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BASIC AND CLINICAL RESEARCH

Alcohol Intake and Osseointegration Around Implants: A Histometric and Scanning Electron Microscopy Study

Bombonato-Prado, Karina Fittipaldi PhD*; Brentegani, Luiz Guilherme PhD; Thomazini, José Antô nio PhD; Lachat, Joã o José PhD; Carvalho, Teresa Lúcia Lamano PhD

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doi: 10.1097/01.id.0000136918.05763.78
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Abstract

Alcohol intake has been known to be a significant contributing factor to osteoporosis and bone loss. 1 Several studies have demonstrated that chronic alcohol abuse may lead to osteopenia and increased incidence of fractures. 2 Although the precise mechanism remains unclear, recent studies suggest that alcohol intake depresses new bone formation with much less effect on bone resorption, leading to a negative bone balance and progressive bone loss. 3

People who drink more than 60 g/day of alcohol have a high risk to become an alcoholic patient, with a tendency to present hip fractures. 4 They may also have large bone defects and insufficient bone volume for application of a dental implant. In these cases, it is required that the defect be restored or that the bone be augmented to obtain correct placement and sufficient retention of the implant. 5 The search for safe and effective alternatives to human graft continues to be explored through the potential use of crystalline minerals, such as hydroxyapatite and tricalcium phosphate. 6 These have proved to be biocompatible with osteoconductive 7 and osteoinductive 8 properties and capable of progressive resorption with gradual replacement by new trabecular bone.

The purpose of the present study was to assess histometrically, in the rat alveolar healing model, the deleterious effects (if any) of an alcoholic beverage (sugarcane brandy) on reparative bone formation around hydroxyapatite/tricalcium phosphate implants inside the alveolar socket immediately after tooth extraction. In addition, the bone-bioceramic interface was analyzed through light and scanning electron microscopy to evaluate biomaterial osseointegration.

Materials and Methods

One hundred and twelve male Wistar rats, 180 g mean body weight, were used for this experiment (64 for the light microscope and 48 for scanning electron microscopy). The animals were housed individually in plastic boxes in a noiseless room under controlled lighting (lights on from 6:00 AM to 6:00 PM) and environmental temperature (23±2°C), divided into four experimental groups: control (C), alcohol-treated (AL), control implanted with a bioceramic (Ci), and alcohol-treated implanted with a bioceramic (Ai).

Groups AL and Ai received the alcoholic beverage (sugarcane brandy, 50° GL) ad libitum starting 30 days before dental extraction in the concentration of 5° GL and in increasing doses every 6 days (10°, 15°, 20°, 25°, and 30° GL), continuing the concentration of 30° GL until sacrifice. Groups C and Ci received only tap water. All of the animals were fed a standard laboratory chow ad libitum.

Tooth Extraction and Sacrifice

The rats were anesthetized with an intraperitoneal injection (25 mg/100 g body weight) of 2,2,2-tribromoethanol (Aldrich Chemical Co., Milwaukee, WI), and the upper right incisors were extracted with forceps after disconnection of the surrounding gingiva. 9 The implanted groups had their middle third alveolar sockets partially filled with a bioceramic, composed of hydroxyapatite and β-tricalcium phosphate (Osteosynt, Einco, Brazil). Immediately after surgery, the gingival tissues were sutured and a single intramuscular dose (0.2 ml/rat) of a polyvalent antibiotic was given, consisting of benzylpenicillin G procaine, benzylpenicillin G benzatine, benzylpenicillin G potassium, dihydrostreptomycin sulphate, and streptomycin sulphate (Veterinary Pentabiotic, Wyeth Laboratories, S ão Paulo, Brazil), mainly to prevent postsurgical infection.

The rats were killed by cardiac perfusion with saline and formalin (10%) 2 and 6 weeks after dental extraction for light microscopy samples and 1 hour, 1 day, and 1, 3, and 6 weeks after surgery for scanning electron microscopy samples. The mandibles were removed, and the heads were immersed in 10% formalin for 48 hours for fixation. All of the procedures were conducted in accordance with the Ethical Principles in Animal Research adopted by the Brazilian College of Animal Experimentation.

Histological Processing

After fixation, the maxillae were dissected and divided along the median sagittal plane. The right halves were cut tangentially to the distal surface of the molars, decalcified during 4 days with 20% sodium citrate and 30% formic acid, 10 washed, and processed for paraffin embedding. Semiserial longitudinal 6 μm-thick sections cut at 60-μm intervals were stained with hematoxylin and eosin.

