Clinical and histologic outcomes of socket grafting after flapless tooth extraction: A systematic review of randomized controlled clinical trials

SYSTEMATIC REVIEW

Clinical and histologic outcomes of socket grafting after flapless tooth extraction: A systematic review of randomized controlled clinical trials Shantanu Jambhekar, BDS, MDS,a Florian Kernen, Dr med Dent,b and Avinash S. Bidra, BDS, MSc

ABSTRACT Statement of problem. Several biomaterials and techniques have been reported for socket grafting and alveolar ridge preservation. However, the evidence for clinical and histologic outcomes for socket grafting with different types of materials in flapless extraction is not clear. Purpose. The purpose of this systematic review was to analyze the outcomes of a socket grafting procedure performed with flapless extraction of teeth in order to determine which graft material results in the least loss of socket dimensions, the maximum amount of vital bone, the least remnant graft material, and the least amount of connective tissue after a minimum of 12 weeks of healing. Secondary outcomes, including the predictability of regenerating deficient buccal bone, necessity of barrier membranes, and coverage with autogenous soft tissue graft, were also evaluated. Material and methods. An electronic search for articles in the English-language literature was performed independently by multiple investigators using a systematic search process with the PubMed search engine. After applying predetermined inclusion and exclusion criteria, the final list of randomized controlled clinical trials (RCTs) for flapless extraction and socket grafting was analyzed to derive results for the various objectives of the study. Results. The initial electronic search resulted in 2898 titles. The systematic application of inclusion and exclusion criteria resulted in 32 RCTs studying 1354 sockets, which addressed the clinical and histologic outcomes of flapless extraction with socket grafting and provided dimensional and histologic information at or beyond the 12-week reentry period. From these RCTs, the mean loss of buccolingual width at the ridge crest was lowest for xenografts (1.3 mm), followed by allografts (1.63 mm), alloplasts (2.13 mm), and sockets without any socket grafting (2.79 mm). Only 3 studies reported on loss of width at 3 mm below the ridge crest. The mean loss of buccal wall height from the ridge crest was lowest for xenografts (0.57 mm) and allografts (0.58 mm), followed by alloplasts (0.77 mm) and sockets without any grafting (1.74 mm). The mean histologic outcomes at or beyond the 12-week reentry period revealed the highest vital bone content for sockets grafted with alloplasts (45.53%), followed by sockets with no graft material (41.07%), xenografts (35.72%), and allografts (29.93%). The amount of remnant graft material was highest for sockets grafted with allografts (21.75%), followed by xenografts (19.3%) and alloplasts (13.67%). The highest connective tissue content at the time of reentry was seen for sockets with no grafting (52.53%), followed by allografts (51.03%), xenografts (44.42%), and alloplast (38.39%). Data for new and emerging biomaterials such as cell therapy and tissue regenerative materials were not amenable to calculations because of biomaterial heterogeneity and small sample sizes. Conclusions. After flapless extraction of teeth, and using a minimum healing period of 12 weeks as a temporal measure, xenografts and allografts resulted in the least loss of socket dimensions compared to alloplasts or sockets with no grafting. Histologic outcomes after a minimum of 12 weeks of healing showed that sockets grafted with alloplasts had the maximum amount of vital bone and the least amount of remnant graft material and remnant connective tissue. There is a limited but emerging body of evidence for the predictable regeneration of deficient buccal bone with socket grafting materials, need for barrier membranes, use of tissue engineering, and use of autogenous soft tissue grafts from the palate to cover the socket. (J Prosthet Dent 2015;-:---)

a

Assistant Professor, Terna Dental College Nerul, Mumbai, India; Former ITI Scholar, Department of Reconstructive Sciences University of Connecticut Health Center, Farmington, Conn. b Former prosthodontics fellow, Department of Reconstructive Sciences, University of Connecticut Health Center, Farmington, Conn. c Program Director, Department of Reconstructive Sciences, Post-Graduate Prosthodontics, University of Connecticut Health Center, Farmington, Conn.

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Clinical Implications After a flapless tooth extraction, socket grafting is recommended as a preprosthetic procedure to minimize the loss of socket width and buccal wall height. Xenografts or allografts are a good choice for minimizing the loss of buccolingual width, while alloplasts attain the maximum amount of vital bone after 12 weeks. A minimum healing period of over 12 weeks is recommended for favorable biologic outcomes before implant placement. The alveolar process is a tooth-dependent tissue, which develops along with the eruption of the teeth. The extraction of a tooth initiates a series of reparative processes involving both hard tissue (alveolar bone) and soft tissues (periodontal ligament, gingiva).1-4 The chronological sequence of biologic events occurring during the healing of an extraction socket result in alveolar ridge resorption.1-8 This phenomenon appears to be progressive and irreversible, resulting in myriad prosthodontic, esthetic, and functional challenges during the replacement of missing teeth. Several human studies evaluating the healing of extraction socket have confirmed that the alveolar process atrophies after the loss of single or multiple teeth.9-53 Smukler et al54 reported that resorption is more pronounced in the mandible than in the maxilla and that the buccal side loses more volume than the lingual. The greatest amount of bone loss occurs in the horizontal dimension, mainly on the facial aspect of the ridge. Loss of vertical ridge height has been described as most pronounced on the buccal aspect.9,55-58 Socket grafting or ridge preservation involves grafting the extraction socket with biomaterial alone or in combination with barrier membrane and/or an advanced or rotated pedicle flap/connective tissue/free gingival graft.59 The popular term “socket preservation” is a misnomer, as it may imply preservation or maintenance of the socket in its original or existing state, which is obviously undesirable. A number of biomaterials and techniques for socket grafting have been reported and can be grouped into 4 categories (Table 1).59 In recent years, 13 systematic reviews have addressed the healing of extraction sockets and the dimensional changes (height and width) of the hard and soft tissues of the alveolar ridge.60-72 A general consensus among the results of these 13 systematic reviews is that although socket grafting did not completely prevent bone resorption, it appeared to be effective in preserving the alveolar ridge volume compared with extraction alone. Nevertheless, many deficiencies remain from previous 13 systematic reviews. No systematic reviews have attempted to compare the clinical and histologic outcomes between various socket grafting materials or answer questions relating to temporal measures and THE JOURNAL OF PROSTHETIC DENTISTRY

