ORIGINAL ARTICLE
Alveolar Ridge Preservation With Deproteinized Bovine Bone Graft and Collagen Membrane and Delayed Implants Chaoyuan Pang, Yuxiang Ding, DDS, Hongzhi Zhou, DDS, Ruifeng Qin, DDS, Rui Hou, DDS, Guoliang Zhang, MD, and Kaijin Hu, DDS Abstract: To evaluate clinically and radiographically an alveolar ridge, preservation technique with deproteinized bovine bone graft and absorbable collagen membrane and then restoration with delayed implants were done. The study included 30 patients. The trial group’s sockets were filled with deproteinized bovine bone graft (Bio-Oss) and covered with absorbable collagen membrane (Bio-Gide). The control group’s sockets healed without any treatment. Panoramic radiograph and computed tomography were taken immediately after graft and 3 and 6 months later to evaluate the height, width, and volume change of the alveolar ridge bone. Dental implants were inserted in all sockets at 6 months, and osseointegration condition was evaluated in the following 12 months. All sockets healed uneventfully. In the trial group, the mean (SD) height reduction of the alveolar ridge bone was 1.05 (0.24) mm at 3 months and 1.54 (0.25) mm at 6 months. The width reduction was 1.11 (0.13) mm at 3 months and 1.84 (0.35) mm at 6 months. Bone volume reduction was 193.79 (21.47) mm3 at 3 months and 262.06 (33.08) mm3 at 6 months. At the same trend, in the control group, the bone height reduction was 2.12 (0.15) mm at 3 months and 3.26 (0.29) mm at 6 months. The width reduction was 2.72 (0.19) mm at 3 months and 3.56 (0.28) mm at 6 months. Bone volume reduction was 252.19 (37.21) mm3 at 3 months and 342.32 (36.41) mm3 at 6 months. There was a significant difference in alveolar ridge bone height, width, and volume reduction in the 2 groups. The osseointegration condition had no significant difference between the 2 groups. This study suggested that the deproteinized bovine bone graft and absorbable collagen membrane were beneficial to preserve the alveolar ridge bone and had no influence on the osseointegration of delayed implant.
From the Department of Stomatology, State Key Laboratory of Military Stomatology, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China. Received October 24, 2013. Accepted for publication February 9, 2014. Address correspondence and reprint requests to Kaijin Hu, Department of Oral Surgery, School of Stomatology, Fourth Military Medical University, 145 Western Changle Road, Xi’an, 710032, PR China; E-mail: [email protected]; and Yuxiang Ding, Department of Oral Surgery, School of Stomatology, Fourth Military Medical University, 145 Western Changle Road, Xi’an, 710032, PR China; E-mail: [email protected] Chaoyuan Pang and Yuxiang Ding equally contributed to this article. The authors report no conflicts of interest. Copyright © 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000000887
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Key Words: Socket preservation, tooth extraction, Bio-Oss, Bio-Gide, delayed implant (J Craniofac Surg 2014;25: 1698–1702)
D
ental implant is more and more popular because there are no damages on the adjacent teeth. The implant inserted in the alveolar ridge bone has the same function as the natural tooth root, which can bear and transfer chewing force well. The condition of alveolar ridge bone after tooth extraction is very important, which can influence the delayed dental implant placement. Periodontitis, bony wall fracture, or lack of intraoperative intervention usually leads to the deficiency of alveolar ridge bone volume. Dental implant placement also becomes impossible because of serious bone resorption. Buccal side lamella bone of the anterior tooth is very thin and easily causes bone resorption and gingival recession after tooth extraction, which results in esthetic risks mostly. It always needs autogenous bone graft or bone splitting technique to increase bone thickness. However, the operation procedure is difficult and causes esthetic risks easily. In the molar area, lack of alveolar ridge bone height usually results in maxillary sinus or inferior alveolar nerve damage easily. So before dental implant placement, it always needs maxillary sinus lifting or alveolar ridge augmentation, which demands high operation level of physician and results in some complications. The bone volume of alveolar ridge decides the diameter, the length of the implant that influences stability, and the bearing chewing force ability in the long run. During the socket natural healing process, alveolar ridge bone resorption and soft tissue shrinkage are the common problems; the estimated structural loss is approximately 40% in height and 60% in width of the alveolar ridge bone1 and continues with a rate of 0.25% to 0.5% per year.2 Alveolar ridge bone resorption mainly happens during the first 3 months after tooth extraction, so intraoperative intervention is very important and necessary for delayed dental implant. During the last decade, efforts have been made to confirm procedures that can prevent bone resorption after extraction. The use of bone grafts aim to promote bone healing and assist bone regeneration. Various types of materials are used for socket preservation, such as autogenous bone, allograft bone,3–5 xenograft materials,6–8 and alloplast materials.9 The autogenous bone graft material is recognized to be the gold standard in bone grafting because it can transfer osteogenic cells within the grafts.10 However, the amount of bone available is limited around the socket and needs a second surgical procedure, so the development of substitutes to replace the autogenous bone should be imperative.11,12 The deproteinized bovine bone has been tested in vitro and in vivo in the alveolar ridge preservation and plays a positive role in osteoconductive function.13 Guided bone regeneration (GBR) procedure has been developed to counteract alveolar ridge bone resorption. Lekovic et al14
The Journal of Craniofacial Surgery • Volume 25, Number 5, September 2014
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 25, Number 5, September 2014
Alveolar Ridge Preservation
reported that GBR technology with barrier membrane performed better in alveolar ridge preservation. Hämmerle and Lang15 concluded that GBR technology with biocompatibility materials, such as the deproteinized bovine bone mineral, could lead to bone regeneration. The aim of this study was to perform a clinical and radiographic evaluation of an alveolar ridge preservation technique using deproteinized bovine bone graft and GBR procedure, to observe the conditions of the alveolar ridge bone 3 and 6 months after tooth extraction. Delayed dental implants were inserted 6 months later, and osseointegration condition was evaluated through a 1-year follow-up.
PATIENTS AND METHODS The study was carried out in accordance with the Helsinki Declaration of 2000. The protocol was approved by the ethics committee of the School of Stomatology, Fourth Military Medical University. Before being enrolled in the study, all patients were informed about the purpose and process of the study, and they all signed an informed consent form. Patients were advised that 1 tooth should be extracted and that the diagnosis was confirmed by clinical and radiographic examination. The missing tooth subsequently restored with delayed dental implant therapy was enrolled in this study. All procedures were carried out in the Department of Oral Surgery, School of Stomatology, Fourth Military Medical University, from January 2010 to December 2012. A total of 30 patients were included, without current pregnancy or breastfeeding or any sign of acute inflammation. There were 16 women and 14 men (mean age, 37 y; range, 22–47 y). Before extraction, the patients were assigned to the trial group or the control group randomly; each group included 15 patients. All patients were nonsmokers; systemically healthy, without any medical compromising conditions; and not taking any medications, which could affect their ability to undergo the operation with local anesthesia or delay the healing of the bone and soft tissue. Preoperatively, a panoramic radiograph (Orthopantomograph OP100D, Finland) was taken for each patient. Mouthwash was done for 1 minute with 0.2% of chlorhexidine gluconate. All patients received systemic antibiotics (penicillin VK of 250 mg) 1 hour before surgery. The tooth was extracted with atraumatic extraction technique under local anesthesia (articaine with 1:100000 epinephrine). All inflammation granulation tissue that remained in the extraction sockets was removed. After the socket curettage, 2 vertical incisions
FIGURE 1. A, The tooth was extracted atraumatically, and all inflammation granulation tissue was removed. B, The socket was filled with deproteinized bovine bone graft without excessive force. C, The grafted socket was covered with absorbable collagen membrane. D, The flap was released and sutured with 4-0 silk to close the wound.
FIGURE 2. A, The decayed second molar needed to be removed in the right mandible. B, The socket was grafted immediately after extraction. C, The socket was remodeled at 3 months after extraction. D, The socket was remodeled at 6 months after extraction.
were made in the mesial and distal roots of the socket and extended to the mucosal vestibular groove at the buccal side. A rectangular full-thickness flap was elevated. The sockets were filled with deproteinized bovine bone graft (Bio-Oss; Geistlich, Pharma AG, Wolhusen, Switzerland), without excessive force.16 A previous study suggested that overpacking the bone graft could impede socket healing and new bone regeneration.17 So the sockets were filled loosely until the bone grafts reached the top level of the bony walls. The grafted sockets were then covered with absorbable collagen membrane (Bio-Gide; Geistlich, Pharma AG, Wolhusen, Switzerland). The flap was released and sutured with 4-0 silk to close the socket (Fig. 1). Panoramic radiograph and computed tomography (CT) (Bright Speed, EDGE) were taken immediately after grafting surgery to measure the alveolar ridge height and width and bone volume at the baseline. After the grafting surgery, systemic antibiotics were prescribed to all patients for 3 to 5 days (penicillin VK of 250 mg every 8 h for 3–5 d), and they could use analgesics (ibuprofen of 800 mg every 8 h if needed) for postoperative pain control. The patients were advised not to wear any prosthesis around the surgical socket for at least 2 weeks. Patients were reviewed at 3 and 6 months later, and panoramic radiograph and CT were taken to evaluate the signs of bone remodeling (Fig. 2). The working station was used to measure the alveolar ridge bone height and width. The CT data were inputted into a computer. We used Mimics software (10.01, Platform V10.2.1.2, Materialisen.v.) to construct three-dimensional models for volumetric analysis; the regions of interest concluded mesial-distal
FIGURE 3. The CT data were inputted into a computer, and Mimics software was used to construct three-dimensional models for volumetric analysis.
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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TABLE 2. Alveolar Ridge Bone Width Reductions Mean (SD), mm Timing 3 mo 6 mo
Trial Group
Control Group
1.11 (0.13) 1.84 (0.35)
2.72 (0.19)* 3.56 (0.28)*
n = 15. *P < 0.05, statistical difference from the control by independent t-test.
