© 2002 Lippincott Williams & Wilkins, Inc. Volume 11(2

Ovid: Nociti: Implant Dent, Volume 11(2).June 2002.176-182

© 2002 Lippincott Williams & Wilkins, Inc.

Volume 11(2) June 2002 pp 176-182

Nicotine and Bone Density Around Titanium Implants: A Histometric Study in Rabbits[BASIC AND CLINICAL RESEARCH]

Nociti, Francisco H. Jr. DDS, MS, PhD*; Stefani, Cristine M. DDS, MS, PhD**; Sallum, Enilson A. DDS, MS, PhD***; Duarte, Poliana M. DDS, MS†; Sallum, Antonio W. DDS, MS, PhD‡

*Assistant Professor, Department of Prosthodontics and Periodontics, Division of Periodontics, School of Dentistry at Piracicaba, UNICAMP, São Paulo, Brazil.**Senior Researcher, Department of Prosthodontics and Periodontics, Division of Periodontics, School of Dentistry at Piracicaba, UNICAMP, São Paulo, Brazil.***Assistant Professor, Department of Prosthodontics and Periodontics, Division of Periodontics, School of Dentistry at Piracicaba, UNICAMP, São Paulo, Brazil.†Student, Department of Prosthodontics and Periodontics, Division of Periodontics, School of Dentistry at Piracicaba, UNICAMP, São Paulo, Brazil.‡Chairman and Professor, Department of Prosthodontics and Periodontics, Division of Periodontics, School of Dentistry at Piracicaba, UNICAMP, São Paulo, Brazil.Reprint requests and correspondence to:Francisco H. Nociti Jr., PhDAv. Limeira 901Caixa Postal: 052CEP: 13414–903PiracicabaS.P., BrazilFax: 55–19–4305218E-mail: [email protected] authors claim to have no financial interest in any company or any of the products mentioned in this article.

Outline

● Abstract● Materials and Methods

❍ Animals❍ Implant Surgery❍ Experimental Design❍ Histometric Procedure❍ Statistical Analysis

● Results● Discussion● Conclusions● Acknowledgments

http://gateway2.ovid.com/ovidweb.cgi?QS=WWabAU%...tsuL3n7rJ1%2bYw8wtFNTZAbbXU%3d_I0zJUQLvNiHIMQdC (1 of 16)13/7/2004 08:33:20


● References❍ Abstract Translations [German, Spanish, Portuguese, Japanese]

Graphics

● Table 1● Table 2● Fig. 1● Fig. 2● Fig. 3● Figure. No caption a...

Abstract

This study investigated the influence of nicotine on bone density around titanium implants inserted in rabbits. Thirty-two New Zealand rabbits were included. After anesthesia, the tibiae surfaces were exposed and two screw-shaped, commercially available, pure titanium implants of 7.0 mm in length and 3.75 mm in diameter were placed bilaterally. A total of 128 implants were inserted: 64 blasted with Al2O3 particles (group 1) and 64 with a machined surface finish (group 2). The animals were randomly assigned to one of four treatment subgroups, and daily subcutaneous injections of nicotine were administered. After 42 days, the animals were killed and undecalcified sections were prepared. The bone density was measured in the cortical passage of the implant. Statistical analysis (two-way analysis of variance) revealed no significant difference neither regarding the effect of nicotine nor the effect of surface design on bone density around the implants (P > 0.05). Within the limits of the present study, it can be assumed that daily nicotine administration may not statistically influence bone density around titanium implants.

Local and systemic factors, which may impair bone healing or may interfere with the maintenance of osseointegration, have been described to affect the success rate of osseointegrated implants. 1 Smoking is one of the factors often discussed in relation to implant failure. 1–5 It is well recognized that cigarette smoking is associated with impaired wound healing after surgical treatment in the oral cavity, 6 reduced bone height, 7 increased bone loss rate, 8 increased resorption of the alveolar ridge, 7 higher incidence of periodontitis, 9 and type IV bone. 10 In addition, smoking has been found to be an important factor in periimplant soft tissue changes. 11