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healing. Additionally, previous systematic reviews have all grouped socket grafting outcomes after flapless and flap surgical approaches of teeth extractions.60-72 Flapless approach for teeth extractions is known to be a simple, atraumatic, and conservative method. Various authors have reported improved clinical outcomes with the flapless approach for teeth extractions with reduced healing times, discomfort, and inflammation.23,46,47 Flapless extraction of teeth entails nondetachment of the periosteum and therefore preserves blood supply to the underlying buccal bone and has been accounted for the reduced loss of alveolar bone compared to a flapless extraction.23,46,47,73-77 In a recent randomized clinical trial, Barone et al47 showed that the flapless technique could preserve the horizontal hard tissue dimension and increase the keratinized gingiva more successfully than the flapped technique for tooth extraction. The primary purpose of this systematic review was to analyze the clinical outcomes of socket grafting procedures performed with the flapless extraction of teeth to find out which graft material results in the least loss of socket dimensions, the maximum amount of vital bone, the least remnant graft material, and the least connective tissue after a minimum of 12 weeks of healing. Secondary outcomes, including the predictability of regenerating deficient buccal bone, the need for barrier membranes, and coverage with autogenous soft tissue grafts, were also evaluated. MATERIAL AND METHODS An independent electronic search of the Englishlanguage literature was performed by multiple investigators using the PubMed search engine and the Cochrane Library database. The specific terms that were used for the electronic search were tooth extraction and socket grafting OR tooth extraction and socket preservation OR tooth extraction and ridge preservation or tooth extraction and alveolar ridge preservation OR tooth extraction and socket seal OR tooth extraction and allograft OR tooth extraction and bio-oss OR tooth extraction and fdba OR tooth extraction and bovine bone OR tooth extraction and collagen OR tooth extraction and dfdba OR tooth extraction and biomaterial OR tooth extraction and ridge augmentation OR tooth extraction and platelet OR tooth extraction and plasma OR tooth extraction and calcium sulfate OR tooth extraction and calcium phosphate OR tooth extraction and site development OR tooth extraction and alloplast OR tooth extraction and porcine bone OR tooth extraction and ridge healing OR tooth extraction and bone morphogenic protein OR tooth extraction and buccal bone OR tooth extraction and hydroxyapatite OR tooth extraction and bioceramic material OR tooth extraction and post extraction OR tooth extraction and membrane OR tooth extraction and autogenous bone OR tooth extraction and Jambhekar et al

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Table 1. Overview of biomaterials used for socket grafting59 Biomaterial Type

Definition*

Autogenous bone graft

Bone graft taken from an intraoral or extraoral site and placed in same individual. Origin of graft will determine whether it is cortical, corticocancellous, or cancellous in nature.

Allogenic bone graft (allograft)

Graft between genetically dissimilar members of same species. Iliac cancellous bone and marrow, freeze-dried bone allograft (FDBA), and demineralized freeze-dried bone allograft (DFDBA) are available commercially from tissue banks.

Xenogenic bone graft (xenograft)

Graft obtained from a donor of another species; also termed heterograft.

Alloplastic bone graft (alloplast)

Graft material such as hydroxyapatite (HA), tricalcium phosphate (TCP), polymethylmethacrylate (PMMA), and hydroxyethyl methacrylate (HEMA) polymer, or bioactive glass that is derived either synthetically or from a foreign, inert source.

Other materials

Platelet-rich plasma (PRP), platelet-rich fibrin (PRF), gone morphogenetic protein (BMP), Emdogain (EMD), cell therapy.

*Glossary of Oral and Maxillofacial Implants.

bone regeneration OR tooth extraction and bone substitute OR tooth extraction and connective tissue graft OR tooth extraction and flap OR tooth extraction and flapless OR tooth extraction and ridge change OR tooth extraction and socket healing OR tooth extraction and synthetic graft OR tooth extraction and xenograft OR tooth extraction and beta tcp. The Patient-Intervention-Control-Outcome (PICO) question for this systematic review was, in patients with flapless extraction of teeth, does socket grafting with a specific type of material (xenograft, allograft, alloplast, or other materials) compared to sockets with no graft material, provide superior clinical and histologic outcomes after a 12-week healing period? The publication dates searched were of studies published from January 1, 1990, to November 12, 2013. The only search limits applied to the electronic search was the English language and the publication date range. The predetermined inclusion and exclusion criteria are reported in Table 2. The electronic search process was systematically conducted in 3 stages. In stage 1, the investigators independently screened all relevant titles of the electronic search, and any disagreement was resolved by discussion. In situations where the application of the exclusion criteria was not clear, the controversial article was included for consideration in the abstract stage. In stage 2, the investigators independently analyzed the abstracts of all selected titles, and disagreements were resolved by discussion. In situations of uncertainty, the abstract was included for the subsequent full-text stage. After the application of the exclusion criteria, the definitive list of articles was screened at stage 3 by the investigators to extract qualitative and quantitative data. A supplemental search was conducted on the basis of the references from the definitive list of fulltext articles from stage 3 and additional articles published beyond the terminal search date (November 12, 2013, to July 1, 2014). Data from all included randomized controlled trials (RCTs) were then tabulated, analyzed, and compared for various graft materials. RESULTS The initial electronic search using the specific search terms from the PubMed search engine resulted in a total Jambhekar et al

Table 2. Predetermined eligibility criteria for inclusion and exclusion Inclusion Criteria 

Any English-language articles published in peer-reviewed journal.



Any RCT involving any of search terms.

Exclusion Criteria 

Articles that did not pertain to items described in inclusion criteria.



RCTs that did not describe data on flapless extraction of teeth.



RCTs that did not describe data at or beyond 12-week healing period after flapless extraction.



Articles that did not pertain to objectives of systematic review.



Nonrandomized clinical studies, review articles, or technique articles without associated clinical study and data.



Articles that did not report on follow-up period before reentry into socket.



Articles that reported on socket grafting for purposes other than site development for implant placement.



Patients or data repeated in other included articles.



Article description that would not allow extraction of quantitative data related to study objectives.

RCT, randomized controlled trial.

of 2898 titles, out of which 181 abstracts were applicable to the study. Further scrutiny resulted in the elimination of 162 full-text articles. A supplementary search for articles published after the terminal search date (November 12, 2013, to July 1, 2014) was done; articles were directly subjected to full-text analysis and predetermined exclusion criteria were applied. This eventually resulted in a total of 32 RCTs that reported the clinical and histologic outcomes at or beyond the 12-week reentry period. These 32 RCTs were included for qualitative and quantitative data extraction and analysis, and data were grouped into various types of graft materials and techniques, all of which were intended to answer the PICO question and the study objectives (Tables 3, 4, Fig. 1). Sockets without any graft material A total of 22 of 32 RCTs reported on the flapless extraction of teeth with no graft material being placed into the socket. A total of 397 extraction sockets in 17 studies10,12-14,16-24,26-29 reported histologic outcomes and/ or changes in the buccolingual dimension and buccal wall height at reentry at or beyond 12 weeks. The mean loss of the buccolingual width at the crest level was 2.79 mm (9 studies),12,16,17,18,19,21,26,27,29 and the mean loss was 1.74 mm (10 studies)10,12,13,17,18,21,22,24,26,27 in the buccal wall height from the ridge crest. Similarly, for a 12- week THE JOURNAL OF PROSTHETIC DENTISTRY

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Table 3. Qualitative analysis of 32 randomized controlled clinical trials Study

Year

Nahles

10

Specified Reason for Tooth Extraction

Age (y), Mean (Range)

Sex Distribution

Method of Measurement for Dimensional Changes

Extraction Site

2013

NR

54.5 (30-73)

18 M, 15 F

Various teeth in both jaws

NR

Aimetti12

2009

Root or crown fractures, nonrestorable caries, residual roots

51.2 (36-68)

18 M, 22 F

Anterior maxilla

Direct measurements using a template and Williams periodontal probe

Crespi13

2009

NR

51.3 (28-72)

8 M, 7 F

1 on each side of jaw, in molar or premolar regions (n=30), and 1 additional random tooth, used for control (n=15)

Radiographic bone measurement

Heberer14

2011

NR

49.9 (36-67)

15 M, 10 F

Maxillary and mandibular molars

NR

2010

NR

NR (15-87)

63 M, 62 F

NR

Cast-based measurements

2012

Tooth fracture, endodontic reasons, severely decayed, nonrestorable teeth, periodontal reasons

40.5 (20-63)

20 M, 39 F

Premolars and molars

Direct measurements using periodontal probe

2012

Tooth fracture, periodontal involvement, endodontic treatment failures, advanced caries lesions

47.2 (24-71)

24 M, 17 F

Premolars and molars

Cast-based measurements using UNC probe

2011

NR

53.7 (32-70)

8 M, 7 F

3 teeth (1 molar or premolar from each side and 1 random as control)

NR

2011

NR

53.7 (32-70)

6 M, 9 F

2013

Root fractures, advanced caries lesions, endodontic failures with intact buccal plate

46.2 (24-72)

13 F

2013

NR

NR (28-58)

2010

NR

2013

Oghli

16

Barone17

Cardaropoli

18

Crespi19

Crespi20

Premolar and molar

NR

Anterior maxilla up to second premolar

Casts scanned and superimposed

6 M, 9 F

Symmetrical maxillary or mandibular contralateral premolars

Direct measurements via customized acrylic template and k file

47.5 (28-70)

7 M, 6 F

Anterior teeth

Direct measurements using periodontal probe

Caries, periodontitis, endodontic complications (eg, root fracture), orthodontic, prosthetic

NR (48-65)

18 M 23 F

1 maxillary or mandibular asymptomatic anterior tooth or premolar

Direct measurements using periodontal probe

2013

NR

NR (25-54)

NR

Maxillary and mandibular anteriors and premolars

NR

Schneider29

2014

Caries, endodontic complications, root fracture, periodontitis, orthodontic, prosthetic

NR

NR

Maxillary and mandibular incisors, canines, premolars

Cast digitized and assessed for volumetric changes

Brownfield32

2012

Compromised or nonrestorable nonmolar teeth with adjacent teeth present

NR (25-69)

5 M, 12 F

Nonmolar teeth

Direct measurement, radiographic guide, and cone beam computerized tomography

Toloue33

2012

NR

NR (18-75 M; 18-50 F)

11 M, 10 F

Single-rooted nonmolar tooth

Direct measurements using UNC-15 probe and caliper

22

Thalmair

Festa

24

Pelegrine Jung

26

27

Lindhe

Fotek

28

34

2009

NR

NR (29-77)

5 M, 13 F

Central incisor, canine, premolar

Direct measurements using acrylic template, UNC probe, caliper

35

2012

NR

56.7 (20-78)

13 M, 20 F

Single-rooted nonmolar tooth

Direct measurements using UNC-15 probe and caliper

Eskow36

2013

Various reasons, but all teeth had <50% buccal bone loss

54 (27-79)

18 M, 17 F

Nonmolar teeth

Direct measurements using vacuumformed matrix and caliper

Huh37

2011

Various reasons, but all teeth had <50% vertical bone loss

NR (35-65)

42 M, 30 F

Premolars or molars

NR

2012

Nonrestorable teeth

53 (19-75)

8 M, 8 F

Maxillary anterior teeth maxillary and mandibular premolars

Direct measurements using acrylic template and implant spacer probe (20 mm)

2013

Caries or failure of endodontic treatment

53 (45-67)

3 M, 7 F

Maxillary second premolars

Direct measurements using periodontal probe

2008

NR

48 (25-69) test, 49 (36-76) control

13 M, 17 F

Maxillary premolars

Direct measurements using UNC probe calipers

2014

Compromised teeth with buccal bone destruction requiring extraction due to endodontic infection, vertical root fracture, facially positioned in arch

NR (33-79)

12 M, 8 F

Various teeth in maxillary and mandibular arches

Cone beam computerized tomograph-based measurements

Wood

Kutkut

38

Shakibaie-M Neiva

40

Coomes41

39

(continued on next page)

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Table 3. Qualitative analysis of 32 randomized controlled clinical trials (continued) Age (y), Mean (Range)

Sex Distribution

NR

54 (43-67)

10 F

NR

Direct measurements using acrylic template and probe

2013

NR

NR

NR

NR

NR (study only reported histologic outcomes)

2012

Fractured teeth, nonvital teeth without possibility of endodontic treatment or restoration, chronic periodontitis, endodontic treatment failure, periodontal disease; extraction sockets with 4 intact walls and occlusion suitable for planned prosthodontic treatment

NR (20-55)

8 M, 12 F

Canine, premolars, molars

Direct measurements using calipers and probe

Alkan46

2013

NR

NR (40-58)

4 M, 6 F

Symmetrical single-rooted maxillary teeth to be extracted

NR

Barone47

2014

NR

32.7 (18-47)

26 M, 38 F

Premolars and molars

Direct measurements using template and calibrated probe

2012

Fractured teeth, nonrestorable teeth, periodontal disease, endodontic treatment failure with up to 50% buccal wall loss

56.1 (29-76)

15 M, 15 F

Molars

Direct measurements using calipers and UNC probe

2013

Compromised teeth for periodontal, traumatic, or caries reasons showing bone defect 3-5 mm at buccal wall and without soft tissue recession

NR (30-60)

7 M, 13 F

Maxillary and mandibular incisors, canines, premolars

Direct measurements using acrylic template and calipers

Study

Year

Checchi42

2011

43

Mahesh Brkovic

Hoang

44

48

Calasans-Maia

50

Specified Reason for Tooth Extraction

Method of Measurement for Dimensional Changes

Extraction Site

NR, not reported; UNC, University of North Carolina.

Table 4. Overview of 32 randomized controlled clinical trials based on type of socket grafting material Characteristic

Variable

No Graft Material

Allograft

Alloplast

Xenograft

Other

22

6

14

21

10

19

5

14

20

7

10, 12-24, 26-2929

32, 33, 34, 35, 36

12, 13, 22, 27, 29, 33, 37-44

10, 18-20, 22-24, 27-29, 39, 42, 45-50

16, 26, 37-39, 41, 45

397

117

224

427

189

Studies

10, 12-24, 26-29

32, 33, 34, 35, 36

12, 13, 22, 27, 29, 33, 37-44

14, 15, 17-20, 22-25, 27-29, 39, 42, 45, 47, 49, 50

16, 26, 37-39, 41, 45

3

Total no. of studies Studies reporting histologic and/or dimension changes outcomes at or beyond 12 weeks

No. of studies

Studies Extraction sockets studied with a reentry period of minimum of 12 weeks

No. of participants in a geographic region

No. of participants in a specific setting

Time for reentry at implant placement beyond 12 weeks

No. of sockets

Europe

17

0

8*

17*

United States

0

6

4

1

3

South America

2

-

-

2

1

Asia

3

-

2*

3*

3

University

17

6

10*

16*

8

Private clinic

1

0

2*

2*

1

Independent center

4

0

2

5

1

Average time (wk)

17.2

16.5

19.5

18.1

NA

Reference

10, 12-14, 16-24, 26-29

32, 33, 34, 35, 36

12, 13, 22, 27, 29, 33, 37-44

14, 15, 17-20, 22-24, 25, 27-29, 39, 42, 45, 47, 49, 50

NA, not amenable to calculation due to biomaterial heterogeneity. *Multicenter study.

or longer reentry time from implant placement, the cores obtained for the evaluation of histologic outcomes showed a mean value of 41.07% for vital bone Jambhekar et al

formation (8 studies),12-14,18-20,26,28 0% for remnant graft material, and 52.53% for the connective tissue (6 studies).13,14,18-20,28 THE JOURNAL OF PROSTHETIC DENTISTRY

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18 16

None Allograft Alloplast Xenograft Other

No. of Studies

14 12 10 8 6 4 2 0 Europe

USA

South America

Asia

Geographic Region Figure 1. Distribution of region of studies and different materials used for socket grafting in identified RCTs.

