Corrosion of Dental Implants and Peri-implant Disease

Study of synergistic effects of mechanical loads and bacteria on the surface of dental implants:

Dental implants (DI) are replacements for natural teeth to overcome partial (or) complete edentulism. The ability of titanium DI to osseointegrate with the biological propelled them to a huge commercial success. In the USA, DI boast a billion dollar market with 500,000 implants placed every year. Reports have shown 95% implantation success rates. But, recently a rising number of failures have been reported due to a clinical condition known as peri-implantitis. Peri-implantitis is the continuous loss of bone surrounding an osseointegrated DI due to inflammatory reactions (Figure 1). There are several factors associated with this clinical condition such as excessive cement particles, occlusal overload, smoking, previous periodontal history, poor plaque control and genetic polymorphism. So far, bacterial biofilm is assumed to be the primary etiological factor for peri-implantitis.

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Figure 1. A scheme of implant failure: top left: osseointegrated implant; top right: a retrieved implant from a patient with peri-implantitis; center: peri-implantitis, a condition of loss of bone surrounding dental implants and loss of osseointegration exposing implant body.

In our current studies we hypothesized that the dissolution of metal ions in the oral environment can play a vital role causing inflammatory reactions leading to peri-implantitis. In general, DI are highly corrosion resistance due to the protective surface oxide layer formed on the titanium substrate in the presence of oxygen. But, under abnormal mechanical occlusal loading and highly acidic electrochemical environments, the oxide layer can be permanently damaged leading to continuous dissolution of metal ions.

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Figure 2. A schematic diagram showing dental implant exposed to various factors of the complex oral environment.

Oral environment involves a combination of mechanical occlusal forces that can cause micro-motion of an osseointegrated DI and electrochemical environment which can be acidified by ingested substances, bacteria, bacteria biofilm and inflammatory reactions (Figure 2). The synergistic effect of micromotion and acidic electrochemical environment can lead to tribocorrosion. This can permanently damage the oxide layer leading continuous dissolution of metal ions. In our previous study of DI retrievals extracted from patients with peri-implantitis, there were tribocorrosion surface features observed (Figure 3) like discoloration, pitting, fatigue cracks, surface etching and scratches. The study revealed a high possibility of dissolution of metal ions in the oral environment.

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Figure 3. Surface features observed in one of the retrievals associated with peri-implantitis. (a) Note the purple and yellow discoloration, which are evidence of titanium bulk attack (arrow); (b) presence of a pit, which served as nucleation site for branched cracks (arrow).

We are currently studying four separate conditions (Figure 4) to better evaluate the effect of oral environmental factors on the surface of dental implants. Conditions were designed to analyze the individual and combinatorial effects of mechanical and electrochemical environments on the surface of dental implants. This study will help to provide a better understanding on the effects of oral environmental factors on the surface of the implant. Preliminary studies have shown that these factors could lead to dissolution of metal ions in-vivo.

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Figure 4. Condition 1: In-vitro insertion test of DI to evaluate the effects of mechanical forces in surgical insertion; Condition 2: In-vitro immersion test to investigate the effect of bacteria on the surface of DI; Condition 3: Mechanical fatigue testing to study the effect of cyclic occlusal loading in a wet environment; Condition 4: Mechanical fatigue testing of DI immersed in bacteria to evaluate the synergistic effect of bacteria and mechanical occlusal forces.

Detoxification of titanium dental implants: evaluation of implant surface and cell compatibility:

Dental implants have altered the face of dentistry over the last 25 years. More than 500,000 implants are placed every year [1] with a success rate of 90-95% [2]. Success of a dental implant is primarily assessed by the condition of the implant’s surface and its capability to biologically integrate with the surrounding soft and hard tissues [3]. Therefore, it is critical to choose appropriate materials to design implants for long term function. But even with a high success rate, 5-10% of implants fail which is a significant number [2]. In general, dental implant failures are classified into early and late stage failures. Bacteria/bacteria biofilm has been assumed as the primary reason for both early- and late- stage complications.

Recently, a rising number of implant failures have been reported due to peri-implantitis, which is a clinical condition characterized by inflammation and continued loss of integrated bone around the implant [4, 5]. A study reported that 28%-56% of patients who receive an implant suffer from this severe clinical condition [6]. Even though, a list of individual and synergistic factors is associated with failure, adhesion of bacterial biofilm on the implant surface is considered as a primary reason for failure [7]. That is why it is critical to mitigate bacterial biofilm formation on implant surfaces.

When peri-implantitis does occur, the clinician has the option to either remove the infected implant or perform debridement and detoxification of the implant surfaces to remove bacteria and its metabolites present on the surface in order to re-establish osseointegration [8]. There are many different methods to treat implants affected by peri-implantitis including: chemical, mechanical and laser treatments [5]. Chemical treatment is employed for debridement of surfaces with biofilm; common chemicals used include citric acid, tetracycline, saline, chlorhexidine, hydrogen peroxide and doxycycline [7, 8, 9-11]. These chemicals are used along with mechanical means such as Er: YAG, CO2 lasers, curettes, and powder blasting [5]. However, mechanical debridement is most preferred and the most common treatment method for peri-implantitis.