Nicotine is one of the 2000 potentially toxic substances in tobacco smoke. Nicotine and its metabolite cotinine have been found in the saliva and gingival crevicular fluid of smokers. 12In vitro studies have shown that nicotine can inhibit neutrophil/monocyte defensive functions, 13 potentiate lipopolysaccharide-stimulated human peripheral blood monocyte secretion of PGE2, 14 and have direct adverse effects on various functions



of the periodontal cells. 15In vivo, it has been reported that nicotine administration may enhance the effects of the local components of periodontitis. 16,17 In an experimental study in rats, in which subperiosteal bone formation was stimulated, Boyne and Herford 18 found that animals exposed to cigarette smoke produced less bone than the control animals. Rats that were not exposed to cigarette smoke and received 1.0 mg of nicotine exhibited 35% less bone growth than those exposed to smoke and 50% less bone growth than the control group. Recently, we have reported that nicotine by itself may not be responsible for the decreased success rates reported for osseointegrated implants placed in smokers. 19 Because cigarette consumption has also been associated with poor bone quality, 10 the purpose of the present study was to investigate the effects of daily nicotine administration on bone density around titanium implants with different surface designs inserted in the tibiae of rabbits.

Materials and MethodsAnimals

Thirty-two adult New Zealand rabbits, aged 9 to 12 months (3000–3500 g), were used for this study. The animals were kept in individual cages with access to food and water ad libitum. Before the surgical procedures, all animals were allowed to acclimatize to the laboratory environment for a period of 7 days. The University of Campinas Institutional Animal Care and Use Committee approved the protocol.

Implant Surgery

General anesthesia was obtained by intramuscular administration of ketamine (0.5 mL/kg). Skin was cleansed with iodine surgical soap. An incision of approximately 3 cm in length was made and the bone surface of the tibiae surgically exposed by blunt dissection. Unicortical implant beds were prepared and two screw-shaped, commercially available, pure titanium implants of 7.0 mm in length and 3.75 mm in diameter were placed bilaterally until the screw thread had been completely introduced into the bone cortex. Finally, soft tissues were replaced and sutured. Postoperatively, the animals received antibiotic (Pentabiótico; Wyeth-Whitehall Ltda, São Paulo, SP, Brazil) given as a single intramuscular injection.

Experimental Design

From the total amount of four implants inserted in each animal, two different implant surfaces were used: two implants blasted with Al2O3 particles/60–100 µm (group 1) and two with a machined surface finish (group 2). The animals were randomly assigned to one of the four treatment subgroups (8 animals/group), and daily subcutaneous injections were given: (A) saline solution (n = 8); (B) 0.37 mg of nicotine/kg (n = 8); (C) 0.57 mg of nicotine/kg (n = 8); and (D) 0.93 mg of nicotine/kg (n = 8). Therefore, there were two experimental groups composed of titanium implants with Al2O3-blasted (group 1) and machined surfaces (group 2) subdivided into four subgroups each (subgroups A, B, C, and D).

Histometric Procedure

After the animals were killed (42 days), the tibiae were removed and fixed in 4% neutral formalin for 48 hours. Undecalcified sections were prepared as previously described, 31 ie, the blocks were dehydrated by



using an ascending series of ethanol (60–100%) and embedded in glycolmethacrylate (Technovit 7200; Heraeus Kulzer GmbH, Wehrheim, Germany). Subsequently, the sections (20–30 µm) were obtained (Exakt Technologies, Hamburg, Germany) and stained using toluidine blue staining. The bone density (ie, the proportion of mineralized bone in a 550 µm-wide zone lateral to the implant) was obtained bilaterally in the cortical passage of the implants (Image-Pro; Media Cybernetics, Silver Spring, MD).

Statistical Analysis

A two-way analysis of variance ([alpha] = 0.05) was used to investigate the influence of nicotine administration, implant surface design, and its interaction on the bone density around the implants.

Results

Statistical analysis did not reveal significant differences between nicotine and saline subgroups (P = 0.74) regarding the bone densities (Table 1). Similarly, statistical analysis did not reveal significant influence (P = 0.38) of the implant design on the bone density around the implants. In addition, there was not a statistically significant interaction between treatment (nicotine) and implant design (machined and Al2O3-blasted implants) (P = 0.54). Furthermore, Table 2 illustrates the amount (%) of nonmineralized tissues in the 550 µm-wide zone lateral to the implant. Figures 1 to 3 illustrate the histological aspects of the bone around the implants for subgroups A, B, and D.

Table 1. The Bone Density in a 550 µm-Wide Zone From the ImplantMean (%) and SD for groups 1 and 2 and subgroups A to D.

Table 2. The Amount of Nonmineralized Tissues in the 550 µm-Wide Zone Lateral to the ImplantMean (%) and SD for groups 1 and 2

and subgroups A to D.



Fig. 1. Photomicrographs A (machined) and B (Al2O3-blasted) illustrate the histological aspect of the bone around the implant for

subgroup A. Toluidine blue/Original magnification = ×15.75.



Fig. 2. Photomicrography A (machined) and B (Al2O3-blasted) illustrate the histological aspect of the bone around the implant for

subgroup B. Toluidine blue/Original magnification = ×15.75.



Fig. 3. Photomicrography A (machined) and B (Al2O3-blasted) illustrate the histological aspect of the bone around the implant for

subgroup D. Toluidine blue/Original magnification = ×15.75.

Discussion

The predictability of titanium implants have been well documented. 20–23 Long-term success rates of 96% to 99% in the edentulous mandible and 90% over 5 years and 80% over 10 years have been reported in the edentulous maxilla. 24 As well, a number of local and systemic conditions that may impair bone healing or may interfere with the maintenance of osseointegration, including smoking, have been discussed. 1

Bain and Moy 2 were the pioneers to report the negative effect of smoking on the success rate of osseointegrated implants. The smokers’ failure rate was 11.28% (44/390), whereas the nonsmokers’ failure rate was significantly lower at 4.76% (86/1804). This observation was later confirmed in different populations using different implant systems. De Bruyn and Collaert 3 described the effect of smoking on initial fixture failure before functional loading with fixed prosthetic restorations. The failure rate before loading was 9% in smokers versus 1% in nonsmokers and was statistically significant. They concluded that smoking is a significant factor in the failure of implants before functional loading. Gorman et al 25 analyzed more than 2000 implants regarding their survival at second stage surgery and concluded that smoking is detrimental to implant success. Lindquist et al 5 showed that smoking was the most important factor of those correlated with increased periimplant bone loss. Lambert et al 26 reported that after 3 years, osseointegrated implants placed in smokers may be almost 1.5 times more likely to fail than in nonsmokers (2.9% difference), but both groups



demonstrated a high success rate (94% versus 91.1% for nonsmokers and smokers, respectively). The difference between smokers and nonsmokers reported by Lambert et al 26 (2.9%) is almost half of that reported by Bain and Moy 2 (6.52%). Possibly, the reason is that Bain and Moy’s work was on 100% machined implants, whereas Lambert’s was mostly textured implants (HA-coated), which means that the percentage of failures may be influenced by the implant design.

Among the substances that make up cigarette smoke, nicotine is one of the most studied. In vitro and in vivo, nicotine has been associated with decreased neutrophil/monocyte defensive functions, adverse effects on various functions of the periodontal cells, enhanced bone loss in ligature-induced periodontitis, and less bone growth. 13,15–18 The second reason to study the specific effects of nicotine concerns the now common use of this drug (usually transdermal patches of nicotine) for smoking cessation. If nicotine itself is injurious to the bone healing around titanium implants, then issues of dose, pharmacokinetics, and critical period all become essential elements in smoking cessation strategies for implant placement. Data from our laboratory, 19 using similar doses of nicotine other than in the present study, demonstrated that nicotine administration may not influence bone healing in a region close to the implant, ie, bone-to-implant contact and bone area into the limits of the implants threads. These are encouraging results because a smoking-cessation protocol using nicotine patches may be an alternative to actual smoking during the surgical phase of implant treatments. However, because this was the first study that investigated the relationship between the presence of nicotine and bone healing around titanium implants, caution must be used to interpret its results. Whether higher doses of nicotine would promote different results remains to be investigated. Therefore, further studies should be considered to provide a safe protocol to propose an interruption or cessation of smoking before placing an implant.

