J Int Acad Periodontol v.17, n 1, jan 2015 revista completa

Journal of the International Academy of Periodontology The official journal of the International Academy of Periodontology

Volume 17 Number 1 January 2015

Published by The International Academy of Periodontology

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Reference to a chapter in a book: Chesney J, Patters MR and BudreauPatters A. Oral Infections. In Long S, Prober C and Pickering L. (Eds): Principles and Practice of Pediatric Infectious Disease. New York. John Wiley and Sons, 1996.

Reference to a dissertation or thesis: James A. On the immune response to GTR membranes in periodontics. PhD, Liverpool, UK. 1994; 15-25.

Reference to a report: Committee on Mercury Hazards in Dentistry. Code of Practice for Dental Mercury Hygiene. London: Department of Health and Social Security, 1979; Publication No. DHSS 79-F372.

Reference to an abstract: Patters MR, Shiloah J, Dean JW, Bland P and Toledo G. The consequence of infection of treated periodontal pockets by microbial pathogens. Journal of Dental Research 1997; 76 (special issue), 111 (Abst).

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Volume 17 Number 1 January 2015 ISSN 1466–2094

Journal of the International Academy of Periodontology

EDITORIAL BOARD Mark R Patters Editor Memphis, TN, USA Andrea B Patters Associate Editor Sultan Al Mubarak Riyadh, Saudi Arabia P Mark Bartold Adelaide, SA, Australia Michael Bral New York, NY, USA Cai-Fang Cao Beijing, People’s Republic of China Ahmed Gamal Cairo, Egypt

Evaluation of Platform Switching on Crestal Bone Stress in Tapered and Cylindrical Implants: A Finite Element Analysis Amir Alireza Rasouli-Ghahroudi, Allahyar Geramy, Siamak Yaghobee, Afshin Khorsand, Hosnieh Yousefifakhr, Amirreza Rokn and Ahmad Soolari

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Gingival Cysts of Adults: Retrospective Analysis from Two Centers in South Brazil and a Review of the Literature Vivian P. Wagner, Manoela D. Martins, Marina Curra, Marco A. T. Martins and Maria C. Munerato

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A Novel Surgical Approach for Treatment of Class II Furcation Defects Using Marginal Periosteal Membrane Hala H. Hazzaa, Heba El Adawy and Hani M. Magdi

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Francis Mora Paris, France Vincent J Iacono Stony Brook, NY, USA Francis Mora Paris, France Hamdy Nassar Cairo, Egypt Rok Schara Ljubljana, Slovenia Uros Skaleric Ljubljana, Slovenia Shogo Takashiba Okayama, Japan Ahmad Soolari Tehran, Iran Thomas E Van Dyke Boston, MA, USA Warwick Duncan Dunedin, New Zealand Nicola Zitzmann Basel, Switzerland

The Journal of the International Academy of Periodontology is the official journal of the International Academy of Periodontology and is published quarterly (January, April, July and October) by The International Academy of Periodontology, Boston, MA, USA and printed by Dennis Barber Limited, Lowestoft, Suffolk. UK. Manuscripts, prepared in accordance with the Information for Authors, should be submitted electronically in Microsoft Word to the Editor at the jiap@uthsc.edu.The Editorial Office can be contacted by addressing the editor, Dr. Mark R.Patters, at jiap@uthsc.edu.

All enquiries concerning advertising, subscriptions, inspection copies and back issues should be addressed to Ms. Alecha Pantaleon, Forsyth Institute, 245 First Street, Suite 1755, Cambridge, MA, USA 02142, Telephone: +1 617-892-8536, Fax: +1 617-2624021, E-mail: apantaleon@forsyth.org. Whilst every effort is made by the publishers and Editorial Board to see that no inaccurate or misleading opinion or statement appears in this Journal, they wish to make clear that the opinions expressed in the articles, correspondence, advertisements etc., herein are the responsibility of the contributor or advertiser concerned. Accordingly, the publishers and Editorial Board and their respective employees, offices and agents accept no liability whatsoever for the consequences of any such inaccurate or misleading opinion or statement. ©2015 International Academy of Periodontology.

All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, photocopying, or otherwise, without permission of the Academy.

Produced in Great Britain by Dennis Barber Limited, Lowestoft, Suffolk

Journal of the International Academy of Periodontology 2015 17/1: 2–13

Evaluation of Platform Switching on Crestal Bone Stress in Tapered and Cylindrical Implants: A Finite Element Analysis Amir Alireza Rasouli-Ghahroudi1, Allahyar Geramy2, Siamak Yaghobee1, Afshin Khorsand1, Hosnieh Yousefifakhr3, Amirreza Rokn1 and Ahmad Soolari4 Dental Implant Research Center and Department of Periodontology, Tehran University of Medical Sciences, Tehran, Iran; 2 Department of Orthodontics, Tehran University of Medical Sciences, Tehran, Iran; 3Periodontist, Private Practice, Tehran, Iran; 4Private Practice, Silver Spring, Maryland, USA 1

Abstract Purpose: To analyze and compare the stress distribution around tapered and cylindrical implants and investigate how different abutment diameters influence crestal bone stress levels.

Materials and Methods: Six finite element models of an abutment (5 mm, 4.3 mm, and 3.5 mm in diameter) and supporting implants (tapered and cylindrical) were designed.

A vertical force of 100 N and a 15-degree oblique force of 100 N were applied separately on the occlusal surface, and von Misses stresses were evaluated in the cortical and cancellous bone.

Results: Higher stress was observed under oblique loading than under vertical loading of both tapered and cylindrical implants. Tapered implants demonstrated more stress under both vertical and oblique loading. Platform switching reduced peri-implant crestal bone stress in all models under vertical and oblique forces. The peri-implant crestal bone around tapered implants experienced 4.8% more stress under vertical loading and 35% more stress under oblique loading in comparison to bone around cylindrical implants (2.62 MPa with vertical loading, 8.11 MPa under oblique loading). Oblique loads resulted in much higher stress concentrations in the peri-implant crestal bone than vertical loads (238% in cylindrical and 308% in tapered implants). When the abutment diameter decreased, both models showed reductions of stress in the crestal bone under both types of loading.

Conclusion: In this finite element analysis, tapered implants increased crestal bone stress upon loading, and platform switching minimized the stress transmitted to the crestal bone in both tapered and parallel wall implants.

Key words: Finite element analysis, platform switching, dental implants, crestal bone stresses, implant loading, stress distribution

Introduction The peri-implant bone level has been used as a criterion to determine the success of dental implants (Albrektsson et al., 1986; Albrektsson and Isidor, 1994; Misch et al., 2008; Smith and Zarb, 1989; Buser et al., 1990;

Correspondence to: Ahmad Soolari, 11616 Toulone Dr., Potomac, MD, USA 20854. Phone: +1 301 299 6664. Fax: +1 240 845 1087. E-mail: asoolari@gmail.com Š International Academy of Periodontology

Roos et al., 1997) because a stable bone level is an important prerequisite for preserving the integrity of the gingival margins and interdental papillae (Tarnow et al., 1992; Choquet et al., 2001). Implant success is typically assessed by serial radiographs at 1-year intervals from the date of implant placement. If the observed marginal bone loss is less than 1.5 mm in the first year and less than or equal to 0.2 mm in subsequent years, the implant can be considered successful (Albrektsson and Isidor, 1994). When the patient undergoes stagetwo surgery (abutment placement) or if the abutment is

Rasouli-Ghahroudi et al.: Platform switching in tapered and cylindrical implants

placed immediately after the implant, which may expose the implant to the oral environment, peri-implant bone remodeling is initiated. The remodeling process involves marginal bone resorption, which is influenced by one or more of the following factors: (a) surgical trauma (Becker et al., 2005); (b) excessive loading (Kim et al., 2005); (c) the location, shape, and size of the implantabutment microgap and its microbial contamination (Hermann et al., 2001; Weng et al., 2008; Ericsson et al., 1995); (d) the biologic width and soft tissue considerations (Myshin and Wiens, 2005; Berglundh and Lindhe, 1996); (e) a peri-implant inflammatory infiltrate (Broggini et al., 2006); (f) micromovements of the implant and prosthetic components (Hermann et al., 2001; King et al., 2002); (g) repeated screwing and unscrewing of prosthetic components (Abrahamsson et al., 1997); (h) the geometry of the implant neck (Bratu et al., 2009); and (i) the infectious process (Roos-Jansåker et al., 2006). Hence, modifications to implant designs are now focused on reducing the bone stress around implants.

In addition, changes in the design of the connection between an abutment and an implant, such as restoring an implant with a smaller-diameter abutment (the “platform-switching” concept), using microthreads at the coronal portion of the implant body (Schrotenboer et al., 2008), and augmentation of implant diameter and/ or length (Cynthia et al., 2005), have also been suggested for this purpose.

Platform switching, which was introduced in 1991 (Lazzara and Porter, 2006), is an uncomplicated and effective means to control circumferential bone loss around dental implants. It also has the advantage of acceptable responses from hard and soft tissue. Thus, implants restored with a platform switch could be used for esthetic and biologic purposes (Canullo et al., 2011).

In addition, it is assumed that tapered implants have some advantages over implants with a cylindrical shape, for example, in challenging situations such as ridge concavities, extraction sites, and immediate loading or provisionalization, especially in the esthetic zone because of the improved primary stability (Alves and Neves, 2009; Rokn et al., 2011). However, some studies have shown that the tapered implant design actually results in increased crestal bone stress (Cynthia et al., 2005) or at least produces no positive effect on bone level changes (Vigolo and Givani, 2009). Currently, there is insufficient data, either experimental or clinical, regarding bone loss and mechanical stability when platform switching is used together with a tapered implant. Therefore, more studies are needed (Kitamura et al., 2005) to explore this subject.

We aimed to evaluate crestal bone stress around dental implants with mismatched abutments and two different implant body forms (cylindrical and tapered) via finite element analysis (FEA). Finite element models were created to measure the amount of stress in the bone

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around tapered and cylindrical implants with matched abutments and to compare this with the same implants with mismatched abutments. The main hypothesis was that the crestal bone stresses are higher around tapered implants, and a mismatched abutment can compensate for this greater stress in a positive manner.

Materials and methods Tapered and cylindrical implants, both with a coronal diameter of 5 mm, were selected to be matched with three different abutment diameters. The implant designs were unique but based on the design of the popular Replace Tapered Groovy (Nobel Biocare), which is threaded and features a rough surface. Six three-dimensional finite element models of an implant, an abutment, and the supporting structures were designed (two different implants x three different abutment diameters).

Computed tomographic (CT) images from a volunteer patient, a candidate for implant therapy who provided written consent to use the images in this study (ethical approval 90-03-114-14704 Tehran University of Medical Sciences), were used to design the supporting structures for FEA. Each model consisted of a cancellous bone core surrounded by a cortical bone layer, 1 mm thick.

The cortical bone thickness was derived from the patient’s CT scans and from the literature (Kunavisarut et al., 2002; Tabata et al., 2010). The models were identical except for the type of implant (cylindrical or tapered) and abutment diameter (platform 1 [P1] = 5 mm [same diameter as the implant], P2 = 4.3 mm, and P3 = 3.5 mm; Figure 1).