Understanding the effect bacterial adhesion and peri-implantitis detoxification treatment method has on the implant surface is crucial to designing an implant for long-term success. We developed a new testing methodology to investigate the surface performance of titanium when exposed to bacterial biofilms and host cells. The study’s main goal is investigating the impact of bacterial adhesion, detoxification with acid chemicals and growth of bone forming cells post-detoxification on Ti surface and verify cell behavior (proliferation and differentiation) on the surface which can be an indicative of re-osseointegration. This experimental setup has the versatility to accommodate different dental implant material as well as different peri-implantitis treatment methods.

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Figure 5. CpTi disks immersed in polyclonal bacterial strain for 5 days.

In a previous study we conducted, titanium disks (cpTi) were immersed in polyclonal bacterial strain containing aggregatibacter actinomycetemcomitans, streptococcus mutans, streptococcus sanguinis, and streptococcus salivarius for 5 days (Figure 5) allowing for a white film (biofilm) to grow. Then detoxification was carried out using rubbing (Figure 6b) and immersion (Figure 6a) methods. Chemicals used in this study were: citric acid (CA- 30%), chlorhexidine (CH- 0.12%), saline (SA 0.9%) & doxycycline (DO 50:50). After the detoxification treatment, MC3T3-E1 osteoblasts were cultured on disk surface for 7 days. After which MTT cell proliferation assay was conducted.

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Figure 6. (A)(left) Immersion of CpTi disks; (B) (right) Rubbing method for CpTi disks.

Results obtained from MTT assay showed percentage cell viability for each chemical and detoxification method used as demonstrated in the bar graph in Figure 7. Results we obtained were unexpected because we hypothesized that due to low pH content of chemical agents used in detoxification of disks, uniform re-osseointegration would be hindered, thus decreasing the possibility of re-growth of cells on the surface of disks. This was not the case, results showed a 66.32% cell viability with citric acid (pH 1.74) versus 32.04% viability from chlorhexidine treatment which had a pH of 2.74. This indicated that bone forming cells favored acidic environments. This might be due to the possibility that acidic chemicals made the surface of the implants rough, thereby allowing for better attachment of cells for growth. Further testing has to be done to conclude on this observation. We are currently carrying out ALP , SEM and XPS analysis of the titanium disks.

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Figure 7. Cell viability measurements post treatment with chemicals using rubbing and immersion methods.

Preliminary studies conducted showed that corrosion and pitting of the samples were present in pure titanium as well as Ti6Al4V grades with immersion and rubbing methods when employing more acidic solutions, which had pH <3. Mildly acidic solutions caused surface discoloration when coupled with rubbing but did not cause corrosion with immersion. Neutral or basic treatments resulted in no signs of corrosion with both methods.

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Figure 8 (A-B). Rubbing treatment with peroxyacetic acid (A) Ti6Al4V AFM 2D treated (B) Ti6Al4V OM image treated. (C-D). Rubbing treatment with citric acid (C) cpTi AFM 2D control (D) cpTi OM image treated.

Our previous studies investigated in depth the effects of three solutions of varying pH used in decontamination: peroxyacetic acid (35% in acetic acid, pH ~0), citric acid (40% in D.I. water pH = ~1), and 0.12% sodium fluoride (in D.I. Water pH ~8). Results of this investigation were published in Clinical Oral Implants Research in January 2011 [12]. CpTi and Ti6Al4V disks were subjected to two different methods of contact with these solutions: immersion in solution, and mechanical debridement in the form of a cotton swab soaked in solution for 8 minutes. The surface of the samples was analyzed using optical microscopy (OM) and Atomic Force Microscopy (AFM) before and after treatment to mark surface differences. It was found that acidic solutions (pH < 3) inflicted mild corrosion on the surface in the immersion treatment, while the addition of mechanical debridement exaggerated these corrosive effects shown in Figure 8. The more neutral solutions were found to inflict no visible damage to the titanium surface. Corrosion was qualified by the identification of pitting through AFM and the Ti3+ (Violet) and Ti4+ (Yellow) oxidative states through optical microscopy. Our preliminary results show that although these solutions can remove the bacterial biofilm they can also inflict surface damage to the implant surface.

References:

[1] http://www.aaid.com/about/Press_Room/Dental_Implants_FAQ.html.
[2] Mellado-Valero, A.; Buitrago-Vera, P.; Sola-Ruiz, M.F; Ferrer-Garcia, J.C. Decontamination of Dental Implant Surface in Peri-Implantitis Treatment: A Literature Review. Med. Oral Patol. Oral Cir. Bucal 2013, 18 (6), e869-e876.
[3] Albrektsson T, Hansson HA, Ivarsson B. Interface analysis of titanium and zirconium bone implants. Biomaterials. 1985;6:97-101.
[4] Koldsland, O. C.; Scheie, A. A.; Aass, A. M. Prevalence of Peri-Implantitis Related to Severity of the Disease with Different Degrees of Bone Loss. J. Periodontol. 2010, 81 (2), 231–238.
[5] Mouhyi, J.; Dohan Ehrenfest, D. M.; Albrektsson, T. The Peri-Implantitis: Implant Surfaces, Microstructure, and Physicochemical Aspects. Clin. Implant Dent. