Ridge Preservation Surgery after Single and Multiple Adjacent Tooth Extractions: A Microcomputed Tomography Study in Dogs Nawwaf Al-Hamoudi, DDS, MSD1/Nabil F. Bissada, DDS, MSD2/ Mansour H. Al-Askar, BDS, MSc3/Khalid A. Al-Hezaimi, BDS, MSc4 Purpose: The aim of this study was to determine, before implant placement, the outcome of ridge preservation surgery after extractions of one or more adjacent teeth on the dimensions of the edentulous ridge. Materials and Methods: Nineteen extraction sites in four dogs were randomly divided into three groups: group 1 = single premolars (n = 7 sites); group 2 = two adjacent premolars (n = 6 sites); group 3 = three adjacent premolars (n = 6 sites). Extraction was followed by ridge preservation surgery using a combination of xenograft and collagen membrane after full-thickness flap reflection. All animals were sacrificed 4 months later, and each extraction site was sectioned in the sagittal plane so that alveolar bone measurements could be made in both the buccolingual and apicocoronal directions using microcomputed tomography. Results: Mean buccolingual width of the ridges postsurgery was 4.80 ± 2.78 mm, 4.98 ± 2.65 mm, and 4.79 ± 2.79 mm in groups 1, 2, and 3, respectively. The mean vertical distance from the cementoenamel junction to the crest of the ridge was 1.94 ± 0.42 mm, 2.05 ± 0.48 mm, and 2.60 ± 0.67 mm in groups 1, 2, and 3, respectively. No statistically significant difference was seen between single and multiple extraction sites. Conclusion: Ridge preservation surgery results in a similar pattern of bone remodeling in the horizontal and vertical dimensions of the edentulous ridge after single and multiple adjacent tooth extractions. Int J Oral Maxillofac Implants 2015;30:315–320. doi: 10.11607/jomi.3818 Key words: ridge dimensions, ridge preservation surgery, tooth extractions
H
ealing of extraction sockets after tooth removal includes resorption and remodeling of the alveolar
1 Assistant
Professor, Department of Periodontics and Community Dentistry, King Saud University, Riyadh, Saudi Arabia. 2Professor and Chairman, Department of Periodontics, Case Western Reserve University School of Dental Medicine, Cleveland, Ohio, USA. 3Assistant Professor and Chairman, Department of Periodontics and Community Dentistry, King Saud University, Riyadh, Saudi Arabia. 4 Associate Professor and Chairman, Engineer Abdullah Bugshan Research Chair for Growth Factors and Bone Regeneration, Department of Periodontics and Community Dentistry, College of Dentistry, King Saud University, Riyadh, Saudi Arabia. Correspondence to: Dr Nabil F. Bissada, Department of Periodontics, School of Dental Medicine, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, OH 44106, USA. Fax: +216-368-3204. Email: [email protected] ©2015 by Quintessence Publishing Co Inc.
ridge. The repair process results in reduced height and width of the residual ridge.1–5 The reduction in the alveolar bone ridge is much greater when multiple adjacent teeth are extracted, rather than a single tooth.6 This is also true when implants are placed immediately after extraction.7,8 Al-Hezaimi et al9 attributed the difference in the extent of bone loss to a reduction in the blood supply during healing of multiple adjacent extraction sites. Various treatment strategies have been proposed to reduce resorption of the alveolar ridge after tooth extraction. Human and animal studies showed improved dimensions of the ridge after ridge preservation procedures than after tooth extraction only.10,11 In the present study, the authors hypothesized that, with ridge preservation, no difference in the extent of bone remodeling would be found between single and multiple adjacent extraction sites. The aim of this threedimensional microcomputed tomographic study was to determine the effect of ridge preservation surgery in single and multiple adjacent tooth extraction sites on the future buccolingual and apicocoronal dimensions of the edentulous ridge before implant placement. The International Journal of Oral & Maxillofacial Implants 315
© 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Al-Hamoudi et al
L
U
L
U
L
U
b
a
L
U
c
d
Fig 1 Occlusal view of extraction sites in (a) animal 1, (b) animal 2, (c) animal 3, and (d) animal 4. Group 1 sites are depicted in green, group 2 in blue, and group 3 in red. U = maxillary; L = mandibular.
