DR.

ZUHAIR S NATTO (Orcid ID : 0000-0003-2723-0255)

Accepted Article
Received Date : 20-Oct-2016
Revised Date : 08-Feb-2017
Accepted Date : 12-Mar-2017
Article type : Randomized Clinical Trial

Efficacy of Collagen Matrix Seal and Collagen Sponge on Ridge Preservation in

Combination with Bone Allograft: A Randomized Controlled Clinical Trial

Running Title: ARP with collagen matrix seal or collagen sponge and FDBA

Zuhair S. Natto1-2, Andreas Parashis2, Bjorn Steffensen2, Rumpa Ganguly3, Matthew D.

Finkelman4&Y. Natalie Jeong2.

1
Department of Dental Public Health, School of Dentistry, King Abdulaziz University,

Jeddah, Saudi Arabia;

2
Department of Periodontology, School of Dental Medicine, Tufts University, Boston, MA,

USA;
3
Department of Diagnosis and Health Promotion, School of Dental Medicine, Tufts

University, Boston, MA, USA;

4
Department of Public Health, School of Dental Medicine, Tufts University, Boston, MA,

USA.

Correspondence to: Dr. Zuhair Natto, Department of Dental Public Health, School of

Dentistry, King Abdulaziz University, P.O.BOX 40311, Jeddah 21499 Saudi Arabia.

E-mail: znatto@kau.edu.sa
This article has been accepted for publication and undergone full peer review but has not
been through the copyediting, typesetting, pagination and proofreading process, which may
lead to differences between this version and the Version of Record. Please cite this article as
doi: 10.1111/jcpe.12722
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 Key words: Collagen matrix; extracellular matrix; collagen sponge; alveolar ridge
Accepted Article preservation; extraction socket; bone allograft.

Conflict of Interest: The authors have stated explicitly that there are no conflicts of interest

in connection with this article

Source of Funding: This research has been funded through the Department of

Periodontology, the Division of Oral and Maxillofacial Radiology, the Advance Graduate

Education Committee and the Implant Committee of Tufts University School of Dental

Medicine.

ABSTRACT

Aim: To test whether the use of collagen matrix seal (CMS) results in similar hard and soft

tissue remodeling to that with collagen sponge (CS) used as barriers 4 months following

alveolar ridge preservation (ARP), in combination with freeze-dried bone allograft (FDBA).

Materials and methods: Twenty-eight patients were randomly assigned to the two groups.

Clinical and radiographic measurements were recorded with the same stent at baseline and 4

months for standardization. The flapless technique following atraumatic extraction was used

for the two types of barriers.

Results: All patients completed the study, 14 in the CMS group and 14 in the CS group.

Reduction in coronal ridge width (1.21 mm-14.91%CMS and 1.47 mm-20.40% CS)and

vertical buccal bone resorption (0.30 mm CMS and 0.79 mm CS) were not significantly

different. A slight increase in buccal gingival thickness at the coronal part was observed in

both groups (0.9 mm CMS and 0.5 mm CS).

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 Conclusions: CMS and CS, when combined with FDBA, significantly minimized ridge
Accepted Article resorption in all dimensions and maintained buccal soft tissue thickness in sockets with a

buccal plate loss of <2 mm in comparison to previously reported findings recorded after tooth

extraction without ARP.

ClinicalTrials.gov (NCT02697890).

CLINICAL RELEVANCE

Scientific rationale for the study

One of the serious consequences of tooth extraction is the ridge resorption that follows

because resorption may create aesthetic problems and compromise future implant placement.

Although ARP procedures have several benefits, they also have several risks, complications

and limitations. Therefore, any modifications of the technique that could simplify the

procedure and reduce complications would be advantageous.

Principal findings

CMS and CS, when combined with FDBA, significantly minimized ridge resorption in all

dimensions and maintained buccal soft tissue thickness in sockets with a buccal plate loss of

<2 mm in comparison to previously reported findings recorded after tooth extraction without

ARP.

Practical implications

Within the limitation of this study, use of CMS or CS in combination with FDBA and a

flapless approach is a valuable alternative for ARP in sockets with a buccal plate loss of <2

mm to simplify the procedure.

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 INTRODUCTION
Accepted Article One of the serious consequences of tooth extraction is resorption of the alveolus that may

create esthetic problems and compromise future implant placement. In the first 6 months

following tooth extraction, 11–22% of the alveolar bone height and 29–63% of the alveolar

bone width maybe lost(Esposito et al., 2009, Ten Heggeler et al., 2011, Hammerle et al.,

2012, Wang and Lang, 2012).Therefore, it is important to preserve as much bone as possible

at the time of the extraction and to reduce subsequent alveolus bone resorption to prevent

performing additional procedures needed to regenerate sufficient bone for implant placement

and restorative procedures(Cardaropoli and Cardaropoli, 2008, Nevins et al., 2009, Weng et

al., 2011, Hammerle et al., 2012).

