Journal of Osseointegration by Ariesdue srl

jo j o u r n a l o f osseointegration

issn 2036-413X march 2014 n. 1 vol. 6 www.journalofosseointegration.eu

Editorial board editors-in-chief

board of reviewers

Adriano Piattelli

Professor of Oral Pathology and Medicine Dental School, University of Chieti Pescara (Italy) apiattelli@unich.it

Arthur Belem Novaes Jr.

Dental School of Ribeirão Preto, University of São Paulo (Brazil) novaesjr@forp.usp.br

Biomaterials

Yasumasa Akagawa Hiroshima (JPN) Victor Arana Chavez Sao Paulo (BRA) Carlos Roberto Grandini Ilha Solteira (BRA)

Adalberto Luiz Rosa Ribeirão Preto (BRA)

Lior Shapira Jerusalem (ISR) Paulo Tambasco de Oliveira Ribeirão Preto (BRA)

associate editors Biomaterials

Clinical Research

New York (USA)

Rochester (USA)

Biomaterials and Tissue Engineering

Implant Science

Georgios Romanos

Paulo Coelho

Marco Degidi

Jose M. Granjeiro

Bologna (Italy)

Niterói (Brazil)

JosE Luis Calvo Guirado

Murcia (Spain)

Carlo Mangano

Jamil Shibli

Guarulhos (Brazil) Clinical Innovations

Gravedona (Italy) Basic Research

Devorah Schwartz-Arad

Tel Aviv (Israel)

Pablo Galindo Moreno

Granada (Spain)

assistant editors Vittoria Perrotti

Department of Dentistry and Oral Science, Dental School, University of Chieti-Pescara (Italy) v.perrotti@unich.it

Nilson T. C. Oliveira

Departamento de Engenharia de Materiais DEMa / CCDM - Universidade Federal de São Carlos UFSCAR, SP (Brazil) n.oliveira@journalofosseointegration.eu

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Biomaterials and Tissue Engineering

Paolo Amerio Chieti (ITA) Timothy G. Broomage New York (USA) Martin Lorenzoni Graz (AUT) Mario Raspanti Varese (ITA) Cristina Teixeira New York (USA) Michael Yost Columbia (USA) Vincenzo Zizzari Chieti (ITA) Basic Research

Luciano Artese Chieti (ITA) Raquel R.M. Barros Ribeirão Preto (BRA) Giuseppe Cardaropoli New York (USA) Francesco Carinci Ferrara (ITA) Joni A. Cirelli Araraquara (BRA) Magda Feres Guarulhos (BRA) Giovanna Iezzi Chieti (ITA) Ramon Martinez Corrià Lerida (ESP) Gabriella Mincione Chieti (ITA) Raffaella Muraro Chieti (ITA) Gianpaolo Papaccio Naples (ITA) Rachel Sammons Birmingham (GBR) Clinical Research

Direttore responsabile

Dino Sergio Porro redazione

Barbara Bono

Paola Cappelletti

b.bono@ariesdue.it

p.cappelletti@ariesdue.it

farma@ariesdue.it

doctoros@ariesdue.it

Cristina Calchera

osseo_colophon.indd 3

Heverson Tavares Araraquara (BRA) Van P. Thompson New York (USA) Flavia Iaculli Chieti (ITA) Carmen Mortellaro Novara (ITA)

Simona Marelli

Sergio Caputi Chieti (ITA) Massimo Del Fabbro Milan (ITA) Carlo Ercoli Rochester (USA) German Gomez-Roman Tübingen (DEU) Ole Jensen Denver (USA) Gregorio Laino Naples (ITA) Voja Lekovic Belgrade (SRB) Eloà R. Luvizuto Araçatuba (BRA) Elcio Marcantonio Jr Araraquara (BRA)

Ziv Mazor Ra'anana (ISR) Valdir Antonio Muglia Ribeirão Preto (BRA)

Joerg Neugebauer Cologne (DEU) Ana Pontes Barretos (BRA) Pâmela L. Santos Araçatuba (BRA) Sérgio L. Scombatti de Souza Ribeirão Preto (BRA) Pascal Valentini Paris (FRA) Paul Weigl Frankfurt am Main (DEU) Implant Science

Carlos R.P. Araujo Bauru (BRA) Bartolomeo Assenza Chieti (ITA) Luigi Califano Naples (ITA) James Doundoulakis New York (USA) Massimo Frosecchi Florence (ITA) Enrico Gherlone Milan (ITA) Ana Becil Giglio New York (USA) Graziano Giglio New York (USA) Luigi Guida Naples (ITA) Giulio Leghissa Milan (ITA) Giuseppe Luongo Naples (ITA) Rogério Margonar Araraquara (BRA) Emeka Nkenke Erlangen (DEU) Marco E. Pasqualini Milan (ITA) Thallita Pereira Queiroz Araraquara (BRA) Lorenzo Ravera Chieti (ITA) Gilberto Sammartino Naples (ITA) Antonio Scarano Chieti (ITA) Tiziano Testori Milan (ITA) Stefano Tetè Chieti (ITA) Clinical Innovations

Zvi Artzi Tel Aviv (ISR) Giuseppe Corrente Turin (ITA) Nilton De Bortoli Jr São Paulo (BRA) Paolo Della Casa Genoa (ITA) Stefano Fanali Chieti (ITA) Carlos Ademar Ferreira Tucuruvi (BRA) Luis Fujimoto New York (USA) Heracles Goussias Athens (GRC) Robert Horovitz New York (USA) Fouad Khoury Münster (DEU) Georg H. Nentwig Frankfurt (DEU) Vula Papalexiou Curitiba (BRA) Waldemar Polido Porto Alegre (BRA) Ludovico Sbordone Pisa (ITA) Aris Tripodakis Athens (GRC)

14/04/14 16:15

Raquel Rezende Martins de Barros1, Arthur Belém Novaes Junior2, VULA PAPALEXIOU3, SÔNIA MARA LUCZYSZYN3, STYLIANOS NICOLAS PAPALEXIOU NETO4, CASSIANA MARIA GARCEZ RAMOS5, ADRIANA LUISA GONÇALVES DE ALMEIDA6, ADRIANO PIATTELLI7, BARTOLOMEO ASSENZA8 1

Postdoctoral student, DDS, MS, PhD. Department of Bucco-Maxillo-Facial Surgery and Traumatology and Periodontology, School of Dentistry of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil 2 Full Professor of Periodontics, DDS, MS, PhD. Department of Bucco-Maxillo-Facial Surgery and Traumatology and Periodontology, School of Dentistry of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil 3 Professor of Periodontics, DDS, MS, PhD. Center of Biologic and Health Science, School of Dentistry, Catholic Pontifical University, PR, Brazil 4 Postgraduate student, MS. Center of Biologic and Health Science, School of Dentistry, Catholic Pontifical University, PR, Brazil 5 Professor of Veterinary, MS. Center of Biologic and Health Science, School of Dentistry, Catholic Pontifical University, PR, Brazil 6 Microscopic and Image Analysis Laboratory Technician. Department of Bucco-Maxillo-Facial Surgery and Traumatology and Periodontology, School of Dentistry of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil 7 Full Professor of Oral Pathology and Medicine Periodontics, DDS, MS, PhD. School of Dentistry, University of Chieti-Pescara, Chieti, Italy 8 DDS. Private Practice, Milan, Italy

Evaluation of contiguous implants with cement-retained implant-abutment connections. A minipig study to cite this article De Barros RRM, Novaes AB Jr, Papalexiou V, Luczyszyn SM, Papalexiou Neto SN, Ramos CMG, Almeida ALG, Piattelli A, Assenza B. Evaluation of contiguous implants with cement-retained implant-abutment connections. A minipigstudy. J Osseointegr 2014;6(1):3-10.

