The Stability of Augmented Bone Between Two

The Stability of Augmented Bone Between Two Different Membranes Used for Guided Bone Regeneration Simultaneous with Dental Implant Placement in the Esthetic Zone Sirida Arunjaroensuk, DDS1/Soontra Panmekiate, DDS, PhD2/Atiphan Pimkhaokham, DDS, PhD3 Purpose: This randomized controlled clinical trial compared the stability of augmented bone between a synthetic resorbable membrane and a collagen resorbable membrane with guided bone regeneration (GBR) simultaneous with dental implant placement in the esthetic zone in terms of facial bone thickness. Materials and Methods: A total of 60 dental implants from patients requiring implant placement with simultaneous GBR in the esthetic zone were equally allocated to the test group or control group by block randomization. Biphasic calcium phosphate ceramic bone was used in combination with either a polylactic acid (PLA) membrane (test group, 30 implants) or a resorbable collagen membrane (control group, 30 implants). Cone beam computed tomographic (CBCT) images were used to assess the facial bone thickness postimplantation and then 6 months later at four levels: implant platform and 2 mm, 4 mm, and 6 mm apical to the implant shoulder. Results: All implants were osseointegrated, and no implant loss was found during this study. Facial bone was detected in all cases; however, the thickness of the facial bone was reduced at the 6-month follow-up in both groups. The percentage of facial bone thickness reduction was 34.30%, 27.94%, 24.25%, and 19.81% in the test group and 34.80%, 24.06%, 19.52%, and 20.45% in the control group at the level of the implant platform and at 2 mm, 4 mm, and 6 mm apical to the implant shoulder, respectively. Nevertheless, there was no statistically significant difference between the groups (P > .05). Conclusion: A synthetic resorbable membrane revealed an amount of stable augmented bone similar to that of a collagen resorbable membrane. Int J Oral Maxillofac Implants 2017 (11 pages). doi: 10.11607/jomi.5492 Keywords: cone beam computed tomography, dental implant, facial bone thickness reduction, guided bone regeneration, resorbable membrane, stability of augmented bone

A

deficient alveolar ridge may result in dehiscence or fenestration after implant placement and jeopardizes the esthetic outcome, especially facial bone resorption in the anterior maxilla.1 Therefore, many surgical techniques have been suggested to not only augment the alveolar ridge but also treat the bone defect. 1Master

Student, Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Chulalongkorn University, Bangkok, Thailand. 2 Associate Professor, Department of Radiology, Faculty of Dentistry, Chulalongkorn University, Bangkok, Thailand. 3Associate Professor, Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Chulalongkorn University, Bangkok, Thailand. Correspondence to: Dr Atiphan Pimkhaokham, Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Chulalongkorn University, 34 Henri Dunant Road, Wangmai, Patumwan, Bangkok, Thailand 10330. Fax: +66 2218 8581. Email: [email protected] ©2017 by Quintessence Publishing Co Inc.

Guided bone regeneration (GBR)2–5 is one of the most frequently used techniques and has predictable results in terms of contour augmentation simultaneous with implant placement. Various materials and membranes have been used in conjunction with GBR over the years. Recent clinical studies6–10 have focused on the use of bone substitutes as alternative graft materials, including allografts, xenografts, and synthetic bone grafts, and reported no significant differences across the various bone fillers and autogenous bone. For success in GBR, a barrier membrane is one of the important components of this technique, serving to isolate overlying soft tissue and permitting the regeneration of bone tissue.11 Barrier membrane use shows increased bone formation compared to sites without the application of a membrane for treatment of a bone defect.12–15 Nonresorbable membrane has been accepted as the gold standard despite many disadvantages, including the requirement for second surgery for removal, increased patient morbidity, early membrane exposure, and wound dehiscence and subsequent The International Journal of Oral & Maxillofacial Implants 1

Arunjaroensuk et al

infection.16–18 Currently, collagen resorbable membrane is popularly used and considered the standard resorbable membrane in clinical situations with equal effectiveness as nonresorbable membrane.19,20 However, collagen membrane still has some drawbacks, such as immune responses, transmission of infectious agents, fast biodegradation, and being soft and easily collapsible, resulting in a reduced ability to maintain space and isolate the wound area.2,21–24 To overcome these shortcomings, a synthetic resorbable membrane that can be reproduced in unlimited quantities under controlled conditions was developed to serve as an alternative barrier membrane. Nevertheless, the documentation of clinical studies using a synthetic resorbable membrane is still lacking, and limited data are available that report on the stability of this membrane for contour augmentation simultaneous with dental implant placement. Therefore, the aim of this study was to compare synthetic resorbable membrane with collagen resorbable membrane combined with the use of a synthetic bone substitute material for GBR in terms of the stability of augmented bone at the facial aspect of dental implants.