Ridge preservation procedures typically use a combination of a scaffold and a membrane.

Scaffolds most commonly used are autogenous bone grafts, allografts, xenografts, and

alloplasts (Iasella et al., 2003, Ten Heggeler et al., 2011, Heberer et al., 2011, Wood and

Mealey, 2012, Cook and Mealey, 2013).Resorbable or non-resorbable membranes with or

without primary closure are used to prevent epithelial and connective tissue in growth into the

regenerating site and to stabilize the wound. The benefits of alveolar ridge preservation

(ARP) should be weighed against risks of membrane infection, loss or fibrous encapsulation

of graft particles, a longer healing period prior to implant placement, additional cost, and

possible soft tissue dehiscences in the grafted sites compared with non-grafted sites(Wang

and Lang, 2012, Horvath et al., 2013). Therefore, any modifications of existing technique that

could reduce such risks and limitations would be advantageous.

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 Collagen sponge (CS) has been proposed as an alternative to avoid potential complications
Accepted Article from the use of membranes in ridge preservation procedures. In the extraction socket, CS

would protect and maintain the bone graft material in place. A clinical study that evaluated

the efficacy of the ARP technique using CS and a xenograft after tooth extraction concluded

that the combination prevents the horizontal resorption of the alveolar ridge, blocks the

infiltration of soft tissues, and has the advantage of enhancing bone fill(Kim et al., 2011).

However, the fast degradation of the CS raises questions about its effectiveness during ridge

preservation procedures.

A xenogeneic non-cross-linked extracellular collagen matrix (CM) membrane of porcine

origin (Mucograft®, Geistlich Pharma AG, Wolhusen, Switzerland) consisting of type I and

III collagen and specifically designed for soft tissue regeneration has become available into

clinical practice. It has a bilayer structure which promotes in growth, regeneration, cellular

and extracellular integration within the host tissue (Ghanaati et al., 2011). Histological

studies of the CM in a non-submerged or submerged environment with a coronally

repositioned flap have revealed complete integration with mature mucosal and submucosal

tissues and revascularization of the membrane after 3 months(Ghanaati et al., 2011, Jung et

al., 2011, Rocchietta et al., 2012, Schmitt et al., 2013). Clinically, this new collagen matrix

was associated with a sufficient width of newly formed keratinized gingiva on teeth and

implants and coverage of Miller class I and II recession defects (Sanz et al., 2009, McGuire

and Scheyer, 2010, Nevins et al., 2011, Lorenzo et al., 2012, Cardaropoli et al., 2012, Schmitt

et al., 2013, Schwarz et al., 2012, Jepsen et al., 2013).The structural characteristics of the CM

are designed to ensure that it maintains its barrier function for at least 30 days and therefore

can be used as a guided bone regeneration device(Ghanaati et al., 2011, Cioban et al., 2013,

Parashis et al., 2014, Parashis et al., 2016, Lindhe et al., 2014).

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Accepted Article In addition to the CM membrane, a xenogeneic non-cross-linked extracellular collagen matrix

seal (CMS) [Mucograft®, Geistlich Pharma AG, Wolhusen, Switzerland]also was introduced.

The sealis a small round modification of the CM and is designed to seal sockets with

preserved buccal walls following ridge preservation with bone grafts. The CMS is easy to

handle and does not require treatment or hydration prior to placement (Jung et al., 2013).

Two recent studies with small sample sizes showed that soft tissue profiles can be maintained

and hard tissue dimensional changes reduced following ridge preservation with xenogenic

bone graft using either a free gingival graft punch (6-8 mm in diameter) or a punch

modification of the CM with the same diameter (similar to the CMS) (Jung et al., 2013,

Schneider et al., 2014).

Initial evidence for the potential benefits of using the CMS in ridge preservation is available

only from two studies(Jung et al., 2013, Schneider et al., 2014),and for the CM membrane

from a case series(Parashis et al., 2014)and a recent clinical study(Parashis et al., 2016).

There is a lack of data comparing the CMS with other methods of ridge preservation. If

complications related to membrane exposure and extensive flap reflection and advancement

could be avoided, this would result in an easier procedure, less discomfort for the patient, a

better esthetic outcome, and improved soft tissue healing.

