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Basic and Clinical Research

Influence of Titanium Surface Roughness on Attachment of Streptococcus Sanguis: An In Vitro Study

Pereira da Silva, Cristiano Henrique Figueiredo DDS, MSc*; Vidigal, Guaracilei Maciel Jr DDS, MSc, PhD; de Uzeda, Milton DDS, PhD; de Almeida Soares, Gloria PhD§

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doi: 10.1097/
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Endosseous implants are anchored in cortical and medullar bone and emerge from the mucosa to the oral cavity. Therefore, dental implants are in an exclusive situation, because they function in two distinct environments: the internal (i.e., in contact with bone and soft tissues) and the external (i.e., in contact with the oral cavity).1 This unique situation emphasizes the necessity of establishing the bacterial plaque formation mechanisms around oral implants, because their presence can cause peri-implantitis,2,3 implant failure,4 or loss after the osseointegration period. Peri-implantitis is the main reason for implant loss after an implant is osseointegrated, and it is assumed that this disease is related to occlusal trauma5,6 or to bacteria and their products.7 Meffert8 defined peri-implantitis as the progressive loss of peri-implant bone as well as soft tissue inflammatory changes. In cases of peri-implantitis associated with bacteria, it is important to understand the relationship between bacterial biofilms and the characteristics of the implant surface.

After the osseointegration period, abutments are connected to endosseous implants, exposing them to the oral cavity. At this time, the implant/abutment surfaces are bathed in saliva and become coated by an acquired pellicle derived from saliva. The implant pellicle-coated surface provides specific binding receptors for adhesions that are bacterial membrane proteins involved in the bacteria adhesion process. Adherence model studies generally use Streptococcus sanguis because it plays an important role in the formation of bacterial plaque.9,10S. sanguis exhibited better adherence to saliva-coated surfaces than other micro-organisms, although S. sanguis was not associated with sites presenting active bone loss in peri-implantitis or periodontitis.11

Beyond the physical/chemical interactions between bacterial and titanium surfaces, the surface roughness is one of the most important aspects involved in bacterial colonization.12,13 The quantity and quality of bacterial plaque seem to be influenced by the surface properties of the materials.14 Currently, there are many different implant surfaces available clinically, with great differences in surface roughness. Some implant systems have smooth surfaces, whereas others have rough surfaces, and one way to increase roughness is by blasting the implant surface with particles such as titanium or aluminum oxides. A marginal bone loss occurs around all endosseous implant systems in the first year after the healing period,15–18 although most of these implant systems showed good long-term results.19–23

The reasons for this initial bone loss could be a local infection caused by micro-organisms from bacterial plaque or an occlusal trauma that causes microleakage on the marginal bone around endosseous implants. When peri-implantitis begins around an osseointegrated implant, a protocol of treatment described by Jovanovic et al24 as a “decontamination protocol” can be employed. Some questions arise from this protocol, such as “what is the real efficacy of this protocol on bacterial removal?” and “Is this treatment equally effective for different implant surfaces?” The answers to those questions may have important implications for the management of ailing implants and peri-implant tissue health.

Materials and Methods

Thirty commercially pure titanium sheets, 10 × 10 × 1 mm with three different levels of surface roughness, were used in the present study. Group 1 was composed of 10 as-machined titanium sheets and Groups 2 and 3 of titanium sheets blasted with aluminum oxide (alumina; Al2O3) particles with different diameters: group 2 was blasted with 65-μm particles and group 3 with 250-μm particles. The other blasting parameters (distance and pressure) remained constant. The arithmetic average roughness (Ra) was determined using a SLOAN Dektak II stylus profilometer (Veeco Instruments GmbH, Mannheim, Germany) with vertical precision of 5 Å; and for each surface condition, at least 10 measurements per sample were performed.

