Original study - ZZI 01/2013

Lateral bone augmentation applying different biomaterials

M. Merli1, M. Moscatelli1, A. Mazzoni2, M. Merli1, G. Mariotti1, M. Nieri3

A clinical and histological evaluation of a case report

Introduction: This paper describes the treatment of horizontal osseous defects around implants in a one-stage split-mouth approach in a middle-aged female patient.

Method and Material: The same identical reconstruction technique was performed in both surgical sites using different biomaterials: a ? -tricalciumphosphate (Ceros TCP granules) grafting material and a porcine, collagen pericardium resorbable membrane (Remotis) were employed on the test side and a deproteinized, bovine bone matrix (Bio-Oss) and a porcine, collagen resorbable membrane (Bio-Gide) on the control side. Bone substitutes were mixed with autologous bone (approximately 10 %) harvested during implant insertion procedures.

Results: Substantial bone regrowth was evident in both ridges, although only the test side underwent complete regeneration. Histological examination of the regenerated areas showed the presence of mature bone organized around particles of biomaterial during the incorporation phase.

Conclusion: Both therapeutic approaches have proved favorable in terms of covering the initially exposed implant threads.

Keywords: ?-tricalciumphosphate; bone augmentation; collagen membrane; dental implants; deproteinized bovine bone matrix


Merli M, Moscatelli M, Mazzoni A, Merli M, Mariotti G,
Nieri M: Lateral bone augmentation applying different
biomaterials A clinical and histological evaluation of a case report. Z Zahnärztl Implantol 2013;29:70-79.
DOI 10.3238/ZZI.0070-0079


A principle anatomic condition for implant therapy is the presence of sufficient bone volume to result in implant stability. Clinical situations in which the bone quantity is inadequate very often require regenerative bone therapy. Bone augmentation procedures may be carried out prior to (two-stage procedure) or simultaneously to implant placement (one-stage procedure) and these procedures can be performed using different materials and techniques [8].

The augmentation procedure is classified as horizontal or vertical bone augmentation according to the bone-type defect [8]. In one-stage horizontal bone augmentation treatments, resorbable collagen barrier membranes in combination with a variety of graft materials, such as autogenous bone, allografts, xenografts and alloplastic materials are often used [7, 13, 14, 15, 17, 18, 21]. In addition, the titanium implant surface characteristics may play a role in bone regeneration in dehiscence-type defects, such as the development of sandblasted/thermal acid-etched surface technology [16]. This new conditioning process, performed immediately before surgical placement, increases the implant surface hydrophilic [5, 19]. In animal studies, the conditioned surface reduced the healing period and increased bone apposition in the early healing phase [5, 19].

There are several systematic reviews that examine horizontal bone augmentation [7, 8]. However, in humans, one-stage randomized clinical trials (RCTs) are scarce [1, 9, 10, 11]. Recently, a RCT was published comparing a synthetic bioresorbable polyethylene glycol hydrogel (PEG) membrane and a standard collagen membrane grafted with natural bone matrix of bovine origin [11]. No differences were detected in the percentage of vertical bone defect filling after 6 months, with the exception of a greater frequency of soft tissue complications observed with the PEG membrane, and a shorter preparation and application time for the PEG hydrogel membrane [11].

Another RCT compared the amount of newly formed bone in sites with the application of a cross-linked collagen membrane versus that of a native collagen membrane for the treatment of dehiscence-type defects at titanium implants [1]. A natural bone mineral of bovine origin was also used. Four patients in the cross-linked membrane group prematurely discontinued the study (3 due to wound infection) and one patient in the native collagen group discontinued the study due to wound infection. No statistical differences regarding the change in vertical defect length, the change in horizontal defect width and the quality of newly formed tissue at the fourth month were observed.

Presently, there are no studies that compare a standard collagen membrane and natural bone mineral of bovine origin directly with another system consisting of multilayer, porcine pericardium natural collagen membrane and ?-tricalciumphosphate for horizontal bone augmentation [4, 20].

The aim of this case report is to investigate these two different procedures in a split-mouth approach using a novel implant surface with increased hydrophilicity.


Methods and Material

A 43-year-old female patient, non-smoker, classified as ASA-Physical Status (PS) I (good systemic health status) [12] exhibited missing first molars in the mandible. The two areas presented similar bone defects (Fig. 1–3). After scaling and root planing an integrated treatment plan was established based on the collected data and patient desires.