RESULTS FIGURE 4. A, Full-thickness mucoperiosteal flap was elevated at 6 months after the socket was grafted; the new formed bone in the trial group was soft. B, The implant was inserted into the grafted socket. C, Dental film was taken immediately after dental implant placement. D, Dental film was taken at 6 months after dental implant placement.
areas and ridge summit to the mandibular edge or maxillary sinus/ nasal cavity floor of the extracted tooth (Fig. 3). At 6 months after grafting surgery, it was ready to insert dental implants into the sockets in both groups. After local anesthesia, a full-thickness mucoperiosteal flap was elevated. Each socket was inserted with endosseous implant with a diameter of 3.3, 4.1, or 4.8 mm and a length of more than 8 mm (Straumann Dental Implant System, Switzerland). The incision was closed with 4-0 silk sutures. After the dental implant surgery, every patient was taken with a common dental apical film to observe the osseointegration condition. Antibiotics were used 1 hour before the surgery and lasted for 3 days after the surgery. All patients were followed up at 1 week, 3 months, 6 months, and 1 year (Fig. 4). Osseointegration condition included implant stability and bone resorption around the implant. Dental implant stability was evaluated with resonance frequency analysis, and implant stability quotient (ISQ) of the 2 groups was compared. We took normal dental apical film to evaluate the alveolar ridge bone resorption around the dental implant neck at the same time. The degree of bone resorption was contrasted with dental implant thread.
STATISTICAL ANALYSIS Alveolar ridge bone height and width and bone volume changes at 3 and 6 months after alveolar preservation surgery and implant ISQ were compared between the trial and control groups. The SPSS (version 16.0; Chicago, IL) software was used to conduct an independent t-test, to assess the difference between the 2 groups. P < 0.05 was accepted as statistically significant.
TABLE 1. Alveolar Ridge Bone Height Reductions
General Observation All sockets healed uneventfully, and no signs of acute infection or excessive inflammatory response were observed during the 6-month clinical healing period. The buccal side bone resorption and soft tissue shrinkage in the control group were more obvious than in the trial group. The contour of alveolar bone in the trial group was more favorable for the prosthesis esthetics. All implants did not have peri-implantitis or loose or lost implant.
Alveolar Ridge Bone Height Changes As shown in Table 1, at 3 months, the mean (SD) alveolar ridge height reduction was 1.05 (0.24) mm in the trial group and 2.12 (0.15) mm in the control group. The height reduction at 6 months was 1.54 (0.25) mm in the trial group and 3.26 (0.29) mm in the control group. The difference in the 2 groups was statistically significant, P < 0.05.
Alveolar Ridge Bone Width Changes As shown in Table 2, at 3 months, the mean (SD) alveolar ridge width reduction was 1.11 (0.13) mm in the trial group and 2.72 (0.19) mm in the control group. The width reduction at 6 months was 1.84 (0.35) mm in the trial group and 3.56 (0.28) mm in the control group. The difference in the 2 groups was statistically significant, P < 0.05.
Alveolar Ridge Bone Volume Changes As shown in Table 3, at 3 months after extraction, the volume of alveolar ridge bone resorption was 193.79 (21.47) mm3 in the trial group and 252.19 (37.21) mm3 in the control group. At 6 months, the bone resorption was 262.06 (33.08) mm3 in the trial group and 342.32 (36.41) mm3 in the control group. The difference in the 2 groups was statistically significant, P < 0.05.
Osseointegration Condition The mean (SD) ISQ at 3 months was 70.25 (2.77) in the trial group and 72.33 (3.52) in the control group. The difference in the 2 groups was not significant (P > 0.05). At the same time, we TABLE 3. Alveolar Ridge Bone Volumes Changes Mean (SD), mm3
Mean (SD), mm Timing 3 mo 6 mo
Trial Group
Control Group
1.05 (0.24) 1.54 (0.25)
2.12 (0.15)* 3.26 (0.29)*
Timing 3 mo 6 mo
Trial Group
Control Group
193.79 (21.47) 262.06 (33.08)
252.19 (37.21)* 342.32 (36.41)*
n = 15.
n = 15.
*P < 0.05, statistical difference from the control by independent t-test.
*P < 0.05, statistical difference from the control by independent t-test.
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© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 25, Number 5, September 2014
observed that there was bone resorption around dental implant in 5 patients—3 patients in the trial group and 2 patients in the control group—and the bone resorption volume was within the first thread of the implant. There was no significant difference in osseointegration condition between the 2 groups.