Allograft A total of 6 of 32 studies reported flapless extraction and allografts placed into the sockets. All studies on allograft were conducted in the United States because this material is not readily available in Europe and in many other regions of the world. A total of 117 extraction sockets in 5 studies32-36 reported histologic outcomes and/or changes in the buccolingual dimension and buccal wall height at reentry at or beyond 12 weeks. For the reentry point at implant placement 12 weeks, the mean loss of buccolingual width at the crest level was 1.63 mm (4 studies),32-35 and the mean loss of buccal wall height from the ridge crest was 0.58 mm (5 studies).32-36 Similarly, histologic outcomes at the reentry point for implant placement at 12 weeks, the mean values of vital bone formed was 29.93% (5 studies),32-36 remnant graft material was 21.75% (5 studies),32-36 and connective tissue was 51.03% (5 studies).32-36 Cortical mineralized freezedried bone allograft (FDBA) (4 studies)33-36 was more commonly used than cortical demineralized freeze-dried bone allograft (DFDBA) (1 study).35 Only 1 study used a combination of FDBA and DFDBA and reported 41.5% of vital bone and 3.45% of remnant graft.36 DFDBA resulted in vital bone of 38.42% and remnant graft of 8.8%,35 while FDBA resulted in vital bone of 23.54% and remnant graft of 26.94%.33-36 Among the allografts for flapless extraction and socket grafting, the mean loss of ridge dimensions was least for the combination of FDBA and DFDBA (1 mm), followed by FDBA only (1.65 mm) and DFDBA only (2.18 mm). The loss of buccal wall height was least for DFDBA (0.37 mm), followed by FDBA (0.64 mm) and DFDBA+FDBA (0.8 mm).32-36 Alloplast A total of 14 of 32 RCTs reported on flapless extraction and alloplast graft material placed into the socket. Almost all regions of the world reported on studies with alloplast THE JOURNAL OF PROSTHETIC DENTISTRY

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graft materials. A total of 224 extraction sockets in 14 studies12,13,22,27,29,33,37-44 reported histologic outcomes and/or changes in the buccolingual dimension and buccal wall height at reentry at or beyond 12 weeks. For a 12week reentry point at implant placement, the mean loss of the buccolingual width at the crest level was 2.13 mm (10 studies),12,27,29,33,38,37,39,40,41,44 and the loss of buccal wall height was 0.77 mm (8 studies).13,14,27,33,37,38,40,44 Similarly, histologic outcomes at the reentry point for implant placement at 12 weeks were as follows: the mean value of vital bone formed was 45.53% (9 studies),12,13,22,33,38,40,42-44 remnant graft material was 13.67% (7 studies),13,22,33,40,42-44 and connective tissue was 38.39% (6 studies).13,22,33,40,42,44 The most commonly used alloplast was medical-grade calcium sulfate (5 studies),12,13,33,38,40 followed by hydroxyapatite (HA),13,22,37,39,42 b-tricalcium phosphate (b-TCP) (4 studies),3,37,29,44 calcium phosphosilicate putty (1 study),43 and P15 putty (1 study).39 Xenograft A total of 21 of 32 RCTs reported on flapless extraction and xenografts placed into the socket. The majority of these studies were conducted in European countries, where allograft is not available. A total of 427 extraction sockets in 20 studies14,15,17-20,22-25,27-29,39,43,45-47,49,50 reported histologic outcomes and/or changes in the buccolingual dimension and buccal wall height at reentry at or beyond 12 weeks. For reentry point at implant placement 12 weeks, the mean loss of buccolingual width at the crest level was 1.3 mm (9 studies),17,18,24,27,29,39,46,49,50 and the mean loss of buccal wall height from the ridge crest was 0.57 mm (9 studies).17,18,22,24,27,39,46,49 Similarly, histologic outcomes at the reentry point for implant placement at 12 weeks were as follows: the mean value of vital bone formed was 35.72% (10 studies),14,18,28,39,43,45-47,49,50 remnant graft material was 19.30% (10 studies),14,18,19,20,28,43,47,49,50 and connective tissue was 44.42% (9 studies).14,18-20,28,47,49,50 Among the xenografts, the combination of bovine and porcine bone (8 studies)10,14,18,23,25,27-29 was most commonly used, followed by porcine bone alone (6 studies)17,19,22,24,46,47 and bovine bone alone (6 studies).15,39,43,45,49,50 Other materials This category of socket grafting material included new and emerging materials that did not belong to any of the 3 previously mentioned categories. These materials included growth factors, human platelet-derived materials, platelet rich fibrin, stem cells, cell therapy materials like Escherichia coli-derived recombinant human bone morphogenetic protein-2 (ErhBMP-2), enamel matrix derivatives (EMD), recombinant human bone morphogenetic protein-2/acellular collagen sponge (rhBMP-2/ Jambhekar et al

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ACS), and bone marrow. A total of 10 of 32 RCTs reported on flapless extraction and these types of grafting material placed into the socket. A total of 189 extraction sockets in 7 studies16,26,37-39,41,45 reported histologic outcomes and/or changes in the buccolingual dimension and buccal wall height at reentry at or beyond 12 weeks. The heterogeneity of biomaterials in this group and manner of reporting did not make the data amenable to calculations. A total of 56 sites in 2 studies38,41 reported the use of rhBMPs with a mean time for reentry of 16 weeks at implant placement. There was a loss of 1.86 mm in the buccolingual width at the ridge crest. A loss of 0.059 mm in the buccal wall height was reported by 1 study.38 None of the studies reported on the histologic outcome at reentry. Coomes et al41 reported better predictability of buccal wall regeneration with rhBMP-2/ACS (gain of 4.75 mm) versus control (gain of 1.85 mm). For EMD, Alkan et al45 reported a mean vital bone of 34.57% (10 sites). On the basis of 15 sites and a 24-week reentry interval, Pelegrine et al26 reported a mean loss of buccolingual width of 1.14 mm and buccal wall height of 0.62 mm and mean vital bone of 45.47% when 5 mL of collected bone marrow from iliac crest was used for socket grafting. DISCUSSION The aim of this systematic review was to determine if a specific type of socket grafting material can provide better clinical and histologic outcomes in patients with flapless extraction of teeth after a minimum healing period of 12 weeks. Though extractions of teeth have been performed since ancient times, the knowledge related to the advantages of flapless extractions and the preservation of buccal bone and importance of socket grafting dates back only a few decades. This systematic review searched only the data from clinical RCTs, as they are considered the most progressive level of scientific evidence.78 A 12-week healing period was selected as a cutoff point for inclusion because it has been demonstrated that the typical healing time for a socket is 12 weeks.8,61 Additionally, a minimum socket healing period of 12 weeks before reentry for implant placement has been used empirically by clinicians for decades. Various authors have demonstrated that after a 12-week healing period, bone formation is adequate for implant placement.10,40 The 12-week time point also allows adequate potential for the replacement of graft materials by new relatively mature well-formed bone (86.5%) because the active zone of bone formation in the extraction socket begins shifting to the coronal region after 12 weeks.40 Finally, this systematic review was restricted to studies with flapless extractions of teeth, as flapless extraction is a simple, conservative, and biologically friendly approach to extractions. It preserves the Jambhekar et al