SolidWorks 2010 (Concord, MA, USA) software was selected for the modeling phase. Then the models were transferred to ANSYS Workbench (version 11.0, ANSYS Inc, Canonsburg, PA, USA) for calculation of stresses. All the vital tissues were presumed elastic, homogeneous and isotropic, and the corresponding elastic properties (Young’s modulus and Poisson ratio) were taken from the literature (Table 1) (Yang et al., 1999; El Charkawi and El Waked, 1996; Fejerdy et al., 2008; Ash, 2005; Craig and Farah, 1978; Geramy, 2000). Models were meshed and included 117,161 to 201,611 nodes to make up the 10-node quadratic tetrahedral body elements. All nodes at the mesial and distal extremes of the models were restrained so that all rigid body motions were prevented. A vertical force of 100 N was applied at the center of the occlusal surface of the abutment, and an oblique force of 100 N was applied at the occlusal surface with 15 degrees of angulation. Forces of 100 N were chosen because this figure is widely accepted in the literature as comparable to the average magnitude of occlusal force (O’Mahony et al., 2001; Abu-Hammad et al., 2007; Huang et al., 2006; Siegele and Soltesz, 1989).

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Figure 1. Overall models of the implant and abutment in bone.

Table 1. Mechanical properties of materials used in the models Young’s Modulus Poisson ratio in MPa Implant Cortical bone Cancellous bone

96,000 34,000 13,400

0.36 0.26 0.38

The von Misses stresses were evaluated at nine nodes placed at equal distances from coronal to apical (six in the cortical bone and three in the cancellous bone).

These nodes were in a plane parallel to the distal extremity of the model after “hiding” the implant. Most studies utilize three nodes in cortical bone and three in the cancellous bone for finite analysis; however, we chose six nodes in cortical bone and three in cancellous bone in this mandibular molar section from CT scans of a real patient to provide more exact data on crestal bone. Also, it is clear from the literature (Misch, 1990; Cochran, 2000) that the maximum stress on bone is mostly at the coronal part of the implant body, especially on the crestal cortical bone. And because the load exerts greater force at early stages of osseointegration we focused more on the cortical part. It was determined that the use of six layers would better distinguish the load distribution in this critical location, since the three layers in the most coronal cancellous part tolerate the greatest amount of load among the cancellous bone that surrounds the implant. Earlier studies found that the peak bone stresses resulting from vertical load components and those resulting from horizontal load components arise at the top of the marginal bone, and that they coincide spatially. These peak stresses are then added together to produce the risk of stress-induced bone resorption (Hansson, 2003).

No statistical analyses were performed because the study was designed to emulate a single imaginary clinical situation, and hence the results were not eligible for statistical analysis.

Results The average von Misses stresses produced in the cortical bone and the adjacent cancellous bone in the different models are shown in Tables 2 and 3. Figures 1 - 3 summarize the von Misses stresses that occurred in the peri-implant bone under vertical and oblique loading.

Vertical loading The crestal bone stresses that occurred under vertical loading are shown in Table 2.

Cylindrical implant With the 5 mm abutment (P1), the von Misses stresses ranged from a high of 6.74 MPa and followed a decreasing pattern, reaching 1.70 MPa at the deepest point of the cortical bone. This decrease continued in the cancellous bone to reach a low of 0.74 MPa (Figure 4A).

With the 4.3 mm abutment (P2), the stresses were 5.87 MPa at the most crestal portion and again decreased, similar to the pattern seen with the 5 mm abutment, reaching 1.12 MPa at the deepest portion of the cortical bone. The decreases continued and reached 0.52 MPa in the first layers of cancellous bone (Figure 4A).

With the 3.5 mm abutment (P3), the stresses in the cortical bone area ranged between 4.30 MPa in the crestal area and 1.00 MPa at the deepest point of the cortical bone. These values reached 0.48 MPa in the cancellous bone (Figure 4A).

Tapered implant Under vertical loading of the tapered implant with the 5 mm (P1) abutment, the von Misses stresses began at 7.16 MPa in the most crestal portion and followed a decreasing pattern, reaching 1.62 MPa in the deepest point of the cortical bone. This decrease continued in the cancellous bone to reach 0.64 MPa (Table 2, Figure 4B).

With the 4.3 mm abutment (P2), stresses ranged from a high of 5.64 MPa in the most crestal bone and followed a similar decreasing pattern, reaching 1.49 MPa in the deepest cortical bone. They continued to decrease, reaching 0.59 MPa in the first layers of cancellous bone (Figure 4B).

Rasouli-Ghahroudi et al.: Platform switching in tapered and cylindrical implants

Table 2. The average of von Misses stresses produced in cortical and the adjacent cancellous bone under vertical load in tapered and parallel implants with different abutment sizes (P1 = 5 mm abutment; P2 = 4.3 mm abutment; P3 = 3.5 mm abutment) at nine nodes (1-9) placed at equal distances from coronal to apical points (six in the cortical bone and three in the cancellous bone). The amount of stress is most pronounced in the most coronal part of the cortical bone (node 1) and is higher in tapered than cylindrical implants.

Tapered implant Bone layer nodes

P1

P2

P3

Cylindrical implant P1

P2

P3

Amount of stress in cortical bone 1 7.16 5.63 4.43 2 5.07 3.45 2.50 3 3.71 2.15 1.34 4 2.24 1.82 1.16 5 1.78 1.53 1.11 6 1.62 1.49 1.23

6.73 4.88 2.70 2.22 2.06 1.69

5.86 4.17 2.28 1.99 1.21 1.11

4.30 1.69 1.20 1.02 1.07 0.99

Amount of stress in cancellous bone 7 0.75 0.77 0.72 8 0.66 0.61 0.73 9 0.64 0.59 0.67

0.75 0.74 0.73

0.57 0.55 0.52

0.51 0.50 0.48

Table 3: The average of von Misses stresses produced in cortical and the adjacent cancellous bone under oblique load in tapered and parallel implants with different abutment sizes (P1 = 5 mm abutment; P2 = 4.3 mm abutment; P3 = 3.5 mm abutment) at nine nodes (1-9) placed at equal distances from coronal to apical points (six in the cortical bone and three in the cancellous bone). The amount of stress was most pronounced in the most coronal part of the cortical bone (node 1) and was approximately three times greater with oblique loading compared to vertical loading (21.16 vs 7.16).

Tapered implant Bone layer nodes

P1

P2

P3

Cylindrical implant P1

P2

P3

19.52 6.83 6.43 5.67 5.14 5.03

16.52 5.51 5.48 5.22 4.95 4.72

11.98 4.81 5.07 4.84 4.87 4.05

The von Misses stress in cancellous bone 7 4.40 4.18 4.00 1.91 8 2.31 2.19 2.09 1.68 9 1.93 1.81 1.78 1.59

1.78 1.55 1.42

1.61 1.49 1.39

The von Misses stress in cortical bone 1 21.16 18.64 14.56 2 15.61 13.37 11.21 3 11.30 9.62 8.02 4 6.08 5.13 4.89 5 5.14 5.10 4.38 6 5.03 4.50 4.11

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Figure 2. The von Misses Stress (MPa) findings in cortical and spongy bone under vertical loading. As the diagram demonstrates; the most pronounced stress was in crestal bone and around tapered implants.

Figure 3. The von Misses Stress (MPa) findings in cortical and spongy bone under oblique loading. As the diagram demonstrates; the most pronounced stress was in crestal bone and around tapered implants.

With the smallest (3.5 mm) abutment (P3), stresses in the cortical bone ranged between 4.43 MPa in the crestal area and 1.24 MPa in the depth of the cortical bone. These values reached 0.67 MPa in the cancellous bone (Figure 4B).

Oblique loading Crestal bone stresses that occurred under 15-degree oblique loading are shown in Table 3.

Cylindrical implant Under oblique loading of the cylindrical implant with the 5 mm (P1) abutment, the von Misses stresses be-

gan at 19.52 MPa, followed a decreasing pattern, and reached 5.03 MPa in the deepest point of the cortical bone. This decrease continued in the cancellous bone to reach 1.59 MPa. With the 4.3 mm (P2) abutment, stresses ranged from 16.52 MPa in the most crestal cortical bone to 4.72 MPa in the deepest cortical layer. The decreased stresses continued, reaching 1.43 MPa in the most apical layer of cancellous bone.

With the narrowest (3.5 mm) abutment (P3), the stresses observed in cortical bone ranged from 11.99 MPa in the crestal area to 4.06 MPa in the most apical area. These values reached 1.40 MPa in cancellous bone.

Rasouli-Ghahroudi et al.: Platform switching in tapered and cylindrical implants

 Figure 4. Distribution of von Misses stress around implants with different geometries. A, Model computed by FEA for tapered implant with length of 13 mm and diameter of 5 mm. B, Model computed for parallel implant with length of 13 mm and diameter of 5 mm. area of maximum stress in crestal bone is wider with implant with tapered wall. Red represents locality where maximum stress acts. Values of maximum stress in respective scales are higher for A as well.

Tapered implant In the tapered implant with a 5 mm abutment (P1), the von Misses stresses began at 21.16 MPa, followed a decreasing pattern, and reached 5.04 MPa in the deepest point of cortical bone. This decrease continued in the cancellous bone to reach 1.93 MPa. With the P2 (4.3 mm) abutment, stresses followed the same decreasing pattern: from 18.64 to 4.50 MPa in the cortical bone down to 1.8109 MPa in the deepest layer of cancellous bone.

With the smallest (3.5 mm) abutment (P3), stresses ranged from 14.56 MPa in the crestal area to 4.11 MPa in the apical portion of the cortical bone. These values reached 1.78 MPa in cancellous bone.

Discussion The tapered implant has been a successful design, with many advantages, but the greater stresses in the crestal bone around it constitute a remarkable disadvantage (Cynthia et al., 2005; Alves and Neves, 2009; Rokn et al., 2011), making this implant design a challenge. On the other hand, some clinical reports have demonstrated minimal crestal bone resorption around implants that were restored by the platform-switching concept (Wegenberg and Froum, 2006; Lazzara and Porter, 2006; Maeda et al., 2007; RodrĂ­guez-Ciurana et al., 2009).

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However, the concept of platform switching is not fully understood and is mainly influenced by manufacturers’ recommendations.

The present study focused on the combined effect of a tapered implant body and platform switching on crestal bone stresses. The authors believe that this combination needs to be assessed to help clinicians use better implant-abutment designs in clinical practice and thus treat their patients appropriately.

The purpose of this study was to analyze the effect of platform switching and a tapered implant body on implant crestal bone stress via three-dimensional FEA; for this purpose, the authors designed the prosthetic structures (abutment and crown) and implant body as one solid object. The rationale behind the omission of design elements, such as the abutment connection system, was to consider the suprastructure and the implant as one rigid object so that nodes could be shared between the abutment and the implant body. Because this study did not intend to evaluate small displacements between the abutment and the implant, modeling the components as one piece decreased the number of calculations needed, thereby reducing the time needed to evaluate the stresses.

Although micromovement plays a vital role in implant stability, it was determined that micromovement would have been similar in the different models. Thus, the present model was kept simple to evaluate the effect of platform switching and body tapering without the complexity of additional parameters that were not being investigated in this study.

Regardless of implant design, the result showed that the mean amount of stress induced by oblique forces was much greater than that induced by vertical forces, as expected from the knowledge of off-axis loading.

However, stresses decreased in all groups at the apical part of the implant body. For example, in the tapered implants with 5 mm abutments, the crestal bone stress was 2.62 MPa with vertical force application, whereas the stress increased to as much as 8.11 MPa upon oblique loading, demonstrating that oblique forces can increase the stresses on crestal bone by threefold or more compared to vertical forces.