DISCUSSION The alveolar ridge bone resorption and soft tissue shrinkage always occur after tooth extraction, which compromise the alveolar ridge esthetics and function. Tan et al18 showed that, 6 months after tooth extraction, there were approximately 29% to 63% of alveolar ridge bone width loss and 11% to 22% of bone height loss. Bone resorption rate is rapid in the first 3 months, and in the subsequent days, the resorption rate slows down. Alveolar ridge preservation refers to kinds of techniques carried out immediately after tooth extraction, aiming to minimize the reduction of alveolar ridge bone and maximize the new bone formation.19 The major way of alveolar ridge preservation is socket bone graft combined with GBR techniques. Cardaropoli et al20 reported that filling the socket with bone graft was an effective method to reduce alveolar ridge bone resorption. The main purpose of the bone graft material is to provide a scaffold to conduct the formation of blood vessels, improve the quality and quantity of the new formed bone, protect blood clots, and support the soft tissue flap. The GBR technique provides a new method in exploring the way to preserve the alveolar ridge. It can protect socket space, promote migration of osteoblast cell and angiogenesis in the socket, and help in socket healing. Meanwhile, the barrier membrane can guarantee the stability of the bone graft material and blood clots in the socket, to prevent bone graft material loss or premature resorption. The GBR technologies have been conducted by animal and clinical trials and have good results. Therefore, in our study, we filled the socket with bovine bone graft and covered it with absorbable collagen membrane. The absorbable collagen membrane can isolate the socket from oral environment and prevent the surrounding soft tissue to overgrow into the socket. However, the membrane premature absorption can often lead to the loss of bone graft material, which will weaken the bone graft scaffold function and influence new bone formation. Thus, we sutured the wound after grafted surgery to prevent membrane premature absorption. In our study, all sockets in the trial group did not have wound dehiscence or membrane exposure. In this study, all patients in the trial group did not have rejection or wound infections around the grafting region, which indicated that the deproteinized bovine bone and collagen membrane were safe and biocompatible. The measurement of alveolar ridge showed that, at 3 and 6 months, alveolar bone volume, ridge height, and width reduction in the trial group were less than in the control group. The alveolar ridge height and width reduction in the control group at 6 months were approximately twice more than that in the trial group. The bone reduction differences between the 2 groups have statistical significances. On the other hand, the width reduction was greater than the height reduction in both groups, which was consistent with the results of some studies.21 Because of the support of the Bio-Oss graft, the bone resorption and buccal side soft tissue shrinkage were less, and the contour of alveolar bone was plumper in the trial group than in the control group, which was essential especially for the esthetic areas. The study demonstrated that the socket filled with deproteinized bovine bone graft and GBR with absorbable collagen membrane could reduce alveolar ridge bone resorption effectively at 6 months after tooth extraction. Therefore, when ready to insert dental implant, the trial group has better alveolar ridge condition, more bone volume, and better surgical environment.
Alveolar Ridge Preservation
When opening the gingival flap, again, we found that the grafted zone had more immature bone and connective tissue formation. Meanwhile, when we inserted dental implant, we noticed that the grafted area was softer than the natural healing bone. Probably, because the graft material degraded too slow and occupied the space of the new bone formation, so there was a small amount of new bone formation. It might also be the membrane premature absorption, resulting in fibrous connective tissue overgrowth in the grafted socket. However, during the implant placement process, there was no difference in the primary stability of the implant between the 2 groups. After the 12-month follow-up, the results showed that the soft new bone in the grafted socket did not affect implant osseointegration and stability. The osseointegration conditions of all implants were similar. The ISQ had no significant difference at 3 months. All implants showed good osseointegration. In our study, we compared the dental implant thread with the alveolar ridge bone edge around the implant through a dental film to evaluate the degree of bone resorption. We only found slight bone resorption around the implant in 5 patients. The results showed that both groups had achieved the ideal and stable implant osseointegration. All the implants were loaded competently; the survival rate was 100% during the 1-year follow-up. This study only observed the effect of deproteinized bovine bone graft material with absorbable collagen membrane for alveolar ridge preservation. The new formed bone in the trial group was soft, but this condition did not affect dental implant placement and osseointegration. In further studies, we will explore the mechanism of the new formed bone in the grafted socket and carry out comparative studies with a variety of graft materials and barrier membranes (absorbable or nonabsorbable), to choose the optimal bone graft material and barrier membrane.
CONCLUSIONS The study showed that the deproteinized bovine bone and GBR with absorbable collagen membrane were effective in alveolar ridge preservation. Meanwhile, this kind of ridge preservation technique had no negative effect on delayed dental implant osseointegration and peri-implant bone resorption.