On these bases, the objective of the present study was to evaluate clinically and

radiographically the soft and hard tissue dimensional changes after ARP using either CMS or

CS in combination with FDBA following 4 months of healing.

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 MATERIALS AND METHODS
Accepted Article This study was a prospective, randomized, parallel arm, single center clinical trial of the

addition of CMS or CS to FDBA for ARP, according to the CONSORT statement

(http://www.consort-statement.org/).It was registered at ClinicalTrials.gov(NCT02697890),

approved by the Tufts Health Sciences Institutional Review Board (IRB #11360) and

conducted in accordance with the Helsinki Declaration of 1975 as revised in 2000.

Participants

Patients were recruited from Tufts University School of Dental Medicine (TUSDM) teaching

clinics from August to December2015.Informed consent was obtained by investigators

participating in the study (ZN, NJ).Patients with a single rooted tooth (excluding lower

incisors) that had a treatment plan of extraction and ARP were included in the study.

Reasons for extraction were caries, endodontic complication, root fracture, or trauma with no

evidence of acute infection such as severe swelling, suppuration, abscess, and/or spontaneous

bleeding. If extraction of multiple teeth was planned, only one tooth was included in the

study. Additional inclusion criteria required that participants: be at least 18 years old, smoke

fewer than 10 cigarettes per day, treated for periodontal disease, and show presence of buccal

plate at the extraction site as determined by a sectional cone-beam computed

tomography(CBCT) scan. If the patient qualified based on the CBCT scan (had a buccal plate

present), a second informed consent was obtained by the same investigators (ZN, NJ)for the

remainder of the study. Exclusion criteria included: lactating or pregnant female, medical

conditions that are contraindicated with periodontal surgery, refusal to treatment utilizing

porcine derived materials, and a history of severe psychiatric conditions.

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 Randomization-blinding-allocation concealment
Accepted Article On the day of surgery participants were randomized to the CMS (test) or the CS (control)

groups by one investigator (NJ)using a computer-generated randomization scheme. In

patients with more than 1 tooth that needed to be extracted fulfilling the inclusion criteria, a

second randomization scheme was created to select one of the qualifying teeth for the study.

The group was allocation concealed for each participant throughout the study to avoid bias.

Investigators were not informed of the assigned treatment until the day of the surgery.

The investigator who performed the surgeries and all clinical measurements (ZN) was not

blinded as to which treatment group the patient was assigned. All sectional CBCTs were de-

identified by an investigator not involved in the clinical treatment (RG).Thus, the investigator

(ZN) who performed the radiographic measurements was blinded.

Standardized clinical and radiographic measurements

Design and fabrication of individual stents for standardization of clinical and radiographic

measurements has been described in detail previously(Parashis et al., 2016).Briefly, stents

used for clinical measurements and the sectional CBCTs were fabricated from a 1.5 mm thick

plastic shell on the cast of the patient. Fourteen standardized holes were made in the stent for

reproducible clinical and radiographic measurements (Fig. 1). Three horizontal holes buccally

and 3 lingually corresponding to the teeth to be extracted at 4, 7 and 10mm apical to the CEJ

for horizontal clinical measurements of soft tissue changes and 1 vertical hole on the incisal

or the occlusal edge for vertical measurements. An additional 7 holes with diameters of<1mm

located adjacent to the reference holes were filled with gutta-percha points as landmarks for

measurements of hard tissue changes on the CBCTs.

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 Clinical parameters on the tooth to be extracted and the mesial and distal adjacent teeth
Accepted Article [probing pocket depth (PD), gingival recession (REC), and clinical attachment level

(CAL)]and width of keratinized tissue (WKT) were recorded with a periodontal probe (Hu-

Friedy, Chicago, IL, USA) Buccal gingival thickness (GT) was measured using the

prefabricated stent and its clinical reference points with the addition of endodontic files with

rubber stops(Fig. 1). All distances were measured two times to 0.5mm, and the mean of the

distances was recorded before extraction and 4 months after the ARP.

Sectional CBCT scans were taken with the stent for standardized radiographic measurements

using its radiographic reference points (Voxel size: 0.30 mm, kVp: 120, mAs: 18.66, field of

view [FOV]: 40 X 50 mm[1 jaw]) (Fig. 1). The following measurements were recorded

before extraction and 4 months after the ARP.

a) Width of alveolar ridge (WB)

b) Vertical height to the buccal (VR-BC) and palatal/lingual (VR-PC) alveolar bone

c) Thickness of the buccal (BPT) and palatal/lingual (PPT) alveolar plates(only at the first

sectional CBCT scan)

These distances were measured two times to 0.1mm, and the mean of the distances was

recorded.