ABSTRACT Aim The presence of a microgap at the implant-abutment interface may permit bacterial contamination and lead to bone resorption, interfering with papillae formation. The present study evaluated adjacent implants with cement-retained abutments as an option to control such deleterious effects. Materials and methods Seven minipigs had their bilateral mandibular premolars previously extracted. After 8 weeks, four implants were installed in each hemi-mandible of each animal. The adjacent implants were randomly inserted on one side at the crestal bone level and on the other, 1.5 mm subcrestally. Immediately, a non-submerged healing and functional loading were provided with the abutments cementation and prostheses installation. Clinical examination and histomorphometry served to analyze the implant success. Results A total of 52 implants were evaluated at the end of the study. The subcrestal group achieved statistical better results when compared to the crestal group, clinically in papillae formation (1.97 x 1.57 mm) and histomorphometrically in crestal bone remodeling (1.17 x 1.63 mm), bone density (52.39 x 45.22%) and bone-implant contact (54.13 x 42.46%). Conclusion The subcrestal placement of cement-retained abutment implants showed better indexes of osseointegration and also improved papillae formation and crestal bone remodeling at the interimplant area after immediate loading, making them a promising option for the treatment of esthetic regions.

Keywords Abutment; Bone resorption; Dental implant; Papillae formation.

March 2014; 6(1) © ariesdue

Introduction The bone loss around dental implants may, depending on its extension, compromise their longevity or the aesthetic restorative results. In the case of adjacent implants, especially in the anterior region, this becomes even more worrying since the height of the crestal bone may directly influence the presence or absence of interproximal papillae (1). The real causes for this bone loss remain unknown and among the several hypotheses, such as interimplant distances, the distance between the contact point and the alveolar crest, the macrodesign of the cervical area of the implant, implant surface treatments and surgical technique, the present study focused on the implant-abutment connections and their positioning in relation to the crestal bone (2). Scanning electronic microscope analysis showed a mean 2 to 7 µm gap in the screwed abutment-implant interface (3). They represent a bacterial reservoir (4) that could interfere with the peri-implant tissue health, causing bone loss and potentially playing a role in the etiology of peri-implantitis. In general, implants are placed at the crestal bone level in either a submerged or a non-submerged approach. In special cases, in the esthetic zone for example, it has been suggested the subcrestal placement of implants to minimize the risk of metal exposure and to allow for enough space in the vertical dimension to develop an adequate emergence profile (5-7). However, this procedure moves the implant-abutment interface into the bone tissue and the contamination of this microgap as an empty space could potentially cause a significant bone loss, impairing the final result (8-11). An alternative to screw-retained abutments (SRA) is cement-retained abutments (CRA). Scanning Electron Microscopy (SEM) analysis also revealed microgaps in the CRA interface, but they were always completely filled

De Barros R.R.M. et al.

by the fixation cement (3). In vitro studies showed that neither fluid nor bacterial penetration was observed in CRA implants whereas in all SRA implants, penetration of fluids and bacteria was observed inside the internal cavity of the implant (3,4). Additionally, as a special characteristic, some cement-retained implants provide a double retention connection (mechanical and chemical) of the abutment and of a transmucosal element, in order to bring outside of the peri-implant tissues the sealing interface, favoring the healing of the peri-implant tissues. The dual retention consists in the coupling of the component and transmucosal implant without screws and in a chemical bonding of the abutment within the implant. This approach can reduce the micromovements and the inflammatory agents nearby the crestal bone in order to achieve lower rates of bone resorption (12, 13). The aim of the present study was to compare the crestal and subcrestal placement of adjacent implants with cement-retained abutments, evaluating the osseointegration, the crestal bone remodeling and the formation of papillae between the implants after immediate loading in the minipig model.

MATERIALS AND METHODS A total of seven minipigs (Minipig BR-1; Minipig Comércio e Desenvolvimento; Campina do Monte Alegre, Brasil), aged about 18 months (weight: 20 to 30 kg), were selected for the study. They received antiparasitic treatment, vitamins, a full series of vaccines and prophylactic dental hygiene treatment with ultrasonic scalers (Cavitron 3000, Dentsply Mfg. Co., York, PA, USA). All the surgical procedures were performed under general anesthesia and the whole experimental phase in vivo was accompanied by a veterinary. The Regional Ethics Committee for Animal Research approved the study (protocol number: 561).

Surgical procedures

Food was withheld in the night preceding surgeries. The

animals were pre-anesthetized with Azaperone (Destress - DES-Vet, São Paulo, Brazil; 1 mg/kg, intramuscularly) and after 20 minutes, were anesthetized with Ketamine (Dopalen - Vetbrands, Jacareí, Brazil; initial dose of 5 mg/ kg, intramuscularly). This procedure allowed a working time of about 1 hour, and then other applications of Ketamine were done with the half of the first dose, every 30 minutes until the end of the surgical interventions. Throughout the period of deep sedation, the animals were monitored for heart rate, respiratory rate, temperature, palpebral and intestinal reflexes. The animals underwent two surgical interventions. The first intervention was the extraction of the mandibular premolars on both sides of the mandible and was performed with bilateral full-thickness flap elevation. In order to avoid any damage to the neighboring bony walls, the teeth were sectioned in buccolingual direction at the furcation area and the roots were extracted individually with the use of a periotome. In some animals, the tooth germs that were present in the referred regions were also extracted. The flaps were then repositioned and sutured with absorbable sutures (Vicryl, Ethicon, Inc., Johnson & Johnson Company, São José dos Campos, Brasil.). After eight weeks of healing, implant placement surgeries were performed. Horizontal incisions were made on the crest of the ridges, from the distal of the canines to the mesial of the first molars and after the full-thickness flaps elevation, the complete healing of the alveolar ridges was observed (Fig. 1). The implants were placed according to the manufacturer’s guidelines. 4 cement-retained abutment (CRA) implants of 4.1 mm in diameter and 10 mm in length (Bone System, Milano/ Italy) were placed at the crestal bone level on one side of the jaw (crestal group) (Fig. 2). Contralaterally, CRA implants of 4.1 mm in diameter and 8 mm in length was placed 1.5 mm below the crestal bone level (subcrestal group). Guide devices were manufactured to standardize both the angle and the distance between the implants. Distances of 2 to 3 mm between the adjacent implants were left (Fig. 3). Immediately after the implants placement, the transfers

fig. 1 Note the complete healing of the alveolar ridge after the full-thickness flap elevation for implant placement. fig. 2 Cement-retained abutment implants of 4.1 mm in diameter and 10 mm in length (Bone System, Milano / Italy) placed at the crestal bone level on one side of the jaw.

Experimental study in minipig on contiguous implants with cemented implant connections

fig. 3 Distances of 2 to 3 mm between the adjacent implants were left. fig. 4 The metal prostheses were manufactured in the laboratory and the distance between the contact point of the adjacent crowns to the crestal bone apex was standardized in 3 mm.

fig. 5 Prostheses adapted on the implants.

were adapted for carrying out the moldings and the flaps were sutured with absorbable sutures. The transmucosal element was fitted with friction using a special atraumatic tool, which can exert the force required for the coupling, without causing damage to hard and soft tissues. Then the abutments were cemented through the transmucosal element. With this element, the cementation occurred outside the soft tissue, eliminating the risk of periimplant gingiva contamination. The excess cement leaked to the base of the abutment (which is located outside of the tissues) and was easily removed with a pellet of cotton or gauze, given its semifluid consistency in the presence of oxygen. The metal prostheses were manufactured in the laboratory and the distance between the contact point of the adjacent crowns to the crestal bone apex was standardized in 3 mm (Fig. 4). Finally they were adapted on the implants (Fig. 5). After a week, measurements were taken for the initial clinical evaluation of papilla formation between the implants. After each surgical intervention, tramadol was used (50 mg/ml) with a dosage of 3 mg/kg as analgesic therapy and ketoprofen (20 mg) with a dosage of 1 pil/20 kg as anti-inflammatory therapy. The animals also received an antibiotic therapy (Stomorgyl 10, Merial Animal Health Ltd., PaulĂnia/SP/Brazil), 1 pil/10 kg for 10 days. The animals were fed with moist feed for 14 days, when the sutures were removed. The healing was evaluated weekly and plaque control was maintained by washing the oral cavity with 0.12% chlorhexidine gluconate.