The titanium specimens were sterilized in an autoclave for 20 minutes at 120°C. All samples were incubated in individual tubes containing a suspension of S. sanguis (108 cells/mL) in 5 mL of thioglycollate broth (Difco, Detroit, MI). The medium was changed every 3 days, and the purity of cultures checked at every change.

After the contamination period of 7 days, the specimens were removed from the cultures. Three samples of each group were considered “control sheets,” and the remaining samples were submitted to the decontamination protocol. The standard protocol included the exposure of surfaces to a high-pressure sodium bicarbonate device for 1 minute under aseptic conditions. After the application of decontamination protocol, all specimens (i.e., treated and control samples) were transferred to 0.5 mL of 0.85% sterile saline solution and vortexed for 1 minute. After 10-fold serial dilutions in saline, aliquots of 0.1 mL were plated onto Mitis-Salivarius agar plates and incubated at 37°C for 48 hours. The colony-forming units grown were counted, and a log transformation was calculated. Two untreated contaminated titanium specimens of each condition remained untreated for 2 minutes and were submitted for the serial dilution process and sampled as a control of contamination.

Data obtained from samples of control and treated specimens for all surfaces were statistically analyzed for differences between groups by means of the one-way analysis of variance. The significance level was established at 5% (P < 0.05).


Table 1 summarizes all results. Compared with as-machined titanium sheets (Group 1), the Ra of Groups 2 and 3 increased as a consequence of the blasting process, with all results being statistically significant (P < 0.05). Group 3 exhibited the roughest surface because of the large particles of alumina used in surface preparation. The mean number of bacterial cells in the control specimens reflects the initial samples used as a reference. After the contamination period, machined titanium surfaces (Group 1) remain with 49 × 103 bacterial cells, and the bacterial concentrations of Groups 2 and 3 were 11 × 104 and 35 × 105, respectively. The attachment of bacterial cells is related directly to surface roughness: with the increasing of surface roughness, an exponential increase in bacterial cells was observed. However, after application of the decontamination protocol, no viable bacteria were detected for all surfaces examined.

Table 1
Table 1:
Mean Values of the Quantity of Bacterial Cells on Different Titanium Surfaces


The implant surface properties may influence bioadhesive outcomes,25,26 and with respect to bacterial adhesion and growth, the present results demonstrated that surface roughness has a strong influence on plaque accumulation. Quirynen et al12,27 found similar results in in vivo studies on the influence of the surface roughness of implants on the microbiology of supra- and subgingival plaque. They demonstrated that the initial colonization easily occurs in the depth of surface irregularities and that it is difficult to completely remove plaque from these grooves, which facilitates reaccumulation.

The lowest number of bacterial cells identified on samples from Group 1 (Ra, 0.17 μm) is in agreement with other studies.13,27 Quirynen et al27 and Bollen et al13 showed that surfaces with an arithmetic average roughness (Ra) below 0.2 μm inhibits early plaque accumulation and formation, whereas surfaces with a roughness value (Ra) of 0.82 μm or higher resulted in a 25× greater plaque accumulation than the smooth surfaces.27

In general, there is a preference for rough surfaces, as they seem to increase cellular activity of bone cells compared with smooth surfaces,28 which can lead to an augmentation in the percentage of bone/implant contact around rough surface implants compared with smooth ones.29–31 However, rough surfaces should be used with some criteria. Since bacterial plaque around teeth and implants were similar in healthy and disease conditions32,33 the installation of rough surface implants in partially edentulous patients harboring periodontopathogenic bacteria should be considered a risk factor for the long-term maintenance of the implant.34,35 Therefore, in some patients, conventional fixed partial prostheses may be preferable to implant-supported prostheses,36 although the neck region of the implant is usually less rough than the body of the implant.

The results showed that the decontamination capacity of a clinical protocol treatment was very effective when applied on titanium sheets. The efficacy of the same protocol treatment should also be tested both in dental implants and in the mouth conditions. Dental implants frequently have a cylindrical threaded design resulting in a more difficult access to perform mechanical decontamination with the high-pressure sodium bicarbonate device. Also, the presence of saliva and blood during the surgical procedure makes total decontamination of the implant surface a difficult goal to achieve.