Treatment procedures

After sulcular incisions without flap reflection, teeth were extracted atraumatically utilizing

periotomes and extraction forceps with care to preserve the buccal bone plate and the

surrounding soft tissues. Following debridement, FDBA(Mineross, Biohorizons IPH,

Birmingham, AZ, USA) was rehydrated with saline for 15 minutes and packed into the bony

envelope at least to the level of the palatal/lingual bone plate. Subsequently, the soft tissue

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 borders of the alveoli were de-epithelialized using a diamond bur on a high-speed hand piece
Accepted Article under copious irrigation with water. A CMS or a CS of type I bovine collagen (HeliPLUG,

1cm x 2 cm, Integra Life Sciences, USA)was then applied to cover the margin of the

extraction and secured with monofilament non-resorbable horizontal mattress and interrupted

sutures.(Fig. 2)

Postsurgical instructions

Patients were prescribed amoxicillin 500 mg (tid for 8 days) and chlorhexidine gluconate

0.12% (bid for 3 weeks).For postoperative care, participants were seen after 1, 2, and 4

weeks. Sutures were removed during the 2 week postoperative visits.

Sample Size/Power Calculations

The sample size was determined using the G*power program (version 3.1.9, Faul, F.,

Erdfelder, E., Lang, A.-G., & Buchner, A, Germany). Assuming an effect size of 1.31 based

on a clinically meaningful 10% expected difference in bone width between the two groups

and using the highest standard deviation reported of 7.6%(Kim et al., 2011, Jung et al., 2013,

Schneider et al., 2014, Parashis et al., 2016), a sample size of 22 patients (11 per group) was

adequate to obtain a Type I error rate of 5% and a power of 80%. To account for

approximately 20% potential dropout, 28 patients were recruited, 14 per group.

Statistical Analysis

For demographic information (age), means and ranges were determined. The treatment

procedure was tested as a predictor. Height of keratinized tissue, buccal gingival thickness,

width and height of bone, and clinical parameters on adjacent teeth were tested as outcomes.

For continuous measurements means and standard deviations were calculated and compared

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 via two-sample t-tests. For categorical variables, frequencies and percentages were calculated
Accepted Article and compared via chi-square test or Fisher’s exact test. Reliability of all measurements was

evaluated by intraclass correlation. Analysis of covariance (ANCOVA) was used to compare

the primary outcomes (bone width and bone height) between the two groups at 4 months,

with the baseline score as a covariate. A paired t-test was used to compare clinical parameters

on adjacent teeth within the same group. Multiple linear stepwise regression and proposed

(clinical relevance) models were used to predict the crestal bone width and gingival thickness

at 4 months. All p-values less than 0.05 were considered statistically significant. All analyses

were performed using SAS software (Version 9.3,SAS Institute Inc, Cary, NC, USA).

RESULTS

Thirty-three patients were screened for this study. After inclusion criteria were assessed, 5

patients were excluded, 4 due to absence of buccal bone and 1 for smoking more than 10

cigarettes per day. After randomization, 14 patients were assigned to each group, and one

extraction and ridge preservation procedure was performed for each patient. In all, 28 sites

were treated. All patients were able to complete the study. A flow diagram of participants

through the study is presented in Figure 3.All sites in the CMS and CS groups healed without

complications.

Demographic characteristics

Demographic characteristics were not different between the two groups. The overall mean

age was 55.4 years (range 25-80) and was similar in the CMS group (55.1, range 25-80) and

the CS group (55.6, range 30-74). Most participants were males (60.7%),and there were more

males in the CMS group (71.4%) than in the CS group (50.0%). However, the difference was

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 not statistically significant (p =0.245). Twenty participants (71.4%) were of White Non-
Accepted Article Hispanic origin. The sample also included Asian (10.7%), African-American (7.1%),Hispanic

(7.1%) and more than one ethnicity participants. Race distribution was not statistically

significantly different between groups(p = 0.473).Most of the extracted teeth were maxillary

premolars (12 teeth: 42.9%) followed by maxillary incisors (11 teeth: 39.3%) and mandibular

premolars (5 teeth: 17.9%).

Baseline measurements

All clinical and radiographic measurements were completed twice. The intraclass correlations

for these measurements were above 0.90.

Table 1 presents the clinical soft tissue and radiographic hard tissue measurements at

baseline. There were no statistically significant differences between groups in all variables

with the exception of VR-BC. The gingival thickness was less in the CMS group than the CS

group at all reference points. The bone width was less in the CMS group than in the CS group

at all reference points. BPT and PPT were comparable between CMS and CS groups at all

reference points. There was a significantly higher vertical bone distance buccally in the CS

group compared with the CMS group (9.62±2.07 (SD)mm vs 7.29±2.11(SD)mm) (p=0.04).