MATERIALS AND METHODS Study Protocol
The study protocol was approved by the research ethics committee for animal research at the college of Dentistry, King Saud University, Riyadh, Saudi Arabia. Four beagle dogs with a healthy periodontium were used. The mean age and weight of these dogs were 21 months and 13.7 kg, respectively. Animals with clinical signs of periodontal disease were excluded. The animals were kept individually in cages and vaccinated against rabies and infectious hepatitis. The extraction sites were randomly divided into three groups (Fig 1). • Group 1: single premolars were extracted in seven sites • Group 2: two adjacent premolars were extracted in six sites • Group 3: three adjacent premolars were extracted in six sites
Surgical Protocol
Extraction in all sites was followed by ridge preservation using a combination of xenograft and collagen membrane. All procedures (nonsurgical and surgical) were performed under general anesthesia (Ketalar, Pfizer; 10 mg/kg body weight) and local anesthesia (Xylocaine, Astra). The teeth were extracted atraumatically using a piezosurgical device (Mectron) and forceps (Hu-Friedy). Then, full-thickness flaps with two buccal releasing incisions were elevated to allow coronal advancement of the flaps and to achieve primary wound closure. The extraction sockets were filled with xenograft (LADDEC, Biohorizons) and covered with
collagen membrane (conFORM, ACE Surgical Supply). Flaps were sutured with polyglactin 910, and primary closure was achieved (Fig 2).
Postoperative Management
All animals received an intramuscular injection of amoxicillin (5 mg/kg body weight once a day for 3 days). The animals were placed on a soft diet for 10 days after the surgery. Sutures were removed after 2 weeks. Plaque control procedures, which included topical application of a 0.2% chlorhexidine digluconate solution (GUM), were performed twice weekly. The animals were sacrificed after 4 months with an overdose of 3% sodium pentobarbital.
Tissue Preparation and Measurements
The jaw segments containing each extraction site and associated mesial and distal tooth structures were sectioned in the sagittal plane using an electric saw microtome (Leica) and fixed in 10% neutral formalin. The jaw segments containing the extraction sites, along with the adjacent teeth and alveolar bone, were analyzed three-dimensionally in the buccolingual and apicocoronal planes with a microcomputed tomography (micro-CT) scanner (Skyscan). Reference points for linear measurements of the buccolingual dimension were set at 1-mm intervals starting from 1 mm apical to the cementoenamel junction (CEJ) to 5 mm apically (Fig 3). Linear measurements were then taken at three cross-sectional planes in group 3, two in group 2, and one in group 1. The distance from the CEJ to the ridge crest was measured by drawing a horizontal line between the CEJs of teeth adjacent to the extraction sites and recording the vertical distance from that line to the bone crest in
316 Volume 30, Number 2, 2015 © 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Al-Hamoudi et al
Figs 2a to 2f Surgical steps in ridge preservation (group 3).
Fig 2a Preoperative photograph.
Fig 2b Teeth are hemisected prior to extraction.
Fig 2c Atraumatic extractions.
Fig 2d The sockets have been filled with the graft material.
Fig 2e The collagen membrane has been placed over the graft material.
Fig 2f The site has been closed with interrupted sutures.
Fig 3 (right) Reference points for the linear measurements of buccolingual dimension at 1-mm intervals starting from 1 mm apical to the CEJ. L = lingual; B = buccal.
L
CEJ BC
B
Fig 4 (below) The distance from the CEJ to the ridge crest (group 3) was measured by drawing a horizontal line between the CEJs of teeth adjacent to the extraction sites and measuring the vertical distance from the line to the bone crest at three points in group 3, two points in group 2, and one point in group 1.
1 mm 2 mm 3 mm 4 mm 5 mm
millimeters. These measurements were made at three points in group 3, two points in group 2, and one point in group 1 (Fig 4). The x-ray generator of the micro-CT operated at an accelerated potential of 80 kV with a beam current of 80 μA. The x-ray source combined with a detector operated with a shutter speed of 1,100 ms, which produces images with a voxel size of 18 × 18 × 18 μm3. Computer software (Explore MicroView V.2.0, Analysis Plus, GE Health Care) was used for the visualization of two- and three-dimensional data.
Statistical Analysis
The distance from the CEJ to bone crest, as well as the alveolar bone width at 1, 2, 3, 4, and 5 mm apical to the CEJ, was analyzed using SPSS version 18.00 (IBM).
One-way analysis of variance was performed to assess the differences among groups 1, 2, and 3 and also the differences among individual sites (first, second, and third premolars).
RESULTS At 4 months postsurgery, all extraction sites had healed uneventfully with no complications requiring surgical intervention or administration of antibiotics. Alveolar bone dimensions were measured using micro-CT scans (Fig 5). The mean width of the buccolingual bone according to group is shown in Table 1, and mean widths according to sites are shown in Table 2.
The International Journal of Oral & Maxillofacial Implants 317 © 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Al-Hamoudi et al
Fig 5 Images used for linear measurements of buccolingual dimension in (left) group 1, (middle) group 2, and (right) group 3.