The attachment of bacterial cells was related directly to surface roughness. With the increase of the surface roughness, an exponential increase in bacterial cells was observed. For all surfaces tested, the decontamination protocol treatment with a high-pressure sodium bicarbonate device for 1 minute removed all bacterial cells efficiently. This indicates that high-pressure sodium bicarbonate spray should be used in the maintenance phase of implant treatment. Additional studies are necessary to prove the efficacy of this decontamination protocol in more complex surface geometries such as those observed in dental implants.


The authors claim to have no financial interest in any company or any of the products mentioned in this article.


This study was supported by the National Research Council, the State Research Foundation of Rio de Janeiro, and “José Bonifácio” University Foundation.


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Abstract Translations [German, Spanish, Portugese, Japanese]

AUTOR(EN): Cristiano Henrique Figueiredo Pereira da Silva, DDS, MSc*, Guaracilei Maciel Vidigal Jr., DDS, MSc, PhD**, Milton de Uzeda, DDS, PhD***, und Gloria de Almeida Soares, PhD****. * A.O. Professor, Abteilung Orthodontie, zahnmedizinische Fakultät, Gama Pilho Universität, Rio de Janeiro, Brasilien. ** A.O. Professor, Abteilung Oralimplantologie, zahnmedizinische Fakultät, UNIGRANRIO Universität, Duque de Caxias, Brasilien. *** Leiter des Forschungslabors für orale Mikrobiologie, mikrobiologisches Institut, staatliche Universität von Rio de Janeiro, Rio des Janeiro, Brasilien. ****Professor, Abteilung metallurgische Studien und Materialforschung, staatliche Universität von Rio de Janeiro, Rio des Janeiro, Brasilien. Schriftverkehr: Guaracilei Maciel Vidigal Jr., Rua Almirante Ary Rongel, 960/301, Recreio dos Bandeirantes, Rio de Janeiro, RJ, Brasilien, CEP: 22790 –430. Telefon/Fax: 55 21 22571146. eMail:[email protected]

Auswirkungen einer rauen Oberflächenbeschaffenheit bei Titanimplantaten auf die mögliche Anbindung von Streptococcus Sanguis: ein Laborversuch

ZUSAMMENFASSUNG: Die unternommene Studie zielte darauf ab, die Wirksamkeit des Durchführungsprotokolls bei einer 1-minütigen Hochdruckreinigung unter aseptischen Bedingungen und unter Anwendung von Natriumhydrogencarbonat auf die Entfernung von bakteriellen Anlagerungen auf drei Titanoberflächen unterschiedlicher Oberflächenbeschaffenheit zu untersuchen. Während die 10 Titanbleche von Gruppe 1 unbehandelt blieben, wurden die Titanbleche in Gruppe 2 und 3 mit Aluminiumoxidpartikeln (Al2O3 Aluminiumoxid) unterschiedlichen Durchmessers bestrahlt: für Gruppe 2 wurden Partikel mit einer Gröβe von 65 μm gewählt, der Partikelumfang bei Gruppe 3 betrug 250 μm. Die Titanproben wurden sterilisiert und in einer Röhre gemeinsam mit einer Streptococcus Sanguis-Suspension in den Brutofen gegeben. Die Koloniebildenden Einheiten wurden sowohl vor als auch nach Anwendung des Reinigungsprotokolls gezählt. Der durchschnittliche arithmetische Grad and Rauheit (Ra) ermittelte sich in der Gruppenaufteilung wie folgt: Gruppe 1 −0,17 μm ± 0,01; Gruppe 2 −1,14 μm ± 0,15; Gruppe 3 −3,17 μm ± 0,23. Nach erfolgter Verunreinigung wurden bei Gruppe 1 49 x 103 bakterielle Zellen gezählt, die bakterielle Konzentration bei den Gruppen 2 und 3 betrug 11 × 104 bzw. 35 x 105. Nach Anwendung der Reinigungsprozedur gab es keinerlei Nachweis für den Verbleib lebensfähiger Bakterien. Die überdurchschnittliche Zunahme von bakteriellen Zellen stand in direktem Zusammenhang mit einer Erhöhung der Oberflächenrauheit. Die Untersuchungsergebnisse beweisen, dass durch Anwendung des Reinigungsprotokolls unter Anwendung einer Hochdruckreinigung mit Natriumhydrogencarbonat alle bakteriellen Zellen ungeachtet der unterschiedlichen Oberflächenbeschaffenheit beseitigt werden konnten. Daher empfiehlt es sich, die Hochdruckreinigung mit Natriumhydrogencarbonatspray als Mittel zur Erhaltung der Implantatgesundheit innerhalb der Implantierungsbehandlung zu verwenden.