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The remaining teeth received a monthly ultrasonic instrumentation. During the experimental period, the animals received water without restriction, and were fed suitable for their race (S4, Bravisco, Bastos/SP/Brazil), in a daily amount equivalent to 2% of their weight. Eight weeks later, the clinical evaluation of papillae formation was done and after that the euthanasia of the animals was performed with a lethal dose of thiopental. The hemi-mandibles were removed, dissected and fixed in a 4% solution of formalin at pH 7 for 10 days and transferred to a solution of 70% ethanol until processing. The specimens were dehydrated in ascending ethanol concentrations up to 100%, infiltrated and embedded in LR White resin (London Resin Company, Berkshire, England) sectioned by the technique described by Donath & Breuner (14) for hard tissue. The histological slide was prepared from the most central section of each specimen and was stained with Stevenelâ&#x20AC;&#x2122;s blue and Alizarin red S for light microscopy histological analysis.

Methods of analysis to obtain the results

1) Clinical analysis The evaluation of the papillae formation between the implants was performed measuring the distance between the contact point of the adjacent crowns and the top of the papilla (CP - P) using a compass. The obtained distances were recorded by a slide caliper (0.05mm resolution). 2) Histomorphometric analysis The longitudinal histologic sections (mesiodistal) of each pair of implants were captured by a video camera Leica DFC310 FX coupled to the microscope LEICA DMLB (Leica Microsystems GmbH, Wetzlar, Germany). The images were analyzed with a special program (LAS-4.1.0 VERSION-Image processing and analysis system) in order to determine: the bone density between the implants, the percentage of bone-implant contact, the amount of crestal bone resorption between the adjacent implants and the bone loss around the implants. A single investigator performed all the measures described (A.L.G.A.). 2.1 Bone resorption around the implants The extent

De Barros R.R.M. et al.

fig. 6 Histomorphometric analysis of bone remodeling. The bone resorption around the implant (BR-I) was measured from the shoulder of the implant to the first bone-implant contact of each implant (green line). The resorption or remodeling of the crestal bone between the implants (RCO) was evaluated from the center of the dotted line (imaginary line that joined the adjacent implant shoulders) to the crestal bone peak (yellow line). Stevenel's blue and Alizarin red S stain (Magnification 2.5x)

of resorption around the implants was determined by linear measurements from the coronal portion of the implant (“shoulder”) to the first bone-toimplant contact (Fig. 6, green lines). 2.2 Crestal bone resorption between implants A line was drawn uniting the coronal portions (“shoulders”) of the adjacent implants. Then, a linear measurement was made from the central point of this imaginary line to the highest point of the crestal bone, determining the amount of alveolar crestal bone resorption (Fig. 6, yellow line). 2.3 Bone density Bone density was evaluated in the region between adjacent implants, using a predetermined rectangle as a frame for selecting the areas to be assessed. On this, the percentages of mineralized bone were evaluated, deducting the areas occupied by soft tissue, marrow spaces and implants threads (Fig. 7). 2.4 Bone-implant contact The quality of osseointegration was determined by the percentage of direct contact between bone and implant. This measurement was made for each implant in the maximum length of the rectangle that restricted the area of assessment of bone density.

Statistical analysis

Mann Whitney non-parametric test was used to compare the subcrestal and crestal groups in all the parameters evaluated. Wilcoxon non-parametric test was used for

fig.7 Histomorphometric analysis of bone density. (A) Original image with the predetermined rectangle used as a frame of evaluation in blue. (B) Duplicate image with the mineralized tissue (bone tissue) marked in red, demonstrating the first step for evaluation of this area. After that the marrow spaces, soft tissue areas and adjacent structures such as the implant threads were identified and discounted from the predetermined frame.

comparisons within the different groups (BR-I x BR-E parameters). Differences were accepted as p<0.05 and, data were presented as mean values (M) ± standard deviation (SD).

RESULTS All animals survived during the research period, however in one of them 4 implants were lost. At the end of the study period, a total of 52 implants remained to be evaluated. Clinical analysis showed that the differences between subcrestal and crestal groups were statistically significant (p=0.043), exhibiting a higher papillae formation in the subcrestal group. Results are shown in Table 1. In general, the histological observation showed the presence of parent lamellar bone representing the “preexisting” bone and newly formed bone (Fig. 8, 9, 10). The newly formed bone was present mostly in direct contact to the implant surfaces and above the coronal spires at the interimplantar regions, as evidenced in higher magnification images (Fig. 8, 9). In general, this new tissue was characterized as a parallel-fibered bone with lamellar pattern, but the surface between this and the “pre-existing” bone is evident (Fig. 9). In one specimen,

Experimental study in minipig on contiguous implants with cemented implant connections

Crestal Subcrestal Mean SD p-value

1,98

1,70

0,56

0,42 0.0433

tabLE 1 Evaluation of papillae formation. Description of the final measurements (mm) obtained from the contact point to the top of the interimplantar papilla in the different groups: Mann-Whitney; p â&#x2030;¤ 0,05.

fig.8 (A) subcrestal positioned implant with high level of osseointegration, informed by the high percentages of bone-implant contact and bone density. In (B) magnified image of the region delimited by the rectangle in (A); observe the formation of new bone completely covering the most coronal thread. Stevenel's blue and Alizarin red S stain, image A (Magnification 1.6x) and image B (Magnification 10 x).

fig. 9 New bone formation (more reddish, with wider osteocytes lacunae) in direct contact to the surface of a subcrestal positioned implant and above the most coronal thread . Stevenel's blue and Alizarin red S Stain (Magnification 10x).

fig. 10 (A) interimplantar region. (B) Magnified image delimited by the rectangle in image (A). Note the presence of osteoclasts (arrows) in the upper margin of the crestal bone causing an active resorption (crestal positioned implant). Stevenel's blue and Alizarin red S stain, image A (Magnification 1.6x) and image B (Magnification 10x).

osteoclasts were evidenced at the surface of the crestal bone at the interimplant region, characterizing an active zone of bone resorption (Fig. 11). Histomorphometrically, the parameters currently used to evaluate the osseointegration showed statistically better results for the subcrestal group. Considering the bone density it was observed 52.39% in subcrestal group versus 45.22% in crestal group (p = 0.049) and considering the bone-implant contact (BIC) it was observed 54.13% in subcrestal group and 42.46% in crestal group (p=0.014) (Table 2) (Fig. 8, 10). The crestal bone remodeling, which is evaluated between

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the adjacent implants, also demonstrated statistically better results for the subcrestal group (1.17 mm x 1.63 mm; p=0.012). The other two linear parameters that evaluated the bone resorption around the implants at the interimplantar area (BR-I) and at the free-ends area (BR-E) showed numerical better results for the subcrestal group, but without statistical relevance (Table 2). The comparison of these parameters (BR-I x BR-E) within the groups showed statistically significant differences in both, crestal and subcrestal groups (Table 3), probably evidencing the positive influence of the contact point in bone remodeling.