When the crestal bone stresses in the different implant designs were compared under both vertical and oblique loads, greater crestal stress (around 36% for oblique force and 7% for vertical force) was seen in tapered designs versus the cylindrical implants (Tables 2 and 3, Figures 2 and 3). These results are consistent with previous studies that showed that tapered implants produced more crestal bone stress than cylindrical implants (Cynthia et al., 2005; Patra et al., 1998). Rismanchian et al. (2010) observed increased peak tensile stresses in cortical bone around tapered implants in comparison to cylindrical implants. Mohammed Ibrahim et al. (2011)

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found that a tapered implant exhibited higher stress levels in bone than a cylindrical implant, which seemed to distribute stresses more evenly.

However, some authors claim that tapered implants could decrease the stresses around both cortical and trabecular peri-implant bone (Rieger et al., 1989; Huang et al., 2005). They proposed that threads with increased depth in tapered implants could enlarge the boneimplant contact area, resulting in decreased crestal bone stresses around tapered endosseous implants. However, we believed that, because an increase in the bone-implant interface area could be detected with cylindrical implants (Rismanchian et al., 2010) as well, this could not be an accurate reason for the decreased crestal bone stress around tapered implants.

Our results showed that, although tapered implants have many benefits in implant dentistry, as previously mentioned, they can result in greater crestal bone stress around implants. However, our data suggest that when the abutment diameter was reduced by 14% or 30%, less stress was transferred to the peri-implant bone around both tapered and cylindrical implants, regardless of the direction of force application (vertical or oblique). This finding supports the hypothesis that connecting an implant to a smaller-diameter abutment may decrease bone resorption by shifting the stress concentration away from the crestal bone interface and guiding the forces of occlusal loading along the axis of the implant (Maeda et al., 2007). Furthermore, this result also confirms the serendipitous clinical finding of Lazzara and Porter (2006) in the late 1980s that led to the introduction of the platform-switching concept, in which a narrower prosthetic component is connected to a wider implant, resulting in reduced crestal bone resorption.

In this study, a greater internal shift of the prosthetic components resulted in less crestal bone stress. Becker et al. (2007) declared that, in the clinical situation, because inflammatory cells typically infiltrate the implant complex at the abutment-implant junction and form a 1.5 mm semispherical zone, when the outer edge of the implant-abutment junction is repositioned away from the external outer edge of the implant and adjacent bone, less crestal bone loss will be observed. As seen in Table 2, when a vertical force was applied, the crestal bone stresses in the tapered implant model with a 5 mm abutment were 2.62 MPa; this was reduced to 2.00 MPa with the 4.3 mm abutment, and a further reduction of the abutment size to 3.5 mm (P3) lowered the crestal bone stress to 1.54 MPa. When oblique forces were applied in the tapered and same size abutment group (P1), the mean crestal bone stress was the highest (8.11 MPa); this was reduced to 7.17 MPa in the P2 group and 6.12 in the P3 group. This is in agreement with the results of the recent randomized controlled study of Canullo et al.

(2010), which also demonstrated an inversely propor-

tional relationship between marginal bone loss and the extent of inward shifting of the prosthetic component.

Some other studies have also shown an improved distribution of biomechanical stresses in the peri-implant bone tissue and preservation of interimplant bone height and soft tissue levels (Maeda et al., 2007; Tabata et al., 2011; Annibali et al., 2012).

A study by Schrotenboer et al. (2008) showed that, although the use of microthreads may increase crestal stresses upon loading, a reduced abutment diameter could result in reduction of the stresses transmitted to the crestal bone and thus, perhaps, less bone loss.

However, other studies demonstrated no significant difference in crestal bone loss between platform-switched and platform-matched implants. An animal study conducted by Becker et al. (2007) indicated that smaller abutments could reduce the marginal bone loss in the early days after abutment connection, but the matching and platform-switched implants showed the same amount of bone loss after 28 days. This finding is supported by a recent randomized clinical trial published by Enkling et al. (2011), who observed substantially similar crestal bone loss in platform-switched and platform-matched implants that were placed in the posterior mandible and followed for one year. The bone loss that occurred was thought to be related to the extent of microbial colonization rather than to platform switching.

The authors believe that clinically relevant conclusions can be drawn from this study if the stated assumptions are accepted. Although marginal bone remodeling can be attributed to biological width formation and other many factors, the most common causes of implant-related complications involve excessive stress (Misch, 2008), and according to the data obtained in this study, stress can be managed through the choice of appropriate implant designs and prosthetic components. This theoretical analysis suggests that an inward shifting of the prosthetic component could compensate for the more pronounced crestal bone stress seen around the tapered implants that are so popular today among clinicians because of their better stability and manipulation, especially in the esthetic zone and in compromised bone. The authors believe that this study may lead clinicians to choose an implant system more carefully with regard to geometry (parallel or tapered) and the subsequent implant-abutment connection configuration (matched versus mismatched).

Because one of the main theories of the mechanism of bone resorption around dental implants is stress concentration caused by occlusal loading, it is wise for clinicians to manage this biomechanical aspect in planning implant therapy. This study demonstrated that, in the appropriate quantity of bone in the posterior region of the jaws, the amount of stress is more pronounced than in anterior areas; because it could decrease the boneimplant stress concentration, a parallel-wall implant with

Rasouli-Ghahroudi et al.: Platform switching in tapered and cylindrical implants

an abutment connection with the maximum possible platform switch may contribute to long-term implant success as a result of the minimized microdamage to the peri-implant bone. Cullinane and Einhorn (2002) stated that even loads below the ultimate stress tolerance can cause bone failure, in which the microdamage of the bone can no longer be repaired.

On the other hand, in the anterior zone, which features many bony concavities or depressions (Swasty et al., 2009), the placement of parallel-wall implants is often not feasible because of insufficient bone or the proximity of vital structures. Therefore, clinicians should choose the tapered-design implant with a platform-switched connection in these areas. This selection will assist in better load distribution and minimal bone loss. Studies have demonstrated that crestal bone loss generally coincides with the level of the first thread of the implant and can jeopardize the treatment outcome, especially in esthetically sensitive cases in which facial soft tissue deficiencies make the crown appear longer than desired and gingival papillae support depends on the crestal bone underneath (Lai et al., 2007; Reikie, 1995; Buser et al., 2004; Belser et al., 2004).

Limitations of the study Finite element analysis is a descriptive and numeric method that assesses an individual situation in a specific condition that the researcher defines according to the scientific data to address issues that are questionable or are heavily debated among scientists (such as platform switching) that are not feasible to assess in a clinical setting or human population. Our study has assessed the stress distribution around dental implants with two different types of loads (vertical/axial and oblique).

Thus, in contrast to other types of studies, the FEA analysis does not need statistical analysis. Rather, the significance of the study can be derived through comparison of the results with the large amount of data gathered from previous FEAs. Finite element analysis can help clinicians and implant manufacturers to find the most biologically favorable configurations in which dental implants can be constructed in an attempt to reduce the risks of clinical failure.

An in-depth understanding of stress profiles encountered by the implant — and more importantly, in the surrounding jawbone — can be gained through the use of FEA. This increase in the understanding of stress distributions and magnitudes within the implant and surrounding jawbone will aid the optimization of implant design and insertion technique. It is essential that the clinician have an understanding of the methodology, applications, and limitations of FEA in implant dentistry and become more confident in interpreting the results of FEA studies and extrapolating these results to the clinical situation.

9

The FEA is one of the most frequently used methods in stress analysis in both industry and science. It is used for analyzing hip joints, knee prostheses, and dental implants. The results of the FEA computation depend on many individual factors, including material properties, boundary conditions, interface definitions, and the overall approach to the model. It is apparent that the present model is only an approximation of the clinical situation. The application of a 3-dimensional (3D) model simulation with the non-symmetric loading by the masticatory force on a dental implant resulted in a closer approximation of “clinical reality.”

Other limitations of FEA include the following: 1. Individuals vary in the amount and direction of forces exerted during masticatory function. Although a 15-degree angle and 100 N were chosen because they were shown to be comparable to the status in vivo, the actual forces and vectors can vary among individuals (Richter, 1998; Haraldson et al., 1988; Geng et al., 2001). The technique here was used to illustrate the possible differences between a tapered implant and its cylindrical counterpart, with or without platform switching (Richter, 1998). Any changes in force application (direction or amount) would, of course, change the outcome.

2. In some cases, elements are omitted from FEA to simplify the process and make it feasible. The rationale behind the omission of design elements, such as a Morse taper connection system, was because our model was designed to have node sharing between the abutment and implant body.

3. The use of anisotropic properties, rather than the isotropic properties used here for cortical and cancellous bone, may have had an effect on the results compared to actual bone structures (Patra et al., 1998). Because the goal of this study was to investigate the effects on surrounding bone when only two design aspects (implant body shape and platform size) of an implant system were modified, it was more efficient and minimally complicated to use isotropic values instead of anisotropic values.

Therefore, 3D FEA modeling satisfied the criteria of easily depicting stress differences without using unnecessarily complex geometries that were viewed to have an insignificant impact on this study.

4. A situation with 100% bone-to-implant contact was assumed in our model to create a modern model similar to photoelastic models. In contrast, most histometric studies done in vivo have found bone-toimplant contact of 30% to 70% (Pierrisnard et al., 2003; Richter, 1998; Waskewicz et al., 1994). Also, the biomechanical reaction of the jawbone differs for each patient and some micromovement occurs clinically, so the fixed interface between the implant and bone assumed in this and other FEAs does not accurately represent clinical reality.

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5. The jawbone and implants are very complicated structures. It is difficult to establish an accurate and valid 3D finite element model using conventional modeling techniques. Two-dimensional (2D) representations of implants and jawbone structures were often assumed in previous studies, some of which also failed to recognize the difference between the cortical and trabecular bones. As such, the calculated results are often very different from the actual situation for 2D analysis; hence, they cannot be used to guide implant treatment (Canay et al., 1996; Patra et al., 1998; Lewinstein et al., 1995). In addition, an assumption of homogeneous, linear, elastic material behavior for the jawbone is typical of FEAs, which is characterized by a single Young’s modulus and Poisson’s ratio (Lewinstein et al., 1995; Mihalko et al., 1992; Nishihara and Nakagiri, 1994).

This, again, represents a simplification of the actual bone structure.

6. In most research reported to date, axially applied static loads were assumed, instead of the more realistic dynamic, cyclic loads directed at the occlusal angle encountered during mastication (Geng et al., 2001).

7. With regard to implant surface roughness, the finite element method has not been employed widely to evaluate the effect of surface roughness of an implant on the stress profile produced within the surrounding jawbone. Ronold et al. (2003) experimentally analyzed the optimum value for titanium implant roughness in bone attachment using a tensile test. The results supported observations from earlier studies that suggested an optimal surface roughness for bone attachment to be in the range between 3.62 and 3.90 microns. The analysis also indicated that further attachment depended on mechanical interlocking between bone and implant.

There is still a lack of information regarding the mechanical properties of bone tissue with respect to the time-dependent process of structural rearrangement in response to permanent mechanobiologic stimuli. The clinical relevance of numerical methods in defining the biomechanics of dental implants and in emphasizing the necessity of an integrated clinical-mechanical approach must be confirmed through additional research.

The development of finite element analysis studies with improved geometric models using dynamic loading, if possible, with different bone types, in animal experiments, and in longitudinal clinical trials are still necessary.