1 mm
2 mm
3 mm
4 mm
5 mm
Table 1 Linear Measurements of Bone Width Apical to the CEJ According to Group At 1 mm
At 2 mm
At 3 mm
At 5 mm
Mean
Group 1
0.75 ± 0.80
3.45 ± 1.26
5.33 ± 1.24
6.62 ± 1.36
7.26 ± 1.77
4.80 ± 2.78
Group 2
1.55 ± 2.07
3.61 ± 0.91
5.56 ± 1.16
6.96 ± 0.95
7.66 ± 0.60
4.98 ± 2.65
Group 3
1.07 ± 1.18
3.00 ± 1.41
5.94 ± 0.97
7.26 ± 1.05
7.77 ± 0.71
4.79 ± 2.79
.61
.77
.67
.97
.99
P
At 4 mm
.62
Table 2 Linear Measurements of Bone Width Apical to the CEJ According to Site Site
At 1 mm
At 2 mm
At 3 mm
At 4 mm
At 5 mm
Mean
First premolar
0.89 ± 1.48
2.63 ± 2.10
5.52 ± 1.00
7.0 ± 0.88
8.0 ± 0.89
5.16 ± 3.08
Second premolar
1.06 ± 1.89
3.42 ± 2.19
5.88 ± 1.17
7.09 ± 1.21
7.51 ± 0.97
5.28 ± 2.91
Third premolar
1.79 ± 2.12
4.18 ± 1.73
5.81 ± 1.43
6.98 ± 1.44
7.37 ± 1.55
5.43 ± 2.63
.20
.69
.96
.33
.97
P
.48
Table 3 depicts the mean distance in millimeters from the CEJ to the crest of the edentulous ridge by groups, and Table 4 shows these measurements by site. Differences among groups 1, 2, and 3, as well as between individual sites, were not statistically significant in either the apicocoronal or buccolingual dimensions of the edentulous ridge (P > .05).
DISCUSSION The results of this study showed no difference between single and multiple extraction sites in the extent of bone loss in the horizontal and vertical dimensions of the edentulous ridge at 4 months after ridge preservation surgery. Previous studies reported that bone loss
318 Volume 30, Number 2, 2015 © 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Al-Hamoudi et al
Table 3 Distance from the CEJ to the Crest of the Ridge According to Group Distance (mm) Group 1
Table 4 Distance from the CEJ to the Crest of the Ridge According to Site Site
Distance (mm)
1.94 ± 0.42
First premolar
2.30 ± 0.77
Group 2
2.05 ± 0.48
Second premolar
2.60 ± 1.09
Group 3
2.60 ± 0.67
Third premolar
P
.09
2.0 ± 0.39 .26
P
B P3
P2
P1
Fig 6 Extraction sites of first (P1), second (P2), and third premolars (P3) after full-thickness flap reflection showed similar buccolingual dimensions. B = buccal; L = lingual.
at multiple extraction sites was significantly greater than at single extraction sites when no grafting materials were used or when immediate implants were placed in the extraction sockets.6–8 These studies suggested that extraction of multiple adjacent teeth compromises the blood supply of the alveolar socket and interdental bone. Ridge preservation surgery using bone grafts and barriers may account for the differences in findings between this study and previous ones. Therefore, ridge augmentation surgery may be more critical in multiple extraction sites than for single extraction sites in terms of its ability to reduce bone loss of the edentulous ridge before implant placement. Al-Askar et al6 found that ridge resorption after extraction of multiple adjacent teeth resulted in a large defect that required reconstruction prior to implant therapy. With increased time from extraction to implant placement, progressive ridge resorption may result in further loss of bone volume, to the point at which bone augmentation becomes more challenging, more time consuming, and less predictable.12 The rationale for ridge preservation procedures relies on the fact that alveolar ridge resorption is an unavoidable consequence of tooth loss. Based on understanding of healing events in postextraction sites, the prevention of ridge resorption following tooth extraction seems critical. If the dimensions of the ridge could be maintained, the need for further augmentation procedures would be reduced, simplifying implant surgery at a later time. This pattern of healing is
especially important when esthetics is a major concern for implant restoration, since more bone resorption takes place on the buccal than the lingual aspect of the ridge.13 The present study showed that the placement of a xenograft in fresh extraction sockets may prevent ridge reduction in multiple adjacent extraction sites. This finding is supported by previous studies that showed that bone grafting in combination with collagen membrane placement significantly limited the resorption of hard tissue after tooth extraction.14,15 Araújo et al16 found that, during healing of xenograft, the particles of the graft material became integrated with and further enhanced the dimensions of the bone crest. This is in agreement with findings presented by Nevins et al,17 who reported that sockets treated with bovine bone mineral showed a reduction of < 20% of the buccal plate, whereas ungrafted control sites showed a reduction of > 20%. In the present study, measurements of edentulous ridge width and height were performed 4 months postsurgery using micro-CT. This method generates images with accuracy that is greater than that obtained with other methods of evaluation (eg, cone beam CT).18 Because a micro-CT machine can be used only for limited size specimens, it could not be applied before surgery. Because evaluation of the extraction sites after full-thickness flap reflection did not reveal a notable difference in the buccolingual dimensions among first, second, and third premolars (Fig 6), all the sites were randomly allocated into groups 1, 2, and 3. The International Journal of Oral & Maxillofacial Implants 319
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Al-Hamoudi et al
Based on the finding by Kim et al19 that flapped and flapless ridge preservation lead to similar alveolar bone remodeling and healing, full-thickness flaps were reflected to facilitate primary wound closure in this study. Similar long-term results between flapless and conventional flap techniques were also reported by Caneva et al20 and Bashutski et al21 when implants were placed in extraction sockets. Although the process of alveolar bone modeling and remodeling took place after grafting of the extraction sites, ridge preservation with a combination of xenograft and collagen membranes is a viable treatment to avert severe bone resorption following multiple adjacent tooth extractions. Future studies are needed in humans to compare the outcome of ridge preservation procedures after tooth extraction for periodontal and/or endodontic reasons.