De Barros R.R.M. et al.

fig. 11 Comparison of the bone-implant contact level between the different groups: (A) subcrestal group and (B) crestal group. Stevenel's blue and Alizarin red S stain, image A (Magnification 1.6x) and image B (Magnification 1.6x).

BD (%)

BIC(%)

CBR (mm) BR-I (mm) BR- FE (mm)

Subcrestal Crestal

52,39 ± 7,26 54,13 ± 11,75 1,17 ± 0,41 2,2 7± 0,75 3,35 ± 1,16 45,22 ± 8,55 42,46 ± 16,69

1,63 ± 0,51 2,60 ± 0,86 3,96 ± 1,18

p-value

0,049*

0,012*

0,014*

0,223

In the present study the subcrestal placement of cementretained abutment (CRA) implants revealed better results when compared to the crestal placement in a particular situation featuring adjacent implants immediately loaded in a minipig model. The subcrestal placement of an implant, for esthetic reasons, intends to compensate crestal bone remodeling and to improve the BIC at the neck region of the implant (15, 16), but this may be jeopardized by the implantabutment connection. In 2-piece implants, the crestal bone levels appeared dependent on the location of the microgap that exists at the implant-abutment interface (17-19). The least bone resorption and peri-implant inflammation were observed in the cases where the microgap was located above the alveolar crest (18); indeed, if the microgap is placed below the alveolar crest it can cause crestal bone loss during the healing phase (2, 20). Conversely, in the present study the adjacent cementretained abutment implants showed statistically better results when placed subcrestally, which had already been observed in previous studies using adjacent Morse cone connection implants (21, 22). This may be due to the control of the bacteria penetration at this interface

0,004* 0,003*

0,304

tabLE 2 Histomorphometric analysis. Parameters used to compare the subcrestal and crestal groups (mean ± SD). Mann-Whitney; *: comparisons with statistical significance( p ≤ 0,05) BD: Bone density (percentage) BIC: Bone-to-implant contact (percentage) CBR: Crestal bone resorption between implants (mm) BR-I: Bone resorption around the implants (interimplantar region) (mm) BR-FE: Bone resorption around the implants (free-ends’ regions) (mm)

DISCUSSION

BR-I (mm) BR- FE (mm) p-value Subcrestal 2,2 7± 0,75 3,35 ± 1,16 2,60 ± 0,86 3,96 ± 1,18 Crestal

tabLE 3 Comparisons within groups (crestal and subcrestal, separately) regarding the parameters of resorption around the implants in the region between the adjacent implants and at the free-ends regions (BR-I x BR-FE). Wilcoxon; *: comparisons with statistical significance (p ≤ 0,05). BR-I: Bone resorption around the implants (interimplantar region) (mm) BR-FE: Bone resorption around the implants (free-ends’ regions) (mm)

of union. The Cone Morse connection system provides a precisely machined Morse taper that prevents abutment rotation on the implant and shifts the microgap toward the center of the implant and away from the crestal bone (23); in this system, just a mechanical sealing can be achieved, and it depends from a precise and expensive mechanical union of abutment and implant (24). Whilst in the CRA implants the microgap is always observed, even tough filled by the fixation cement (3): this allows a prevention of the repetitive micromovements between the parts during clinical function and bacteria accumulation, both capable to induce localized inflammation and crestal bone loss (25-27). In Barros et al. (21) the subcrestal positioning of implants resulted in bone located above the Morse cone connection implant shoulder. In the present study it was observed bone above the first threads of some implants of the subcrestal group (Fig. 8, 9), but never in the crestal group. In contrast, Hermann et al. (18) and Piattelli et al. (10) reported that when the implant-abutment junction was positioned deeper within the bone, a more pronounced loss of vertical crestal bone height was observed and, again, this finding was attributed to the implant/abutment connection used. In the present study, statistical better results of crestal

Experimental study in minipig on contiguous implants with cemented implant connections

bone remodeling, BIC and BD were achieved by the CRA subcrestally placed implants compared to the crestally placed implants. These parameters were all quantified at the interimplantar area, because the aim of the study was the analysis of adjacent implants. It is well known that it is much more difficult to maintain the alveolar crest between adjacent implants when compared to single implants, but it is also reported that the preservation of the crestal bone between adjacent implants will dictate the papillae formation, increasing the chances to achieve the desired natural-looking restorations (28). Thus, a special attention was given to this area to focus the problems encountered during the treatment with contiguous immediately loaded implants. Among the factors that required caution in this approach, the interimplant distance can be cited, since it is related to lateral bone loss around the implants and the further vertical crestal bone loss. A previous study has already concluded that adjacent implants should be placed at a distance between 2 and 4 mm to favor the magnitude of the crestal bone (28). The authors evaluated four different situations: group 1 with interimplant distance <2 mm, group 2 with interimplant distance between 2.01 and 3 mm, group 3 with interimplant distance between 3.01 and 4 mm and group 4 with interimplant distance >4 mm and achieved the better results along the time in groups 2 and 3. The authors considered not only the vertical crestal bone loss, but also the successful esthetics achieved in the treated areas. Other studies supported this finding (21, 29, 30) and, additionally, showed that the presence of papilla decreases when the distance between the crestal bone and the contact point was bigger than 5 mm, suggesting a distance of 3 mm. For these reasons in the present study an interimplant distance of 2 to 3 mm was adopted and the distance between the crestal bone to the contact point of the crowns was fixed in 3 mm to favor the preservation of the crestal bone height and the papillae formation in both experimental groups. The statistically better results obtained in the subcrestal group regarding the crestal bone remodelling and the papillae formations (21, 31, 32) are of great importance for the treatment of esthetic regions once the preservation of the bone height combined to the fill of the interdental space by the papilla formation will ensure a final result closer to the natural condition. Furthermore, the non-exposure of the implant into the soft tissues will guarantee that the implant metal will not compromise gingival translucency and, once more, will contribute to the final esthetic result. The bone remodeling of the crestal bone between the implants was not the only parameter used to assess the bone stability in the present study; the bone resorption was also evaluated in each implant individually from the shoulder of the implant to the first bone-to-implant contact in both sides, at the interimplant side and at the free-end side. Subcrestal and crestal groups exhibited bone resorption in both sides evaluated without statistical

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difference between them. This could be related to the establishment of the biologic seal composed by sulcus, junctional epithelium and connective tissue attachment around the implants, but may also be explained as a real bone loss process, usually related to the presence of a bacterial biofilm or overloading. Differently from the canine model, the minipigs used were not obedient and passive. Usually, they became calmer when they were fed and therefore their food was divided in more meals during the day. Another medical recommendation was keeping them in a larger environment for grazing. These factors made the bacterial plaque control more difficult, once each procedure involved the transportation of animals to the operating room and anesthesia. Four implant losses were observed in one minipig of the present study, two in each hemi-mandible. They occurred without the detaching of the crown. The radiographs showed extensive alveolar bone loss, probably caused by the factors listed above. Still on the evaluation around the implants, another interesting result was observed when comparing the rates of bone resorption at the interimplantar area with the free end area. The statistically significant differences obtained were due to the lower values observed in the interimplantar area, confirming that the presence of the contact point may favor the maintenance of the underlying bone structure (29, 30, 32). The present study used a challenging situation defined by the immediate loading in the minipig model to evaluate the CRA implants. Previous studies with the same type of implant-abutment connection, instead, used dogs and a delayed loading protocol, when the implants were probably already osseointegrated (33). Differently from the present study, their objective was to clinically evaluate the incidence of abutment loosening in implants with screw or cement implant-abutment connections, and their relation to the increased crestal bone resorption. Abutment loosening produces wider space between implant and abutment, causing mobility of the whole prosthetic restoration and also facilitating bacterial colonization inside the implant. They found 27% loosened screws in screwed abutments group, whereas no loosening in cemented abutments. In accordance to this finding no abutment loosening was observed in the present study, which has to be considered as an advantage to this protocol, diminishing the time required to the maintenance of prosthetic restorations and the risk of the screw fracture, and finally preventing an increased crestal bone resorption. In terms of bone-to-implant contact, which remains the most common parameter to evaluate the osseointegration around dental implants, the percentages varied a lot between the studies involving minipigs and the results of the present study were within the range of values reported in the literature (34-36). However, the present study was the only one that applied the protocol of immediate loading.