Conclusion and Recommendations Although tapered implants might result in higher crestal bone stress, a reduced abutment diameter can result in lower stresses, with an inverse relationship to the extent of inward shifting of the abutment. There is still a lack

of information regarding the remodeling that occurs in response to permanent mechanobiologic stimuli. The clinical relevance and reliability of numerical methods in defining the biomechanics of dental implants and in highlighting the necessity of an integrated clinicalmechanical approach must be confirmed by additional research.

A realistic jawbone model, with a wider range of characteristics to reflect differences between individual patients, must be constructed. Computed tomography images, which readily distinguish between cortical and trabecular bone, and computer image processing can be used together to construct a precise 3D geometric model using reverse engineering (George and Rasha, 2001; Marco et al., 1998; Wei and Pallavi, 2002).

The unpredictable biomechanical response of the jawbone to a foreign object, i.e., stress shielding, has not been modeled previously using numeric methods.

Ideally, computer software, together with CT images obtained during the healing process, would be developed to predict the degree of stress shielding in the peri-implant jawbone. This will improve our understanding of jawbone remodeling with different implant placement techniques, designs, and loading conditions.

Alternatively, photoelastic stress analysis might be used to evaluate stress shielding experimentally (Waskiewicz et al., 1994).

Numerous investigations have sought to determine the optimal geometry of the implant body, with mixed results (Pierrisnard et al., 2003; Himmlova et al., 2004).

A new methodology, perhaps involving the use of the application programming interface function of commercial software, might be employed to determine the optimal combination of length, diameter, taper, and implant thread dimensions and configuration for each bone type in all three dimensions (Vena et al., 2000).

When an implant is surgically placed into the jawbone, it is mechanically screwed into a drilled hole of a smaller diameter, resulting in high amounts of stress as a result of insertion torque and because the implant is cutting into the jawbone. As such, the stress condition in the jawbone will change accordingly. The long-term effects of such stresses remain unclear and should be investigated so that undesirable stresses can be minimized.

Acknowledgment We wish to thank Dr. Mehrdokht Najafi for her invaluable help. The authors declare no financial interest in any of the products mentioned in the article.

Rasouli-Ghahroudi et al.: Platform switching in tapered and cylindrical implants

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Gingival Cysts of Adults: Retrospective Analysis from Two Centers in South Brazil and a Review of the Literature Vivian P. Wagner1, Manoela D. Martins1, Marina Curra1, Marco A. T. Martins2 and Maria C. Munerato2 Department of Oral Pathology, Dental School, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil.

2 Department of Oral Medicine, Hospital de Clínicas de Porto Alegre (HCPA/UFRGS), Porto Alegre, Rio Grande do Sul, Brazil.

1

Abstract Gingival cysts of adults are rare developmental cysts, with an incidence of 0.3% among all odontogenic cysts. They are benign, well-defined nodules located on the attached gingiva with a fluid-filled appearance. The aim of the present study was to perform an analysis of gingival cysts in adults diagnosed at an oral pathology laboratory and a hospital pathology service in order to determine the frequency of occurrence of this lesion, and to perform a literature review to correlate the present findings with those described in the literature. This study emphasizes the low frequency of gingival cysts in adults and the importance of gathering clinical, radiographic and histopathological information to define the final diagnosis.

Key words: Odontogenic cysts, gingival cysts of adults, gingival lesions

Introduction Gingival mucosa is under constant irritation from masticatory forces, minor trauma, plaque, calculus and iatrogenic factors. The most common gingival lesions represent tissue reactions to these irritant factors (Buchner et al., 2010). In addition, gingival growths can be the result of underlying systemic disease or drug-induced stimulus (Rossmann, 2011). Gingival lesions have been grouped into types, and the most common are inflammatory, reactive, developmental and neoplastic lesions (Effiom et al., 2011).

Odontogenic lesions, presented as soft tissue growths, can originate from remnants of the dental lamina, known as rests of Serres, located in a supraperiosteal position in the gingiva (Giunta, 2002; Manor et al., 2004; Kelsey et al., 2009). Peripheral odontogenic neoplasms are rare and represent 1.5% of all diagnosed gingival lesions (Manor et al., 2004). Among odontogenic cysts, gingival cysts of adults (GCA) are the only lesions that are exclusive to soft tissue (Neville et al., 2008) and

Correspondence to: Manoela Domingues Martins, Rua. Ramiro Barcelos, 2492, Porto Alegre, RS- Brazil. CEP: 90035-003.

Email: manomartins@gmail.com © International Academy of Periodontology

illustrate a rare developmental cyst, with a low incidence of 0.3% among all odontogenic cysts (Ochsenius et al., 2007). The aim of the present study was to perform an analysis of gingival cysts of adults diagnosed at an oral pathology laboratory and in a hospital pathology service to define the frequency of this lesion, and also perform a literature review and correlate the findings of the present study with those described in literature.

Materials and methods A retrospective analysis was performed at two diagnostic centers of a university in southern Brazil. The histopathological records from 1994 to 2013 of the Clinics Hospital Pathology Service and the histopathological records from 2000 to 2013 of the Oral Pathology Laboratory were retrieved. Data on gender, age, race, location, radiographic and surgical aspects were retrieved, and slides stained with hematoxylin and eosin were reviewed by an experienced pathologist to confirm the histopathological diagnosis.

The MedLine electronic database was searched in English and without a time (year) limitation for any publication about GCA. The search strategy combined MeSH with free text words. The MeSH terms used were “odontogenic cysts, periodontal cysts, gingival diseases” and gingival cyst of adult/gingival cyst of adults were

Wagner et al.:Gingival Cysts of Adults

used as keywords. Articles with a case report or case series of GCA were included and data concerning gender, age, race, location, radiographic and surgical aspects were retrieved.

Results Between 2000 and 2013, 12,971 specimens of oral lesions were submitted for histopathological examination at the Oral Pathology Laboratory of the School of Dentistry. In this time period, one case of GCA (Case 1) was diagnosed in this center, representing 0.007% of all diagnosed cases. At the Pathology Service of Clinics Hospital of Porto Alegre, between 1994 and 2013, 6,222 specimens of oral lesions were submitted for histopathological examination. In this time period one case was diagnosed as GCA (Case 2) representing 0.01% of all diagnosed cases.

Case 1: A 60-year-old Caucasian female patient was referred to Oral Pathology Service of the School of Dentistry presenting with a solitary nodule with a fluid-filled appearance. The first diagnostic hypothesis was of GCA; however, other benign lesions were not excluded because GCA is a very unusual lesion. The differential diagnosis of nodular lesions in gingiva, as in the present case, included peripheral ossifying fibroma, peripheral giant cell granuloma, pyogenic granuloma and peripheral odontogenic keratocyst. An excisional biopsy under local anesthesia was performed and the specimen was submitted for histopathological analysis.

The histopathological exam showed a cystic space cov-

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ered by an epithelium lining consisting of cuboidal and squamous cells with few layers and focal thickenings, confirming the diagnosis of GCA. Case 2: A 75-year-old Caucasian female patient was referred to the Oral Medicine Department at the Clinical Hospital of the Federal University of Rio Grande do Sul for control of burning mouth syndrome. During the intraoral examination a solitary nodule situated on the mucogingival junction in the area of the lower incisors was noted (Figure 1a). The lesion was asymptomatic, firm, slightly depressible, presented with a smooth surface, bluish color and was 5 mm in diameter. The patient could not remember any trauma, recent or past, in this area. Pulp testing indicated that both incisors adjacent to the lesion were vital and no radiograph image was observed (Figure 1b). The main diagnostic hypothesis was GCA, as a lateral periodontal cyst (LPC) was excluded from the differential diagnosis based on the absence of a radiographic finding. An excisional biopsy under local anesthesia was performed. During the surgical procedure, an erosion on the bone surface was noted, leading to root exposure at the mesial part of the lower central incisors. As the defect provoked by the lesion was small, the surgeon decided not to perform any specific treatment in the area. The specimen was submitted for histopathological analysis, which confirmed the diagnosis of GCA (Figure 2a and 2b). One year follow-up revealed no recurrence and the patient reported no symptoms.

Figure 1. Illustration of Case 2. a) Solitary and asymptomatic nodule at the mucogingival junction presenting with a smooth surface and bluish color. b) Radiographic image of lower incisor region revealed no bone involvement.

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Figure 2. Illustration of Case 2. a) Histopathological aspects of the surgical specimen revealed a cystic space covered by an epithelium lining that consisted of cuboidal and squamous cells (H&E, 100 X); b) a few layers with focal thickenings (H&E, 200X).

Literature review A literature review found 157 cases of GCA reported in the English language (Table 1). Concerning sex and race, there is no pronounced predilection: the male:female ratio was 1:1.43 and the white:black ratio was 1:0.76.

The mean age was 49.10 years old, ranging from 18 to 78 years. The mandible was more affected than the maxilla, representing 78.87% of all cases. Radiograph involvement was absent in 78.43% of cases, and bone involvement was present in 47.29% of the cases.

Discussion GCA is an uncommon developmental cyst that occurs in either the free or attached gingival soft tissue. GCA are believed to have an odontogenic derivation (Malali et al., 2012) without an inflammatory origin. Potential odontogenic tissue origins include remnants of the dental lamina (cell rests of Serres; Kelsey et al., 2009; Malali et al., 2012). The present study performed a retrospective analysis of two centers in South Brazil and also a literature review concerning GCA. Our results confirmed that GCA represents a very rare lesion with a

frequency in biopsy services of around 0.01%, (Buchner et al., 1979; Manor et al., 2004).

The typical aspect of GCA described in the literature is similar to both cases presented herein, and consists of a well-defined oval to round, firm and elevated nodule located on the attached gingiva. Usually this lesion presents with slow growth and may not show any symptoms.

Most lesions are small, ranging from 0.5 cm to 1 cm in diameter, and often appeared fluid-filled (Sato et al., 2007; Kelsey et al., 2009; Malali et al., 2012). The literature review performed in this study demonstrates that there is no predilection regarding sex and race for this lesion; however, a pronounced preference for the mandible was noticed. The age of patients ranged from 18 to 78 years old, but most cases were in adults in the 4th and 5th decade of life; no case report was found in the English literature of GCA in childhood. GCA can produce a radiographic radiolucency as a result of pressure resorption of the adjacent bone caused by the lesion (Manor et al., 2004); however, less than 20% of all cases described in the literature presented a radiographic image.

Based on clinical aspects the differential diagnosis of GCA includes other lesions presenting as gingival swellings such as fibroma, peripheral ossifying fibroma (POF), peripheral giant cell granuloma (PGCG), pyogenic granuloma (PG) and bone lesions situated in the periapical area (Kelsey et al., 2009). Fibroma can be distinguished based on its clinical aspect of a nodular lesion with a firm consistency and the same color as surrounding tissue (Neville et al., 2008). Both POF and PGCG have a periodontal ligament origin; they are usually located near the gingival margin and present with a firm consistency (Neville et al., 2008; Barot et al., 2013).

Pyogenic granuloma represents an exuberant growth of vessels associated with trauma and has a bleeding tendency (Singh et al., 2013). Periapical lesions, either inflammatory or tumoral, can eventually cause cortical disruption and present with soft tissue manifestations (Khanna et al., 2011). Clinicians often include mucocele incorrectly as a differential diagnosis because of the fluid appearance of the GCA; however, mucoceles do not occur in the attached gingiva (Giunta, 2002). Despite being a rare lesion, clinicians make a correct clinical diagnosis 50% of the time (Giunta, 2002) given that the clinical aspects of this lesion are very distinctive.