Scanning Electron Microscopy Processing

The samples were fixed in 10% formalin, washed in sodium phosphate buffer (0.1 M, pH 7.4), and cut in a size adequate to fit the stubs. Next, they were submitted to dehydration in an crescent concentration of alcohol (30°, 50°, 70°, 90°, and 95° GL, 15 minutes each) and 100° GL (3 ×20 minutes each) performed in a Critical Point Dryer (CPD-030, Baltec Union AG). The samples were attached to stubs with a special glue (Silver Print, Baltec Union AG) and covered with gold (Sputter Coater, SCD-050, Baltec Union AG, Balzers, Liechtenstein). The observations and electron micrographies were performed using a scanning electron microscope (Jeol-JSM 5200, JEOL, Tokyo, Japan), with 120-mm films (ISO 125).

Histometric Analysis

An integration eyepiece with 100 equidistant points fitted to a light microscope was used to estimate the volume fraction of healing alveolar components using a differential point-counting method as described previously. 9 A total of 1200 points were counted from the apical to the cervical areas of each alveolus by the same observer blinded for the sample group, with the percentage of points lying on bone trabeculae being proportional to their volume density.

Differences among groups were analyzed by the nonparametric multiple comparison Kruskal-Wallis test (α = 0.01 for statistical significance).

Results

At the end of each experimental period, blood alcohol concentration averaged 80 ± 0.5 mg/dl in the animals receiving alcoholic diets compared with 9 ± 0.0 mg/dl observed in the control rats.

The alveolar healing begins when the extraction socket is filled by a coagulum, which gradually progresses to an immature connective tissue (granulation tissue) and finally to new bone formation. Compared with the remaining experimental groups, the light microscopy analysis of the histological alveolar sections of alcoholic rats showed greater amounts of coagulum remnants and a reduced amount of neoformed bone trabeculae both 2 and 6 weeks following tooth extraction. This suggests a delay in the alveolar healing process.

The bioceramic particles presenting irregular shapes and variable sizes were observed partially filling the middle third of the alveolar socket. The healing process seemed to proceed likewise in the sockets of control animals. As the osteogenesis developed, the particles were progressively enclosed by increasing amounts of neoformed bone trabeculae, which were interposed among them and, in some cases, apparently in close contact with their surfaces. The bioceramic particles evoked neither a foreign-body reaction nor a persistent inflammatory response (Fig. 1).

Fig. 1.
Fig. 1.:
Intimate contact between neoformed bone (bt) and the biomaterial (M) in the groups Ci (A) and Ai (B) 2 weeks after dental extraction. Six weeks after surgery, while there was intimate contact between material and bone (C), there was still the presence of connective tissue (CT) along with neoformed bone tissue (D). Final augmentation, 225×.

The alveoli from the Ci and Ai groups 2 weeks after surgery showed the biomaterial being involved by connective tissue and bone; whereas after 6 weeks, the bioceramic was surrounded almost solely by bone tissue.

Scanning electron microscopy showed that 1 hour after the extraction, there were several red blood cells from the blood clot in the alveoli of all groups. One day after the surgery, formation of a fibrin net in the alveoli of all groups was observed, which was in intimate contact with the biomaterial in the implanted groups (Fig. 2A). A week after dental extraction, collagen fibers were seen mainly in the C, Ci, and Ai groups (Fig. 2B), whereas the alcoholic group still showed red blood cells and fibrin. After 3 weeks, there was formation of thick bone trabeculae and intimate contact between bone and the bioceramic in the C, Ci, and Ai groups (Fig. 2C) (but still the presence of connective tissue in the alcoholic group). Finally, 6 weeks after extraction, there was a substantial amount of bone tissue in the C, Ci, and Ai groups (Fig. 2D); whereas in the AL group, there was the presence of connective tissue together with neoformed bone.

Fig. 2.
Fig. 2.:
One day after the implantation, fibrin (F) was contacting the material (M) (A); within a week, collagen fibers (CF) were mixed with the bioceramic (B); in 3 weeks, contact between bone (bt) and particles of the biomaterial (M) could be observed (C); and in 6 weeks, bone trabeculae were present together with the bioceramic particles (D).

The histometric analysis (Fig. 3) showed that treatment with the alcoholic beverage (group AL) caused a significant decrease in the volume fraction of neoformed bone both 2 and 6 weeks after dental extraction compared with control rats (group C). However, the alcoholic animals implanted with bioceramic (group Ai) presented an improvement in the alveolar bone neoformation. This led to a partial (after 2 weeks) or total (after 6 weeks) recovery of the volume fraction of neoformed bone trabeculae. The presence of the bioceramic inside the alveolus of control animals (group Ci) did not interfere significantly with bone healing.