MATERIALS AND METHODS This study was a prospective randomized controlled clinical investigation. Patients who had a requirement and were eligible for surgical implant placement simultaneous with GBR for the replacement in a partially edentulous area were enrolled in this study at the Faculty of Dentistry, Chulalongkorn University, between February 2014 and November 2015. The study protocol was approved by the Ethics Committee of the Faculty of Dentistry, Chulalongkorn University (HREC-DCU 2014-034). The inclusion criteria were age over 20 years; good general health or well-controlled disease (ASA Class I or II); and an edentulous area or the presence of a hopeless tooth in the central incisor, lateral incisor, canine, or first premolar region of the maxilla that required extraction and replacement with a dental implant by GBR. The exclusion criteria were uncontrolled diseases; immunodeficiency; history of malignancy, radiotherapy, or chemotherapy for malignancy within the past 5 years; being pregnant or breastfeeding; allergy to any material and/or medication used in the study; or an unwillingness to continue for the follow-up period. Patients who met all the inclusion and exclusion criteria signed their informed consent and were assigned to either the test or control group by block randomization. Moreover, if the patient presented with more than one site for implant placement with GBR, the split-mouth technique was applied. 2 doi: 10.11607/jomi.5492

Surgical Procedure

The operation was performed under local anesthesia by one experienced surgeon. The incision was placed at the mid-crest and minimally extended to the adjacent teeth, with releasing incisions if necessary. A fullthickness mucoperiosteal flap was elevated, and the implant site was prepared following current standard manufacturing instructions. All dental implants used in this study were bone-level implants (Straumann AG) with different implant lengths and diameters according to each patient’s anatomy. Simultaneous GBR was performed on the facial aspect with locally collected autogenous bone to cover the exposed implant surface followed by a superficial layer of biphasic calcium phosphate ceramic bone (Straumann Bone Ceramic, Institut Straumann AG). The augmentation material was then covered with the selected membrane, a synthetic resorbable PLA membrane (Guidor, Sunstar) in the test group or a collagen resorbable membrane (Bio-Gide, Geistlich Biomaterials) in the control group. The barrier membranes were trimmed and adapted to the area of augmentation by circular overlap with a minimum of 2 mm. The flaps were replaced to cover the biomaterials and were secured by tension-free primary wound closure with vertical mattress sutures. Adjustments were made to relieve the force directly at the wound area for cases of prosthesis wearing. The postoperative medication administered included a systemic antibiotic (amoxicillin 1 g, twice a day) and analgesic (mefenamic acid 500 mg, three times a day) for 5 days; in patients with a reported allergy to penicillin, 300 mg clindamycin was administered three times a day. All patients received postoperative care instructions and an appointment for suture removal.

Follow-up Assessment

All patients had an appointment for CBCT 1 week after implant placement with GBR for baseline data with small field of view (FOV) operated by one experienced radiologist and had a second CBCT at the 6-month follow-up by the same radiologist to evaluate the stability of augmented bone at the facial aspect of the dental implant. For the CBCT measurement, the facial bone thickness was measured in millimeters using the distance measurement tool of One Volume Viewer software on the CBCT image (Accuitomo 3D, J. Morita Corp) according to Buser et al25 and Chappuis et al.26 In brief, the buccopalatal section perpendicular to the implant axis at the midfacial aspect of the implant was used to measure facial bone thickness both at baseline and at 6 months on CBCTs at four different levels: implant platform and 2 mm, 4 mm, and 6 mm apical to the implant shoulder. One examiner who was trained and calibrated with an experienced radiologist did the measurements.

Arunjaroensuk et al

Statistical Analysis

All data were collected and analyzed using the Statistical Package for Social Science version 22.0 (SPSS Inc) by one examiner, who performed intraexaminer calibration to ensure reliability. All parameters were tested for difference of means by independent samples t test. A calculated P value less than .05, representing the confidence interval of 95%, was considered statistically significant.

