, whereas the ADMG membrane used in this study has a thickness of 0.5 to 0.9 mm. The choice of the bone graft materials and barrier membrane may have effect on soft-tissue thickness, and the materials chosen for this study produced a 0.7-mm soft-tissue thickening. Another study by Linkevicius et al30 showed that sites with crestal tissue thickness of 2 mm or less around implants can lead to bone loss even when the microgap was placed supracrestally. Hence, using an allograft such as acellular dermal matrix in sites with thin soft-tissue biotype may be beneficial to increase soft-tissue thickness at future implant site.
The histology between the 2 groups was similar when compared with previous literature. Nine histologic cores, 4 from the Autogenous group and 5 from the DBM group, were analyzed, and 35% to 39% vital bone was found with no statistically significant differences between groups (P > 0.05).
In this study, both groups, corticocancellous allograft plus autogenous bone chips (70:30) and the DBM allograft provided similar and significant gains in mean ridge width. Histologically, both the groups had similar (35%–39%) amounts of vital bone at the site of implant placement. Within the limitations of this study, DBM allograft can be considered a good substitute for particulate autogenous bone graft which requires a second surgical site and is associated with donor site morbidity.
The authors claim to have no financial interest, either directly or indirectly, in the products or information listed in the article.
All patients signed informed consent approved by the University of Louisville Institutional Review Board in July 2015. This study was conducted in accordance with the Helsinki Declaration of 1975, as revised in 2000. The study was conducted between August 2015 and May 2016 in the Graduate Periodontics Clinic at the University of Louisville.
Roles/Contributions by Authors
A. Patel: primary investigator, all surgeries are performed by primary investigator. H. Greenwell: research mentor and thesis committee chair. M. Hill: thesis committee member. B. Shumway: thesis committee member. A. Radmall: blinded examiner.
1. Antoun H, Sitbon JM, Martinez H, et al. A prospective randomized study comparing two techniques of bone augmentation: Onlay graft alone or associated with a membrane. Clin Oral Implants Res. 2001;12:632–639.
2. Pikos M. Mandibular block autografts for alveolar ridge augmentation
. Atlas Oral Maxillofac Surg Clin North Am. 2005;13:91–107.
3. Buser D, Bragger U, Lang NP, et al. Regeneration and enlargement of jaw bone using guided tissue regeneration. Clin Oral Implants Res. 1990;1:22–32.
4. Von Arx T, Buser D. Horizontal ridge augmentation using autogenous block grafts and the guided bone regeneration
technique with collagen membranes: A clinical study with 42 patients. Clin Oral Implants Res. 2006;17:359–366.
5. Hammerle CH, Jung RE, Yaman D, et al. Ridge augmentation by applying bioresorbable membranes and deproteinized bovine bone mineral: A report of twelve consecutive cases. Clin Oral Implants Res. 2008;19:19–25.
6. Kassolis JD, Rosen PS, Reynolds MA. Alveolar ridge and sinus augmentation utilizing platelet-rich plasma in combination with freeze-dried bone allograft: Case series. J Periodontol. 2000;71:1654–1661.
7. Misch CM. Bone Augmentation of the atrophic posterior mandible for dental implants using rhBMP-2 and titanium mesh: Clinical technique and early results. Int J Periodontics Restorative Dent. 2011;31:581–589.
8. Jensen SS, Terheyden H. Bone augmentation procedures in localized defects in the alveolar ridge: Clinical results with different bone grafts and bone substitute materials. Int J Oral Maxillofac Implants. 2009;24:218–236.
9. Benic GI, Hammerle CH. Horizontal bone augmentation by means of guided bone regeneration
. Periodontol 2000. 2014;66:13–40.
10. Lyford RH, Mills MP, Knapp CI, et al. Clinical evaluation of freeze-dried block allografts for alveolar ridge augmentation
: A case series. Int J Periodontics Restorative Dent. 2003;23:417–425.
11. Urban IA, Nagursky H, Lozada JL, et al. Horizontal ridge augmentation with a collagen membrane and a combination of particulated autogenous bone and anorganic bovine bone-derived mineral: A prospective case series in 25 patients. Int J Periodontics Restorative Dent. 2013;33:299–307.