The research was conducted in accordance with ethical principles, including the Declaration of Helsinki and the patient gave a written consent according to the above mentioned principles.

The substitution with crowns supported by implants on both sides was preceded by orthodontic treatment. The uprighting of second molars was obtained using miniscrews to improve and accelerate the orthodontic movement.

The patient underwent intravenous conscious sedation and received local anesthesia in both sides of the mandible during the surgical procedure for guided bone regeneration with simultaneous implant insertion. Mucoperiosteal flaps, involving interproximal teeth, with one vertical incision mesial to the second premolar were raised to expose the underlying bone defects. The implant sites were prepared using cylinder burs, gradually increasing the diameter under copious saline irrigation. INICELL implants (Thommen Medical AG, Waldenburg, CH, Switzerland) were conditioned chairside and positioned both in the test and control sites, maintaining a safe distance of 2 mm from the roof of the mandibular canal. INICELL implant surface is a further development of sandblasted/thermal acid-etched surface technology [5, 19]. The one wall dehiscence-type defects were filled with a mixture of the bone substitute (approximately 90 %), autologous bone (approximately 10 %) harvested during implant insertion procedure using disposable filters, and patient’s blood.

Precisely, the test side (right defect) was filled with ?-tricalciumphosphate (?-TCP) (Ceros TCP granules, Thommen Medical AG). Ceros TCP is a resorbable, synthetic ? -TCP bone graft substitute with a pore size of 100 – 500 µm. The site was covered with a porcine collagen resorbable membrane (Remotis Thommen Medical AG) stabilized by four titanium osteosynthesis tacks (Kalos, Nike srl, Grosseto, Italy) (Fig. 4–6). The Remotis membrane is a resorbable multilayer porcine pericardium collagen membrane used for guided bone regeneration in dehiscence defects. On the contralateral side, the defect was filled with deproteinized bovine bone matrix (DBBM) granules (Bio-Oss Spongiosa Granules, particle size 0.25–1 mm; Geistlich Pharma AG) and covered with porcine collagen resorbable membrane (Bio-Gide Geistlich Pharma AG, Wolhusen, Switzerland), fixed with titanium osteosynthesis tacks on both the two oral and the two buccal corners (Fig. 7–9).In both sides, to adequately cover the submerged implants, the flaps were lengthened through periosteal horizontal incisions and the incision lines were sealed by applying double layer suture stitches. Post-surgical instructions regarding diet and home care, as well as pharmacological prescriptions, were dispensed to the patient. In particular, Nimesulide 100 mg twice a day for 2 days and then as needed was prescribed and an ice pack was given to the patient. The patient was instructed to refrain from mechanical plaque removal in the area of implant placement for 1 week, to use chlorhexidine mouthrinse (0,12 %) twice a day from the third postoperative day and to apply chlorhexidine gel on the wound area twice a day for 15 days.

Follow-up visits were scheduled for 7 and 15 days post-surgery and were continued at 1, 3 and 6 months.

During the second phase surgery, bone core biopsies were taken from both the test and control sides in correspondence to the regenerated bone areas using a trephine bur with a 2 mm outer diameter and copious irrigation. Bone biopsies were immediately fixed in 10 % buffered formalin solution (Sigma Chemical, St. Louis, MO, USA) at 4°C for at least 24 h. The specimens were dehydrated in an ascending series of alcohol rinses and then embedded in a London White resin (LR White Resin, London Resin, Theale, Berkshire, UK). After resin polymerization, specimens were sectioned along their longitudinal axis with a high-precision diamond disk at 150 m m and ground to approximately 40 mm with a specially designed milling machine (Micromet, Remet, Casalecchio di Reno, Italy). The non-decalcified ground sections were stained with acid fuchsine or acid fuchsine and toluidine blue staining. The slides were observed under normal transmitted light with an optical microscope (Nikon Eclipse; Nikon, Tokyo, Japan).



After 6 months, during the second surgical phase, where a horizontal primary incision on the mid-crest was performed and the gingiva-former abutments were connected (Fig. 10, 11).

Substantial reconstruction of the alveolar crest deficiency was evident in both ridges although the complete regeneration of the buccal plate is not evident on the control side. The coronal plate of the defect appears as a thin layer of connective tissue and more apically the implant thread is visible (Fig. 11). The test side shows complete regeneration (Fig. 10).