Table 1   Patient Information and Demographic Data Test (n = 30)

Control (n = 30)

 Male

10

11

21

 Female

20

19

39

9

6

15

13

13

26

8

11

19

  Central incisor

13

12

25

  Lateral incisor

6

11

17

 Canine

6

2

8

  First premolar

5

5

10 25

Variables Sex

Age (y)   ≤ 40

RESULTS A total of 60 implants from 48 patients who fulfilled the inclusion criteria were consecutively enrolled in this study. Seventeen patients were male and 31 were female. The average age was 51.22 ± 16.19 years, ranging from 21 to 78 years. All implants were equally allocated to the test or control group by block randomization. The diameter and length of implants used in this study were as follows: 3.3-mm diameter (Narrow CrossFit), 10-mm length; 4.1-mm diameter (Regular CrossFit), 8-mm length; 4.1-mm diameter, 10-mm length; and 4.1-mm diameter, 12-mm length. Implants were placed with GBR in 25 central incisors, 17 lateral incisors, 8 canines, and 10 first premolars (Table 1). All implants were stable with existing facial bone, and no implant loss was found over two consecutive CBCTs (Figs 1 to 4). The mean thickness of facial bone at immediate postoperative implant placement with GBR was 3.22, 3.55, 3.69, and 3.62 mm in the test group and 3.42, 3.90, 4.00, and 3.82 mm in the control group at the level of the implant platform and 2 mm, 4 mm, and 6 mm apical to the implant shoulder, respectively. After 6 months of GBR, the mean facial bone thickness was significantly decreased in both groups (P < .001). The test group had a mean facial bone thickness of 2.07, 2.53, 2.82, and 2.92 mm; the control group showed similar results, with a mean facial bone thickness of 2.30, 3.00, 3.24, and 3.04 mm at the level of the implant platform and 2 mm, 4 mm, and 6 mm apical to the implant shoulder, respectively (Table 2). However, one implant showed no facial bone wall directly at implant platform level (Fig 4 [C6mth10]), while minimal augmented bone was detected along some implants at all levels (Fig 2 [S6mth09, S6mth15, S6mth21], Fig 4 [C6mth09]). The facial bone reduction was analyzed by the percentage of change between the baseline and the 6-month follow-up. In the test group, the percentage of change in facial bone thickness was –34.30%, –27.94%, –24.25%, and –19.81%, whereas that in the control group was –34.80%, –24.06%, –19.52%, and –20.45% at the level of the implant platform and at 2

Total (n = 60)

 41–60   ≥ 61 Implant area

Implant diameter/length (mm)  3.3/10

12

13

 4.1/8

1

0

1

 4.1/10

17

16

33

 4.1/12

0

1

1

mm, 4 mm, and 6 mm apical to the implant shoulder, respectively. However, these percentages of change did not yield a statistically significant difference between the groups (P > .05) (Table 3). Minor complications of gingival inflammation and membrane exposure were observed in three cases in the test group and two cases in the control group, but all sites recovered uneventfully. Regarding the membrane handling and manipulation, the synthetic membranes were stiff and difficult to adapt, so preshaping before adapting to the site of GBR should be recommended. In contrast, the collagen membranes were soft and easily collapsed during flap closure.

DISCUSSION The purpose of contour augmentation by GBR is to establish sufficient facial bone thickness to support soft tissues for esthetic outcomes. There are two important factors for success in GBR: the quality of surgery and the properties of the biomaterials used. All surgical procedures in this study were performed by only one experienced surgeon; thus, the quality standard of the surgery could be controlled, and the results were influenced only by the biomaterials used. The International Journal of Oral & Maxillofacial Implants 3

Arunjaroensuk et al

Simm01

Simm02

Simm03

Simm04

Simm05

Simm06

Simm07

Simm08

Simm09

Simm10

Simm11

Simm12

Simm13

Simm14

Simm15

Simm16

Simm17

Simm18

Simm19

Simm20

Simm21

Simm22

Simm23

Simm24

Simm25

Simm26

Simm27

Simm28

Simm29

Simm30

Fig 1   CBCT images of all implants of the test group at baseline.

4 doi: 10.11607/jomi.5492

Arunjaroensuk et al

S6mo01

S6mo02

S6mo03

S6mo04

S6mo05

S6mo06

S6mo07

S6mo08

S6mo09

S6mo10

S6mo11

S6mo12

S6mo13

S6mo14

S6mo15

S6mo16

S6mo17

S6mo18

S6mo19

S6mo20

S6mo21

S6mo22

S6mo23

S6mo24

S6mo25

S6mo26

S6mo27

S6mo28

S6mo29

S6mo30

Fig 2   CBCT images of all implants of the test group at 6-month follow-up.