CONCLUSION No difference in alveolar bone width and height was seen following ridge preservation using a combination of xenograft and collagen membrane in single and multiple adjacent extraction sites.
ACKNOWLEDGMENTS The authors would like to express their appreciation and thanks to Dr Andre Paes, Dr Imad Nouneh, and Dr Hussein Assaf for their help in this research. No conflicts of interest are related to this study.
REFERENCES 1. Amler MH. The time sequence of tissue regeneration in human extraction wounds. Oral Surg Oral Med Oral Pathol 1969;27:309–318. 2. Evian CI, Rosenberg ES, Coslet JG, Corn H. The osteogenic activity of bone removed from healing extraction sockets in humans. J Periodontol 1982;53:81–85. 3. Trombelli L, Farina R, Marzola A, Bozzi L, Liljenberg B, Lindhe J. Modeling and remodeling of human extraction sockets. J Clin Periodontol 2008;35:630–639. 4. Mecall RA, Rosenfeld AL. Influence of residual ridge resorption patterns on implant fixture placement and tooth position. Int J Periodontics Restorative Dent 1991;11:8–23.
5. Araujo MG, Lindhe J. Dimensional ridge alterations following tooth extraction. An experimental study in the dog. J Clin Periodontol 2005;32:212–218. 6. Al-Askar M, O’Neill R, Stark P, Griffin T, Javed F, Al-Hezaimi K. Effect of single and contiguous teeth extractions on alveolar bone remodeling: A study in dogs. Clin Implant Dent Relat Res 2011;15:569–575. 7. Al-Shabeeb MS, Al-Askar M, Al-Rasheed A, et al. Alveolar bone remodeling around immediate implants placed in accordance with the extraction socket classification: A three-dimensional microcomputed tomography analysis. J Periodontol 2012;83:981–987. 8. Al-Hezaimi K, Al-Shabeeb MS, Al-Askar M, et al. Microcomputed tomographic analysis of the alveolar ridge alteration around extraction sites with and without immediate implants placement: In vivo study. Clin Implant Dent Relat Res 2014;16:223–229. 9. Al-Hezaimi K, Levi P, Rudy A, Al-Jandan B, Al-Rasheed A. An extraction socket classification developed using analysis of bone type and blood supply to the buccal bone in monkeys. Int J Periodontics Restorative Dent 2011;31:421–427. 10. Suaid F, Grisi MF, Souza SL, Palioto DB, Taba M Jr, Novaes AB Jr. Buccal bone remodeling after tooth extraction using the flapless approach with and without synthetic bone grafting. A histomorphometric study in dogs. Clin Oral Implants Res 2013;24:407–413. 11. Iasella JM, Greenwell H, Miller RL, et al. Ridge preservation with freeze-dried bone allograft and a collagen membrane compared to extraction alone for implant site development: A clinical and histologic study in humans. J Periodontol 2003;74:990–999. 12. Zitzmann NU, Schärer P, Marinello CP. Factors influencing the success of GBR. Smoking, timing of implant placement, implant location, bone quality and provisional restoration. J Clin Periodontol 1999;26:673–682. 13. Pietrokovski J, Massler M. Alveolar ridge resorption following tooth extraction. J Prosthet Dent 1967;17:21–27. 14. Fiorellini JP, Nevins ML. Localized ridge augmentation/preservation. A systematic review. Ann Periodontol 2003;8:321–327. 15. Barone A, Aldini NN, Fini M, Giardino R, Guirado JL, Covani U. Xenograft versus extraction alone for ridge preservation after tooth removal: A clinical and histomorphometric study. J Periodontol 2008; 79:1370–1377. 16. Araújo M, Linder E, Wennström J, Lindhe J. The influence of Bio-Oss Collagen on healing of an extraction socket: An experimental study in the dog. Int J Periodontics Restorative Dent 2008;28:123–135. 17. Nevins M, Camelo M, De Paoli S, et al. A study of the fate of the buccal wall of extraction sockets of teeth with prominent roots. Int J Periodontics Restorative Dent 2006;26:19–29. 18. Swain MV, Xue J. State of the art of Micro-CT applications in dental research. Int J Oral Sci 2009;1:177–188. 19. Kim DM, De Angelis N, Camelo M, Nevins ML, Schupbach P, Nevins M. Ridge preservation with and without primary wound closure: A case series. Int J Periodontics Restorative Dent 2013;33:71–78. 20. Caneva M, Botticelli D, Salata LA, Souza SL, Bressan E, Lang NP. Flap vs. “flapless” surgical approach at immediate implants: A histomorphometric study in dogs. Clin Oral Implants Res 2010;21:1314–1319. 21. Bashutski JD, Wang HL, Rudek I, Moreno I, Koticha T, Oh TJ. The effect of flapless surgery on single-tooth implants in the esthetic zone: A randomized clinical trial. J Periodontol 2013;84:1747–1754.