SCHLÜSSELWÖRTER: Titan, Zahnimplantate, Zahnbelag, Rauheit, Entzündungsneigung im Implantierungsbereich

AUTOR(ES): Cristiano Henrique Figueiredo Pereira da Silva, DDS, MSc*, Guaracilei Maciel Vidigal Jr., DDS, MSc, PhD**, Milton de Uzeda, DDS, PhD,*** y Gloria de Almeida Soares, PhD****. *Profesor Asociado, Departamento de Periodóntica, Facultad de Odontología, Gama Filho University, Rio de Janeiro, Brasil. **Profesor Asociado, Departamento de Implantología Oral, Facultad de Odontología, Universidad UNIGRANRIO, Duque de Caxias, Brasil. ***Jefe del Laboratorio de Microbiología Oral, Instituto de Microbiología, Universidad Federal de Rio de Janeiro, Río de Janeiro, Brasil.**** Profesor, Departamento de Metalurgia y Materiales, Universidad Federal de Rio de Janeiro, Rio de Janeiro, Brasil. Correspondencia a: Guaracilei Maciel Vigidal Jr., Rua Almirante Ary Rongel, 960/301, Recreio dos Bandeirantes, Rio de Janeiro, RJ, Brazil, CEP: 22790–430. Teléfono/fax: 55 21 22571146. Correo electrónico:[email protected].com

Influencia de la aspereza de la superficie del titãnio en la colocación de Streptococcus Sanguis: Estudio in vitro.

ABSTRACTO: El propósito de este estudio fue investigar la eficacia del protocolo de descontaminación con un dispositivo de bicarbonato de sodio a alta presión durante 1 minuto bajo condiciones asépticas en la eliminación de bacteria en las superficies de titãnio con tres asperezas diferentes. El grupo 1 estuvo compuesto de diez hojas de titãnio según fueron fabricadas y los grupos 2 y 3 de hojas de titãnio tratadas con partículas de óxido de aluminio (Al2O3, alumina) con diferentes diámetros: el grupo 2 fue tratado con partículas de 65 μm y el Grupo 3 con partículas de 250 μm. Las muestras de titãnio fueron esterilizadas e incubadas en tubos que contienen una suspensión de Streptococcus sanguis. Las unidades que crearon colonias fueron contadas antes y después de la aplicación del protocolo de descontaminación. La mediana aritmética de la aspereza (Ra) por grupo fue: Grupo 1 –0,17 μm + 0,01; Grupo 2 –1,14 μm ± 0,15; Grupo 3 –3,17 μm + 0,23. Después del período de contaminación, el Grupo 1 se mantuvo con 40 x 103 células con bacteria y la concentración de bacterias en los Grupos 2 y 3 fueron 11 × 104 y 35 x 105 respectivamente. Después de la aplicación del protocolo de descontaminación, no se detectó ninguna bacteria viable. Con el aumento de la aspereza de la superficie, se observó un aumento exponencial en las células bacterianas. Los resultados demostraron que el tratamiento con el protocolo de descontaminación, usando un dispositivo de bicarbonato de sodio a alta presión, eliminó eficientemente todas las células bacterianas en todas las superficies estudiadas. Esto indica que el rociado con bicarbonato de sodio a alta presión deberá usarse en la fase de mantenimiento del tratamiento con implantes.