The International Journal of Oral & Maxillofacial Implants 5

Arunjaroensuk et al

Cimm01

Cimm02

Cimm03

Cimm04

Cimm05

Cimm06

Cimm07

Cimm08

Cimm09

Cimm10

Cimm11

Cimm12

Cimm13

Cimm14

Cimm15

Cimm16

Cimm17

Cimm18

Cimm19

Cimm20

Cimm21

Cimm22

Cimm23

Cimm24

Cimm25

Cimm26

Cimm27

Cimm28

Cimm29

Cimm30

Fig 3   CBCT images of all implants of the control group at baseline.

6 doi: 10.11607/jomi.5492

Arunjaroensuk et al

Cimm01

Cimm02

Cimm03

Cimm04

Cimm05

Cimm06

Cimm07

Cimm08

Cimm09

Cimm10

Cimm11

Cimm12

Cimm13

Cimm14

Cimm15

Cimm16

Cimm17

Cimm18

Cimm19

Cimm20

Cimm21

Cimm22

Cimm23

Cimm24

Cimm25

Cimm26

Cimm27

Cimm28

Cimm29

Cimm30

Fig 4   CBCT images of all implants of the control group at 6-month follow-up.

The International Journal of Oral & Maxillofacial Implants 7

Arunjaroensuk et al

Table 2   Facial Bone Thickness at Immediate Postoperative Implant Placement with GBR and 6 Months Later in Both Groups (Mean ± Standard Deviation) Facial bone thickness (mm) Test group Level of measurement

Control group

Immediate

6 months

P value

Immediate

6 months

P value

Platform

3.22 ± 1.00

2.07 ± 0.94

.000*

3.42 ± 0.85

2.30 ± 1.10

.000*

2 mm apical

3.55 ± 0.98

2.53 ± 0.93

.000*

3.90 ± 0.88

3.00 ± 1.01

.000*

4 mm apical

3.69 ± 1.13

2.82 ± 1.18

.000*

4.00 ± 0.91

3.24 ± 0.97

.000*

6 mm apical

3.62 ± 1.18

2.92 ± 1.26

.000*

3.82 ± 0.99

3.04 ± 1.00

.000*

*Statistically significant, P < .05.

Table 3   The Percentage of Facial Bone Thickness Change at Immediate Postoperative Implant Placement with GBR and 6 Months Later in Both Groups (Mean ± Standard Deviation) Change in facial bone thickness (%) Level of measurement Platform

Test group

Control group

P value

–34.30 ± 23.85

–34.80 ± 23.68

.935 .350

2 mm apical

–27.94 ± 17.88

–24.06 ± 13.73

4 mm apical

–24.25 ± 17.59

–19.52 ± 12.39

.233

6 mm apical

–19.81 ± 18.06

–20.45 ± 14.14

.880

The GBR technique involves the use of a barrier membrane with the grafting material for bone regeneration. Many studies12,13,15,27–29 have stated that GBR demonstrated better results than bone graft treatment alone in the correction of bone defects. Therefore, a nonmembrane use group was not designed for comparison in the present study. Moreover, the main focus of this study was to evaluate the stability of the augmented bone at the facial aspect of dental implants with the GBR procedure between two different membranes, not the influence of the membrane on the property of formed bone. The augmented bone at the facial aspect can be assessed by 3D radiographic imaging; therefore, CBCT was used to measure the facial bone thickness. The CBCT results indicated that both a synthetic resorbable membrane and a collagen resorbable membrane were able to provide successful contour augmentation on the facial aspect of a dental implant. The CBCT images demonstrated a mean facial bone thickness of more than 2 mm after 6 months of contour augmentation in both groups. This result was similar to that of a study by Buser et al25 in 2013 that reported the long-term outcome of GBR in single-implant placement by mean facial bone thickness using CBCT. The result exhibited very good success of 20 implants at 6 years postoperatively. However, the authors did not mention the volume change of the augmented bone. Although the present study used a slowly resorbable graft material on the facial surface, bone reduction was found at 6 months after contour augmentation and was most pronounced at platform level in both the test and 8 doi: 10.11607/jomi.5492