Fig. 3.
Fig. 3.:
Bone volume percentage (%) in the alveolar socket of rats divided into the following groups: control (Co), alcoholic (AL), control implanted with a bioceramic (Ci), and alcoholic implanted with a bioceramic (Ai), 2 and 6 weeks after dental extraction. The results are expressed as mean ± SEM. For each period, different letters at the tops of the columns represent statistically significant differences among the experimental groups (Kruskal-Wallis test, A ≠B ≠C, α = 0.01).

Discussion

Experimental trials have demonstrated the interference of alcohol consumption with the wound healing process. Both skin 11 and mucosal 12 repair are retarded by chronic alcohol intake, and a disturbance in the growth factors responsible for the healing process has been suggested.

Alcohol intake has also been known to be a significant contributing factor to bone loss, as showed by an investigation by Sampson and Spears 13 where young rats had their femur diminished in length, diameter, and volume after 2 and 4 weeks of 35% alcohol intake. Six weeks of alcohol intake may result in rat tibiae osteopenia, with less and slender trabeculae compared with control animals. 14In vitro studies also show that ethanol, even at blood concentrations experienced by the social drinker, has an immediate direct effect on bone cells, resulting for example in increased resorption by osteoclasts from long bones of 19-day prehatch chicks. 15 In the present study, the authors observed a delay in new bone formation in the alveolar healing of rats receiving brandy containing 30% ethanol.

The effects of sugarcane brandy in rat alveolar wound healing were studied previously 16 using histologic evaluation, but no reports describing histometric evaluation of bone formation in rats after brandy intake were found in the literature.

The objective of using biomaterials is the possibility of improvement of wound healing through osteoconductive and/or osteoinductive properties in situations such as bone loss. 17 There are several biomaterials that can be used as implants, including metals, polymers, and bioceramics. The bioceramics are materials that possess the capacity of osseointegration and a great biocompatibility. 18 Among the bioceramics are those composed of calcium, phosphate, and hydroxyapatite. 19

A bioceramic implanted inside the alveolar socket immediately after dental extraction evoked neither a foreign-body reaction nor a persistent inflammatory response. It was incorporated within the healing elements and progressively enclosed by increasing amounts of new bone trabeculae. Moreover, the presence of biomaterial improved bone healing in the alveolus of alcohol-treated animals that presented a partial (after 2 weeks) or practically complete (after 6 weeks) recovery of reparative bone volume fraction. This improvement of bone neoformation might be a consequence of the bioceramic osteoconductive properties. These effects were also observed by other authors, such as Gao et al., 20 where great quantities of neo-formed bone were noted around hydroxyapatite, bioactive glasses, and tricalcium phosphate cylinders implanted in sheep tibia.

The bioceramic utilized in this experiment is composed of hydroxyapatite and tricalcium phosphate, optimizing the benefits in a disturbed tissue such as the one affected by alcohol. This suggests that the osteoconductive properties of the biomaterial accelerated bone neoformation to some extent.

Scanning electron microscopy was performed to evaluate the interface between the biomaterial and alveolar tissue. A close contact of bone with the material without interference of connective tissue was described previously. 21 The authors also observed the integration of the particles with a fibrin net, essential to future osseointegration by attracting connective tissue cells, thus originating osteogenic cells. 22 Bone tissue increased gradually and contacted the bioceramic without the presence of a fibrous capsule.

Conclusions

The present study showed a delay in the alveolar wound healing process caused by prolonged alcohol intake. This was seen mainly through a decrease in new bone formation. The presence of a bioceramic composed of hydroxyapatite and tricalcium phosphate in the alveolar socket resulted in a good biocompatibility as well as in an improvement of alveolar wound healing in alcoholic rats, especially in regards to reparative bone. This can mainly be observed 6 weeks after extraction, where bone volume percentage was significantly equivalent to control values.

Acknowledgments

This research was supported by National Counseling Research (CNPq-144765/1998-5) and Paulista University (UNIP/7-02-332/00).