PALABRAS CLAVES: titanio, implantes dentales, placa bacteriana, aspereza, periimplantitis

AUTOR(ES): Cristiano Henrique Figueiredo Pereira da Silva, Cirurgião-Dentista, Mestre em Ciências*, Guaracilei Maciel Vidigal Jr., Cirurgião-Dentista, Mestre em Ciências, PhD**, Milton de Uzeda, Cirurgião-Dentista, PhD*** e Glória de Almeida Soares, PhD****. *Professor Associado, Departamento de Periodontia, Escola de Odontologia, Universidade Gama Filho, Rio de Janeiro, Brasil. **Professor Associado, Departamento de Implantologia Oral, Escola de Odontologia, Universidade UNIGRANRIO, Duque de Caxias, Brasil. ***Chefe do Laboratório de Microbiologia Oral, Instituto de Microbiologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brasil. ****Professor, Departamento Metalúrgico e de Materiais, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brasil. Correspondência para: Guaracilei Maciel Vidigal Jr., Rua Almirante Ary Rangel, 960/301, Recreio dos Bandeirantes, Rio de Janeiro, RJ, Brazil, CEP: 22790–430. Telefone: 55 21 2257–1146, E-mail:[email protected]

Influência da Aspereza da Superfície do Titãnio no “Attachment” do Streptococcus Sanguis: Estudo in Vitro

RESUMO: O propósito deste estudo era investigar a eficácia do protocolo de descontaminação com dispositivo de bicarbonato de sódio de alta pressão durante 1 minuto sob condições assépticas na remoção bacteriana em superfícies de titãnio com três diferentes asperezas. O Grupo 1 era composto de dez folhas de titãnio usinadas e os Grupos 2 e 3 por folhas de titãnio dinamitadas com partículas de óxido de alumínio (Al2O3, alumina) com diferentes diãmetros; o Grupo 2 foi dinamitado com partículas de 65 um e o Grupo 3 com partículas de 250 um. Os espécimes de titãnio foram esterilizados e incubados em tubos contendo uma suspensão de Streptococcus sanguis. A colônia formando unidades foi contada antes e depois da aplicação do protocolo de descontaminação. A aspereza aritmética média (Ru) por grupo foi: Grupo 1 –0,17 um + 0,01; Grupo 2 –1,14 um 0,15; Grupo 3- 3,17 um + 0,23. Depois do período de contaminação, o Grupo 1 fica com 49 x 10 3 de células bacterianas e a concentração bacteriana dos Grupos 2 e 3 foi de 11 × 10 4 e 35 × 10 5, respectivamente. Depois da aplicação do protocolo de descontaminação, nenhuma bactéria viável foi detectada. Com o aumento da aspereza da superfície, um aumento exponencial nas células bacterianas foi observado. Os resultados mostraram que o tratamento por protocolo de descontaminação, usando-se um dispositivo de bicarbonato de sódio de alta pressão removeu eficientemente todas as células bacterianas em todas as superfícies testadas. Isso indica que o spray de bicarbonato de sódio de alta pressão deve ser usado na fase de manutenção do tratamento de implante.

PALAVRAS-CHAVE: titãnio, implantes dentários, placa bacteriana, aspereza, periimplantite

No Caption available.
36. Sugerman PB, Barber MT. Patient selection for endosseous implants: oral and systemic considerations. Int J Oral Maxillofac Implants. 2002;17:191–201.

titanium; dental implants; bacterial plaque; roughness; peri-implantitis

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