ERRATUM In the January/February 2015 issue of JOMI, in the article “Microarchitectural Pattern of Pristine Maxillary Bone” (Int J Oral Maxillofac Implants 2015;30:125–132), the authors brought to our attention that the first sentence of the “Results” section in the abstract on page 125 should read: “The mean BV/TV values showed no significant difference between the maxillary anterior (51.90 ± 28.42) and posterior (46.93 ± 26.2) locations.” This correction has been made to the electronic version of the article, which can be found at www.quintpub.com/journals.
320 Volume 30, Number 2, 2015 © 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
H
ealing of extraction sockets after tooth removal includes resorption and remodeling of the alveolar
1 Assistant
Professor, Department of Periodontics and Community Dentistry, King Saud University, Riyadh, Saudi Arabia. 2Professor and Chairman, Department of Periodontics, Case Western Reserve University School of Dental Medicine, Cleveland, Ohio, USA. 3Assistant Professor and Chairman, Department of Periodontics and Community Dentistry, King Saud University, Riyadh, Saudi Arabia. 4 Associate Professor and Chairman, Engineer Abdullah Bugshan Research Chair for Growth Factors and Bone Regeneration, Department of Periodontics and Community Dentistry, College of Dentistry, King Saud University, Riyadh, Saudi Arabia. Correspondence to: Dr Nabil F. Bissada, Department of Periodontics, School of Dental Medicine, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, OH 44106, USA. Fax: +216-368-3204. Email: [email protected] ©2015 by Quintessence Publishing Co Inc.
ridge. The repair process results in reduced height and width of the residual ridge.1–5 The reduction in the alveolar bone ridge is much greater when multiple adjacent teeth are extracted, rather than a single tooth.6 This is also true when implants are placed immediately after extraction.7,8 Al-Hezaimi et al9 attributed the difference in the extent of bone loss to a reduction in the blood supply during healing of multiple adjacent extraction sites. Various treatment strategies have been proposed to reduce resorption of the alveolar ridge after tooth extraction. Human and animal studies showed improved dimensions of the ridge after ridge preservation procedures than after tooth extraction only.10,11 In the present study, the authors hypothesized that, with ridge preservation, no difference in the extent of bone remodeling would be found between single and multiple adjacent extraction sites. The aim of this threedimensional microcomputed tomographic study was to determine the effect of ridge preservation surgery in single and multiple adjacent tooth extraction sites on the future buccolingual and apicocoronal dimensions of the edentulous ridge before implant placement. The International Journal of Oral & Maxillofacial Implants 315
© 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Al-Hamoudi et al
L
U
L
U
L
U
b
a
L
U
c
d
Fig 1 Occlusal view of extraction sites in (a) animal 1, (b) animal 2, (c) animal 3, and (d) animal 4. Group 1 sites are depicted in green, group 2 in blue, and group 3 in red. U = maxillary; L = mandibular.
MATERIALS AND METHODS Study Protocol
The study protocol was approved by the research ethics committee for animal research at the college of Dentistry, King Saud University, Riyadh, Saudi Arabia. Four beagle dogs with a healthy periodontium were used. The mean age and weight of these dogs were 21 months and 13.7 kg, respectively. Animals with clinical signs of periodontal disease were excluded. The animals were kept individually in cages and vaccinated against rabies and infectious hepatitis. The extraction sites were randomly divided into three groups (Fig 1). • Group 1: single premolars were extracted in seven sites • Group 2: two adjacent premolars were extracted in six sites • Group 3: three adjacent premolars were extracted in six sites
Surgical Protocol
Extraction in all sites was followed by ridge preservation using a combination of xenograft and collagen membrane. All procedures (nonsurgical and surgical) were performed under general anesthesia (Ketalar, Pfizer; 10 mg/kg body weight) and local anesthesia (Xylocaine, Astra). The teeth were extracted atraumatically using a piezosurgical device (Mectron) and forceps (Hu-Friedy). Then, full-thickness flaps with two buccal releasing incisions were elevated to allow coronal advancement of the flaps and to achieve primary wound closure. The extraction sockets were filled with xenograft (LADDEC, Biohorizons) and covered with
collagen membrane (conFORM, ACE Surgical Supply). Flaps were sutured with polyglactin 910, and primary closure was achieved (Fig 2).