De Barros R.R.M. et al.

CONCLUSION The subcrestal placement of cement-retained abutment implants achieved better indexes of papillae formation, crestal bone remodeling, bone density and bone-toimplant contact at the interimplant area when compared to the same implants placed at the crestal level after immediate loading in the minipig model. The clinical significance of these results may be the use of this type of implant in a subcrestal positioning in esthetic areas, in order to favor the crestal bone maintenance and papillae formation at the interimplant area of contiguous immediately loaded implants.

ACKNOWLEDGEMENTS This study was supported in part by FAPESP (process numbers 2010/19035-0 and 2010/19737-5). The authors declare no conflict of interest relevant to the content of this paper.

REFERENCES 1. Tarnow DP, Cho SC, Wallace SS. The effect of inter-implant distance on the height of inter-implant bone crest. J Periodontol 2000; 71:546-9. 2. Oh TJ, Yoon J, Misch CE, Wang HL. The causes ofearly implant bone loss: Myth or science? J Periodontol 2002; 73:322-33. 3. Piattelli A, Scarano A, Paolantonio M, et al. Fluids and microbial penetration in the internal part of cement-retained versus screw-retained implant-abutment connections. J Periodontol 2001; 72:1146-50. 4. Assenza B, Tripodi D, Scarano A, et al. Bacterial leakage in implants with different implant-abutment connections: an in vitro study. J Periodontol 2012; 83:491-7. 5. Palacci P. Optimal implant positioning. In: Palacci P. Esthetic Implant Dentistry. Soft and Hard Tissue Management. Quintessence Publishing Company Inc. 2001:101–37. 6. Palacci P & Ericson L. Implant placement philosophy. In: Palacci P. Esthetic Implant Dentistry. Quintessence Publishing Company Inc. 2001:69–89. 7. Buser D, Martin WC, Belser UC. Surgical considerations for single tooth replacements in the esthetic zone: standard procedures in sites without bone deficiencies. In: Belser UC, Martin W, Jung R, Hammerle CH, Schmid B, Morton D, Buser D. ITI Treatment Guide. Implant Placement in the Esthetic Zone. Single Tooth Replacements. Quintessence Publishing Company Ltd. 2007:26–37. 8. Broggini N, McManus LM, Hermann JS, et al. Periimplant inflammation defined by the implant-abutment interface. J Dent Res 2006; 85:473-8. 9. Todescan FF, Pustiglioni FE, Imbronito AV, Albrektsson T, Gioso M. Influence of the microgap in the periimplant hard and soft tissues: A histomorphometric study in dogs. Int J Oral Maxillofac Implants 2002; 17:467-72. 10. Piattelli A, Vrespa G, Petrone G, Iezzi G, Annibali S, Scarano A. Role of the microgap between implant and abutment: A retrospective histologic evaluation in monkeys. J Periodontol 2003; 74:346-52. 11. Elian N, Bloom M, Dard M, Cho SC, Trushkowsky RD, Tarnow D. Effect of interimplant distance (2 and 3 mm) on the height of interimplant bone crest: a histomorphometric evaluation. J Periodontol. 2011; 82:1749-56. 12. Funato A, Salama MA, Ishikawa T, Garber DA, Salama H. Timing, positioning, and sequential staging in esthetic implant therapy: a four-dimensional perspective. Int J Periodontics Restorative Dent 2007; 27:313-23. 13. Lazzara RJ, Porter SS. Platform Switching: A New Concept in Implant Dentistry for Controlling Postrestorative Crestal Bone Levels. Int J Periodontics Restorative Dent 2006; 26:9-17. 14. Donath K, Breuner G. A method for the study of undecalcified bones and teeth

with attached soft tissues. The Säge-Schliff (sawing and grinding) technique. J Oral Pathol 1982; 11:318-26. 15. Hämmerle CH, Brägger U, Bürgin W, Lang NP. The effect of subcrestal placement of the polished surface of ITI implants on marginal soft and hard tissues. Clin Oral Implants Res 1996; 7:111-9. 16. Welander M, Abrahamsson I, Berglundh T. Placement of two-part implants in sites with different buccal and lingual bone heights. J Periodontol 2009; 80:324-9. 17. Broggini M, McManus LM, Hermann JS, et al. Persistent acute inflammation at the implant-abutment interface. J Dent Res 2003; 82:232-7. 18. Hermann JS, Schofield JD, Schenk RK, Buser D, Cochran DL. Influence of the size of the microgap on crestal bone changes around titanium implants. A histometric evaluation of unloaded non-submerged implants in the canine mandible. J Periodontol 2001; 72:1372-83. 19. Hermann JS, Buser D, Schenk RK, Cochran DL. Crestal bone changes around titanium implants. A histometric evaluation of unloaded non-submerged and submerged implants in the canine mandible. J Periodontol 2000; 71:1412-24. 20. Assenza B, Artese L, Scarano A, et al. Screw vs cement-implant-retained restorations: an experimental study in the beagle. Part 2. Immunohistochemical evaluation of the peri-implant tissues. J Oral Implantol 2006; 32:1-7. 21. Barros RRM, Novaes AB Jr, Muglia VA, Iezzi G, Piattelli A. Influence of interimplant distances and placement depth on peri-implant bone remodeling of adjacent and immediately loaded Morse cone connection implants: a histomorphometric study in dogs. Clin Oral Implants Res 2010; 21:371-8. 22. Weng D, Nagata MJ, Leite CM, de Melo LG, Bosco AF. Influence of microgap location and configuration on radiographic bone loss in nonsubmerged implants: an experimental study in dogs. Int J Prosthodont 2011; 24:445-52. 23. Morris HF, Ochi S, Crum P, Orenstein IH, Winkler S. AICRG, Part I: a 6-year multicentered, multidisciplinary clinical study of a new and innovative implant design. J Oral Implantol 2004; 30:125-33. 24. Tripodi D, Vantaggiato G, Scarano A, et al. An in vitro investigation concerning the bacterial leakage at implants with internal hexagon and Morse taper implantabutment connections. Implant Dent 2012; 21:335-9. 25. Covani U, Marconcini S, Crespi R, Barone A. Bacterial plaque colonization around dental implant surfaces. Implant Dent 2006; 15:298-304. 26. Tenenbaum H, Schaaf JF, Cuisinier FJ. Histological analysis of the Ankylos periimplant soft tissues in a dog model. Implant Dent 2003; 12:259-65. 27. Chou CT, Morris HF, Ochi S, Walker L, DesRosiers D. AICRG, Part II: crestal bone loss associated with the Ankylos implant: loading to 36 months. J Oral Implantol 2004; 30:134-43. 28. Degidi M, Novaes AB Jr, Nardi D, Piattelli A. Outcome analysis of immediately placed, immediately restored implants in the esthetic area: the clinical relevance of different interimplant distances. J Periodontol 2008; 79:1056-61. 29. Novaes AB Jr, Oliveira RR, Muglia VA, Papalexiou V, Taba M. The effects of interimplant distances on papilla formation and crestal resorption in implants with a Morse cone connection and a platform switch: a histomorphometric study in dogs. J Periodontol 2006; 77:1839-49. 30. Papalexiou V, Novaes AB Jr, Ribeiro RF, Muglia V, Oliveira RR. Influence of the interimplant distance on crestal bone resorption and bone density: a histomorphometric study in dogs. J Periodontol 2006; 77:614-21. 31. Degidi M, Iezzi G, Scarano A, Piattelli A. Immediately loaded titanium implant with a tissue-stabilizing/maintaining design (‘beyond platform switch’) retrieved from man after 4 weeks: a histological and histomorphometrical evaluation. A case report. Clin Oral Implants Res 2008; 19:276-82. 32. Novaes AB Jr, Barros RRM, Muglia VA, Borges GJ. Influence of interimplant distances and placement depth on papilla formation and crestal resorption: a clinical and radiographic study in dogs. J Oral Implantol 2009; 35:18-27. 33. Assenza B, Scarano A, Leghissa G, et al. Screw- vs cement-implant-retained restorations: an experimental study in the Beagle. Part 1. Screw and abutment loosening. J Oral Implantol 2005; 31:242-6. 34. Verket A, Lyngstadaas SP, Rønold HJ, Wohlfahrt JC. Osseointegration of dental implants in extraction sockets preserved with porous titanium granules - an experimental study. Clin Oral Implants Res. 2014;25:e100-8. 35. Broggini N, Tosatti S, Ferguson SJ, et al. Evaluation of chemically modified SLA implants (modSLA) biofunctionalized with integrin (RGD)- and heparin (KRSR)binding peptides. J Biomed Mater Res A 2012;100:703-11. 36. Saulacic N, Bosshardt DD, Bornstein MM, Berner S, Buser D. Bone apposition to a titanium-zirconium alloy implant, as compared to two other titanium-containing implants. Eur Cell Mater 2012; 23:273-86.