References

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Abstract Translations [German, Spanish, Portugese, Japanese]

AUTOR(EN): Karina Fittipaldi Bombonato-Prado, PhD*, Luiz Guilherme Brentegani, PhD**, José Antônio Thomazini, PhD***, João José Lachat, PhD***, Teresa Lúcia Lamano Carvalho, PhD**. *Professorin der histologischen Abteilung, Universität von São Paulo - USP, zahnmedizinische Fakultät, Brasilien. **Professor(in) der Abteilung für Oral-pathologie, Universität von São Paulo - USP, zahnmedizinische Fakultät, Brasilien. ***Professor der anatomischen und chirurgischen Abteilung, Universität von Ribeirão Preto-USP, medizinische Fakultät, Brasilien. Schriftverkehr: Prof. Dr. Luiz Guilherme Brentegani, Av. do café s/n - Monte Alegre, Ribeirão Preto - SP - Brasilien, CEP: 14040–904. eMail:[email protected]

Alkoholkonsum und dessen Auswirkungen auf die Knochengewebsintegration des ein Implantat umlagernden Gewebes: eine histometrische und Rasterelektronenmikroskopische Studie

ZUSAMMENFASSUNG:Abstract: Die alveoläre Wundheilung kann durch sowohl lokale als auch systemische Faktoren beeinträchtigt werden. Die vorliegende Studie zielte darauf ab, die möglichen Auswirkungen von Alkoholkonsum (Zuckerrohrschnaps) auf die Knochenwiederherstellung im die Implantate umlagernden Gewebe bei Einbringung von Hydroxylapatit/Trikalziumphosphat-Implantaten in die Alveolarpfanne zu ermitteln. Materialien und Methoden: Bei männlichen Wistar-Ratten wurde der obere rechte Schneidezahn entfernt. In die Alveolen wurden die biokeramischen Granula eingesetzt. Den Tieren wurden zunehmend höhere Konzentrationen des Schnapses bis zu 30° GL verabreicht, beginnend 30 Tage vor Entfernung des Zahnes. Die Alkoholgabe wurde von einer Stunde bis zu sechs Wochen nach Extraktion beibehalten, anschlieβend wurden die Versuchstiere eingeschläfert. Es wurden Analysen des Alkoholgehaltes im Blut sowie histologische und histometrische Analysen mit Hilfe des Licht- und Rasterelektronenmik-roskops durchgeführt, um einen eventuellen Zusammenhang zwischen den Faktoren für eine Alveolarheilung, z.B. die Bildung neuer Knochentrabekel, und den Implantaten zu ermitteln. Ergebnisse: Die Alkoholkonzentration im Blut war bei den behandelten Tieren sehr viel höher als bei den der Kontrollgruppe angehörenden Tieren. Durch Anwendung einer speziellen histometrischen Zählmethode auf Differenzialpunktbasis konnte die maβgebliche Verzögerung der Knochengewebswiederherstellung in den Alveolen der alkoholisierten Ratten festgestellt werden. Allerdings verbesserte sich die alveoläre Wundheilung beträchtlich, wenn diesen Ratten zuvor die biokeramischen Bestandteile in die Alveolarpfanne eingepflanzt worden waren. Schlussfolgerung: Es kann davon ausgegangen werden, dass die Knochenleitenden Eigenschaften der biokeramischen Granula die alveoläre Wundheilung bei alkoholisierten Ratten beschleunigt.

SCHLÜ SSELWÖ RTER: Alkoholkonsum, Knochengewebsintegration, Hydroxylapatit, Trikalziumphosphat, Implantat, Ratte

AUTOR(ES): Karina Fittipaldi Bombonato-Prado, Ph.D.*, Luiz Guilherme Brentegani, Ph.D.**, José Antônio Thomazini, Ph,D.***, João José Lachat, Ph.D.***, Teresa Lucia Lamano Carvalho, Ph.D.**. *Profesor del Departamento de Histología, Facultad de Odontología de la Universidad de San Pablo-USP, San Pablo, Brasil. **Profesor del Departamento de Patología Oral, Facultad de Odontología de la Universidad de San Pablo-USP, San Pablo, Brasil. ***Profesor de Anatomía y Cirugía, Departamento de la Escuela de Medicina de la Universidad de Ribeirão Preto-USP, Brasil. Correspondencia a: Prof. Dr. Luiz Guilherme Brentegani, Av. do café s/n. Monte Alegre, Ribeirão Preto-SP, Brasil CEP 14040-904. Correo electrónico:[email protected]

El consumo de alcohol y la integración ósea alrededor de implantes: Un estudio histométrico y microscopía electrónica con barrido