REFERENCES 1. Araújo MG, Lindhe J. Ridge alterations following tooth extraction with and without flap elevation: an trial study in the dog. Clin Oral Implants Res 2009;20:545–549 2. Fu PS, Wu YM, Tsai CF, et al. Immediate implant placement following minimally invasive extraction: a case report with a 6-year follow-up. Kaohsiung J Med Sci 2011;27:353–356 3. Wood RA, Mealey BL. Histologic comparison of healing after tooth extraction with ridge preservation using mineralized versus demineralized freeze-dried bone allograft. J Periodontol 2012;83:329–336 4. Ozdemir H, Ezirganli S, Isa Kara M, et al. Effects of platelet rich fibrin alone used with rigid titanium barrier. Arch Oral Biol 2013; 58:537–544 5. Le B, Rohrer MD, Prasad HS. Screw “tent-pole” grafting technique for reconstruction of large vertical alveolar ridge defects using human mineralized allograft for implant site preparation. J Oral Maxillofac Surg 2010;68:428–435 6. Mellonig JT. Human histologic evaluation of a bovine-derived bone xenograft in the treatment of periodontal osseous defects. Int J Periodontics Restorative Dent 2000;20:19–29 7. Accorsi-Mendonca T, Conz MB, Barros TC, et al. Physicochemical characterization of two deproteinized bovine xenografts. Braz Oral Res 2008;22:5–10 8. Araújo M, Linder E, Lindhe J. Effect of a xenograft on early bone formation in extraction sockets: an trial study in dog. Clin Oral Implants Res 2009;20:1–6
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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9. Becker W, Urist M, Becker BE, et al. Clinical and histologic observations of sites implanted with intraoral autologous bone grafts or allografts. 15 human case reports. J Periodontol 1996;67:1025–1033 10. Block MS. Treatment of the single tooth extraction site. Oral Maxillofac Surg Clin North Am 2004;16:41–63 11. Clavero J, Lundgren S. Ramus or chin grafts for maxillary sinus inlay and local onlay augmentation: comparison of donor site morbidity and complications. Clin Implant Dent Relat Res 2003;5:154–160 12. Giannoudis PV, Dinopoulos H, Tsiridis E. Bone substitute: an update. Injury 2005;36(suppl 3):S20–S27 13. Berglundh T, Lindhe J. Healing around implants placed in bone defects treated with Bio-Oss. An trial study in the dog. Clin Oral Implants Res 1997;8:117–124 14. Lekovic V, Kenney EB, Weinlaender M, et al. A bone regenerative approach to alveolar ridge maintenance following tooth extraction. Report of 10 cases. J Periodontol 1997;68:563–570 15. Hämmerle CH, Lang NP. Single stage surgery combining transmucosal implant placement with guided bone regeneration and bioresorbable materials. Clin Oral Implants Res 2001;12:9–18
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16. Polimeni G, Albandar JM, Wikesjö UM. Prognostic factors for alveolar regeneration: effect of space provision. J Clin Periodontol 2005:32:951–954 17. Friedmann A, Dard M, Kleber BM, et al. Ridge augmentation and maxillary sinus grafting with a biphasic calcium phosphate: histologic and histomorphometric observations. Clin Oral Implants Res 2009;20:708–714 18. Tan WL, Wong TL, Wong MC, et al. A systematic review of post-extractional alveolar hard and soft tissue volumeral changes in humans. Clin Oral Implants Res 2012;23(suppl 5):1–21 19. Wang RE, Lang NP. Ridge preservation after tooth extraction. Clin Oral Implants Res 2012;23(suppl 6):147–156 20. Cardaropoli D, Tamagnone L, Roffredo A, et al. Socket preservation using bovine bone mineral and collagen membrane: a randomized controlled clinical trial with histologic analysis. Int J Periodontics Restorative Dent 2012;32:421–430 21. Lekovic V, Camargo PM, Klokkevold P, et al. Preservation of alveolar bone in extraction sockets using bioabsorbable membranes. J Periodontol 1998;69:1044–1049
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
Alveolar Ridge Preservation With Deproteinized Bovine Bone Graft and Collagen Membrane and Delayed Implants Chaoyuan Pang, Yuxiang Ding, DDS, Hongzhi Zhou, DDS, Ruifeng Qin, DDS, Rui Hou, DDS, Guoliang Zhang, MD, and Kaijin Hu, DDS Abstract: To evaluate clinically and radiographically an alveolar ridge, preservation technique with deproteinized bovine bone graft and absorbable collagen membrane and then restoration with delayed implants were done. The study included 30 patients. The trial group’s sockets were filled with deproteinized bovine bone graft (Bio-Oss) and covered with absorbable collagen membrane (Bio-Gide). The control group’s sockets healed without any treatment. Panoramic radiograph and computed tomography were taken immediately after graft and 3 and 6 months later to evaluate the height, width, and volume change of the alveolar ridge bone. Dental implants were inserted in all sockets at 6 months, and osseointegration condition was evaluated in the following 12 months. All sockets healed uneventfully. In the trial group, the mean (SD) height reduction of the alveolar ridge bone was 1.05 (0.24) mm at 3 months and 1.54 (0.25) mm at 6 months. The width reduction was 1.11 (0.13) mm at 3 months and 1.84 (0.35) mm at 6 months. Bone volume reduction was 193.79 (21.47) mm3 at 3 months and 262.06 (33.08) mm3 at 6 months. At the same trend, in the control group, the bone height reduction was 2.12 (0.15) mm at 3 months and 3.26 (0.29) mm at 6 months. The width reduction was 2.72 (0.19) mm at 3 months and 3.56 (0.28) mm at 6 months. Bone volume reduction was 252.19 (37.21) mm3 at 3 months and 342.32 (36.41) mm3 at 6 months. There was a significant difference in alveolar ridge bone height, width, and volume reduction in the 2 groups. The osseointegration condition had no significant difference between the 2 groups. This study suggested that the deproteinized bovine bone graft and absorbable collagen membrane were beneficial to preserve the alveolar ridge bone and had no influence on the osseointegration of delayed implant.