After 2 months the provisional crowns were applied. The screw-retained porcelain-fused-to-metal crowns were placed 2 months later (Fig. 12–15). The color, texture and surface of peri-implant mucosa appear very natural although a slight alteration of the soft tissue was present in the buccal site of the implant region (Fig. 14, 15). The patient was very satisfied with the procedure and healing was uneventful.

Results of the histological analysis revealed that the regeneration was mainly represented by areas of bone remodeling where the newly formed bone was already well organized with spotted regions where grafted bone particles were detectable in test and control sides (Fig. 16–19). In these areas, most of the grafted bone particles were fused and only partially distinguishable from the newly formed bone. The regenerated new bone was strongly stained by acid fuchsine and many osteocytes were trapped in their mineralized matrix (Fig. 17, 19).



The results of the case presented were positive, as both ridges showed substantial reconstruction of the alveolar crest deficiency. Moreover, the quantity of the bone reconstructed on the test side appears to be clinically satisfying.

The association of Bio-Gide and Bio-Oss was tested as a control group in two recent RCTs [1, 11]. In these two studies the percentage of linear defect fill was very different: 94 % and 46 %, respectively [1, 11]. In the present study the site treated with Bio-Gide and Bio-Oss obtained only a partial defect fill. In fact, a thread apical to the level of the implant head was exposed. To our knowledge, the association of Remotis and Ceros TCP granules has not been tested in a clinical trial. In this study the site treated with Remotis and Ceros TCP granules obtained a complete defect fill. As this is a case report, the findings should be further examined in randomized clinical trials.

In this case report the defects were filled with a mixture of bone substitute and autogenous bone in proportion respectively 90/10. The autogenous bone component was limited to the bone harvested during implant insertion procedure.

A frequent complication with guided bone regeneration is membrane exposure and infection. This can alter the amount of regenerated bone [2, 3, 6]. The strategy followed to reduce the risk of exposure of the membrane involves appropriate flap management to obtain tension-free closure of the incision and in the same time to stabilize the collagen membranes. In this case the healing was uneventful and there was no membrane exposure.

Further information is needed to better understand the efficacy of the tested biomaterials.

The effectiveness of these procedures should be validated in further clinical trials. In particular, the two systems proposed in this case report seem promising and will be compared by the authors in a new RCT presently underway.



Based on this preliminary report different biomaterials may obtain positive results in terms of bone augmentation, both clinically and histologically.


Acknowledgments: The authors express their deepest appreciation to Heather Dawe, Gabriele Schubert and Marco Bonfini for editing the manuscript.


Conflict of interest: The authors declare that there is no conflict of interest in this study.



Merli M, Moscatelli M, Mazzoni A, Merli M, Mariotti G,
Nieri M: Lateral bone augmentation applying different
biomaterials A clinical and histological evaluation of a case report. Z Zahnärztl Implantol 2013;29:70-79.

DOI 10.3238/ZZI.0070-0079



1. Becker J, Al-Nawas B, Klein MO, Schliephake H, Terheyden H, Schwarz F: Use of a new cross-linked collagen membrane for the treatment of dehiscence-type defects at titanium implants: a prospective, randomized-controlled double-blinded clinical multicenter study. Clin Oral Implants Res 2009;20: 742–749

2. Becker W, Dahlin C, Becker BE et al.: The use of e-PTFE barrier membranes for bone promotion around titanium implants placed into extraction sockets: a prospective multicenter study. Int J Oral Maxillofac Implants 1994;9: 31–40

3. Beitlitum I, Artzi Z, Nemcovsky CE: Clinical evaluation of particulate allogeneic with and without autogenous bone grafts and resorbable collagen membranes for bone augmentation of atrophic alveolar ridges. Clin Oral Implants Res 2010;21:1242–1250

4. Buser D, Hoffmann B, Bernard JP, Lussi A, Mettler D, Schenk RK: Evaluation of filling materials in membrane-protected bone defects. A comparative histomorphometric study in the mandible of miniature pigs. Clin Oral Implants Res 1998;9:137–150

5. Calvo-Guirado JL, Ortiz-Ruiz AJ, Negri B, López-Marí L, Rodriguez-Barba C, Schlottig F: Histological and histomorphometric evaluation of immediate implant placement on a dog model with a new implant surface treatment. Clin Oral Implants Res 2010;21: 308–315