ABSTRACTO:Abstracto: La curación de una herida alveolar puede modificarse por factores locales y sistémicos. El objetivo de este estudio es evaluar el posible efecto de la administración de bebidas alcohólicas (brandy de caña de azúcar) en la formación de hueso de reparación alrededor de implantes de fosfato tricálcico/hidroxiapatita en el interior de la cavidad alveolar. Materiales Y Métodos: Se extrajeron los incisivos superiores derechos de ratas machos Wistar y los gránulos de biocerámica implantados en el alvéolo. Los animales recibieron concentraciones cada vez más altas de brandy hasta los 30° GL comenzando 30 días antes de la extracción dental y mantenidas por períodos que variaron entre una hora y seis semanas, hasta su sacrificio. Se realizaron análisis de concentración de alcohol en la sangre, así como análisis histológicos e histométricos a través de microscopios de luz y de barrido electrónico para examinar la relación entre los componentes de la curación alveolar, incluyendo la trabécula del nuevo hueso y los implantes. Resultados: La concentración de alcohol en la sangre fue significativamente más alta en los animales tratados cuando se los comparó con los controles. Un retraso significativo en la formación de hueso de reparación se detectó en el alvéolo de las ratas alcohólicas a través de un método de cuenteo de puntos histométricos diferenciales, mientras que la presencia de la biocerámica en la cavidad alveolar mejoró la curación de la herida alveolar en las ratas tratadas con alcohol. Conclusión: Se sugiere que las propiedades osteoconductivas de esta biocerámica aceleró la curación de la herida alveolar en ratas alcohólicas.

PALABRAS CLAVES: bebida alcohólica, integración ósea, hidroxiapatita, fosfato tricálcico, implante, rata.

AUTOR(ES): Karina Fittipaldi Bombonato-Prado, Ph.D.*, Luiz Guilherme Brentegani, Ph.D.**, José Antônio Thomazini, Ph.D.***, João José Lachat, Ph.D.***, Teresa Lúcia Lamano Carvalho, Ph.D.**. *Professor do Departamento de Histologia, Escola de Odontologia de Universidade de São Paulo-USP, Brasil. **Professor do Departamento de Patologia Oral, Escola de Odontologia, Universidade de São Paulo-USP, Brasil. ***Professor do Departamento de Anatomia e Cirurgia da Escola de Medicina da Universidade de Ribeirão Preto-USP, Brasil. Correspondência para: Prof. Dr. Luiz Guilherme Brentegani, Av. do Café, s/n–Monte Alegre, Ribeirão Preto-SP-Brasil, CEP: 14040-904. E-mail: [email protected]

Influxo de Á lcool e Osseointegração em Volta de Implantes: Estudo Histométrico e de Microscopia Eletrônica por Varredura

RESUMO:Resumo: A cura da ferida alveolar pode ser modificada por fatores locais e sistêmicos. O objetivo deste estudo foi avaliar o possível efeito de ministração de bebida alcoólica (aguardente de cana) na formação de osso reparador em volta de implantes de hidroxiapatita/fosfato tricálcio dentro do alvéolo. Materiais e Métodos: Ratos machos Wistar tiveram seus incisivos superiores direitos extrá idos e os grānulos biocerāmicos implantados nos alvéolos. Os animais receberam concentrações crescentes de aguardente até 30° GL, começando 30 dias antes da extração dentária e mantidas por períodos que variavam de uma hora a seis semanas, até o sacrifício. Foi realizada análise de concentração alcoólica no sangue, bem como análise histológica e histométrica através de microscopia eletrônica por luz e por varredura para examinar o relacionamento entre os componentes de cura alveolar, incluindo os novos ossos trabeculares, e os implantes. Resultados: A concentração alcoólica no sangue foi significativamente mais alta nos animais tratados quando comparada com os controles. Um atraso significativo na formação de osso reparador foi detectado no alvéolo de ratos alcoolizados por um método de contagem de pontos histométrico diferencial, ao passo que a presença da cerāmica no alvéolo melhorou a cura da ferida alveolar em ratos tratados com álcool. Conclusão: Sugerese que as propriedades osteocondutoras dessa biocerāmica acelerou a cura da ferida alveolar em ratos alcoolizados.

PALAVRAS-CHAVE: bebida alcoólica, osseointegração, hidroxiapatita, fosfato tricálcio, implante, rato.

FIGURE
FIGURE
Keywords:

alcoholic beverage; osseointegration; hydroxyapatite; tri-alcium phosphate; implant; rat

© 2004 Lippincott Williams & Wilkins, Inc.