Smokers have also been clinically associated with poorer bone quality than nonsmokers, 10 and a less dense bone (type IV bone) has also been associated with late implant failures. 27 In a recent study, Ekfeldt et al 28 reported that heavy smokers were associated more with implant failures after loading than before loading. One could relate both facts, ie, implant failures observed in smokers instead of being related to its influence on osseointegration (early failure) is related to its influence on the bone quality around the implant. Consequently, this could impair the prognosis of the implant-supported prostheses. Therefore, the aim of the present study was to investigate the influence of nicotine on the bone density around titanium implants inserted in rabbits. The results of this study are similar to our previous study, 19 ie, nicotine administration did not influence bone density around the implants. Similarly, caution must be used to analyze these results because we are not sure whether such doses of nicotine represented the serum nicotine concentration reached by heavy smokers. In addition, bone turnover in rabbits is quite different than in humans 29 and it may lead to misunderstanding.

Nicotine has been associated with increased alkaline phosphatase production and decreased osteoclastic activity. 30–31 In addition, it has been reported that nicotine may enhance human gingival fibroblast attachment. 32 Thus, these and other possible effects of nicotine lend credence to the opinion that nicotine may not be the culprit of various negative responses to tobacco. Rather, other agents present in tobacco may be responsible for the detrimental effects. At this time we have initiated a study to histologically investigate the effects of cigarette smoke and higher doses of nicotine on such a process. Preliminary results showed that although intermittent cigarette smoke exposure may not seriously affect cortical bone, it may jeopardize bone quality around titanium implants placed in the tibiae of rats in the cancellous bone area. 33



In this study, the influence of implant design on the bone density around titanium implants after nicotine administration was also investigated. Although numerous studies have demonstrated that roughened titanium surfaces presented a higher bone-to-implant contact than polished or machined surfaces, 34–38 in this study an influence of the surface design on the bone density lateral to the implant was not observed. According to Davies, 39 implant surface design would have a profound effect on the fibrin attachment during cell migration in a wound healing process; thus, maintaining a migratory pathway for the differentiating osteogenic cells to reach the implant surface. Therefore, the implant design would only influence the process of bone healing in the region very close to the implant surface and would not affect bone in a 550 µm-wide zone lateral to the implant. It appears to be confirmed by the findings of this study.

Thus, the mechanisms by which smoking influences the success rates of titanium implants remain obscure, and further studies must be considered to determine such a pathway to create strategies to deal with titanium implants and smokers.

Conclusions

Within the limits of the present study, it can be assumed that daily nicotine administration may not statistically influence bone density around titanium implants.

Acknowledgments

The authors greatly appreciate the assistance of AS Technology (São José dos Campos, Brazil), for supplying the implants. Furthermore, the authors would like to thank Fundação de Amparo a Pesquisa do Estado de São Paulo for the financial support (grant 00/09439–5).

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Abstract Translations [German, Spanish, Portuguese, Japanese]

AUTOR(EN): Francisco H. Nociti Jr., DDS, MS, PhD*, Cristine M. Stefani, DDS, MS, PhD**, Enilson A. Sallum, DDS, MS, PhD, ***, Poliana M. Duarte, DDS, MS****, Antonio W. Sallum, DDS, MS, PhD*****. *stellvertretender Professor, Abteilung für Prothetik und Periodontologie, Fachbereich Periodontologie, Zahnheilkundliche Schule in Piracicaba, UNICAMP, Sao Paulo, Brasilien. **Forschungsoberassistent, Abteilung für Prothetik und Periodontologie, Fachbereich Periodontologie, Zahnheilkundliche Schule in Piracicaba, UNICAMP, Sao Paulo, Brasilien. ***Stellvertretender Professor, Abteilung für Prothetik und Periodontologie, Fachbereich Periodontologie, Zahnheilkundliche Schule in Piracicaba, UNICAMP, Sao Paulo, Brasilien. ****Student, stellvertretender Professor, Abteilung für Prothetik und Periodontologie, Fachbereich Periodontologie, Zahnheilkundliche Schule in Piracicaba, UNICAMP, Sao Paulo, Brasilien. *****Vorsitzender und Professor, stellvertretender Professor, Abteilung für Prothetik und Periodontologie, Fachbereich Periodontologie, Zahnheil-kundliche Schule in Piracicaba, UNICAMP, Sao Paulo, Brasilien. Schriftverkehr: Francisco H. Nociti Jr. Av. Limeira 901 - Caixa Postal: 052 - CEP: 13414-903 Piracicaba - S.P. - Brasilien. Fax: ++ 55 19 4305218; eMail: nociti@ fop.unicamp.br