The most important lesion to establish a differential diagnosis is lateral periodontal cyst (LPC). The LPC is also a development odontogenic cyst and the GCA is considered to be the soft tissue counterpart of the LPC (Neville et al., 2008). The main difference between them is that LPC arises from proliferation of the dental lamina within bone, while the GCA arises from dental lamina remnants in soft tissue (Tolson et al., 1996), thus the GCA presents exclusively in soft tissue and the LPC is an intraosseous lesion. The histological appearance, location and

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Table 1. Demographic and clinical information about GCA (adapted from Kelsey et al., 2009) Study

This study Anonymous, 2012 Malali et al., 2012 Ojha et al., 2010 Kelsey et al., 2009 Santos et al., 2009 Noonan et al., 2008 Sato et al., 2007 Anonymous, 2006 Damm and Fantasia, 2006 Cunha et al., 2005 Hegde and Reddy, 2004 McGuff et al., 2003 Giunta, 2002 Cairo et al., 2002 Bell et al., 1997 Tolson et al., 1996 Fardal and Johannessen, 1994 Haring, 1994 Nxumalo and Shear, 1992 Dent et al., 1990 Shade et al., 1986 Wescott et al., 1984 Gregg and O’Brien, 1982 Brannon and Brasher, 1981 Wyscocki et al., 1980 Buchner and Hansen, 1979 Mesa, 1975 Moskow and Weinstein, 1975 Melhado et al., 1973 Young et al., 1973 Moskow et al., 1970 Reeve and Levy, 1968 Henning, 1968 Amar, 1966 Zerden, 1966 Alexander and Griffith, 1966 Mabile, 1965 Grand and Marwah, 1964 Sherman, 1963 Bruce, 1962 Holder and Kunkel, 1958 Kennedy, 1957 Bhaskar and Laskin, 1955 Ritchey and Orban, 1953 Ramfjord, 1953 Cahn, 1936 Total

N

2 1 1 1 1 1 1 1 1 1 1 1 1 22+ 3 8 1 1 1 14 2+ 2+ 2 2 1 10 33 2 3+ 3 1 2 4 1 1 2+ 2 1 1 1 2 1 1 3 8++ 1 1 157

Gender Max:Mand Age/ M:F Mean age 0:2 F M F M F NR M F M F M M 6:15 0:3 1:7 M F F 7:7 M M M 1:1 M 5:4* 14:19 0:2 2:0 NR M NR 1:3 F F M 2:0 F NR F 0:2 M M 0:3 3:2 F NR 57:82

0:1* Mand Max Mand Mand Max Mand Mand Max Max Mand Mand Mand 2:16* 0:3 1:7 Mand Mand Mand 6:8 0:2 0:2 0:2 1:1 Max 1:7* 9:24 1:1 0:3 NR Mand NR 0:4 Mand Mand 0:2 0:2 Mand Max Mand 0:2 Mand Max 0:3 2:5* NR NR 30:112

67.5 38 16 76 54 42 NR 78 56 44 69 18 45 52 46 51 50 41 47 NR 64 47 46 52 40 51 48 45 NR NR 68 NR 61 53 19 52 45 49 62 58 52 40 30 47 34 60 NR 49.10

Race W:B 2:0 W NR B B NR NR NR B NR NR NR NR 0:1* 3:0 6:2 B W NR NR NR B B NR B NR NR 1:1 NR NR NR NR 4:0 NR W B 1:1 B B B 2:0 NR W 0:3 2:0* NR NR 25:19

Radiographic Bone involvement involvement Y:N Y:N 0:1* N N N Y N NR N NR NR Y N N 0:22 0:3 NR Y NR NR NR 2:0 0:2 NR 1:1 N NR 2:31 1:1 0:3 NR N 1:1 4:0 N N 1:1 1:1 Y Y Y 0:2 Y NR 2:0 NR NR NR 22:80

1:0* NR Y NR Y NR NR Y NR NR Y NR NR NR 0:3 NR Y NR NR NR 0:2 1:1 1:1 0:2 Y NR 10:23 NR 3:0 NR N NR 4:0 N Y Y 1:1 Y Y Y 0:2 Y 1:0 1:2 NR NR NR 35:39

*Clinicopathological information was not complete for all cases. +Two cysts in the same patient. ++Three cysts in the same patient. M:F, male:female; Max:Mand, maxilla:mandible; W:B, white:black; Y:N, yes:no; NR, not reported.

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clinical behavior of both lesions are very similar. In some cases there is both radiographic and gingival involvement and the differential diagnosis is hampered because it is hard to establish if it is a GCA causing bone resorption or an LPC eroding the cortical bone (Tolson et al., 1996; Kelsey et al., 2009). Radiographic analysis is important to distinguish both lesions: in the present literature review 25 cases of GCA presented with a radiographic image that could suggest an LPC. In cases in which GCA is causing cortical resorption, it is possible to see only a diffuse radiolucency, whereas LPC appears as a well-defined round or ovoid radiolucency, often with a sclerotic radiopaque margin, (Tolson et al., 1996; Shear and Speight, 2007). It is important to state that 78.43% of the cases reviewed herein revealed no abnormalities in radiographic examination, supporting that the absence of radiographic image can indicate a GCA, although when an image is present, GCA must not be excluded from the differential diagnosis and a deeper analysis has to be performed.

Another situation that can contribute to the differentiation of GCA from LPC is the surgical aspect.

Gingival cysts of adults usually present against the labial bone, whereas an LPC is situated within the bone (Giunta, 2002; Shear and Speight, 2007). Although the present literature review indicated that 47.29% of cases presented with bone involvement, root exposure related to GCA, as founded in Case 2, is a particularly rare finding (Kelsey et al., 2009). The lesion can involve the alveolar bone surface and a “saucer-like” defect might be produced in the lingual or buccal plate (Malali et al., 2012). When necessary, different approaches might be used to achieve resolution of the lesion-associated osseous defect, such as bone allograft, collagen membrane (Kelsey et al., 2009) and hydroxyapatite bone substitute (Malali et al., 2012). In Case 2 the defect provoked by the lesion was small and the use of these therapies was judged unnecessary during the surgical procedure.

Histologically GCA usually presents with a narrow epithelium, closely resembling reduced enamel epithelium with 1-3 layers of flat to cuboidal cells with darkly staining nuclei. Focal thickenings of epithelium may occur as plaques of glycogen-rich clear cells. The junction between the epithelium and the underlying connective tissue is tenuous and easily peels off, leading to an epithelial discontinuity. Generally, the lesion is unicystic and the connective tissue is free of inflammation (Tolson et al., 1996, Shear and Speight, 2007). The histopathological aspect of GCA is exactly the same as that of an LPC; for that reason it is of great importance to provide clinical and radiographic information in the biopsy file to allow the pathologist to make a correct diagnosis. Surgical excision is usually the curative treatment and no recurrence has been reported in the literature. Still, it is important to maintain clinical and radiographic follow-up of the patient (Tolson et al., 1996; Kelsey et al., 2009).

Conclusion Despite being a rare lesion, knowledge about GCA allows dental practitioners to establish a correct differential diagnosis for focal gingival swelling. This study emphasizes the low frequency of occurrence of GCA and the importance of gathering clinical, radiographic and histopathological information to make a correct diagnosis between GCA and LPC, as well as other gingival lesions.

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Journal of the International Academy of Periodontology 2015 17/1: 20–31

A Novel Surgical Approach for Treatment of Class II Furcation Defects Using Marginal Periosteal Membrane Hala H. Hazzaa1, Heba El Adawy2 and Hani M. Magdi3 Department of Oral Medicine, Periodontology, Diagnosis and Radiology, and 2Department of Oral Biology, Faculty of Dental Medicine, Al Azhar University (Girls Branch); 3Regional Center for Microbiology and Biotechnology (RCMB), Al Azhar University (Boys Branch), TEM-Unit, Cairo, Egypt 1

Abstract Objectives: This study was designed to describe and evaluate the use of a vascularized marginal periosteal barrier membrane (MPM) harvested by a semilunar incision, alone or combined with a bone graft, in treatment of class II furcation defects in mandibular molars, compared to open flap debridement (OFD).

Methods: Thirty class II furcation defects in mandibular molars were randomly assigned into three equal groups: Group I included OFD, Group II included defects treated with MPM, and Group III consisted of defects treated with MPM after applying demineralized freeze-dried bone allograft (DFDBA). At baseline and 6-month follow-up, vertical probing depth (VPD), clinical attachment level (CAL) measurements, along with a radiographic measurement of bone height (BH), were obtained for each defect. Transmission electron microscopy (TEM) was used for further evaluation of the histological changes associated with gingival samples related to each line of treatment.

Results: Both Groups II and III reflected significant favorable outcomes in all the assessed parameters compared to OFD. A non-significant difference was found between both groups regarding VPD, while significant improvement in CAL and BH were detected in Group III (p ≤ 0.05). Favorable histological findings were also noticed in the test groups, with more improvement in Group III. Conclusion: Placement of a vascularized MPM as a barrier membrane, using a semilunar incision, demonstrated a significant improvement in both clinical and histological outcomes of class II furcation defects in lower molars. When it was combined with DFDBA, a meaningful difference was found with regard to early wound healing and gain in CAL and BH.

Keywords: Periosteal autogenous membrane, class II furcation defects, demineralized freeze-dried bone allograft, guided tissue regeneration.

Introduction Treatment of furcation lesions is one of the most challenging tasks in periodontal therapy. The furcal anatomical features (e.g., small ridges, peaks and pits forming convexities and concavities) offer limited access for routine periodontal debridement. The presence of accessory canals in the furcation region in up to 25% of permanent molars, as well as

Correspondence to: Hala H. Hazzaa, 2 Farid Nada St., Benha, Qalubia, Egypt. Mobile: +02 01014129297, Telephone: +02 0133249414, E-mail address: hala.hazzaa@yahoo.com

the presence of enamel projections in 29% of mandibular and 17% of maxillary molars, further complicates furcation management (Pradeep et al., 2009).

In class II furcation involvement, the treatment is more uncertain. Although it was shown that this type of defect could be successfully treated by regeneration, the predictability related to the treatment type remains a major issue.

Therefore, proceeding with caution is definitely advised (Avila et al., 2009). It should be remembered that spontaneous and predictable regeneration following meticulous debridement is possible, especially with the availability of bone morphogenetic proteins (BMPs) and enamel matrix derivatives (Sánchez-Pérez and Moya-Villaescusa, 2009).

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However, it might be inadequate for the treatment of deep pockets or wide circumferential furcation defects (Verma et al., 2013).

Tunneling has been proposed as a conservative alternative in cases of furcation class II. However, longterm survival is not ensured, as many complications (among which root caries predominates) may arise after treatment, compromising tooth prognosis (Avila et al., 2009). Root resection is a conservative therapeutic option indicated in some furcation defects to provide a better environment and maintain the tooth. Although it was shown that root-resected teeth have good longterm survival rates, previous studies (Langer et al., 1981; Buhler, 1988), showed that root-resected teeth had survival rates of 85% and 68% after 5 and 10 years, respectively. Therefore, it can be acknowledged that a root-resected tooth has less periodontal support and a less favorable prognosis than a healthy one (Avila et al., 2009).