From the Department of Stomatology, State Key Laboratory of Military Stomatology, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China. Received October 24, 2013. Accepted for publication February 9, 2014. Address correspondence and reprint requests to Kaijin Hu, Department of Oral Surgery, School of Stomatology, Fourth Military Medical University, 145 Western Changle Road, Xi’an, 710032, PR China; E-mail: [email protected]; and Yuxiang Ding, Department of Oral Surgery, School of Stomatology, Fourth Military Medical University, 145 Western Changle Road, Xi’an, 710032, PR China; E-mail: [email protected] Chaoyuan Pang and Yuxiang Ding equally contributed to this article. The authors report no conflicts of interest. Copyright © 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000000887
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Key Words: Socket preservation, tooth extraction, Bio-Oss, Bio-Gide, delayed implant (J Craniofac Surg 2014;25: 1698–1702)
D
ental implant is more and more popular because there are no damages on the adjacent teeth. The implant inserted in the alveolar ridge bone has the same function as the natural tooth root, which can bear and transfer chewing force well. The condition of alveolar ridge bone after tooth extraction is very important, which can influence the delayed dental implant placement. Periodontitis, bony wall fracture, or lack of intraoperative intervention usually leads to the deficiency of alveolar ridge bone volume. Dental implant placement also becomes impossible because of serious bone resorption. Buccal side lamella bone of the anterior tooth is very thin and easily causes bone resorption and gingival recession after tooth extraction, which results in esthetic risks mostly. It always needs autogenous bone graft or bone splitting technique to increase bone thickness. However, the operation procedure is difficult and causes esthetic risks easily. In the molar area, lack of alveolar ridge bone height usually results in maxillary sinus or inferior alveolar nerve damage easily. So before dental implant placement, it always needs maxillary sinus lifting or alveolar ridge augmentation, which demands high operation level of physician and results in some complications. The bone volume of alveolar ridge decides the diameter, the length of the implant that influences stability, and the bearing chewing force ability in the long run. During the socket natural healing process, alveolar ridge bone resorption and soft tissue shrinkage are the common problems; the estimated structural loss is approximately 40% in height and 60% in width of the alveolar ridge bone1 and continues with a rate of 0.25% to 0.5% per year.2 Alveolar ridge bone resorption mainly happens during the first 3 months after tooth extraction, so intraoperative intervention is very important and necessary for delayed dental implant. During the last decade, efforts have been made to confirm procedures that can prevent bone resorption after extraction. The use of bone grafts aim to promote bone healing and assist bone regeneration. Various types of materials are used for socket preservation, such as autogenous bone, allograft bone,3–5 xenograft materials,6–8 and alloplast materials.9 The autogenous bone graft material is recognized to be the gold standard in bone grafting because it can transfer osteogenic cells within the grafts.10 However, the amount of bone available is limited around the socket and needs a second surgical procedure, so the development of substitutes to replace the autogenous bone should be imperative.11,12 The deproteinized bovine bone has been tested in vitro and in vivo in the alveolar ridge preservation and plays a positive role in osteoconductive function.13 Guided bone regeneration (GBR) procedure has been developed to counteract alveolar ridge bone resorption. Lekovic et al14
The Journal of Craniofacial Surgery • Volume 25, Number 5, September 2014
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 25, Number 5, September 2014
Alveolar Ridge Preservation
reported that GBR technology with barrier membrane performed better in alveolar ridge preservation. Hämmerle and Lang15 concluded that GBR technology with biocompatibility materials, such as the deproteinized bovine bone mineral, could lead to bone regeneration. The aim of this study was to perform a clinical and radiographic evaluation of an alveolar ridge preservation technique using deproteinized bovine bone graft and GBR procedure, to observe the conditions of the alveolar ridge bone 3 and 6 months after tooth extraction. Delayed dental implants were inserted 6 months later, and osseointegration condition was evaluated through a 1-year follow-up.
PATIENTS AND METHODS The study was carried out in accordance with the Helsinki Declaration of 2000. The protocol was approved by the ethics committee of the School of Stomatology, Fourth Military Medical University. Before being enrolled in the study, all patients were informed about the purpose and process of the study, and they all signed an informed consent form. Patients were advised that 1 tooth should be extracted and that the diagnosis was confirmed by clinical and radiographic examination. The missing tooth subsequently restored with delayed dental implant therapy was enrolled in this study. All procedures were carried out in the Department of Oral Surgery, School of Stomatology, Fourth Military Medical University, from January 2010 to December 2012. A total of 30 patients were included, without current pregnancy or breastfeeding or any sign of acute inflammation. There were 16 women and 14 men (mean age, 37 y; range, 22–47 y). Before extraction, the patients were assigned to the trial group or the control group randomly; each group included 15 patients. All patients were nonsmokers; systemically healthy, without any medical compromising conditions; and not taking any medications, which could affect their ability to undergo the operation with local anesthesia or delay the healing of the bone and soft tissue. Preoperatively, a panoramic radiograph (Orthopantomograph OP100D, Finland) was taken for each patient. Mouthwash was done for 1 minute with 0.2% of chlorhexidine gluconate. All patients received systemic antibiotics (penicillin VK of 250 mg) 1 hour before surgery. The tooth was extracted with atraumatic extraction technique under local anesthesia (articaine with 1:100000 epinephrine). All inflammation granulation tissue that remained in the extraction sockets was removed. After the socket curettage, 2 vertical incisions
FIGURE 1. A, The tooth was extracted atraumatically, and all inflammation granulation tissue was removed. B, The socket was filled with deproteinized bovine bone graft without excessive force. C, The grafted socket was covered with absorbable collagen membrane. D, The flap was released and sutured with 4-0 silk to close the wound.
FIGURE 2. A, The decayed second molar needed to be removed in the right mandible. B, The socket was grafted immediately after extraction. C, The socket was remodeled at 3 months after extraction. D, The socket was remodeled at 6 months after extraction.