control groups. The reduction at other levels diminished slightly more in the test group compared to the control group. Nevertheless, these changes did not reach a statistically significant difference between the two groups for any level. The possibility exists that this bone reduction resulted from the collapse of the membrane during the flap suturing and the displacement of the coronal part of the bone substitute due to the compressive forces at the area of augmentation.7,30,31 Moreover, the resorption of the thin facial bone plate and the bone remodeling process affected the amount of augmented bone and resulted in the reduction of total facial bone thickness following GBR.32–34 Mir-Mari et al35 examined the influence of flap suturing on volume change following the GBR technique with xenografts and collagen membranes by using CBCT before and after flap closure. The authors reported that the particulate bone grafts at the coronal part were displaced followed by a partial collapse of the membrane during the flap suturing. Although all cases were performed with a tension-free wound closure, the area of GBR could not be deprived of the compressive forces, especially at the coronal site. Membrane fixation was desired to enhance the stabilization of the collagen membranes and for successful outcome of ridge augmentation; however, the use of a fixation pin or screw has several risks, such as injury to adjacent roots or anatomical vital structures and the need of reentry for pin/screw removal.36,37 Consequently, fixation pins are not recommended for current routine use with GBR in cases of bone augmentation with single implant placement.38,39

Arunjaroensuk et al

Another reason for the bone reduction was the early membrane exposure. In spite of the fact that the resorbable membrane can be exposed and had self-healing without infection, the premature exposure had a negative effect on barrier function and resulted in unsuccessful bone integration at the recipient site and less bone formation in GBR.28,40–42 In this study, membrane exposure was found in three cases of the test group and two cases of the control group. Patients were instructed regarding home oral hygiene care and observed every 2 weeks until complete gingival coverage and uneventful healing were obtained. The CBCT results at 6 months later demonstrated sufficient formed facial bone in all membrane-exposed patients. With regard to some cases in this study with minimal augmented bone along the implant in the CBCT images, no membrane exposure was recorded. One of these implants was placed following tooth extraction due to trauma, which may have a great influence on bone resorption. However, acceptable clinical findings were found with no implant loss during this study, and long-term follow-up should be considered. The clinical study of Schneider et al43 in 2011 evaluated the stability of peri-implant tissue using techniques different from those used in this study. The authors used cast models based on alginate impressions to assess the dimensional changes of periimplant tissue. The casts were optically scanned and digitally superimposed to compare the dimensions of surrounding soft tissue at different time points. The authors concluded that augmented peri-implant tissue volume remained stable within 1 year of crown delivery, with a mean loss of 0.04 mm in the labial direction and a mean gingival recession of 0.22 mm. The mean loss of labial prominence was assessed by the measurement of volume alteration following the augmentation of both bone and soft tissue. In the assessment of only bone alteration, the mean volume gain was 0.72 mm in the labial direction after 6 months of bone augmentation. However, the facial bone thickness immediately postoperation was not reported, so the volume change could not be calculated. Facial bone resorption has also been supported in other recent prospective studies25,26,44–46 by consecutive CBCT images. Among these, Chappuis et al26 in 2016 compared facial bone crest dimensions following implantation with GBR of two different implant neck designs at 5 to 9 years in the esthetic zone using CBCT. They measured the bone crest at various levels: implant shoulder and 2 mm, 4 mm, and 6 mm below shoulder level. The authors reported that the facial crest thickness showed statistical significance between the bone-level neck design (1.2 mm) and the soft tissue–level neck design (0 mm) at implant