Postoperative Management
All animals received an intramuscular injection of amoxicillin (5 mg/kg body weight once a day for 3 days). The animals were placed on a soft diet for 10 days after the surgery. Sutures were removed after 2 weeks. Plaque control procedures, which included topical application of a 0.2% chlorhexidine digluconate solution (GUM), were performed twice weekly. The animals were sacrificed after 4 months with an overdose of 3% sodium pentobarbital.
Tissue Preparation and Measurements
The jaw segments containing each extraction site and associated mesial and distal tooth structures were sectioned in the sagittal plane using an electric saw microtome (Leica) and fixed in 10% neutral formalin. The jaw segments containing the extraction sites, along with the adjacent teeth and alveolar bone, were analyzed three-dimensionally in the buccolingual and apicocoronal planes with a microcomputed tomography (micro-CT) scanner (Skyscan). Reference points for linear measurements of the buccolingual dimension were set at 1-mm intervals starting from 1 mm apical to the cementoenamel junction (CEJ) to 5 mm apically (Fig 3). Linear measurements were then taken at three cross-sectional planes in group 3, two in group 2, and one in group 1. The distance from the CEJ to the ridge crest was measured by drawing a horizontal line between the CEJs of teeth adjacent to the extraction sites and recording the vertical distance from that line to the bone crest in
316 Volume 30, Number 2, 2015 © 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Al-Hamoudi et al
Figs 2a to 2f Surgical steps in ridge preservation (group 3).
Fig 2a Preoperative photograph.
Fig 2b Teeth are hemisected prior to extraction.
Fig 2c Atraumatic extractions.
Fig 2d The sockets have been filled with the graft material.
Fig 2e The collagen membrane has been placed over the graft material.
Fig 2f The site has been closed with interrupted sutures.
Fig 3 (right) Reference points for the linear measurements of buccolingual dimension at 1-mm intervals starting from 1 mm apical to the CEJ. L = lingual; B = buccal.
L
CEJ BC
B
Fig 4 (below) The distance from the CEJ to the ridge crest (group 3) was measured by drawing a horizontal line between the CEJs of teeth adjacent to the extraction sites and measuring the vertical distance from the line to the bone crest at three points in group 3, two points in group 2, and one point in group 1.
1 mm 2 mm 3 mm 4 mm 5 mm
millimeters. These measurements were made at three points in group 3, two points in group 2, and one point in group 1 (Fig 4). The x-ray generator of the micro-CT operated at an accelerated potential of 80 kV with a beam current of 80 μA. The x-ray source combined with a detector operated with a shutter speed of 1,100 ms, which produces images with a voxel size of 18 × 18 × 18 μm3. Computer software (Explore MicroView V.2.0, Analysis Plus, GE Health Care) was used for the visualization of two- and three-dimensional data.
Statistical Analysis
The distance from the CEJ to bone crest, as well as the alveolar bone width at 1, 2, 3, 4, and 5 mm apical to the CEJ, was analyzed using SPSS version 18.00 (IBM).
One-way analysis of variance was performed to assess the differences among groups 1, 2, and 3 and also the differences among individual sites (first, second, and third premolars).
RESULTS At 4 months postsurgery, all extraction sites had healed uneventfully with no complications requiring surgical intervention or administration of antibiotics. Alveolar bone dimensions were measured using micro-CT scans (Fig 5). The mean width of the buccolingual bone according to group is shown in Table 1, and mean widths according to sites are shown in Table 2.
The International Journal of Oral & Maxillofacial Implants 317 © 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Al-Hamoudi et al
Fig 5 Images used for linear measurements of buccolingual dimension in (left) group 1, (middle) group 2, and (right) group 3.
1 mm
2 mm
3 mm
4 mm
5 mm
Table 1 Linear Measurements of Bone Width Apical to the CEJ According to Group At 1 mm
At 2 mm
At 3 mm
At 5 mm
Mean
Group 1
0.75 ± 0.80
3.45 ± 1.26
5.33 ± 1.24
6.62 ± 1.36
7.26 ± 1.77
4.80 ± 2.78
Group 2
1.55 ± 2.07
3.61 ± 0.91
5.56 ± 1.16
6.96 ± 0.95
7.66 ± 0.60
4.98 ± 2.65
Group 3
1.07 ± 1.18
3.00 ± 1.41
5.94 ± 0.97
7.26 ± 1.05
7.77 ± 0.71
4.79 ± 2.79
.61
.77
.67
.97
.99
P
At 4 mm
.62
Table 2 Linear Measurements of Bone Width Apical to the CEJ According to Site Site
At 1 mm
At 2 mm
At 3 mm
At 4 mm
At 5 mm
Mean
First premolar
0.89 ± 1.48
2.63 ± 2.10
5.52 ± 1.00
7.0 ± 0.88
8.0 ± 0.89
5.16 ± 3.08
Second premolar
1.06 ± 1.89
3.42 ± 2.19
5.88 ± 1.17
7.09 ± 1.21
7.51 ± 0.97
5.28 ± 2.91
Third premolar
1.79 ± 2.12
4.18 ± 1.73
5.81 ± 1.43
6.98 ± 1.44
7.37 ± 1.55
5.43 ± 2.63
.20
.69
.96
.33
.97
P
.48
Table 3 depicts the mean distance in millimeters from the CEJ to the crest of the edentulous ridge by groups, and Table 4 shows these measurements by site. Differences among groups 1, 2, and 3, as well as between individual sites, were not statistically significant in either the apicocoronal or buccolingual dimensions of the edentulous ridge (P > .05).