P. Diotallevi1, L. Dal Carlo2, M.E. Pasqualini2, S. Mazziotti3, M. Nardone4, E. Moglioni2 1

Radiology Unit, Eosmed - Rome, Italy ARASS Association for research and social activities in Stomatology, Non profit Entity, Rome, Italy - Private practice 3 Department of Radiological Sciences, University of Messina, Italy 4 Department of Public Health, Ministry of Health, Rome, Italy 2

Radiological evaluation of long term complications of oral rehabilitations of thin ridges with titanium blade implants to cite this article Diotallevi P, Dal Carlo L, Pasqualini ME, Mazziotti S, Nardone M, Moglioni E. Radiological evaluation of long term complications of oral rehabilitations of thin ridges with titanium blade implants. J Osseointegr 2014;6(1):11-14.

Keywords Blade implants; Implant radiology; Oral implantology.

ABSTRACT

Introduction

Aim The aim of this study was to assess the sensitivity of orthopantomography (OPT) in the diagnosis of long term complications in oral rehabilitations with blade implants. Materials and methods A total of 235 blade implants in 189 patients, inserted between 1988 and 2003, were retrospectively analyzed. The records consisted of a first OPT taken between January and December 2010, and a second one 12 months after. The evaluation of implant health considered: integrity of the blade, normal radiological representation of the bone around the implant, dense and cortical appearance of bone around the implant collar. The evaluation of radiological complications considered: implant fracture, bone resorption around the implant, recession of the bone around the implant collar. Results The sensitivity of the panoramic evaluation was equal to 100%. The complications detected were 5 cases of periimplantitis, 9 cases of bone pericervical bone recession and 3 cases of fracture of the implant body. In cases of pericervical bone resorption the following radiological check up 12 months after the first one showed the progression of the disease in 6 out of 9 cases, with irreversible implant failure. In subjects with a radiological pattern of implant health there were no complications in the subsequent check up after 12 months. In the subjects with complications the specificity was equal to 100%. Conclusion The radiographic evaluation by the means of OPT has shown high sensitivity in the diagnosis of long term complications of oral rehabilitations with blade implants and allows prompt therapeutic interventions. Radiological complications appeared mostly in the long term check ups and mainly consisted in recession of the bone around the neck or around the entire implant. More rarely implant fractures occurred, which, in the case of blades, sometimes were not associated with any clinical symptoms: therefore, postsurgical evaluation should not be separated from diagnostic imaging.

The alveolar crest is defined as alveolar bone with a thickness lesser than 4 mm. This condition represents about 10% of the anatomical situations which an implantologist usually deals with (1, 2, 3). Different surgical approaches exist for the rehabilitation of thin crests. Demolitive techniques, such as split crest, are based on the principle that the anatomy can be adjusted to the implant: the cortical bone tissue is fractured, usually at the vestibular level, in order to artificially create the space necessary to insert the screws (4, 5, 6, 7, 8, 9). Conservative techniques imply the use of thin implants, capable of penetrating between the two cortical bones, exploiting their stiffness to acquire stability. An example are blade implants, similar in shape to surgical scalpels, which are driven into the bone with a press fit technique, or rather with light percussions. Compared to screws, these implants are less used, though published data report similar results about their osteointegration, which always occurs (10, 11, 12, 13, 14, 15). However, blade implants are sometimes affected by complications whose prompt diagnosis is fundamental for implant survival. The aim of this study was to evaluate the sensitivity of orthopantomography in the diagnosis of long term complications in oral rehabilitations with blade implants.

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MATERIALS AND METHODS For the study were retrospectively analyzed all patients who had previously been rehabilitated by the authors with blade implants (between 1988 and 2003) and who underwent long term radiographic control in the period between January and December 2010. The orthopantomographies of 189 subjects, 73

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males and 116 females, with an average age of 68, wew analyzed. The blade implants had been inserted by the authors in the period between 1988 and 2003 in patients with thin crests (thickness equal or less than 5 mm), as assessed by means of a CT scan in 118 cases, a surgical feeler gauge in 27 cases and intraoperative measurement in 44 cases (Fig. 1). In total, 41 subjects underwent rehabilitations in the upper maxilla, with 43 blade implants of which 27 in the central sectors and 16 in the distal ones; 148 subjects underwent rehabilitations of the mandible, with a total of 192 blade implants, 18 of which in the distal zones and 12 in the central ones. In all patients, due to the typical radiological artifacts generated by the blades in the CT scans, the postsurgical check-ups were carried out by means of orthopantomography (OPT). All the subjects whose implants had not been removed underwent a second orthopantomography after 12 months (between January and December 2011) in order to re-assess the reliability of the radiological indices through implant monitoring. Therefore, all radiographs were retrospectively analyzed. The evaluation of implant health considered: integrity of the blade, normal radiological representation of the bone around the implant, dense and cortical appearance of bone around the implant collar. The evaluation of radiological complications considered: implant fracture, bone resorption around the implant, and recession of the bone around the implant collar (15, 20, 21).

All the subjects involved signed an informed consent form. The study was evaluated and approved by the Arass Ethical Committee.

RESULTS The overall percentage of healthy implants was equal to 93.2% (219/235). In detail: up to 12 years after surgery, implant survival was 99% (102/103), while in the check up after more than 12 years, the percentage dropped to 86.3% (114/132). The complications detected were 5 cases of peri-implantitis, 9 cases of pericervical bone recession and 3 cases of fracture of the implant body. In 14 cases out of 17 there were signs of local phlogosis associated to pain. In cases of pericervical bone recession the radiological check-up performed after 12 months showed the progression of the disease in 6 out of 9 cases, associated to hypermobility, with irreversible failure of the implant. These 6 patients included 4 who refused the therapeutic attempts (occlusal treatment and antibiotic therapy in the pocket) aimed to avoid blade failure. In treated subjects 3 out of 5 implants were still stable after 12 months. In subjects whose radiographs showed healthy implants, neither clinical signs nor complications were detected at the following check up 12 months later. The sensitivity of OPT was therefore equal to 100%. In subjects with complications the specificity was equal to 100%.

fig. 1 TC image of a thin crest (1a) and corresponding anatomical appearance in the intraoperative image (1b).

fig. 2 Bone resorption around the neck of the blade, mild (a), moderate (b) and severe (c).