12. Urban IA, Lozada JL, Jovanovic SA, et al. Vertical ridge augmentation with titanium-reinforced, dense-PTFE membranes and a combination of particulated autogenous bone and anorganic bovine bone-derived mineral: A prospective case series in 19 patients. Int J Oral Maxillofac Implants. 2014;29:185–193.
13. Urist MR. Bone: Formation by autoinduction. Science. 1965;150:893–899.
14. Urist MR, Strates BS. Bone morphogenetic proteins. J Dent Res. 1971;50:1392–1406.
15. Seibert JS. Reconstruction of deformed, partially edentulous ridges, using full thickness onlay grafts. Part I. Technique and wound healing. Compend Contin Educ Dent. 1983;4:437–453.
16. Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand. 1964;22:121–135.
17. Lobene RR, Weatherford T, Ross NM, et al. A modified gingival index for use in clinical trials. Clin Prev Dent. 1986;8:3–6.
18. Laster L, Laudenbach K, Stoller N. An evaluation of clinical tooth mobility measurements. J Periodontol. 1975;46:603–607.
19. Greenwell H, Vance G, Munninger B, et al. Superficial-layer split-thickness flap for maximal flap release and coronal positioning: A surgical technique. Int J Periodontics Restorative Dent. 2004;24:521–527.
20. Rompen EH, Biewer R, Vanheusden A, et al. The influence of cortical perforations and of space filling with peripheral blood on the kinetics of guided bone generation. A comparative histometric study in the rat. Clin Oral Implants Res. 1999;10:85–94.
21. Beitlitum I, Artzi Z, Nemcovsky CE. Clinical evaluation of particulate allogeneic with and without autogenous bone grafts and resorbable collagen membranes for bone augmentation of atrophic alveolar ridges. Clin Oral Implants Res. 2010;21:1242–1250.
22. Caldwell GR, Mills MP, Finlayson R, et al. Lateral alveolar ridge augmentation
using tenting screws, acellular dermal matrix, and freeze-dried bone allograft alone or with particulate autogenous bone. Int J Periodontics Restorative Dent. 2015;35:75–83.
23. Mordenfeld A, Johansson CB, Albrektsson T, et al. A randomized and controlled clinical trial of two different compositions of deproteinized bovine bone and autogenous bone used for lateral ridge augmentation. Clin Oral Implants Res. 2014;25:310–320.
24. Milinkovic I, Cordaro L. Are there specific indications for the different alveolar bone augmentation procedures for implant placement? A systematic review. Int J Oral Maxillofac Surg. 2014;43:606–625.
25. Toscano N, Holtzclaw D, Mazor Z, et al. Horizontal ridge augmentation utilizing a composite graft of demineralized freeze-dried allograft, mineralized cortical cancellous chips, and a biologically degradable thermoplastic carrier combined with a resorbable membrane: A retrospective evaluation of 73 consecutively treated cases from private practice. J Oral Implantol. 2010;36:467–474.
26. Geurs NC, Korostoff JM, Vassilopoulos PJ, et al. Clinical and histologic assessment of lateral alveolar ridge augmentation
using a synthetic long-term bioabsorbable membrane and an allograft. J Periodontol. 2008;79:1133–1140.
27. Schwartz Z, Mellonig JT, Carnes DL Jr, et al. Ability of commercial demineralized freeze-dried bone allograft to induce new bone formation. J Periodontol. 1996;67:918–926.
28. Kan JY, Rungcharassaeng K, Morimoto T, et al. Facial gingival tissue stability after connective tissue graft with single immediate tooth replacement in the esthetic zone: Consecutive case report. J Oral Maxillofac Surg. 2009;67:40–48.
29. Puisys A, Vindasiute E, Linkevciene L, et al. The use of acellular dermal matrix membrane for vertical soft tissue augmentation during submerged implant placement: A case series. Clin Oral Implants Res. 2015;26:465–470.
30. Linkevicius T, Apse P, Grybauskas S, et al. The influence of soft tissue thickness on crestal bone changes around implants: A 1-year prospective controlled clinical trial. Int J Oral Maxillofac Implants. 2009;24:712–719.