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blood supply to the buccal bone, preserves soft tissues. and decreases surgical morbidity for the patient. The predetermined inclusion criteria for this systematic review were broad to permit the inclusion of as many articles as possible. Scrutiny of all articles was performed by multiple investigators to decrease any errors during the review process and minimize the selection bias of the articles included. Disagreement was resolved by discussion, and, when in doubt, the article was carried forward to the subsequent stage. Articles determined for exclusion in the full-text analysis stage were analyzed in depth before finalizing their exclusion with various predetermined criteria. Because of the heterogeneity of data from the various RCTs studied, data from each arm of a parallel group trial for all RCTs were isolated, collated, and analyzed. This systematic review provided data favoring the socket grafting procedure to limit the loss of buccolingual width and buccal wall height against extraction and no grafting. The use of xenografts resulted in the least loss of buccolingual width (1.3 mm), followed by allografts (1.63 mm). These dimensions are interestingly similar to a recent study by Tarnow et al79 on immediate implant placement. These authors demonstrated that flapless maxillary anterior extraction sockets with immediate implant placement and allograft material in the buccal gap, followed by placement of a contoured healing abutment or a provisional restoration, resulted in minimal loss of buccolingual width (average loss of 1mm).80 An argument can be made against measuring changes in buccolingual width at the crest level because of the collapse of the soft tissues and rounding off the crest during the remodeling of the buccal wall of the socket. The authors attempted to identify studies that reported changes in the buccolingual width at 3 mm below the crest after a tooth extraction. However, only 3 studies reported these data. Coomes et al41 reported a mean change in buccolingual dimensions of 3.4 mm for collagen sponge and 2.07 mm for rhBMP-2/ACS at 3 mm below the crest. Similarly Kim et al15 reported an average rate of resorption of 20.74% for no socket grafting and 14.26% for xenograft. Huh et al37 reported a change of 0.006 mm at 25% extraction socket length (ESL), 0.542 mm at 50% ESL, and 1.405 mm at 75% ESL, all with bTCP/HA material. The same authors reported 1.279 mm at 25% ESL, 1.239 mm at 50% ESL, and 1.863 mm at 75% ESL with ErhBMP-2+b-TCP/HA material. Xenografts and allografts resulted in similar loss of buccal wall height at 0.57 mm and 0.58 mm, respectively. Alloplasts had a slightly higher loss of buccal wall height at 0.77 mm, and sites with no grafting showed a loss of 1.74 mm. These numbers are important because the values reported in the previous 13 systematic reviews are much higher. The mean loss of buccolingual width from previous systematic reviews is 3.8 mm. This is because all THE JOURNAL OF PROSTHETIC DENTISTRY

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Table 5. Mean dimensional change at 12 weeks of reentry for socket grafting procedure using different biomaterials No Graft Material Change (mm)

Loss

Allograft Change (mm)

Studies

Alloplast Change (mm)

Studies

Xenograft Change (mm)

Studies

Studies

Other

Loss of buccolingual width at crestal level

2.79

12, 16, 17, 19, 18, 21, 26, 27, 29 (9 studies)

1.63

32, 33, 35, 36 (4 studies)

2.13

12, 27, 29, 38, 33, 37, 39, 40, 41, 44 (10 studies)

1.3

14, 16, 17, 18, 24, 27, NA 46, 49, 50 (9 studies)

Loss of buccal wall height from ridge crest

1.74

10, 12, 13, 17, 18, 21, 22, 24, 26, 27 (10 studies)

0.58

32, 33, 34, 35, 36 (5 studies)

0.77

12, 13, 27, 33, 37, 38, 40, 44 (8 studies)

0.57

17, 18, 23, 24, 27, 46, NA 48, 49 (8 studies)

Mean Dimensional Change (mm)

3 Loss of buccolingual width at the crestal level(mm) Loss of buccal wall height from the ridge crest(mm)

2.5

2

1.5

1

0.5

Mean Histological Outcome (mm)

NA, not amenable to calculation due to biomaterial heterogeneity.

60%

Vital bone

CT tissue

Remnant graft

50% 40% 30% 20% 10% 0% No graft material

Allograft

Alloplast

Xenograft

0 No graft material

Allograft

Alloplast

Xenograft

Method of Socket Grafting

Method of Socket Grafting

Figure 3. Mean histologic outcomes (in percentage) at reentry at or beyond 12 weeks.

Figure 2. Mean dimensional change (in mm) on reentry at or beyond 12 weeks.