ZUSSAMENFASSUNG: Innerhalb der vorliegenden Studie wurden die Auswirkungen von Nikotin auf die Dichte des an in Kaninchen eingepflanzten Titanimplantaten angelagerten Knochengewebes untersucht. Die Versuchreihe wurde mit 32 neuseeländischen Kaninchen als Versuchstieren durchgeführt. In Narkose wurden jeweils die Oberflächen des Schienbeins freigelegt und bilateral zwei handelsübliche schraubenförmige reine Titanimplantate von 0,7 mm Länge und 3,75 mm Durchmesser eingesetzt. Die Gesamtanzahl von 128 eingepflanzten Implantaten splittet sich in Gruppe 1, 64 mit Al2O3Partikeln gestrahlten Implantaten, und Gruppe 2, 64 Implantaten mit einer maschinell gefertigten Oberfläche, auf. Zur anschließenden Behandlung wurden die 32 Versuchstiere nach einem Zufallsprinzip einer von vier Untergruppen zugeteilt. Nikotin wurde subkutan auf täglicher Basis injiziert. Nach 42 Tagen erfolgte nach Einschläferung der Tiere die Präparation nicht entkalkter Sektionen; im Rindenbereich der Implantate wurde eine Messung der Knochendichte durchgeführt. Die statistische Analyse (Zweiweg-ANOVA) ergab keine nachvollziehbare Verbindung zwischen der Knochendichte im um die Implantate angelagerten Gewebe (P>0,05) und der Einwirkung von Nikotin bzw. der spezifischen Oberfläche des Implantats. Die Ergebnisse der vorliegenden Studie lassen den statistischen Rückschluss zu, dass die Knochendichte in der Implantatsumgebung durch tägliche Nikotinzufuhr nicht beeinträchtigt wird.

SCHLÜSSELWÖRTER: Nikotin, Knochendichte, Zahnimplantate

AUTOR(ES): Francisco H. Nociti, Jr., DDS, MS, PhD*, Cristine M. Stefani, DDS, MS, PhD**,



Enilson A. Sallum, DDS, MS, PhD,***, Poliana M. Duarte, DDS, MS****, Antonio W. Sallum, DDS, MS, PhD*****. *Profesor Asistente, Departamento de Odontología Protética y Periodontología, División de Periodontología, Facultad de Odontología en Piracicaba, UNICAMP, San Pablo, Brasil.**Investigador Principal, Departamento de Odontología Protética y Periodontología, División de Periodontología, Facultad de Odontología en Piracicaba, UNICAMP, San Pablo, Brasil. ***Profesor Asistente, Departamento de Odontología Protética y Periodontología, División de Periodontología, Facultad de Odontología en Piracicaba, UNICAMP, San Pablo, Brasil.****Estudiante, Departamento de Odontología Protética y Periodontología, División de Periodontología, Facultad de Odontología en Piracicaba, UNICAMP, San Pablo, Brasil.******Jefe y Profesor, Departamento de Odontología Protética y Periodontología, División de Periodontología, Facultad de Odontología en Piracicaba, UNICAMP, San Pablo, Brasil. Correspondencia a: Francisco H. Nociti Jr., Av. Limeira 901 - Caixa Postal: 052 - CEP: 13414-903, Piracicaba, Sao Pablo, Brazil. Fax: ++ 55 19 4305218. Correo electrónico: [email protected]