To increase the predictability and clinical success of regenerative therapy, factors related to the patient, furcation, surgical treatment, and postoperative period should be also considered. The rationale for guided tissue regeneration is to exclude gingival epithelium and connective tissue from the alveolar bone and root surfaces by placing a physical barrier, thus creating areas into which progenitor cells from the periodontal ligament and alveolar bone can migrate. Guided tissue regeneration has many indications in periodontal therapy, among the most important being treatment of class II furcation lesions. However, the resulting improvements are modest and variable. The revascularization of any flap may be further compromised by blockage of the potential blood supply from the periodontal ligament and bone defect to the connective tissue flap by a membrane (Novaes et al., 2005).

Perhaps the most important factor affecting guided tissue regeneration outcome is the periosteal isolation (Gamal and Iacono, 2013).

Periosteum is an attractive alternative to the existing barrier techniques, because it is biologically accepted.

The utilization of an autogenous marginal periosteal membrane (MPM) apical to the furcation lesion provides several clinical benefits, among which is that a second graft donor site is not required. The vitality of the barrier may be ensured by a proper blood supply from the base of the mucoperiosteal flap, and possibly the gingival flap itself, which may further modify the cellular dynamics of the wound in favor of clinical outcome. The supposed physiologic mode of growth factors delivery that could be achieved by periosteal osteoprogenitor cells offers an advantage to the use of MPM as a biologic barrier, representing a promising way to get a more predictable amount of periodontal regeneration (PR; Gamal et al., 2010).

JIAP 14-013-Hazzaa.indd 21

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Periosteum is a highly vascular connective tissue comprised of two distinct layers: a thick, outer nonosteogenic fibrous layer and a thin inner cellular osteogenic-cambium layer. It was reported that reverting the periosteum such that the fibrous layer is in contact with the defect provided reliable results in the treatment of class II furcations. However, histological findings have questioned the cellular differentiation in the defect area, as bone-forming cells migrated from the inner to the outer layer of periosteum during healing (Amicarelli and Alonso, 1999). Hence, it is preferable to find a technique that directly uses the inner cambium, known to have the potential to stimulate bone formation (Ito et al., 2001).

In 2003, Murphy and Gunsolley concluded that use of augmentation materials with physical barriers enhances the regenerative outcome in furcation treatment. They function as a scaffold to ensure clot stabilization and to provide a space for regeneration.

Allogeneic or autogenous materials were used with no significant differences. However, because of the limited amount of intraoral donor bone, it is preferable to use demineralized freeze-dried bone allograft (DFDBA) in large defects (Abolfazli et al., 2008).

Therefore, this study was designed in an attempt to describe and evaluate the use of a vascularized MPM, harvested by the semilunar incision, in treatment of mandibular class II buccal furcation defects. Clinical and histological assessments were undertaken to evaluate MPM, with and without DFDBA, versus open flap debridement (OFD).

Materials and methods This study was divided into two parts: the first part dealt with the clinical efficacy of MPM in treatment of class II furcation defects in chronic periodontitis patients, either alone or combined with DFDBA, versus OFD. The second was a qualitative part aimed at evaluating the potential induced structural changes of the gingiva with each line of treatment.

Pre-surgical therapy and patient selection Twenty-six subjects (15 women and 11 men) participated in the study, ranging in age from 37 to 52 years (mean = 42.6), diagnosed with chronic periodontitis according to clinical and radiographic findings (Armitage, 1999). They were selected from the outpatient clinic of the Department of Periodontology, Faculty of Dental Medicine, Al Azhar University (Girls Branch).

Inclusion criteria Patients were screened for the following criteria: 1) the presence of a class II buccal furcation defect in a mandibular molar according to Glickman’s classification (1953); 2) no systemic diseases that could influence

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the outcome of the therapy, as evaluated by modified Cornell medical index (Abramson, 1996); 3) good compliance with plaque control instructions following initial therapy, using the plaque index values (0 or 1) according to Silness and Löe (1964); 4) vertical probing pocket depths (VPD) of ≥ 5 mm and clinical attachment levels (CAL) ≥ 4 mm four weeks following initial therapy; 5) gingival margin positioned coronally to the furcation fornix. Each subject had undergone initial periodontal therapy without occlusal adjustment (as such adjustment was not indicated in any of the cases).

Exclusion criteria Smoking patients, former smokers, pregnant and lactating females, and previously treated subjects, along with those taking oral contraceptives, were excluded from participating in this study. Patients were also excluded if they presented with inadequate compliance with the oral hygiene maintenance schedule.

Before acceptance into the study, each patient received a brief description of the investigation and provided signed informed consent. The Ethical Committee of Al Azhar University approved the experimental protocol.

Patient grouping All participants were re-evaluated 4 weeks following the initial therapy to confirm the need for regenerative furcation reconstructive surgery for the selected sites (Nejad et al., 2004). A total of 30 defects were randomly assigned, using a computer-generated table, to one of the following equal treatment groups (n = 10 defects/ group) in a parallel, double-masked design. Group I (control) included defects treated with OFD, Group II (Test 1) included defects treated with MPM, and Group III (Test 2) included defects treated with MPM plus DFDBA.

Clinical parameters Baseline data for all sites were collected just prior to the surgical phase of treatment. Soft tissue measurements included VPD and CAL measurements using a calibrated periodontal probe with William’s markings to the nearest millimeter as the distance from the base of the pocket to the gingival margin and the cementoenamel junction (CEJ), respectively. Measurements were recorded at three sites for each tooth: mesio-buccal line angle, disto-buccal line angle and mid-buccal line angle.

The mean of the three readings was taken. The precise position of the periodontal probe was recorded using custom-made acrylic occlusal stents.

A computer program (Dür DBS Win image processing software) for image processing and manipulation was used to evaluate the linear measurements related to the changes in each defect bone level from routine diagnostic standardized periapical views, using the long cone/paralleling technique and aiming devices.

All radiographs were digitized using a flatbed scanner with a scanning resolution of 600 dpi (UMAX-A8TRA 12208). In each digitized radiograph, three lines were drawn from the furcation roof to the base of each defect, representing the defect bone height (BH), and the means were calculated.

Clinical and radiographic measurements (Figures 1a, 1b) were re-assessed six months after therapy by one calibrated masked examiner to evaluate the quantitative changes in each defect. Intra-examiner reproducibility was assessed with a calibration exercise performed on two separate occasions 48 hours apart. Calibration was accepted if ≥ 90% of the recordings could be reproduced within a difference of 1.0 mm.

Figure 1. a) A preoperative periapical radiograph of the class II furcation defect; b) A periapical radiograph of the same site taken at six months.

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Surgical protocol One surgeon performed all surgeries. For Groups II and III, following administration of a local anesthetic agent (lidocaine 2% with epinephrine 1:80,000), two vertical releasing incisions that extended into the alveolar mucosa were placed no closer than one tooth mesial and distal to the selected tooth. An intrasulcular incision was then performed to join the vertical incisions. A partial thickness flap was raised at the buccal aspect of the tooth using a Bard-Parker blade No. 11. Granulation tissue was removed, and root surfaces were thoroughly scaled and planed with hand and rotary instruments. A high-speed finishing bur was used to remove any enamel projections.

Following the dissection, periosteum remained on bone and a partial thickness of the gingival connective tissue remained on the periosteum. A semilunar incision was made to fenestrate the periosteum 3-4 mm apical to the

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defect osseous margin, excluding a sufficient mucoperiosteal insertion zone coronal to the incision (Figures 2a, 2b); followed by careful elevation of periosteum using a mucoperiosteal elevator (Figures 3a, 3b).

In Group III, furcation defects were filled with DFDBA (SurossTM manufactured by Hans Biomed Corp., Sungdong-gu, Seoul, Korea). The periosteum was then coronally moved to seal the furcation lesion such that the cambium layer was juxtaposed to the exposed furcation, (Figure 4a,b). Using a sling-suture technique, a bioresorbable ligature was used to tightly secure the coronal portion of the periosteum to the tooth. Finally, the flap was coronally repositioned and secured with interrupted sutures using 4-0 black silk suture. In Group I, full thickness mucoperiosteal flaps were elevated, then replaced after defect debridement and secured with interrupted suturing.

Figure 2. a) A diagram showing the periosteal barrier semilunar incision design. Notice that the design excludes a mucoperiosteal insertion zone coronal to the osseous margin. b) A clinical photograph showing the semilunar incision using Bard-Parker blade No. 11 to fenestrate the periosteum 3-4 mm apical to the osseous margin of the defect, excluding a sufficient mucoperiosteal insertion zone coronal to the osseous margin to ensure blood irrigation.

Figure 3. a) A diagram showing the elevation of the periosteum using the mucoperiosteal elevator; b) A clinical photograph showing the careful elevation of periosteum using the mucoperiosteal elevator.

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Figure 4. a) A diagram showing the coronal direction of mobilizing the periosteum (the white arrows), to seal the defect such that the cambium layer is juxtaposed to the exposed furcation; b) A clinical photograph showing the coronal mobilization of the periosteum.

Post-operative care A platinum foil was used to cover the operation site, followed by a perio-pack. Removal of sutures was done 14 days after surgery. Analgesics (400 mg ibuprofen) were used for patients experiencing post-surgical discomfort.

Patients were placed on an infection control program including seven days of systemic antibiotic therapy (amoxicillin-clavulanic acid, 2 gm/day) and 6 weeks of chemical plaque control (0.12 % chlorhexidine gluconate rinses, twice daily).

Patients were instructed to forego mechanical plaque control 2 weeks post-operatively. Oral hygiene procedures were then gently initiated in the surgical areas with a soft brush. Professional prophylaxis for plaque removal was performed at weekly intervals for 4 to 6 weeks, then monthly until the end of the study.

Histological study Gingival specimens were taken from chronic peritonitis patients (7 samples in each group) who had buccal furcation-affected mandibular molars diagnosed as hopeless for dental-periodontal reasons and designated for extraction. Each of the furcation defects was subjected to OFD, MPM or MPM+DFDBA. On day 10 after surgery, teeth were extracted and gingival biopsy specimens were obtained full length along the dentogingival region and immediately above the alveolar crest (Lafzi et al., 2007). The gingival tissues were carefully dissected and cut into 1 x 1 mm cubes, then placed in labeled jars for histological evaluation.

Preparation for transmission electron microscopic examination (TEM) Specimens for TEM examination were prepared according to Bancroft and Stevens (1982). Fixation was done by immersion of the specimens in a mixture of 2.5% glutaraldehyde and 10% formaldehyde (F/G solution) for 24- 48 hrs (Dard et al., 1989). Then, specimens were

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washed several times in phosphate buffer solution with pH 7.2 – 7.4, post-fixed in 1% osmium tetroxide for 1 hr, and washed again in phosphate buffer. The specimens were passed through ascending concentrations of ethyl alcohol for dehydration. They were then infiltrated and embedded in flat rubber molds filled with embedding resin (Epon 812). After polymerization, the blocks were cut into semi-thin sections (1 µm) with a glass knife via ultramicrotomy. Sections were then mounted on glass slides and stained with 1% toluidine blue. Certain areas of interest were selected for ultrathin sectioning. Ultrathin sections were obtained at 60 nm using a diamond knife and placed/collected on a grid of copper. Grids were stained with uranylacetate. The grids, with the specimen side down, remained in 4% uranyl acetate for 25 minutes and were then rinsed in a series of four beakers of pure water. After rinsing, the grids were then stained with 1% lead citrate for 5 minutes and rinsed again in pure water. The specimens were examined with a JEOL-Japan 1010 TEM and photographed using an AMT XR40 digital camera with 2k x 2k pixels at the Regional Center for Mycology and Biotechnology (RCMB)-Al Azhar University.