DISCUSSION The results of this study showed no difference between single and multiple extraction sites in the extent of bone loss in the horizontal and vertical dimensions of the edentulous ridge at 4 months after ridge preservation surgery. Previous studies reported that bone loss
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Al-Hamoudi et al
Table 3 Distance from the CEJ to the Crest of the Ridge According to Group Distance (mm) Group 1
Table 4 Distance from the CEJ to the Crest of the Ridge According to Site Site
Distance (mm)
1.94 ± 0.42
First premolar
2.30 ± 0.77
Group 2
2.05 ± 0.48
Second premolar
2.60 ± 1.09
Group 3
2.60 ± 0.67
Third premolar
P
.09
2.0 ± 0.39 .26
P
B P3
P2
P1
Fig 6 Extraction sites of first (P1), second (P2), and third premolars (P3) after full-thickness flap reflection showed similar buccolingual dimensions. B = buccal; L = lingual.
at multiple extraction sites was significantly greater than at single extraction sites when no grafting materials were used or when immediate implants were placed in the extraction sockets.6–8 These studies suggested that extraction of multiple adjacent teeth compromises the blood supply of the alveolar socket and interdental bone. Ridge preservation surgery using bone grafts and barriers may account for the differences in findings between this study and previous ones. Therefore, ridge augmentation surgery may be more critical in multiple extraction sites than for single extraction sites in terms of its ability to reduce bone loss of the edentulous ridge before implant placement. Al-Askar et al6 found that ridge resorption after extraction of multiple adjacent teeth resulted in a large defect that required reconstruction prior to implant therapy. With increased time from extraction to implant placement, progressive ridge resorption may result in further loss of bone volume, to the point at which bone augmentation becomes more challenging, more time consuming, and less predictable.12 The rationale for ridge preservation procedures relies on the fact that alveolar ridge resorption is an unavoidable consequence of tooth loss. Based on understanding of healing events in postextraction sites, the prevention of ridge resorption following tooth extraction seems critical. If the dimensions of the ridge could be maintained, the need for further augmentation procedures would be reduced, simplifying implant surgery at a later time. This pattern of healing is
especially important when esthetics is a major concern for implant restoration, since more bone resorption takes place on the buccal than the lingual aspect of the ridge.13 The present study showed that the placement of a xenograft in fresh extraction sockets may prevent ridge reduction in multiple adjacent extraction sites. This finding is supported by previous studies that showed that bone grafting in combination with collagen membrane placement significantly limited the resorption of hard tissue after tooth extraction.14,15 Araújo et al16 found that, during healing of xenograft, the particles of the graft material became integrated with and further enhanced the dimensions of the bone crest. This is in agreement with findings presented by Nevins et al,17 who reported that sockets treated with bovine bone mineral showed a reduction of < 20% of the buccal plate, whereas ungrafted control sites showed a reduction of > 20%. In the present study, measurements of edentulous ridge width and height were performed 4 months postsurgery using micro-CT. This method generates images with accuracy that is greater than that obtained with other methods of evaluation (eg, cone beam CT).18 Because a micro-CT machine can be used only for limited size specimens, it could not be applied before surgery. Because evaluation of the extraction sites after full-thickness flap reflection did not reveal a notable difference in the buccolingual dimensions among first, second, and third premolars (Fig 6), all the sites were randomly allocated into groups 1, 2, and 3. The International Journal of Oral & Maxillofacial Implants 319
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Al-Hamoudi et al
Based on the finding by Kim et al19 that flapped and flapless ridge preservation lead to similar alveolar bone remodeling and healing, full-thickness flaps were reflected to facilitate primary wound closure in this study. Similar long-term results between flapless and conventional flap techniques were also reported by Caneva et al20 and Bashutski et al21 when implants were placed in extraction sockets. Although the process of alveolar bone modeling and remodeling took place after grafting of the extraction sites, ridge preservation with a combination of xenograft and collagen membranes is a viable treatment to avert severe bone resorption following multiple adjacent tooth extractions. Future studies are needed in humans to compare the outcome of ridge preservation procedures after tooth extraction for periodontal and/or endodontic reasons.