shoulder level, but the other levels did not exhibit significant differences. Unfortunately, there were no data on the facial bone wall immediately postoperation, so the alteration of facial bone wall dimension could not be analyzed. Regardless of the type of membrane, the timing of implant placement is another factor that influences the stability of facial bone thickness. Greater labial bone resorption was reported in immediate implant placement than in delayed implant placement, both vertically and horizontally.47,48 Miyamoto and Obama49 reported that the labial bone resorption in a group with immediate implant placement was higher than that in a group with delayed implant placement. Moreover, gingival recession was negatively related to horizontal labial bone resorption but showed a significant positive correlation with vertical bone loss after implant placement. The authors concluded that gingival recession was significantly greater when performing immediate implant placement, and the recession decreased in the case of labial bone thickness ≥ 2 mm for both methods due to the minimal vertical bone loss. In contrast to the present study, there was no statistically significant difference in the change in facial bone thickness between immediate and delayed implant placement. This might have been due to the small number in each group. The present study has several methodological limitations. First, a dental titanium implant is a radiodense material that can cause beam hardening artifacts and difficulty in visualization of the bone boundaries.50 Moreover, scattered radiation is higher in larger FOV.51 To minimize this problem, a small FOV with a voxel size of 0.125 mm and high-resolution CBCT images were used for more accuracy of measurement in this study following the recommendations of Molen.52 The other limitation of this study is the absence of records of the initial existing facial plate and bone augmentation materials used in this study, which had radiopacity not much different from human bone, so it is difficult to discriminate new bone formation, bone grafting material, and the initial existing facial buccal wall. One should keep in mind that this study focused on the assessment of the augmented bone remaining by measuring facial bone thickness in two consecutive CBCTs after implantation with GBR. The baseline data of facial bone thickness included both the initial existing facial wall and bone graft material recorded for comparison with 6-month data. For this reason, the initial existing facial plate did not need to be investigated. However, further studies with long-term follow-up as well as consideration of various factors, such as type of implant placement, type of prosthesis, and duration of function, are required to improve the understanding of sustainable esthetic outcomes. The International Journal of Oral & Maxillofacial Implants 9

Arunjaroensuk et al

CONCLUSIONS Despite its limitations, this study was able to compare two different types of resorbable membranes in maintaining the amount of stable augmented bone by using the GBR technique over a short period.

ACKNOWLEDGMENTS This research was supported by the 90th Anniversary of Chulalongkorn University Rachadapisek Sompote Fund. The authors report no conflicts of interest related to this study.

REFERENCES 1. Belser UC, Buser D, Hess D, Schmid B, Bernard JP, Lang NP. Aesthetic implant restorations in partially edentulous patients—A critical appraisal. Periodontol 2000 1998;17:132–150. 2. Hämmerle CH, Jung RE. Bone augmentation by means of barrier membranes. Periodontol 2000 2003;33:36–53. 3. Aghaloo TL, Moy PK. Which hard tissue augmentation techniques are the most successful in furnishing bony support for implant placement? Int J Oral Maxillofac Implants 2007;22(suppl):s49–s70. 4. Chiapasco M, Casentini P, Zaniboni M. Bone augmentation procedures in implant dentistry. Int J Oral Maxillofac Implants 2009;24(suppl):s237–s259. 5. Benic GI, Hämmerle CH. Horizontal bone augmentation by means of guided bone regeneration. Periodontol 2000 2014;66:13–40. 6. Fiorellini JP, Kim DM, Nakajima Y, Weber HP. Osseointegration of titanium implants following guided bone regeneration using expanded polytetrafluoroethylene membrane and various bone fillers. Int J Periodontics Restorative Dent 2007;27:287–294. 7. Schwarz F, Herten M, Ferrari D, et al. Guided bone regeneration at dehiscence-type defects using biphasic hydroxyapatite + beta tricalcium phosphate (Bone Ceramic) or a collagen-coated natural bone mineral (BioOss Collagen): An immunohistochemical study in dogs. Int J Oral Maxillofac Surg 2007;36:1198–1206. 8. Chiapasco M, Zaniboni M. Clinical outcomes of GBR procedures to correct peri-implant dehiscences and fenestrations: A systematic review. Clin Oral Implants Res 2009;20(suppl):s113–s123. 9. Mardas N, Chadha V, Donos N. Alveolar ridge preservation with guided bone regeneration and a synthetic bone substitute or a bovine-derived xenograft: A randomized, controlled clinical trial. Clin Oral Implants Res 2010;21:688–698. 10. Van Assche N, Michels S, Naert I, Quirynen M. Randomized controlled trial to compare two bone substitutes in the treatment of bony dehiscences. Clin Implant Dent Relat Res 2013;15:558–568. 11. Hämmerle CH, Jung RE, Feloutzis A. A systematic review of the survival of implants in bone sites augmented with barrier membranes (guided bone regeneration) in partially edentulous patients. J Clin Periodontol 2002;29(suppl):s226–s231. 12. Calvo-Guirado JL, Ramírez-Fernández MP, Delgado-Ruíz RA, MatéSánchez JE, Velasquez P, de Aza PN. Influence of biphasic β-TCP with and without the use of collagen membranes on bone healing of surgically critical size defects. A radiological, histological, and histomorphometric study. Clin Oral Implants Res 2014;25:1228–1238. 13. Gordh M, Alberius P, Johnell O, Lindberg L, Linde A. Effects of rhBMP-2 and osteopromotive membranes on experimental bone grafting. Plast Reconstr Surg 1999;103:1909–1918. 14. Blanco J, Alonso A, Sanz M. Long-term results and survival rate of implants treated with guided bone regeneration: A 5-year case series prospective study. Clin Oral Implants Res 2005;16:294–301. 15. Jovanovic SA, Hunt DR, Bernard GW, Spiekermann H, Wozney JM, Wikesjö UM. Bone reconstruction following implantation of rhBMP-2 and guided bone regeneration in canine alveolar ridge defects. Clin Oral Implants Res 2007;18:224–230.