Changes in clinical and radiographic measurements

Table 2 shows the clinical changes of soft tissues after 4 months of healing. There was a

significant increase of GT within the CMS group at the 4mm reference point of 0.90±0.90

(SD) mm (p = 0.01) and only slight increases at the 7mm and 10mm of 0.47±1.16(SD) mm

(p=0.15) and 0.05±1.62 (SD) mm (p=0.92) respectively. There was a slight increase in GT in

the CS group at the 4mm reference point (0.59±1.28(SD) mm) and a slight decrease at the

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 7mm (0.23±1.42(SD) mm) and the 10mm (0.13±1.07(SD) mm). However, these changes
Accepted Article were not statistically significantly different. WKT decreased by an average of 0.08mm in

both groups. PD, REC and CAL at adjacent teeth increased in the CS group by 0.16±0.27

(SD) mm (p=0.04),0.20±0.42 (p=0.11) mm, and 0.34±0.44 (SD)mm (p=0.01) respectively,

and to a lesser extent in the CMS group by 0.06±0.59 (SD) mm (p=0.74), 0.02±0.11 (p=0.55)

mm, and 0.05±0.52 (SD) mm (p=0.75) respectively. Overall, differences between the two

groups were not statistically significant for all clinical soft tissue measurements variables.

Radiographic measurements recorded a significant decrease in bone width at the 4 mm and 7

mm reference points in both groups (p=0.01) [Table 3]. The average reduction of bone width

was higher in the CS group at 4mm and 7 mm compared with the CMS group

(20±25.10(SD)% vs 15±15.17(SD)% and 12±15.7(SD)% vs 10±11.63(SD)%, respectively).

However, those results were not statistically significantly different between groups. The

average vertical bone loss buccally was less (0.30±1.09 (SD) mm) in the CMS group

compared with the CS group [0.79±3.07(SD)]. The vertical loss on the palatal/lingual was

0.27±2.30(SD) mm and 0.49±2.59 (SD) mm with no significant differences between the

CMS and CS groups.

Associations between the gingival thickness and the bone width at four months with several

predictors

Table 4 shows the associations between the GT at the 4 mm reference point at4 months with

several variables. Data from both groups were combined because no statistically significant

differences were noted in any clinical or radiographic measurements at baseline between the

two groups. The stepwise model showed that only GT at the 4 mm reference point at baseline

was a significant predictor for GT at 4 mm at 4 months and could explain 50% of its

variability (p =0.001). When WKT at baseline and BPT at the 4 mm reference point at

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 baseline were included in the proposed model, the coefficient of determination improved to
Accepted Article 52%. A multiple linear regression model showed that only GT at the 4 mm reference point at

baseline was related to the change in coronal GT after extraction and ARP (p=0.002)

indicating that he greater the thickness of the crestal soft tissue at 4 mm at baseline, the

thicker was the gingival tissue at 4 months. Correlation of change in WB at the 4 mm

reference point was assessed with several predictors. However, a statistically significant

association was observed only with WB at the 7 mm reference point at baseline in the

stepwise model (p=0.006) indicating that the greater the bone width at 7mm at baseline, the

better was the preservation of crestal bone width at 4 months

DISCUSSION

The findings of this prospective randomized study indicate that ridge preservation using

either CMS or CS combined with bone allograft with a flapless approach minimized ridge

resorption in all dimensions in comparison to previously reported findings recorded after

tooth extraction without ARP.CMS, a small round modification of the CM8mm in diameter

recently introduced in clinical practice, was designed to seal sockets following bone grafting

with preserved buccal walls. To the best of our knowledge this is one of the first studies

evaluating the effect of CMS on ridge preservation.

A decrease in radiographic bone height and width in both groups was observed. There were

no significant differences in vertical and horizontal changes between the two groups.

Horizontal bone loss in the coronal part was less, but not significantly different, in the CMS

group (1.21 mm, 14.91%) compared to the CS group (1.47 mm, 20.40%). A decrease in bone

width at the 7 mm and 10 mm apical reference points of 0.90 mm and0.54 mm (10.22% and

5.94%) in the CMS group and 0.96mm and0.57 mm (11.74% and6.94%), in the CS group

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 was also observed. More vertical bone reduction occurred on the buccal aspect (0.30mm in
Accepted Article the CMS group and 0.79mm in the CS group) than on the palatal aspect (0.27mm in the CMS

group and 0.49 mm in the CS groups).