A single examiner performed examination of TEM micrographs after masking the group number to make the evaluation unbiased.

Statistical analysis Clinical data were presented as mean and standard deviation (SD) values. Kruskal-Wallis test was used to compare between the three groups. Mann-Whitney U test was used in the pair-wise comparisons between the groups. The significance level was set at p ≤ 0.05. Statistical analysis was performed with SPSS 16.0 (Statistical Package for Scientific Studies, SPSS, Inc., Chicago, IL, USA) for Windows.

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Results Clinical parameters All patients completed treatment and post-treatment phases successfully, and healing was satisfactory. Before treatment, there was no statistically significant difference between the three groups in all parameters. Changes in PD, CAL and BH are shown in Table 1.

At 6 months postoperatively, the mean percentage of reduction in PD in Group I was 28.7% ± 18.3, 60% ± 8.6 in Group II, and 57.3% ± 6.8 in Group III (p < 0.001), respectively. At the end of the study, the statistically significantly lowest percentage reduction was shown in Group I, while a non-significant difference was found between Groups II and III. The mean percentage of reduction in CAL in Groups I, II and III at 6 months was 29.0% ± 23, 63.7% ± 8.8 and 77% ± 13.6, respectively (p < 0.001). Concerning the post-operative mean percentage of changes in BH, Groups I, II and III showed a reduction of 11.9% ± 10.8, 59.7% ± 13.4 and 67.2% ± 8.5 at 6 months respectively, (p < 0.001). Group III showed the statistically significantly highest mean percentage reduction both in CAL and BH, followed by Group II. Descriptive histology The epithelial phase For Group I, severe ultra-structural alterations were detected, while the orientation of epithelial cell layers was more or less clear. The most common feature was represented by vacuolization, edema and interruption of intercellular cell junctions.

The basal lamina was obviously corrugated and interrupted in definite small areas along its course. The basal epithelial cell membranes appeared irregular and severely corrugated.

The cytoplasmic organelles showed severe vacuolization and hyalinization. The intermediate cells appeared compressed with wide extracellular matrix (ECM). Superficially, the cells

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were very pyknotic and no keratin flakes were detected (Figure 5a). However, enhanced ultra-structural features were noticed in Group II. The cellular membranes were well defined but irregular. The cytoplasmic components showed moderate degrees of hyalinization and vacuolization (Figure 5b). In Group III, more favorable features were reflected. The epithelial cell layers had a regular shape and orientation along the different areas of gingival epithelium. Their cell membranes showed clear, regular and smooth outlines. Their nuclei were markedly open-faced with regular nuclear membranes and chromatin distribution. The intercellular junctions, mostly desmosomes, were numerous and dominant, especially between the basally situated cells, with better configuration (Figure 5c).

The connective tissue phase In Group I, fibroblasts appeared shrunken and ovoid, with marked reduction in cytoplasmic and nuclear volume and short cytoplasmic extensions. The cytoplasm appeared hyalinized with poorly defined cytoplasmic organelles. Dilated and irregular nuclear membranes with chromatin clumping were observed. The intercellular junctions between the fibroblastic cell processes were completely lost. The ECM expressed dispersed areas of hyalinization, vacuolizations and dilated blood vessels.

Some transversal and longitudinal collagen fibers were seen extra-cellularly (Figure 6a). In Group II, fibroblasts preserved their spindle shape with normal cytoplasmic process. Numerous longitudinal and transverse collagen fibers were proliferating among the ECM and in close proximity to fibroblasts (Figure 6b). In Group III, fibroblasts possessed favorable morphology with normal cytoplasmic processes and organelles, such as prominent amounts of rough endoplasmic reticulum and mitochondria. Densely packed collagen bundles were detected close to the fibroblastic cell processes (Figure 6c).

Table 1. The means, standard deviation (SD) values and results of comparison among the three groups.

Variable

VPD

CAL

BH

Time Baseline 6 months % reduction Baseline 6 months % reduction Baseline 6 months % reduction

Group I

Group II

Group III

Mean

SD

SE

Mean

SD

SE

Mean

SD

SE

4 2.8a 28.7b 3.8 2.8a 29c 5.4 4.8a 11.9c

0.9 0.8 18.3 0.8 1.2 23 1.1 1.2 10.8

0.3 0.2 5.8 0.2 0.4 7.3 0.3 0.4 3.4

3.6 1.4b 60a 3.8 1.3b 63.7b 5 2b 59.7b

1.4 0.5 8.6 0.8 0.5 8.8 0.9 0.7 13.4

0.5 0.2 2.7 0.2 0.2 2.8 0.3 0.2 4.3

3.8 1.6b 57.3a 4 1b 77a 5.8 1.9b 67.2a

1.2 0.5 6.8 0.7 0.7 13.6 0.8 0.4 8.5

0.4 0.2 2.2 0.2 0.2 4.3 0.2 0.2 2.7

p value 0.668 0.001* <0.001* 0.748 0.003* <0.001* 0.215 <0.001* <0.001*

*Significant at p ≤ 0.05. Means with different letters (a, b and c) are statistically significantly different. VPD, vertical probing depth; CAL, clinical attachment level; BH, bone height

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Figure 5a. An electron micrograph of Group I (open flap debridement only) showing basal epithelial cells with irregular cell membrane (CM), irregular nuclear membrane (NM), chromatin clumping (C), vacuolized cytoplasm (V), vacuolized intercellular cell junctions (CJ), basal lamina (BL) interrupted (arrow), anchoring fibers (AF), lamina propria (LP). Original magnification 12000X.

Figure 5b. An electron micrograph of Group II (open flap debridement plus marginal periosteal barrier membrane) showing basal epithelial cells, cell membrane (CM), enhanced nuclear membrane (NM), peripheral chromatin (C), central nucleolus (N), vacuolized intercellular cell junctions (CJ), desmosomes (D).

Original magnification 10000X.

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Figure 5c. An electron micrograph of Group III (open flap debridement plus marginal periosteal barrier membrane after applying demineralized freeze-dried bone allograft) showing basal epithelial cells with regular smooth nuclear membrane (NM), open-faced central nucleus (N), less vacuolized intercellular cell junctions (CJ), desmosomes (D) and swollen mitochondria (M). Original magnification 6000X and 10000X.

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Figure 6a. An electron micrograph of Group I (open flap debridement only) showing fibroblastic cell with short cytoplasmic process, irregular nuclear membrane (NM), peripheral and central chromatin condensation (C), hyalinized reduced cytoplasmic volume (CV). Original magnification 8000X and 12000X.

Figure 6b. An electron micrograph of Group II (open flap debridement plus marginal periosteal barrier membrane) showing spindle shaped fibroblastic cell with normal cytoplasmic process, irregular nuclear membrane (NM), swollen cytoplasmic organelles, prominent rough endoplasmic reticulum (RER), extracellular matrix (ECM), collagen bundles (CB). Original magnification 10000X.

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Figure 6c. An electron micrograph of Group III (open flap debridement plus marginal periosteal barrier membrane after applying demineralized freeze-dried bone allograft) showing fibroblastic cell with normal cytoplasmic process (CP), open faced nucleus (N), rough endoplasmic reticulum (RER), mitochondria (M), extracellular matrix (ECM). Original magnification 6000X and 10000X.

Discussion The regeneration of class II furcation lesions, although possible, is not considered a totally predictable procedure, especially in terms of complete bone fill. Furcation morphology may restrict access for adequate debridement and may have a reduced source of available cells and blood supply from the periodontal ligament and bone defect (Novaes et al., 2005).

There are several regenerative techniques, used alone or in combination, considered to achieve PR (Verma et al., 2013).

This study was conducted to describe and evaluate the use of MPM harvested for the first time by the semilunar incision, with and without DFDBA, for treating class II buccal furcation defects, compared to OFD. Coronally positioned flaps may have the advantage of using the periosteum as a barrier membrane. However, if the PD is â&#x2030;Ľ 5 mm in the furcation area, the flap tissue cannot be successfully coronally positioned. In the pocket area, a pathological transformation occurs of the flap tissue into a pocket wall; thus, the periosteum may get infected and destroyed with a defective regenerative ability. Therefore, periosteum displacement techniques are much preferred (Verma et al., 2011). In terms of viability, the environment of the recipient site less affects a vascularized periosteum than a free periosteum. Besides, it does not require a second operation, and so there is less surgical trauma, fewer post-operative complications and better patient satisfaction (Krishna and Vijaya, 2012).

However, periosteum-harvesting techniques are usually accompanied by some technical difficulties such as the complexities of surgery, they are time consuming, and need a skillful operator to protect the membrane from laceration (Verma et al., 2011). Importantly, it has been reported that

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bone formation is affected by the degree of surgical damage to the periosteum and the form of the periosteum while harvesting it (Cohen and Lacroix, 1955). In this respect, we can declare that our novel approach is simple and time saving, with careful handling of the MPM through blunt dissection. A recent immunohistochemical study was conducted to quantify human periosteal cells (Frey et al., 2013).

The authors reported that all stained cells were located in the inner cambium layer, and mostly consisted of stromal stem cells and osteoblastic precursor cells. Cells positive for markers of osteoblast, chondrocyte, and osteoclast lineages were also found. In the present study, an MPM harvested by the semilunar incision was coronally mobilized such that the cambium layer was juxtaposed to the exposed furcation.

Accordingly, the cambium layer may directly work to initiate and drive the cell differentiation process of bone repair, as suggested by Grover et al. (2012).

Our approach seems to have an additional advantage related to the surgical stimulating effect secondary to the forceful displacement of the periosteum. In accord, Goldman and Smukler (1978) proposed the transfer of a pedicle flap with stimulated periosteum, using a needle before graft transplantation, to enhance the graft healing potential over the root. They further studied stimulated periosteal pedicle grafts in dogs, concluding that the healing of the stimulated flaps was accompanied by the formation of a relatively short dentogingival epithelium, cementogenesis, and new connective fiber insertion into cementum (Goldman et al., 1983).

Regarding the clinical assessment, none of the investigated parameters in all study groups showed any statistical difference at baseline, thus ensuring the same starting point for all the tested procedures. The clinical parameters used in this study were chosen according to the 1989 World

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Hazzaa et al.:A Novel Surgical Approach for Treatment of Class II Furcation Defects

Workshop in Clinical Periodontics. A 6-month follow-up period was chosen; although it may be too short to fully evaluate the effect of periodontal therapy, this seemed to be the standard time frame for this type of research (Hartman et al., 2004).

In Group II, the absolute values of the observed added benefits at the end of follow-up were 1.4 ± 0.5 mm for PD and 1.3 ± 0.5 mm for CAL. Our results confirm findings described by Gamal and Mailhot (2008), where clinical attachment gain and pocket resolution were achieved using marginal periosteal pedicle flaps and proved superior to treatment with OFD. Our results are also supported by the findings of Graziani et al. (2011), who reported that conservative surgery provides an additional benefit compared with closed debridement alone in treatment of intra-bony defects. However, the outcomes were generally inferior with respect to the regenerative techniques. Nevertheless, the costs of regenerative surgery are significant. In this context, our proposed approach is multi-advantageous; periosteum is safe, biologically accepted, highly regenerative (owing to the structural and molecular values of periosteum), and inexpensive (being a patient’s own), in agreement with Gamal et al. (2010).