10 doi: 10.11607/jomi.5492

16. Gottlow J. Guided tissue regeneration using bioresorbable and non-resorbable devices: Initial healing and long-term results. J Periodontol 1993;64(suppl):s1157–s1165. 17. Simion M, Trisi P, Maglione M, Piattelli A. A preliminary report on a method for studying the permeability of expanded polytetrafluoroethylene membrane to bacteria in vitro: A scanning electron microscopic and histological study. J Periodontol 1994;65:755–761. 18. Lorenzoni M, Pertl C, Keil C, Wegscheider WA. Treatment of periimplant defects with guided bone regeneration: A comparative clinical study with various membranes and bone grafts. Int J Oral Maxillofac Implants 1998;13:639–646. 19. Carpio L, Loza J, Lynch S, Genco R. Guided bone regeneration around endosseous implants with anorganic bovine bone mineral. A randomized controlled trial comparing bioabsorbable versus non-resorbable barriers. J Periodontol 2000;71:1743–1749. 20. Zitzmann NU, Naef R, Schärer P. Resorbable versus nonresorbable membranes in combination with Bio-Oss for guided bone regeneration. Int J Oral Maxillofac Implants 1997;12:844–852. 21. Sela MN, Kohavi D, Krausz E, Steinberg D, Rosen G. Enzymatic degradation of collagen-guided tissue regeneration membranes by periodontal bacteria. Clin Oral Implants Res 2003;14:263–268. 22. Hämmerle CH, Karring T. Guided bone regeneration at oral implant sites. Periodontol 2000 1998;17:151–175. 23. Schwartzmann M. Use of collagen membranes for guided bone regeneration: A review. Implant Dent 2000;9:63–66. 24. Sogal A, Tofe AJ. Risk assessment of bovine spongiform encephalopathy transmission through bone graft material derived from bovine bone used for dental applications. J Periodontol 1999;70:1053–1063. 25. Buser D, Chappuis V, Kuchler U, et al. Long-term stability of early implant placement with contour augmentation. J Dent Res 2013;92(suppl):s176–s182. 26. Chappuis V, Bornstein MM, Buser D, Belser U. Influence of implant neck design on facial bone crest dimensions in the esthetic zone analyzed by cone beam CT: A comparative study with a 5-to-9-year follow-up. Clin Oral Implants Res 2016;27:1055–1064. 27. von Arx T, Cochran DL, Hermann JS, Schenk RK, Buser D. Lateral ridge augmentation using different bone fillers and barrier membrane application. A histologic and histomorphometric pilot study in the canine mandible. Clin Oral Implants Res 2001;12:260–269. 28. Alberius P, Dahlin C, Linde A. Role of osteopromotion in experimental bone grafting to the skull: A study in adult rats using a membrane technique. J Oral Maxillofac Surg 1992;50:829–834. 29. Antoun H, Sitbon JM, Martinez H, Missika P. 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. 30. Zellin G, Gritli-Linde A, Linde A. Healing of mandibular defects with different biodegradable and non-biodegradable membranes: An experimental study in rats. Biomaterials 1995;16:601–609. 31. Mellonig JT, Nevins M, Sanchez R. Evaluation of a bioabsorbable physical barrier for guided bone regeneration. Part I. Material alone. Int J Periodontics Restorative Dent 1998;18:139–149. 32. Strietzel FP, Khongkhunthian P, Khattiya R, Patchanee P, Reichart PA. Healing pattern of bone defects covered by different membrane types–A histologic study in the porcine mandible. J Biomed Mater Res B Appl Biomater 2006;78:35–46. 33. Araújo MG, Wennström JL, Lindhe J. Modeling of the buccal and lingual bone walls of fresh extraction sites following implant installation. Clin Oral Implants Res 2006;17:606–614. 34. Ferrus J, Cecchinato D, Pjetursson EB, Lang NP, Sanz M, Lindhe J. Factors influencing ridge alterations following immediate implant placement into extraction sockets. Clin Oral Implants Res 2010;21:22–29. 35. Mir-Mari J, Wui H, Jung RE, Hämmerle CH, Benic GI. Influence of blinded wound closure on the volume stability of different GBR materials: An in vitro cone-beam computed tomographic examination. Clin Oral Implants Res 2016;27:258–265. 36. Siar CH, Toh CG, Romanos G, Ng KH. Subcutaneous reactions and degradation characteristics of collagenous and noncollagenous membranes in a macaque model. Clin Oral Implants Res 2011;22:113–120.