6. Carpio L, Loza J, Lynch S, Genco R: Guided bone regeneration around endosseous implants with anorganic bovine bone mineral. A randomized controlled trial comparing bioabsorbable versus non-resorbable barriers. J Periodontol 2000;71:1743–1749

7. Chiapasco M, Zaniboni M: Clinical outcomes of GBR procedures to correct peri-implant dehiscences and fenestrations: a systematic review. Clin Oral Implants Res 2009;20 Suppl 4:113–123

8. Esposito M, Grusovin MG, Felice P, Karatzopoulos G, Worthington HV, Coulthard: Interventions for replacing missing teeth: horizontal and vertical bone augmentation techniques for dental implant treatment. Cochrane Database Syst Rev 2009;(4):CD003607

9. Friedmann A, Gissel K, Soudan M, Kleber BM, Pitaru S, Dietrich T: Randomized controlled trial on lateral augmentation using two collagen membranes: morphometric results on mineralized tissue compound. J Clin Periodontol 2011;38:677–685

10. Jensen SS, Terheyden H: Bone augmentation procedures in localized defects in the alveolar ridge: clinical results with different bone grafts and bone-substitute materials. Int J Oral Maxillofac Implants 2009;24 Suppl:218–236

11. Jung RE, Hälg GA, Thoma DS, Hämmerle CH: A randomized, controlled clinical trial to evaluate a new membrane for guided bone regeneration around dental implants. Clin Oral Implants Res 2009; 20:162–168

12. Maloney WJ, Weinberg MA: Implementation of the American Society of Anesthesiologists Physical Status classification system in periodontal practice. J Periodontol 2008;79:1124–1126

13. Merli M, Lombardini F, Esposito M: Vertical ridge augmentation with autogenous bone grafts 3 years after loading: resorbable barriers versus titanium-reinforced barriers. A randomized controlled clinical trial. Int J Oral Maxillofac Implants 2010;25:801–807

14. Merli M, Migani M, Esposito M: Vertical ridge augmentation with autogenous bone grafts: resorbable barriers supported by ostheosynthesis plates versus titanium-reinforced barriers. A preliminary report of a blinded, randomized controlled clinical trial. Int J Oral Maxillofac Implants 2007;22: 373–382

15. Merli M, Bernardelli F, Esposito M: Horizontal and vertical ridge augmentation: a novel approach using osteosynthesis microplates, bone grafts, and resorbable barriers. Int J Periodontics Restorative Dent 2006;26:581–587

16. Schwarz F, Sager M, Kadelka I, Ferrari D, Becker J: Influence of titanium implant surface characteristics on bone regeneration in dehiscence-type defects: an experimental study in dogs. J Clin Periodontol 2010;37:466–473

17. Schwarz F, Rothamel D, Herten M et al.: Immunohistochemical characterization of guided bone regeneration at a dehiscence-type defect using different barrier membranes: an experimental study in dogs. Clin Oral Implants Res 2008;19:402–415

18. Schwarz F, Herten M, Ferrari D et al.: Guided bone regeneration at dehiscence-type defects using biphasic hydroxyapatite + beta tricalcium phosphate (Bone Ceramic) or a collagen-coated natural bone mineral (Bio-Oss Collagen): an immunohistochemical study in dogs. Int J Oral Maxillofac Surg 2007;36:1198–1206

19. Stadlinger B, Lode AT, Eckelt U et al.: Surface-conditioned dental implants: an animal study on bone formation. J Clin Periodontol 2009;36:882–891

20. Tadic D, Epple M: A thorough physicochemical characterisation of 14 calcium phosphate-based bone substitution materials in comparison to natural bone. Biomaterials 2004;25: 987–994

21. Zitzmann NU, Naef R, Schärer P: Resorbable versus nonresorbable membranes in combination with Bio-Oss for guided bone regeneration. Int J Oral Maxillofac Implants 1997;12: 844–852


Mauro Merli

Viale Settembrini 17/o

47923 Rimini (Italien)

Tel.: +39–0541–52025

Fax: +39–0541–52308



Private practice, Rimini, Italy

Fellow researcher, Department SAU&FAL, University of Bologna, Italy; Laboratory of Cell Biology & Laboratory of Immunorheumatology and Tissue Regeneration – Ramses Laboratory, Rizzoli Orthopedic Institute, Bologna, Italy

Fellow researcher, Department of Periodontology, University of Florence, Italy

PAGE: 1 | 2 | 3 | 4