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Radiographic detection of delayed complications in thin ridges rehabilitated with blade implants

DISCUSSION The long term X-ray evaluation of blade implants was carried out with orthopantomography, since these implants produce radiological artifacts in the TC scan, including those with ‘cone beam’ systems (22, 23, 24). Orthopantomography was highly reliable in the diagnosis of complications, with 100% sensitivity. This technique leads to prompt therapeutic interventions, which in some cases delay or prevent irreversible implant loss (25). In the present retrospective study, it was observed that in 9 cases of pericervical bone recession the radiological signs were accompanied by the clinical detection of peri-implant pocket inflammation. Moreover, the radiographic signs of pericervical bone regression were mainly observed in the distal regions of the lower arch, that was the area where the implants are subjected to the greatest stress from a biomechanical point of view (26). Considering the development observed in our case series, we believe that such a finding clearly indicates the need for a new treatment, even if not immediately (as in the

case of the peri-implantitis). An alteration of the pericervical bone must, in any case, be pointed out by the radiologist, so that immediate interventions aiming to heal the lesion can be performed (Fig. 2). In the five cases in which bone rarefaction around the whole implant was radiographically observed, clinical examination always showed implant hypermobility, associated to local signs of phlogosis and pain when pressure was applied. In these situations the implant was immediately removed and replaced (Fig. 3). In 2 out of the 3 cases of implant fracture, both clinical examination and X-ray highlighted the fracture around the emerging collar, associated neither to phlogosis nor local pain, or to X-ray alterations of the peri-implant bone (Fig. 4a). In the third case, the fracture occurred in the endosseous part of the blade, an area not clinically evaluable and without any signs of local phlogosis; moreover, the stability of the fractured blade seemed to be mantained: such complication was therefore only visible through radiological examination which allowed the diagnosis of an otherwise asymptomatic fracture (Fig. 4b). This fracture was considered an adaptation of the implant to the local anatomy and physiology: moreover, it wasn’t removed, since the amount of blade still intact continued to properly function. In all cases radiographically analyzed, the cortical bone around the blade collar, as well as the peri-implant spongy bone appeared to be normal. This pattern was always combined with a clinical absence of pain, a correct peri-implant sounding and absence of implants mobility. In this study mid term success rates resulted to be better than those reported in the literature for implant-supported rehabilitations obtained with split crest techniques; whereas in the long term, the results of the present study do not significantly differ from those reported by other authors (9, 27, 28, 29, 30).

CONCLUSION

fig. 3 Radiological appearance of peri-implantitis with bone resorption around the entire implant.

Orthopantomography was highly reliable in the diagnosis of long-term complications in oral rehabilitations with blade implants, showing a sensitivity equal to 100% and allowing the prompt adoption of adequate

fig. 4 Fracture of the blade implant, in correspondence of the collar (4a) and of the intra-osseous part (4b).

Diotallevi P. et al.

fig. 5 Radiological pattern of normality in post-surgical checkups (OPT details): regular representation of the cortical bone around the neck of the blade and of the peri-implant cancellous bone.

therapeutic interventions preventing irreversible implant failure. Radiological complications appeared mostly in the long term check-up and mainly consisted in recession of the bone around the neck or around the entire implant. More rarely implant fractures occurred, which, in the case of blades, sometimes were not associated with any clinical symptoms; therefore, post-surgical evaluation should not be separated from diagnostic imaging. Compared with the data in the literature relating to rehabilitation using alternative techniques, such as the split crest, complications resulting from blade implants were less frequent in the 12 year checkups: after that time the results do not differ significantly.

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J.L. Calvo-Guirado1, A. Boquete-Castro2, J. Guardia3, A. Aguilar Salvatierra Raya3, J.M. Martínez González4, G. Gómez-Moreno5 1

Senior Lecturer of General Dentistry and Implantology, DDS, MS, PhD. Faculty of Medicine and Dentistry, University of Murcia, Murcia, Spain 2 Postgraduate Student, Master in Integrated Dentistry and Implantology, DDS, Faculty of Medicine and Dentistry, University of Murcia, Murcia, Spain 3 Collaborator of Pharmacological Interactions in Dentistry, DDS, PhD. Faculty of Dentistry, University of Granada, Ganada, Spain 4 Senior Lecturer of Oral Surgery, DDS, MS, PhD. University Complutense of Madrid, Madrid, Spain 5 Full Professor of Pharmacological Interactions in Dentistry, DDS, PhD. Faculty of Dentistry, University of Granada, Granada, Spain

Osteonecrosis of the jaw after dental implant placement. A case report to cite this article Calvo-Guirado JL, Boquete-Castro A, Guardia J, Aguilar Salvatierra Raya A, Martínez González JM, Gómez-Moreno G. Osteonecrosis of the jaw after dental implant placement. A case report. J Osseointegr 2014;6(1):15-18.

ABSTRACT Background In the past few years, the occurrence of an oral lesion, called osteonecrosis of the jaw, has increasingly been reported in patients undergoing treatment with systemic bisphosphonates (BPs); however, few papers dealing with oral biphosphonates related osteonecrosis of the jaws (BRONJ) can be found in the literature. The purpose of the present case was to report an occurrence of BRONJ after implant insertion. Case report Ten years ago, eight dental implants were inserted in the jaw of a 65-year-old female. After 5 years of treatment with alendronic acid, a breakdown of the oral mucosa covering the implants occurred with a purulent discharge in the left side of the jaw; periapical radiolucency was present around both distal implants. An en-block resection of the alveolar bone including the two implants was performed. Thirthy-five hyperbaric sessions were taken and no signs of recurrence of the lesion were observed after a follow-up of 20 months. Before the new implant insertion, the patient had suspended the treatment with alendronic acid for 6 months. At the interface of one of the implants, a gap was observed between bone and implant. This bone was non vital, and many osteocyte lacunae were empty. Moreover, this bone appeared to be partially demineralized. Conclusion There is certainly a temporal association between oral BPs use and development of BRONJ, but a correlation does not necessarily mean causation. In patients undergoing oral treatment, clinicians must be aware of the increased risk of implant failure. Keywords Alendronate; Bisphosphonates; Bisphosphonaterelated osteonecrosis of the jaw (BRONJ); Dental implants.

Introduction Oral bisphosphonates are commonly prescribed for patients with osteoporosis to arrest bone loss and preserve bone density. Nitrogen-containing bisphosphonates, such as alendronate, risedronate, ibandronate, and zoledronate, are agents that inhibit bone resorption (1, 2). Recent reports have shown a link between these medications and osteonecrosis of the jaw, which is a complication resulting in exposed non vital maxillary or mandibular bone (3, 4,5,6). Attempts have recently been made to predict the development of bisphosphonate-related osteonecrosis of the jaw (BRONJ). Several prospective studies have investigated the predictive value of serum levels of C-terminal telopeptide of collagen I for the development of BRONJ. Despite measurement of serum levels of Cterminal telopeptide of collagen I is not a definitive predictor of BRONJ, it plays an important role in the risk assessment before oral surgery (4). Bisphosphonateassociated osteonecrosis is a complication that almost exclusively affects the jaw bones. As this complication has only been recognized within the past 10 years, management of patients with biphosphonate- associated osteonecrosis is poorly defined. The clinical presentation of BRONJ often mimics that of other conditions, such as routine dental disease, osteoradionecrosis or avascular necrosis; therefore, diagnosis can be difficult. Physicians have to choose between continuing the bisphosphonate therapy (to reduce the risk of skeletal complications in patients with metastatic bone disease or osteoporosis) or discontinuing the drug (to possibly improve the odds for tissue healing) (7). The incidence of BRONJ after oral surgery involving bone is greater among patients receiving frequent, high doses of intravenous biphosphonates than among patients taking oral BPs (8). BRONJ seems resistant to conventional treatment approaches. Resection of the

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necrotic bone followed by an adequate wound closure is a surgical technique that shows high success rates, so patients may benefit from this approach (9). Future research should focus on the pathobiological mechanisms involved in the development of BRONJ, which could help to explain why this complication affects only a small number of those who use bisphosphonates, and also suggest strategies for prevention and management (7).