Bone loss recorded at the coronal part and on the buccal aspect of the ridge are within the

range of results reported in previous studies testing various ARP surgical techniques (e.g.,

flapped versus flapless and primary intention healing versus no primary closure) and

materials (e.g., occlusive membranes and/or bone grafts)(Lekovic et al., 1998, Artzi et al.,

2000, Iasella et al., 2003, Darby et al., 2008, Fickl et al., 2008b, Araujo and Lindhe, 2009b,

Barboza et al., 2010, Mardas et al., 2010, Engler-Hamm et al., 2011, Weng et al., 2011,

Brownfield and Weltman, 2012, Barone et al., 2013, Barone et al., 2014)]. These studies and

systematic reviews(Esposito et al., 2009, Ten Heggeler et al., 2011, Hammerle et al., 2012,

Wang and Lang, 2012, Vignoletti et al., 2012, Willenbacher et al., 2015)point to a significant

reduction, but not complete elimination, in vertical and horizontal bone resorption compared

to unassisted socket healing after ARP procedures. The present findings confirm that

complete preservation of the alveolar ridge dimensions after tooth extraction is unlikely to be

attainable even if ARP procedures are employed.

The hard tissue dimensional changes that we report in this study resemble changes reported in

recent studies of tooth extraction and ridge preservation by others that used either an

autogenous soft tissue (free gingival graft) punch (6-8 mm in diameter) or a punch

modification of the CM with the same diameter (similar to the CMS) to cover the bone graft

(Jung et al., 2013, Schneider et al., 2014).Those changes are also consistent with the results

observed in a recent study that performed ARP with a combination of FDBA and CM or an

extracellular collagen matrix as barriers (Parashis et al., 2016).

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 FDBA was used in this study based on the ability to function as an osteoconductive scaffold
Accepted Article for new bone formation (Piattelli et al., 1996), allowing osteoprogenitor cells from the host to

produce new bone while maintaining space in the site before graft resorption. (Wood and

Mealey, 2012). Recent literature has shown that FDBA was effective in ARP maintaining

bone dimensions following tooth extraction with a mean 25% of new vital bone formation,

25% of residual graft and 50% of total bone area following 3 and 6 months of healing (Wood

and Mealey, 2012, Borg and Mealey, 2015).

As of today, a limited number of studies evaluated the combination of FDBA with a CS used

as barrier for ARP(Kim et al., 2011, Wood and Mealey, 2012, Spinato et al., 2014, Eskow

and Mealey, 2014). The results of the current study indicate that CS can form an effective

barrier for the bone graft in ARP procedures and are similar to those of(Kim et al., 2011)and

(Spinato et al., 2014)who evaluated the efficacy of CS placed over xenograft or allograft,

respectively, in ARP performed with a flapless approach and compared it with extraction

only.

Anatomical characteristics of the extraction socket such as thickness or loss of the buccal

plate can significantly affect the outcomes of the ARP procedure. Clinical studies

(Cardaropoli et al., 2014, Cardaropoli et al., 2015, Spinato et al., 2014)and systematic

reviews (Wang and Lang, 2012, MacBeth et al., 2016)indicate that thickness and vertical loss

of the buccal plate influence the reduction in the crestal ridge width and height following

ARP. In our investigation, the mean coronal thickness of the buccal plate was >1 mm and the

vertical loss <2 mm in both groups. Thus, part of the favorable results observed may be

attributed to the favorable characteristics of the extraction sockets. Only 7 sites in both

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 groups had a buccal plate thickness of <1mm which precluded a possible comparison
Accepted Article between sites with thin or thick buccal plates.

We used a flapless approach in this study, and regenerative materials were left exposed

during healing because elevation and advancement of a full-thickness flap may cause

postoperative bone resorption, marginal recession at the adjacent teeth, defective papillae,

and loss of keratinized mucosa. The amount of bone resorption occurring after flapped or

flapless tooth extraction remains controversial. Flapless surgery in dogs reduced the

volumetric alterations on the buccal aspect irrespective of whether a grafting material was

used (Fickl et al., 2008a). In addition, a clinical study indicated that a flapless technique in

combination with a xenograft and a resorbable membrane for ARP increased the WKT and

reduced the horizontal bone loss, but slightly increased vertical bone resorption on the buccal

aspect in comparison with a full-thickness mucoperiosteal flap elevation and two releasing

incisions(Barone et al., 2014).However, other authors did not report any significant

differences with or without flap elevation (Araujo and Lindhe, 2009a) and a recent systematic

review found that flap elevation had a beneficial effect on preservation of buccal alveolar

bone height(Avila-Ortiz et al., 2014).Although it is suggested that wound dehiscence and

membrane exposure could result in infection and lack of bone formation, recent studies show

that the intentional exposure of bioabsorbable barriers does not seem to adversely affect ARP

procedures (Barone et al., 2013, Jung et al., 2013, Parashis et al., 2016). We observed no

adverse effects in this study where the barriers were left exposed to the oral cavity, and

sutures were used primarily to stabilize the barriers in place.