previous systematic reviews have combined data for socket grafting performed with and without flap surgery after tooth extractions (Table 5, Fig. 2). The authors contend that elevating a surgical flap for tooth extraction can compromise blood supply and result in the loss of buccal bone height and width. The ability to limit dimensional changes of the alveolar ridge depends on the rate of resorption of a given grafting material and its ability to encourage bone formation.81 Both xenografts and allografts products can be categorized as osteoconductive materials. Xenografts are usually obtained from an organic bovine/porcine/equine bone that is chemically treated to remove its organic components and is sterilized to be used as a biomaterial without causing an immune response.10,18-20,22-24,27-29,39,42,45-50 Bone allografts are obtained from cadavers, usually available through tissue banks that process and store the allografts under sterile conditions. This review identified significantly more studies with xenografts than with allografts. The authors believe that this is largely due to the lack of availability and popularity of allografts outside the United States because of cultural, social, religious, or political beliefs about using cadaver bone. FDBA was the most commonly used form of allograft identified in this systematic review.33-36 It may regenerate bone or participate in new bone formation by osteoinduction or osteoconduction. The freezing and freeze-drying process essentially lowers the THE JOURNAL OF PROSTHETIC DENTISTRY

antigenicity.57,58,61,82 DFDBA has been reported to include bone morphogenic proteins (BMP), which are mitogens proven to exert osteoinductive property.34,61 However, the variability of BMPs in DFDBA varies with donor age and heterogeneity among different tissue banks. This probably accounts for the higher values reported for the amount of vital bone (29.93%) at reentry for implant placement.34 These outcomes were similar to previous reports.61,64,79 In this systematic review, alloplast was reported to have the highest percentage of vital bone formation (45.53%) and the least remnant graft material (13.67%) (Table 4, Fig. 3). This could be attributed to osteoconductive potential and the rapid rate of resorption of the biomaterial. The rate of resorption has been reported to be highest for calcium sulfate, followed by bioactive glass and then HA. This observation was similar to a previous report by Chan et al.61 Although studies by Coomes et al41 and Rasperini et al77 were excluded from the final analysis, these 2 articles are remarkable. Rasperini et al,77 in a parallel-arm multicenter RCT on socket grafting, reported that 7 of 9 sites in the test group (Bio-Oss collagen) maintained the buccal wall compared to 4 of 9 sites in the control group (no graft material) and reduced the need for sinus augmentation (Table 6). Coomes et al41 in an RCT reported that when rhBMP-2/ACS was used for socket grafting, 5 of 18 sites required secondary grafting, 1 of 18 needed implant site development, and 12 of 18 sites needed no augmentation at implant placement, while in Jambhekar et al

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Table 6. Mean histologic outcomes at or beyond 12 weeks for socket grafting procedure using different biomaterials No Graft Material Biomaterial

Outcome (%)

Vital bone Remnant graft Connective tissue

Studies

Allograft Outcome (%)

Alloplast

Studies

Outcome (%)

Studies

Xenograft Outcome (%)

Studies

Other

41.07

12, 13, 14, 18-20, 26, 28 (8 studies)

29.93

32, 33, 34, 35, 36 (5 studies)

45.53

12, 13, 33, 38, 22, 40, 42, 43, 44 (9 studies)

35.72

14, 18, 28, 39, 42, NA 45-47, 49, 50 (10 studies)

0

10, 14, 26, 28 (5 studies)

21.75

32, 33, 34, 35, 36 (5 studies)

13.67

13, 22, 33, 40, 42-44 (7 studies)

19.30

14, 18, 19, 20, 28, 42, 47, 49, 50 (9 studies)

NA

52.53

13, 14, 18-20, 28 (6 studies)

51.03

32, 33, 34, 35, 36 (5 studies)

38.39

13, 22, 33, 40, 42, 44 (6 studies)

44.42

14, 18, 19, 20, 28, 47, 49, 50 (8 studies)

NA

NA, not amenable to calculation due to biomaterial heterogeneity.

Table 7. Studies reporting on use of barrier membranes and autogenous grafts Characteristic No barrier membrane

Collagen-based barrier membrane Autogenous gingival grafts

No Graft Material

Allograft

Alloplast

Xenograft

10-17, 21, 23-26, 29, 30 (16 studies)

0

12, 13, 27, 29, 33, 37, 39, 40, 41, 42, 44 (12 studies)

10, 14, 15, 19, 22, 25, 50 (7 studies)

NA

Other

18, 19, 27 (3 studies)

32, 33, 34, 35, 36 (5 studies)

13, 22, 38, 44 (4 studies)

17, 18, 19, 20, 24, 27, 28, 29, 39, 46 (10 studies)

NA

21-23 (3 studies)

0

0

23, 27, 45, 46 (4 studies)

NA

NA, not amenable to calculation due to biomaterial heterogeneity.

sites with collagen sponge alone, 7 of 16 sites required secondary grafting, 6 of 16 needed implant site development, and 3 of 16 sites needed no augmentation at implant placement. In this systematic review, data for some emerging materials/substances such as bone morphogenic proteins (BMPs) and platelet derivatives (platelet rich plasma and platelet rich-fibrin) were not amenable to data analysis because of biomaterial heterogeneity and limited samples. Although few studies have reported the use of BMPs, their clinical usefulness has been limited, as researchers continue to identify adequate carriers to immobilize BMPs for a sufficient duration, determining optimal dosages, and high costs. Further use of these materials for socket grafting procedures does not seem to offer any significant advantages over other available materials that are less expensive. There is inconclusive evidence for the use of collagenbased barrier membranes and/or autogenous gingival grafts to protect the socket orifice after the use of a graft material. The authors recommend using collagen-based barrier membranes to contain the graft material until the epithelial closure of the socket opening and to protect the graft material from epithelial infiltration during the healing of the socket55,56 (Table 7). A few studies have reported the use of autogenous gingival grafts to cover the graft materials in extraction sockets to increase keratinized tissue and enhance the esthetic outcomes.16,23,27 Jung et al27 reported on the application of a slowly resorbing biomaterial covered with either autogenous soft tissue punch or a collagen matrix revealed the least contraction of the extraction socket over 6 months. However, no evidence of any beneficial effect was observed on the soft tissue graft for the buccolingual Jambhekar et al