were made in the mesial and distal roots of the socket and extended to the mucosal vestibular groove at the buccal side. A rectangular full-thickness flap was elevated. The sockets were filled with deproteinized bovine bone graft (Bio-Oss; Geistlich, Pharma AG, Wolhusen, Switzerland), without excessive force.16 A previous study suggested that overpacking the bone graft could impede socket healing and new bone regeneration.17 So the sockets were filled loosely until the bone grafts reached the top level of the bony walls. The grafted sockets were then covered with absorbable collagen membrane (Bio-Gide; Geistlich, Pharma AG, Wolhusen, Switzerland). The flap was released and sutured with 4-0 silk to close the socket (Fig. 1). Panoramic radiograph and computed tomography (CT) (Bright Speed, EDGE) were taken immediately after grafting surgery to measure the alveolar ridge height and width and bone volume at the baseline. After the grafting surgery, systemic antibiotics were prescribed to all patients for 3 to 5 days (penicillin VK of 250 mg every 8 h for 3–5 d), and they could use analgesics (ibuprofen of 800 mg every 8 h if needed) for postoperative pain control. The patients were advised not to wear any prosthesis around the surgical socket for at least 2 weeks. Patients were reviewed at 3 and 6 months later, and panoramic radiograph and CT were taken to evaluate the signs of bone remodeling (Fig. 2). The working station was used to measure the alveolar ridge bone height and width. The CT data were inputted into a computer. We used Mimics software (10.01, Platform V10.2.1.2, Materialisen.v.) to construct three-dimensional models for volumetric analysis; the regions of interest concluded mesial-distal
FIGURE 3. The CT data were inputted into a computer, and Mimics software was used to construct three-dimensional models for volumetric analysis.
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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TABLE 2. Alveolar Ridge Bone Width Reductions Mean (SD), mm Timing 3 mo 6 mo
Trial Group
Control Group
1.11 (0.13) 1.84 (0.35)
2.72 (0.19)* 3.56 (0.28)*
n = 15. *P < 0.05, statistical difference from the control by independent t-test.
RESULTS FIGURE 4. A, Full-thickness mucoperiosteal flap was elevated at 6 months after the socket was grafted; the new formed bone in the trial group was soft. B, The implant was inserted into the grafted socket. C, Dental film was taken immediately after dental implant placement. D, Dental film was taken at 6 months after dental implant placement.
areas and ridge summit to the mandibular edge or maxillary sinus/ nasal cavity floor of the extracted tooth (Fig. 3). At 6 months after grafting surgery, it was ready to insert dental implants into the sockets in both groups. After local anesthesia, a full-thickness mucoperiosteal flap was elevated. Each socket was inserted with endosseous implant with a diameter of 3.3, 4.1, or 4.8 mm and a length of more than 8 mm (Straumann Dental Implant System, Switzerland). The incision was closed with 4-0 silk sutures. After the dental implant surgery, every patient was taken with a common dental apical film to observe the osseointegration condition. Antibiotics were used 1 hour before the surgery and lasted for 3 days after the surgery. All patients were followed up at 1 week, 3 months, 6 months, and 1 year (Fig. 4). Osseointegration condition included implant stability and bone resorption around the implant. Dental implant stability was evaluated with resonance frequency analysis, and implant stability quotient (ISQ) of the 2 groups was compared. We took normal dental apical film to evaluate the alveolar ridge bone resorption around the dental implant neck at the same time. The degree of bone resorption was contrasted with dental implant thread.
STATISTICAL ANALYSIS Alveolar ridge bone height and width and bone volume changes at 3 and 6 months after alveolar preservation surgery and implant ISQ were compared between the trial and control groups. The SPSS (version 16.0; Chicago, IL) software was used to conduct an independent t-test, to assess the difference between the 2 groups. P < 0.05 was accepted as statistically significant.
TABLE 1. Alveolar Ridge Bone Height Reductions
General Observation All sockets healed uneventfully, and no signs of acute infection or excessive inflammatory response were observed during the 6-month clinical healing period. The buccal side bone resorption and soft tissue shrinkage in the control group were more obvious than in the trial group. The contour of alveolar bone in the trial group was more favorable for the prosthesis esthetics. All implants did not have peri-implantitis or loose or lost implant.
Alveolar Ridge Bone Height Changes As shown in Table 1, at 3 months, the mean (SD) alveolar ridge height reduction was 1.05 (0.24) mm in the trial group and 2.12 (0.15) mm in the control group. The height reduction at 6 months was 1.54 (0.25) mm in the trial group and 3.26 (0.29) mm in the control group. The difference in the 2 groups was statistically significant, P < 0.05.
Alveolar Ridge Bone Width Changes As shown in Table 2, at 3 months, the mean (SD) alveolar ridge width reduction was 1.11 (0.13) mm in the trial group and 2.72 (0.19) mm in the control group. The width reduction at 6 months was 1.84 (0.35) mm in the trial group and 3.56 (0.28) mm in the control group. The difference in the 2 groups was statistically significant, P < 0.05.
Alveolar Ridge Bone Volume Changes As shown in Table 3, at 3 months after extraction, the volume of alveolar ridge bone resorption was 193.79 (21.47) mm3 in the trial group and 252.19 (37.21) mm3 in the control group. At 6 months, the bone resorption was 262.06 (33.08) mm3 in the trial group and 342.32 (36.41) mm3 in the control group. The difference in the 2 groups was statistically significant, P < 0.05.
Osseointegration Condition The mean (SD) ISQ at 3 months was 70.25 (2.77) in the trial group and 72.33 (3.52) in the control group. The difference in the 2 groups was not significant (P > 0.05). At the same time, we TABLE 3. Alveolar Ridge Bone Volumes Changes Mean (SD), mm3
Mean (SD), mm Timing 3 mo 6 mo
Trial Group
Control Group
1.05 (0.24) 1.54 (0.25)
2.12 (0.15)* 3.26 (0.29)*
Timing 3 mo 6 mo
Trial Group
Control Group
193.79 (21.47) 262.06 (33.08)
252.19 (37.21)* 342.32 (36.41)*
n = 15.
n = 15.