The potential values of such anatomic variables as baseline GT, WKT, and BPT as predictors

of changes in tissue thickness and ridge bone width after ARP were also investigated. The

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 analyses indicate that the preoperative bone width at the middle part of the ridge was
Accepted Article significantly correlated with changes in coronal bone width. The greater the ridge width at the

7 mm apical reference point, the less was the crestal alveolar ridge width reduction. A

possible explanation for this observation is that a triangularly shaped ridge will better

preserve the materials from collapsing. In addition, only GT and not WKT or BPT at the 4

mm reference point at baseline was related to the change in coronal GT after extraction and

ARP. The greater the thickness of the crestal soft tissue at baseline, the thicker was the

gingival tissue at 4 months.

The current study also investigated changes in periodontal parameters (PD, CAL and REC) at

the neighboring teeth following tooth extraction and ARP. PD and CAL at adjacent teeth

increased in the CS group by 0.16mm and 0.34 mm, respectively. However, these minor

losses are not clinically significant. These variables were unchanged in the CMS group.

Overall, the changes in the proximal sites of the neighboring teeth to the extracted one

indicated no deleterious effect of the ARP procedure on the periodontal apparatus in adjacent

teeth.

All treatments and clinical measurement recording were performed by one investigator. The

lack of masking is recognized as a potential limitation. However, one could argue that the

study also benefited from reduced variability. In addition, the use of individual stents for

clinical soft tissue and radiographic hard tissue changes at baseline and 4 months further

limited sources of variability in the clinical and radiographic measurements. In addition, a

blinded investigator performed all radiographic measurements on CBCTs. A recent study

indicated that radiographic measurements of buccal plate thickness at extraction sites on

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 CBCTs are accurate within 0.2 mm when compared to direct clinical measurements (Behnia
Accepted Article et al., 2015).

CONCLUSION

Within the limitation of this study, the use of CMS and CS, when combined with FDBA,

significantly minimized ridge resorption in all dimensions and maintained buccal soft tissue

thickness in sockets with a buccal plate loss of <2 mm in comparison to previously reported

findings recorded after tooth extraction without ARP.

ACKNOWLEDGEMENTS

The authors acknowledge Dr Haemin Chin for her assistance with data entry and patient

recruitment.

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 Table 1: Baseline clinical and radiographic measurements
Accepted Article
Variable CMS CS p
mm, mean ±SD n=14 n=14
Clinical
GT-4 1.66±0.96 2.03±1.77 0.50
GT-7 2.11±1.20 2.46±2.34 0.63
GT-10 2.68±1.56 2.76±1.91 0.90
WKT 4.02±1.09 3.97±2.04 0.94
PD 2.61±0.45 2.26±0.76 0.72
REC 0.02±0.07 0.28±0.51 0.08
CAL 2.63±0.42 2.55±1.05 0.79

Radiographic
WB-4 7.87±1.42 8.15±1.26 0.58
WB-7 8.22±1.24 8.55±1.36 0.27
WB-10 8.52±1.93 8.85±1.66 0.55
VR-BC 7.29±2.11 9.62±2.07 0.04*
VR-PC 7.85±1.95 9.48±2.16 0.08
BPT-4 1.55±0.27 1.47±0.21 0.35
BPT-7 1.55±0.23 1.66±0.68 0.57
BPT-10 1.52±0.25 1.85±0.80 0.16
PPT-4 1.48±0.13 1.60±0.25 0.13
PPT-7 1.99±0.66 2.22±0.62 0.34
PPT-10 2.66±0.99 3.19±0.99 0.17
*p value< 0.05

GT, Buccal gingival thickness; WKT, width of keratinized tissue; WB, width of alveolar

ridge; VR-BC, vertical height to the buccal; VR-PC, vertical height to palatal/lingual; BPT,

thickness of the buccal alveolar plates(only 1st CBCT); PPT, thickness of the palatal/lingual

alveolar plates (only 1st CBCT);-4, at 4 mm apical reference point; -7, at 7 mm apical

reference point; -10, at 10 mm apical reference point

PD, pocket depth; REC, gingival recession; and CAL, clinical attachment level were

measured on the teeth adjacent to the extracted tooth.