A 65-year-old woman has been taking oral alendronic acid (Fosavance®, MS&D, Whitehousestation, USA) as a treatment of postmenopausal osteoporosis disease during the last 5 years. The dose of the bisphosponate was one tablet of 70 mg once a week. The woman was non-smoker and had a good oral hygiene. No other risk factors for osteonecrosis were present. In the first surgery, 10 years ago, eight SteriOss (Nobelbiocare, Göteborg, Sweden) implants were placed in the mandible in the positions 4.6, 4.5, 4.3, 4.2, 4.1, 3.1, 3.2, 3.3, 3.5, 3.6 and a screwed implant-supported prosthesis was realized. After 5 years of oral biphosphonates use, the patient referred punching pain, numbness and paresthesia. In an oral exploration, sequestrum formation was noted at the left side of mandible (Fig. 1). Radiolucency was

present around both left posterior implants (Fig. 2). A resection of the alveolar bone including the two distal implants was performed under local anesthesia, with deep margins in an apparently healthy bone; the flaps were accurately sutured. The implants and the surrounding tissues were stored immediately after removal in 10% neutral buffered formalin. Microscopical analysis of the specimens was carried out (Fig. 3). Osteonecrosis process continued advancing, so five of the eight initial implants were lost. Only implants in position 3.1, 3.6 and 4.6 survived (Fig. 4, 5). The histopathological examination of the specimens revealed BRONJ. After the surgical resection of affected areas and the pharmacological treatment (Amoxiciline 500 mg/6h + Clorhedixine 0.12%) bone did not achieve the adequate level of regeneration; therefore, the patient underwent 6-months sessions of hyperbaric camera (Naval Hospital, Cartagena, Murcia, Spain). Sessions were daily, with a duration of an hour. Moreover, the patient underwent a strict clinical and radiological follow-up. After the evaluation period, bone remodeling of the defects was successful and no signs of recurrence of osteonecrosis were detectable. On postoperative follow-up the wound was well healed and X-ray showed good periapical bone remodeling. Subsequently, four additional M4 Implants (MIS, Tel Aviv Israel) were inserted in the lower jaw (3.3, 3.2, 4.2, 4.3). Before implant insertion, the patient had

fig. 1 Sequestrum formation in the mandible; intraoral aspect.

fig. 2 Sequestrum formation in mandible; radiographic aspect.

fig. 3 Tissues resected for microscopic evaluation.

fig.4 Loss of implant 3.6.

CASE REPORT

A case of bisphosphonate-related osteonecrosis of the jaw

fig. 5 Remaining implants.

suspended the oral biphosphonate treatment for 6 months after indication of her specialist, and according to the approved protocol in use. No preexisting bone lesions were present at the preoperative panoramic radiography. After 4 months, implants osseointegration was successful and prosthetic rehabilitation was carried out (Fig. 6). The histopatological examination was carried out. Microscopic analysis of the specimens revealed as follows. - Fragment 1: the sample corresponded to trabecular bone. The main part of the sample was constituted by small pieces of bone presenting normal characteristics, but surrounded of several necrotic focuses with frequent images of â&#x20AC;&#x153;ghost trabeculesâ&#x20AC;? situated in the centre of wide friables and disorganized necrotic areas. - Fragment 2: The other fragment corresponded to spongy bone with multiple necrotic areas of irregular disposition. Those areas were present in both samples, on the edges of them. Diagnosis was the same for both samples: bone fragment with several necrotic areas, in other words, bone sequestration.

DISCUSSION Bisphosphonates suppress bone resorption by interfering with osteoclast activity. Several of these agents have been shown to prevent fractures and increase bone mineral density in patients with osteoporosis. Longterm bisphosphonate therapy has been associated with osteonecrosis of the jaw and atypical femur fractures (10). Since 2003, there have been flurry of case reports and case series suggesting that bisphosphonate use may be associated with a condition called ONJ (osteonecrosis of the jaw) (11). Recent systematic reviews indicate that the use of bisphosphonates for osteoporosis is associated with an ONJ incidence of less than 1 in 100,000 patientyears of exposure (12, 13). ONJ appears to occur most often in patients with advanced cancer, particularly

March 2014; 6(1) ÂŠ ariesdue

fig. 6 Final panoramic radiograph after BRONJ treatment and implant replacement.

in those with multiple myeloma or breast cancer, and specifically in those undergoing dental procedures (12, 14). The current definition of ONJ is based on clinical findings and includes nonhealing lesions with exposed bone, but without evidence of bone necrosis (12, 15). Many pathogenic factors have been postulated to explain how bisphosphonates may play a role in ONJ. These include effects on blood supply, angiogenesis, excessive bone turnover in jaws leading to increased bisphosphonate uptake, excessive suppression by bisphosphonates of osteoclastic bone resorption, impaired mucosal healing, and use of other drugs (e.g., immunosuppressives and glucocorticoids) (16, 17). Health care providers have been encouraged to advise their patients to practice good oral hygiene and have regular dental visits. If an invasive dental procedure is required, there is no evidence that discontinuation of bisphosphonate therapy improves dental outcomes, although many guidelines recommend some form of interruption (12, 18). Ozone therapy had proven efficacy on improving the benefits of surgical and pharmacologic treatments, favoring the complete healing of the lesions with the disappearance of symptoms and even had brought cases of lesion progression down to zero. Thus, ozone therapy is a reliable option in treatment of ONJ; its benefits are remarkable and it improves significantly the outcomes of the surgical approach. Into the chamber, patients breath compressed air through oronasal mask, tube or endotraqueal intubation. Bisphosphonates exert their therapeutic effects by reducing bone resorption, and this leads to a reduction in bone remodeling and turnover (19). The degree of reduction of bone turnover achieved by each bisphosphonate, as well as the duration of action appears to be associated with their mineral-binding affinity and skeletal retention. Bisphosphonates with higher mineral-binding affinity and potential retention, such as alendronate and zoledronate, are associated with greater reduction of bone turnover and have a longer duration of effect after treatment ending. Bisphosphonates with

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lower mineral-binding affinity and retention, such as risedronate and etidronate, appear to reduce bone turnover less and this effect seems to be more readily reversible when therapy stops (2). A recent review of the available evidence on long-term efficacy and safety of osteoporosis treatments, indicated that it may be beneficial to continue osteoporosis therapy indefinitely in the majority of patients, with discontinuation of treatment in some specific cases, such as need of oral surgery.

CONCLUSION Osteoporosis poses an increased risk of fractures, which lead to significant pain, morbidity, functional disability and dependence, and mortality. In our opinion, the significant positive benefits of bisphosphonates offered to patients with osteoporosis outweigh the relatively small risk of developing ONJ. Nevertheless, prescribing clinicians should understand and recognize this clinical entity and fully explain all the benefits and risks of bisphosphonate therapy to their patients.

Conflict of interests

All materials used in this study were purchased by the main author and it is therefore free of any commercial or institutional interests.

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