ABSTRACTO: Este estudio investigó la influencia de la nicotina en la densidad del hueso alrededor de los implantes de titanio insertados en conejos. Se usaron treinta y dos conejos de Nueva Zelandia. Después de la anestesia, se abrieron la superficie de la tibia y se colocaron bilateralmente dos implantes de titanio puro disponibles comercialmente con forma de tornillo de 7,0 mm de longitud y 3,75 mm de diámetro. Se insertaron un total de 128 implantes: 64 con chorro de partículas de AL2O3 (Grupo 1) y 64 con una terminación de las superficies a máquina (Grupo 2). Los animales recibieron una asignación aleatoria a uno de los cuatro subgrupos de tratamiento y se le administraron inyecciones subcutáneas diarias de nicotina. Después de cuarenta y dos días, se sacrificaron los animales y se prepararon secciones sin descalcificar. La densidad del hueso se midió en el paso cortical del implante. El análisis estadístico (ANOVA bidireccional), no demostró una diferencia significativa en el efecto de la nicotina ni en el efecto del diseño de la superficie sobre la densidad del hueso alrededor de los implantes. (P>0,05). Dentro de los límites del presente estudio, se puede suponer que la administración diaria de nicotina no ejerce una influencia estadística en la densidad del hueso alrededor de los implantes de titanio.

PALABRAS CLAVES: nicotina, densidad del hueso, implantes dentales.

AUTORES: Francisco H. Nociti Jr., DDS, MS, PhD*, Cristine M. Stefani, DDS, MS, PhD**, Enilson A. Sallum, DDS, MS, PhD, ***, Poliana M. Duarte, DDS, MS****, Antonio W. Sallum, DDS, MS, PhD*****. *Professor Assistente, Departamento de Prostodontia e Periodontia, Divisão de Periodontia, Faculdade de Odontologia de Piracicaba, UNICAMP, São Paulo, Brasil. **Pesquisador Sênior, Departamento de Prostodontia e Periodontia, Divisão de Periodontia, Faculdade de Odontologia de Piracicaba, UNICAMP, São Paulo, Brasil. ***Professor Assistente, Departamento de Prostodontia e Periodontia, Divisão de Periodontia, Faculdade de Odontologia de Piracicaba, UNICAMP, São Paulo, Brasil. ****Aluno, Departamento de Prostodontia de Periodontia, Divisão de Periodontia, Faculdade de Odontologia de Piracicaba, UNICAMP, São Paulo, Brasil. *****Diretor e Professor, Departamento de Prostodontia e Periodontia, Divisão de Periodontia, Faculdade de Odontologia de Piracicaba, UNICAMP, São Paulo, Brasil. Correspondências devem ser enviadas a: Francisco H. Nociti Jr. Av. Limeira 901 - Caixa Postal:



052. CEP: 13414-903 Piracicaba - S.P. - Brasil. Fax: (++55) (19) 430-5218. e-mail: [email protected]

SINOPSE: este estudo investiga a influência da nicotina na densidade óssea ao redor dos implantes de titânio inseridos em coelhos. Trinta e dois coelhos da Nova Zelândia foram incluídos. Após a anestesia, a superfície da tíbia foi exposta e dois implantes em forma de parafuso, de titânio puro, disponíveis comercialmente, com 7 mm de comprimento e 3,75 mm de diâmetro, foram situados de maneira bilateral. Um total de 128 implantes foram inseridos: 64 tratados com jato de partículas Al2O3 (Grupo 1) e 64 com um acabamento de superfície usinado (Grupo 2). Os animais foram distribuídos de maneira aleatória a cada um dos quatro subgrupos de tratamento e receberam injeções subcutâneas de nicotina. Após quarenta e dois dias, os animais foram sacrificados e seções descalcificadas foram preparadas. A densidade óssea foi avaliada na passagem cortical do implante. A análise estatística (ANOVA de duas vias) não revelou nenhuma diferença significativa em relação ao efeito da nicotina ou ao efeito do design da superfície na densidade óssea ao redor dos implantes (P>0,05). Dentro dos limites do presente estudo, pode-se presumir que a administração diária de nicotina pode não influenciar estatisticamente a densidade óssea ao redor de implantes de titânio.

PALAVRAS-CHAVES: nicotina, densidade óssea, implantes odontológicos.

FIGURE





Figure. No caption available.

Key Words: nicotine; bone density; dental implants

Accession Number: 00008505-200204000-00020

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© 2002 Lippincott Williams & Wilkins, Inc. Volume 11(2