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 Table 2: Clinical changes in soft tissues from baseline to 4 months
Accepted Article Variable CMS CS p*
mm, mean ±SD n=14 n=14
Δ P value Δ P value
GT-4 +0.90±0.90 0.01** +0.59±1.28 0.11 0.46
GT-7 +0.47±1.16 0.15 -0.23±1.42 0.55 0.17
GT-10 +0.05±1.62 0.92 -0.13±1.07 0.65 0.73
WKT -0.08±0.54 0.89 -0.08±1.24 0.81 0.13
PD +0.06±0.59 0.74 +0.16±0.27 0.04** 0.56
REC +0.02±0.11 0.55 +0.20±0.42 0.11 0.16
CAL +0.05±0.52 0.75 +0.34±0.44 0.01** 0.13
*p value for changes between CMS and CS

**p value<0.05

-means decreased; + means increased; GT, Buccal gingival thickness; WKT, width of

keratinized tissue; -4, at 4 mm apical reference point; -7, at 7 mm apical reference point; -10,

at 10 mm apical reference point

PD, pocket depth; REC, gingival recession; and CAL, clinical attachment level were

measured on the teeth adjacent to the extracted tooth.

Table 3: Radiographic changes in hard tissues from baseline to 4 months

Variable CMS CS p*
mean±SD n=14 n=14
Δ in mm Δ in % p Δ in mm Δ in % p
WB-4 -1.21±1.22 -14.91±15.17 0.01** -1.47±1.29 -20.40±25.10 0.01** 0.49
WB-7 -0.90±1.02 -10.22±11.63 0.01** -0.96±0.97 -11.74±15.70 0.01** 0.77
WB-10 -0.54±0.95 -5.94±11.03 0.05 -0.57±0.99 -6.94±14.34 0.05 0.84
VR-BC -0.30±1.09 -5.69±16.86 0.32 -0.79±3.07 -10.87±35.82 0.35 0.58
VR-PC -0.27±2.30 -7.99±28.21 0.67 -0.49±2.59 -8.53±31.34 0.49 0.81
*p value for changes between CMS and CS

**p value< 0.05

-means decreased; WB, width of alveolar ridge; VR-BC, vertical height to the buccal; VR-

PC, vertical height to palatal/lingual;-4, at 4 mm apical reference point; -7, at 7 mm apical

reference point; -10, at 10 mm apical reference point

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 Table 4: Regression analysis for gingival thickness and width of bone at the 4mm
Accepted Article reference point

Variable Stepwise model Proposed model

B SE t p B SE t p
GT

GT0-4 0.72 0.15 23.1 0.001* 0.65 0.19 3.41 0.002*

WKT0 - - - - -0.60 0.15 -0.23 0.820
BPT0-4 - - - - -0.10 0.89 -0.30 0.764

R2 0.50 0.52
WB

WB0-7 0.46 0.15 9.1 0.006* - - - -

GT0-4 - - - - -0.24 0.16 -1.53 0.14
WKT0 - - - - -0.61 0.85 -0.72 0.48
BPT0-4 - - - - -0.10 0.14 -0.76 0.45

R2 0.28 0.15
*p value<0.05

0at baseline; GT, Buccal gingival thickness; WKT, width of keratinized tissue; WB, width of

alveolar ridge; BPT, thickness of the buccal alveolar plates(only 1st CBCT); -4, at 4 mm

apical reference point; -7, at 7 mm apical reference point.

FIGURE LEGENDS

Figure 1: (A) Stent with reference holes (arrows) used for standardized clinical and

radiographic measurements. Cross sectional CBCT images (B) before extraction and (C) 4

months after ridge preservation. (D) Schematic illustration of clinical and radiographic

measurements. (WB, width of alveolar ridge; VR-BC, vertical height to the buccal; VR-PC,

vertical height to palatal/lingual; BPT, thickness of the buccal alveolar plates (only 1st

CBCT); PPT, thickness of the palatal/lingual alveolar plates (only 1st CBCT); GT, Buccal

gingival thickness;-4, at 4 mm apical reference point; -7, at 7 mm apical reference point; -10,

at 10 mm apical reference point.

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 Figure 2: Surgical procedure. (A) Pretreatment clinical view. Clinical view after (B)sulcular
Accepted Article incisions and atraumatic extraction using flapless approach, (C) FDBA placement to the level

of the bony crest, (D) adaptation of the collagen matrix seal and(E) suturing.

Figure 3: CONSORT 2010 flow diagram.

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Accepted Article

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