In this clinical trial, the quantification of bone fill by radiographic analysis was preferable to re-entry procedures, as well as more convenient for the patients. In addition, the new connective tissue attachment may be disturbed and replaced by a long junctional epithelium as a consequence of surgical re-entry. Crestal bone resorption may also occur as a result of the re-entry procedure (Sullivan et al., 2000).

In Group II, the observed added benefit was 2.0 ± 0.7 mm of BH; a statistically significant value compared to OFD. Similar results were reported by some investigators following application of MPM in mandibular class II furcation defects (Amicarelli and Alonso, 1999). This could be attributed to the periosteum potentiality to stimulate bone formation when used as a graft material (Mahajan, 2012). Other researchers have shed light on the critical roles of BMPs, fibroblast growth factor, platelet-derived growth factor and inflammation signaling in periosteal-mediated bone regeneration, fostering the path to novel approaches in bone-regenerative therapy (Lin et al., 2013).

Reviewing data published from studies carried out only on humans, the conclusions indicated that in furcation defects, better results are obtained with the combination of a bone grafting material plus a membrane (Alpiste-Illueca et al., 2006). Moreover, Bowers et al. (2003) concluded that a successful clinical closure of class II furcations was achievable following combination therapy with an expandedpolytetrafluoroethylene membrane and DFDBA. Furcations with vertical or horizontal bone loss of ≥ 5 mm responded with the lowest frequency of complete clinical closure.

Nevertheless, complete furcation closure was achievable in 50% of molars with extensive bone loss. In agreement with that, Group III showed a more favorable outcome with the combined use of a vascularized MPM with DFDBA.

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The enhanced improvement of the combined treatment group might be attributed to the unique action of MPM in bone healing (Malizos and Papatheodorou, 2005) when coupled with DFDBA that has a potential role in augmenting the healing process. It acts as a spacemaker for the blood clot and prevents barrier collapse in the osseous lesion, allowing osteoconduction for new bone formation (Zenobio and Shibli, 2004).

Additionally, numerous animal experiments indicated that demineralization and freeze-drying of cortical bone allograft greatly enhanced its osteogenic potential.

However, it was noted that the allograft can provide only initial mechanical support of the regenerative process.

Preparation of a bone graft by freezing or radiation largely destroys its vital cellular components, reducing its osteogenic capacity (Van der Donk et al., 2003).

To maintain good long-term PR, adequate new bone formation is needed. Periosteum plays a major role in promoting bone growth and repair, and contains multiple cells with osteoblastic potential through the maintained proliferative capability of the transplanted cambium layer (Barckman et al., 2013). In particular, periosteum plays a unique role in revascularization of the bone graft in the early stages of healing (Yang et al., 2014).

Given that the healing process is a highly orchestrated and structured process, gingival wound healing is important to the periodontal surgery outcome (Kim et al., 2011). Therefore, it was very beneficial to examine the ultra-structural events associated with the early gingival wound healing in each line of treatment. Although 10 days may be too short a duration to observe structural changes, other authors found a considerable difference in both the cellular and extracellular phases of grafted and non-grafted sites in the same time frame (Lafzi et al., 2007).

Fortunately, our TEM results were in harmony with the clinical findings. Concerning the epithelial phase, the results showed obvious improvement in the two test groups. In view of the connective tissue phase, non-classical apoptotic features were revealed consistent with OFD sites in terms of cytoplasmic vacuolization, chromatin condensation and swollen mitochondria. The ECM mainly contained sparse, fragmented, incompletely formed collagen fibers and shrunken fibroblasts, indicating that OFD is accompanied by para-apoptotic changes that interfere with PR (Cattaneo et al., 2003).

On the other hand, Group II showed numerous proliferating fibroblasts and abundant collagen bundles.

From the biological point of view, a protective effect of MPM may induce earlier healing features by enhancing proliferation and differentiation of the resident progenitor cells and those supplied by the cambium layer (Lin et al., 2013). Interestingly, a new look should be taken towards an immune response coming from the periosteum, as

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major histocompatibility complex II positive immune cells were detected in the cambium, suggesting the presence of dendritic cells (Frey et al., 2013).

In Group III, active fibroblasts and well organized collagen fibers were reflected; suggesting that the combination therapy favored the transformation of fibroblasts to metabolically active (formative) cells, which in turn enhance colonization of the root surface. Similarly, a recent histological study reported that the bioactivity of morselized allograft bone was found to be highlighted when added to the transplanted cambium owing to its content of bone-competent cells (Barckman et al., 2013). Moreover, it was suggested that periosteum may prevent soft tissue infiltration into the bone graft, and can inhibit osteoclasts that originate from the recipient site, reducing bone graft resorption compared to block graft alone (Yang et al., 2014).

Overall, the semilunar approach is proposed to give better results than the previous techniques described in the literature owing to the dual blood supply; firstly from the pedicle periosteum and secondly from the periosteum present below the furcation. In that way, the osteoinductive mechanism of MPM may be multi-factorial; the cambium layer maintains its relation to the original periosteum tissue, which might extend its regenerative effect on avascular roots. In addition, the potential liberation of essential bone-stimulating substances acting immediately once the cambium cells touch it may provide a signal for improved regenerative response, facilitating initial bone healing with better predictability.

The limitation of this technique remains that it cannot be used for cases with thin gingival biotypes. Also, long-term results are yet to be assessed. However, healing of periosteal grafts and good achievable results makes it a viable procedure for class II furcation defects.

Conclusion In light of the findings of this study, it was demonstrated that the semilunar approach used in harvesting MPM represents a promising way to get a better clinical situation with a more predictable amount of PR. It represents also an alternative explanation for the potential efficacy of MPM in gingival wound healing. Meaningful improvements in both clinical parameters and features of gingival wound healing were revealed with the combination of MPM and DFDBA, supporting their adjunctive use in treatment of class II furcation defects.

Recommendation Larger randomized clinical trials are needed to fully evaluate whether combined graft and MPM procedures offer an advantage over MPM alone. Additionally, longitudinal studies with long-term follow-up are needed to better quantify the value of such regenerative and economic techniques in improving the survival rate of furcation-affected molar teeth.

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IAP Meeting – Chile 2015 Update and New Developments in Periodontics and Implant Dentistry for the Specialist and General Dentist, 17-18 April 2015, Santiago Chile Organized by: The International Academy of Periodontology, Sociedad de Periodoncia de Chile, and Facultad de Odontología U. de Chile Registration and information at http://www.iapchile.cl Registration Fees Students (with proof of student status): CLP100,000 (US$200) Members of Societies of Periodontology: CLP120,000 (US$ 250) Others: CLP 150,000 (US$ 300) Poster Competition Cash prizes of US$ 2000 for first place and US$ 1000 for second place will be awarded in both clinical and basic science research categories Rules Governing Abstract Submissions Abstract must be written in English Abstract cannot contain previously published or publicly presented material All submitters of accepted abstracts must pre-register, pay the registration fee and present the poster at the meeting (registration deadline 31 March 2015) Abstracts must be submitted on-line at http://www.iapchile.cl and must be sent by e-mail to postersiap2015@gmail.com Submission deadline is Monday, 16 March 2015 at 00.00 hours Abstract must include the following terms –‘objectives’, ‘methods’, ‘results’ and ‘conclusions’ Abstract cannot contain illustrations or photos or report results using unidentified drugs or materials External funding support must be disclosed within the abstract including the grant number The abstract is limited to 250 words – larger abstracts will not be accepted For further information: contact Romina Fiabane, SPCh, telephone (56 2) 2335 7692, e-mail: inscripcionesiap2015@gmail.com

IAP Meeting – Chile 2015 Scientific Program: FRIDAY, 17 APRIL 2015

SATURDAY, 18 APRIL 2015

09:00 Opening Ceremony Periodontal Diseases – Etiology and Treatment SESSION 1: Periodontal Sciences Moderator - Thomas Van Dyke (USA)

Periodontal Regeneration and Implantology SESSION 3: Periodontal Regeneration Moderator – Ahmed Gamal (Egypt)

09:30 George Hajishengallis (USA) - Models of Periodontal Disease Etiology 10:15 Gustavo Garlet (Brazil) - Periodontal Disease Pathogenesis 11:00 Coffee Break 11:30 Ricardo Teles (USA) - Biomarkers for Periodontal Disease Progression 12:15 Alp Kantarci (USA) - Hypoxia and Pathogenesis of Periodontal Disease 13:00 Lunch and Poster Session 14:00 Rolando Vernal (Chile) - Periodontal Disease: Linking the Microbiological Etiology to Bone Loss 14:45 Jorge Gamonal (Chile) Characterization of Bleeding on Probing in Subjects with Chronic Periodontitis

09:00 Mark Bartold (Australia) Mechanisms of Periodontal Tissue Regeneration 09:45 Anton Sculean (Switzerland) Regeneration of Periodontal Tissues: What Works?

10:30 Coffee Break SESSION 4: Implantology Moderator – Vincent Iacono (USA) 11:00 Antonio Sanz (Chile) – Regeneration and Stem Cells 11:45 Joerg Meyle (Germany) - Dental Implants in Periodontitis Patients 12:30 Lunch and Poster Session SESSION 5: Peri-implantitis Moderator – A. Kumarswamy (India)

15:30 Coffee Break

13:30 Lisa Mayfield (Australia) - What Is Peri-implantitis? What Causes It and Can It Be Prevented?

SESSION 2: Periodontal Treatment Moderator - Sebastian Ciancio (USA)

14:15 Jamil Shibli (Brazil) - Treatment of Peri-implantitis

16:00 Fernando Fuentes (Chile) – Adjunctive Treatments to Scaling and Root Planing: Mechanical and Chemical Therapies

15:00 Coffee Break

16:45 Magda Feres (Brazil) - Adjunctive Treatments to Scaling and Root Planing: Systemic Antibiotics

16:15 Gustavo Massey (Chile) - State of the art of Implant Dentistry in Chile

17:30 to 18:30 Panel Discussion

© International Academy of Periodontology

15:30 Niklaus Lang (Switzerland) - Teeth versus Implants

17:00 to 17:30 Panel Discussion 17:30 Closing Ceremony

Organized

INTERNATIONAL ACADEMY OF PERIODONTOLOGY

IAP MEETING CHILE 2015 Update and New Developments in Periodontics and Implants for the Specialist and General Dentist

Santiago-Chile A p r i l 1 7 t h -1 8 t h / 2 0 1 5 Aula Magna Universidad San Sebastiån Campus Bellavista,Bellavista N° 07 (intersection with Pio Nono) Speakers: Niklaus Lang; ThomasVan Dyke; George Hajishengallis; Gustavo Garlet; Ricardo Teles; Alp Kantarci; Sebastian Ciancio; Magda Feres; Ahmed Gamal; Mark Bartold; Anton Sculean; Vincent Iacono; Joerg Meyle; Lisa Mayfield, Jamil Shibli, Jorge Gamonal; Rolando Vernal; Fernando Fuentes; Gustavo Mazzey and Antonio Sanz Poster competition: cash prizes for the outstanding poster presentations _

Contact_ Romina Fiabane SPCh 02 - 23357692 soc.periodoncia@gmail.com

REGISTRATION FEES_ > students USD 200 > peridontal society members USD 250 > non members USD 300