width or buccal wall height dimensions. Additional disadvantages associated with the use of a palatal soft tissue graft are the need for a secondary site for obtaining tissue grafts, necrosis of the palatal soft tissue grafts, and subsequent clinical fibrous healing.83 From a practical and patient-centered standpoint, when the flapless approach for tooth extraction and alveolar ridge preservation technique is used to simplify a clinical procedure and reduce surgical morbidity for the patient, an additional procedure to obtain the autogenous soft tissue graft from the palate, may not justify the purpose. Though this systematic review satisfied most of the checklist of PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines, there are some limitations to this review. First, some aspects of the results section were not applicable or amenable to the PRISMA checklist, and hence authors did not report this systematic review based on the PRISMA guidelines. Second, the data of outcomes from multiple sites treated using different graft materials from studies that did not lend themselves for data extraction are unaccounted for. This is a result of the manner of data reporting in those studies where qualitative outcomes were grouped together or the outcomes were not reported at all. Although the total number of participants enrolled onto the selected studies can be considered sufficient for the assessment of effect size differences among groups for the main outcomes of interest, the reported analysis results should be interpreted by the clinician with caution. No attempt was made to segregate the studies on the basis of the anatomic socket location because these data were not well reported in the included RCTs. This is a significant limitation of this systematic review. The evaluation techniques used in all the THE JOURNAL OF PROSTHETIC DENTISTRY

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included studies did not necessarily provide critical information on availability of bone for implant placement planning. Thus, developing and applying research protocols that would allow a precise and objective quantification of the total 3-dimensional changes after tooth extraction in future studies are needed.64,84 Data reporting in future RCTs may benefit if they are standardized through the use of CONSORT (Consolidated Standards of Reporting Trials) statement guidelines. The effect of the vital bone formed, residual graft, and connective tissue on long-term implant success needs to be investigated. To the authors’ knowledge, this is the first systematic review analyzing data exclusively for flapless extractions and comparing different biomaterials with clinical and histologic outcomes. New knowledge on loss of socket dimensions from this systematic review differs from all previous systematic reviews because previous reviews combined data for socket grafting performed with and without flap surgery after teeth extractions. CONCLUSIONS On the basis of the findings of this systematic review of RCTs, the following conclusions were drawn: 1. After flapless extraction of teeth, using a minimum healing period of 12 weeks as a temporal measure, xenografts and allografts resulted in the least loss of socket dimensions compared to alloplasts or sockets with no grafting. In this systematic review, xenografts were the most documented material in RCTs for socket grafting. 2. Histologic outcomes after a minimum healing period of 12 weeks showed that sockets grafted with alloplasts had the maximum amount of vital bone and the least amount of remnant graft material and connective tissue. Histologic outcomes also indicate that a healing period greater than 12 weeks can provide favorable outcomes before implant placement. 3. A limited but emerging body of evidence is available for the predictable regeneration of deficient buccal bone using socket grafting materials, use of barrier membranes, or coverage of sockets with autogenous soft tissue grafts from the palate. 4. Little evidence is available for using innovative tissue regenerative and cell therapy approaches such as growth factors, human platelet-derived materials, platelet-rich fibrin, stem cells, cell therapy materials such as ErhBMP-2, EMD, rhBMP-2/ACS, and bone marrow. REFERENCES 1. Trombelli L, Farina R, Marzola A, Bozzi L, Liljenberg B, Lindhe J. Modeling and remodeling of human extraction sockets. J Clin Periodontol 2008;35: 630-9. 2. Sclar AG. Strategies for management of single-tooth extraction sites in aesthetic implant therapy. J Oral Maxillofac Surg 2004;62(9 Suppl 2):90-105.

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3. Schropp L, Wenzel A, Kostopoulos L, Karring T. Bone healing and soft tissue contour changes following single-tooth extraction: a clinical and radiographic 12-month prospective study. Int J Periodontics Restorative Dent 2003;23: 313-23. 4. Bartee BK. Extraction site reconstruction for alveolar ridge preservation. Part 1: rationale and materials selection. J Oral Implantol 2001;27:187-93. 5. Araújo MG, Lindhe J. Dimensional ridge alterations following tooth extraction. An experimental study in the dog. J Clin Periodontol 2005;32:212-8. 6. Araújo MG, Lindhe J. Ridge alterations following tooth extraction with and without flap elevation: an experimental study in the dog. Clin Oral Implants Res 2009;20:545-9. 7. Evian CI, Rosenberg ES, Coslet JG, Corn H. The osteogenic activity of bone removed from healing extraction sockets in humans. J Periodontol 1982;53: 81-5. 8. Amler MH. The time sequence of tissue regeneration in human extraction wounds. 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Beta-tricalcium phosphate/type I collagen cones with or without a barrier membrane in human extraction socket healing: clinical, histologic, histomorphometric, and immunohistochemical evaluation. Clin Oral Investig 2012;16:581-90. Alkan EA, Parlar A, Yildirim B, Sengüven B. Histological comparison of healing following tooth extraction with ridge preservation using enamel matrix derivatives versus Bio-Oss Collagen: a pilot study. Int J Oral Maxillofac Surg 2013;42:1522-8. Barone A, Toti P, Piattelli A, Iezzi G, Derchi G, Covani U. Extraction socket healing in humans after ridge preservation techniques: comparison between flapless and flapped procedures in a randomized clinical trial. J Periodontol 2014;85:14-23. Barone A, Borgia V, Covani U, Ricci M, Piattelli A, Iezzi G. Flap versus flapless procedure for ridge preservation in alveolar extraction sockets: a histological evaluation in a randomized clinical trial. Clin Oral Implants Res. In press. 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83. Sisti A, Canullo L, Mottola MP, Covani U, Barone A, Botticelli D. Clinical evaluation of a ridge augmentation procedure for the severely resorbed alveolar socket: multicenter randomized controlled trial, preliminary results. Clin Oral Impl Res 2012;23:526-35. 84. 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;92:195S-201S. Corresponding author: Dr Avinash S. Bidra University of Connecticut Health Center 263 Farmington Avenue, L6078 Farmington, CT 06030 Email: [email protected] Copyright © 2015 by the Editorial Council for The Journal of Prosthetic Dentistry.

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