CONCLUSION No difference in alveolar bone width and height was seen following ridge preservation using a combination of xenograft and collagen membrane in single and multiple adjacent extraction sites.
ACKNOWLEDGMENTS The authors would like to express their appreciation and thanks to Dr Andre Paes, Dr Imad Nouneh, and Dr Hussein Assaf for their help in this research. No conflicts of interest are related to this study.
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5. Araujo MG, Lindhe J. Dimensional ridge alterations following tooth extraction. An experimental study in the dog. J Clin Periodontol 2005;32:212–218. 6. Al-Askar M, O’Neill R, Stark P, Griffin T, Javed F, Al-Hezaimi K. Effect of single and contiguous teeth extractions on alveolar bone remodeling: A study in dogs. Clin Implant Dent Relat Res 2011;15:569–575. 7. Al-Shabeeb MS, Al-Askar M, Al-Rasheed A, et al. Alveolar bone remodeling around immediate implants placed in accordance with the extraction socket classification: A three-dimensional microcomputed tomography analysis. J Periodontol 2012;83:981–987. 8. Al-Hezaimi K, Al-Shabeeb MS, Al-Askar M, et al. Microcomputed tomographic analysis of the alveolar ridge alteration around extraction sites with and without immediate implants placement: In vivo study. Clin Implant Dent Relat Res 2014;16:223–229. 9. Al-Hezaimi K, Levi P, Rudy A, Al-Jandan B, Al-Rasheed A. An extraction socket classification developed using analysis of bone type and blood supply to the buccal bone in monkeys. Int J Periodontics Restorative Dent 2011;31:421–427. 10. Suaid F, Grisi MF, Souza SL, Palioto DB, Taba M Jr, Novaes AB Jr. Buccal bone remodeling after tooth extraction using the flapless approach with and without synthetic bone grafting. A histomorphometric study in dogs. Clin Oral Implants Res 2013;24:407–413. 11. Iasella JM, Greenwell H, Miller RL, et al. Ridge preservation with freeze-dried bone allograft and a collagen membrane compared to extraction alone for implant site development: A clinical and histologic study in humans. J Periodontol 2003;74:990–999. 12. Zitzmann NU, Schärer P, Marinello CP. Factors influencing the success of GBR. Smoking, timing of implant placement, implant location, bone quality and provisional restoration. J Clin Periodontol 1999;26:673–682. 13. Pietrokovski J, Massler M. Alveolar ridge resorption following tooth extraction. J Prosthet Dent 1967;17:21–27. 14. Fiorellini JP, Nevins ML. Localized ridge augmentation/preservation. A systematic review. Ann Periodontol 2003;8:321–327. 15. Barone A, Aldini NN, Fini M, Giardino R, Guirado JL, Covani U. Xenograft versus extraction alone for ridge preservation after tooth removal: A clinical and histomorphometric study. J Periodontol 2008; 79:1370–1377. 16. Araújo M, Linder E, Wennström J, Lindhe J. The influence of Bio-Oss Collagen on healing of an extraction socket: An experimental study in the dog. Int J Periodontics Restorative Dent 2008;28:123–135. 17. Nevins M, Camelo M, De Paoli S, et al. A study of the fate of the buccal wall of extraction sockets of teeth with prominent roots. Int J Periodontics Restorative Dent 2006;26:19–29. 18. Swain MV, Xue J. State of the art of Micro-CT applications in dental research. Int J Oral Sci 2009;1:177–188. 19. Kim DM, De Angelis N, Camelo M, Nevins ML, Schupbach P, Nevins M. Ridge preservation with and without primary wound closure: A case series. Int J Periodontics Restorative Dent 2013;33:71–78. 20. Caneva M, Botticelli D, Salata LA, Souza SL, Bressan E, Lang NP. Flap vs. “flapless” surgical approach at immediate implants: A histomorphometric study in dogs. Clin Oral Implants Res 2010;21:1314–1319. 21. Bashutski JD, Wang HL, Rudek I, Moreno I, Koticha T, Oh TJ. The effect of flapless surgery on single-tooth implants in the esthetic zone: A randomized clinical trial. J Periodontol 2013;84:1747–1754.
ERRATUM In the January/February 2015 issue of JOMI, in the article “Microarchitectural Pattern of Pristine Maxillary Bone” (Int J Oral Maxillofac Implants 2015;30:125–132), the authors brought to our attention that the first sentence of the “Results” section in the abstract on page 125 should read: “The mean BV/TV values showed no significant difference between the maxillary anterior (51.90 ± 28.42) and posterior (46.93 ± 26.2) locations.” This correction has been made to the electronic version of the article, which can be found at www.quintpub.com/journals.
320 Volume 30, Number 2, 2015 © 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