Arunjaroensuk et al

37. Lorenzoni M, Pertl C, Polansky RA, Jakse N, Wegscheider WA. Evaluation of implants placed with barrier membranes. A restrospective follow-up study up to five years. Clin Oral Implants Res 2002;13:274–280. 38. Buser D. Implant placement with simultaneous guided bone regeneration: Selection of biomaterials and surgical principles. In: Buser D (ed). 20 Years of Guided Bone Regeneration in Implant Dentistry, ed 2. Chicago: Quintessence, 2009:123–152. 39. Urban IA, Lozada JL, Wessing B, Suárez-López del Amo FSL, Wang HL. Vertical bone grafting and periosteal vertical mattress suture for the fixation of resorbable membranes and stabilization of particulate grafts in horizontal guided bone regeneration to achieve more predictable results: A technical report. Int J Periodontics Restorative Dent 2016;36:153–159. 40. Donos N, Kostopoulos L, Karring T. Augmentation of the rat jaw with autogeneic cortico-cancellous bone grafts and guided tissue regeneration. Clin Oral Implants Res 2002;13:192–202. 41. Donos N, Kostopoulos L, Karring T. Alveolar ridge augmentation by combining autogenous mandibular bone grafts and non-resorbable membranes. Clin Oral Implants Res 2002;13:185–191. 42. Simion M, Baldoni M, Rossi P, Zaffe D. A comparative study of the effectiveness of e-PTFE membranes with and without early exposure during the healing period. Int J Periodontics Restorative Dent 1994;14:166–180. 43. Schneider D, Grunder U, Ender A, Hämmerle CH, Jung RE. Volume gain and stability of peri-implant tissue following bone and soft tissue augmentation: 1-year results from a prospective cohort study. Clin Oral Implants Res 2011;22:28–37. 44. Chappuis V, Engel O, Reyes M, Shahim K, Nolte LP, Buser D. Ridge alterations post-extraction in the esthetic zone: A 3D analysis with CBCT. J Dent Res 2013;92(suppl):s195–s201.

45. Misawa M, Lindhe J, Araújo MG. The alveolar process following single-tooth extraction: A study of maxillary incisor and premolar sites in man. Clin Oral Implants Res 2016;27:884–889. 46. Kaminaka A, Nakano T, Ono S, Kato T, Yatani H. Cone-beam computed tomography evaluation of horizontal and vertical dimensional changes in buccal peri-implant alveolar bone and soft tissue: A 1-year prospective clinical study. Clin Implant Dent Relat Res 2015;17(suppl):e576–e585. 47. Botticelli D, Berglundh T, Lindhe J. Hard-tissue alterations following immediate implant placement in extraction sites. J Clin Periodontol 2004;31:820–828. 48. Botticelli D, Persson LG, Lindhe J, Berglundh T. Bone tissue formation adjacent to implants placed in fresh extraction sockets: An experimental study in dogs. Clin Oral Implants Res 2006;17:351–358. 49. Miyamoto Y, Obama T. Dental cone beam computed tomography analyses of postoperative labial bone thickness in maxillary anterior implants: Comparing immediate and delayed implant placement. Int J Periodontics Restorative Dent 2011;31:215–225. 50. Razavi T, Palmer RM, Davies J, Wilson R, Palmer PJ. Accuracy of measuring the cortical bone thickness adjacent to dental implants using cone beam computed tomography. Clin Oral Implants Res 2010;21:718–725. 51. Scarfe WC, Farman AG. What is cone-beam CT and how does it work? Dent Clin North Am 2008;52:707–730. 52. Molen AD. Considerations in the use of cone-beam computed tomography for buccal bone measurements. Am J Orthod Dentofacial Orthop 2010;137(suppl):s130–s135.

The International Journal of Oral & Maxillofacial Implants 11