*P < 0.05, statistical difference from the control by independent t-test.
*P < 0.05, statistical difference from the control by independent t-test.
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The Journal of Craniofacial Surgery • Volume 25, Number 5, September 2014
observed that there was bone resorption around dental implant in 5 patients—3 patients in the trial group and 2 patients in the control group—and the bone resorption volume was within the first thread of the implant. There was no significant difference in osseointegration condition between the 2 groups.
DISCUSSION The alveolar ridge bone resorption and soft tissue shrinkage always occur after tooth extraction, which compromise the alveolar ridge esthetics and function. Tan et al18 showed that, 6 months after tooth extraction, there were approximately 29% to 63% of alveolar ridge bone width loss and 11% to 22% of bone height loss. Bone resorption rate is rapid in the first 3 months, and in the subsequent days, the resorption rate slows down. Alveolar ridge preservation refers to kinds of techniques carried out immediately after tooth extraction, aiming to minimize the reduction of alveolar ridge bone and maximize the new bone formation.19 The major way of alveolar ridge preservation is socket bone graft combined with GBR techniques. Cardaropoli et al20 reported that filling the socket with bone graft was an effective method to reduce alveolar ridge bone resorption. The main purpose of the bone graft material is to provide a scaffold to conduct the formation of blood vessels, improve the quality and quantity of the new formed bone, protect blood clots, and support the soft tissue flap. The GBR technique provides a new method in exploring the way to preserve the alveolar ridge. It can protect socket space, promote migration of osteoblast cell and angiogenesis in the socket, and help in socket healing. Meanwhile, the barrier membrane can guarantee the stability of the bone graft material and blood clots in the socket, to prevent bone graft material loss or premature resorption. The GBR technologies have been conducted by animal and clinical trials and have good results. Therefore, in our study, we filled the socket with bovine bone graft and covered it with absorbable collagen membrane. The absorbable collagen membrane can isolate the socket from oral environment and prevent the surrounding soft tissue to overgrow into the socket. However, the membrane premature absorption can often lead to the loss of bone graft material, which will weaken the bone graft scaffold function and influence new bone formation. Thus, we sutured the wound after grafted surgery to prevent membrane premature absorption. In our study, all sockets in the trial group did not have wound dehiscence or membrane exposure. In this study, all patients in the trial group did not have rejection or wound infections around the grafting region, which indicated that the deproteinized bovine bone and collagen membrane were safe and biocompatible. The measurement of alveolar ridge showed that, at 3 and 6 months, alveolar bone volume, ridge height, and width reduction in the trial group were less than in the control group. The alveolar ridge height and width reduction in the control group at 6 months were approximately twice more than that in the trial group. The bone reduction differences between the 2 groups have statistical significances. On the other hand, the width reduction was greater than the height reduction in both groups, which was consistent with the results of some studies.21 Because of the support of the Bio-Oss graft, the bone resorption and buccal side soft tissue shrinkage were less, and the contour of alveolar bone was plumper in the trial group than in the control group, which was essential especially for the esthetic areas. The study demonstrated that the socket filled with deproteinized bovine bone graft and GBR with absorbable collagen membrane could reduce alveolar ridge bone resorption effectively at 6 months after tooth extraction. Therefore, when ready to insert dental implant, the trial group has better alveolar ridge condition, more bone volume, and better surgical environment.
Alveolar Ridge Preservation
When opening the gingival flap, again, we found that the grafted zone had more immature bone and connective tissue formation. Meanwhile, when we inserted dental implant, we noticed that the grafted area was softer than the natural healing bone. Probably, because the graft material degraded too slow and occupied the space of the new bone formation, so there was a small amount of new bone formation. It might also be the membrane premature absorption, resulting in fibrous connective tissue overgrowth in the grafted socket. However, during the implant placement process, there was no difference in the primary stability of the implant between the 2 groups. After the 12-month follow-up, the results showed that the soft new bone in the grafted socket did not affect implant osseointegration and stability. The osseointegration conditions of all implants were similar. The ISQ had no significant difference at 3 months. All implants showed good osseointegration. In our study, we compared the dental implant thread with the alveolar ridge bone edge around the implant through a dental film to evaluate the degree of bone resorption. We only found slight bone resorption around the implant in 5 patients. The results showed that both groups had achieved the ideal and stable implant osseointegration. All the implants were loaded competently; the survival rate was 100% during the 1-year follow-up. This study only observed the effect of deproteinized bovine bone graft material with absorbable collagen membrane for alveolar ridge preservation. The new formed bone in the trial group was soft, but this condition did not affect dental implant placement and osseointegration. In further studies, we will explore the mechanism of the new formed bone in the grafted socket and carry out comparative studies with a variety of graft materials and barrier membranes (absorbable or nonabsorbable), to choose the optimal bone graft material and barrier membrane.
CONCLUSIONS The study showed that the deproteinized bovine bone and GBR with absorbable collagen membrane were effective in alveolar ridge preservation. Meanwhile, this kind of ridge preservation technique had no negative effect on delayed dental implant osseointegration and peri-implant bone resorption.
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Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
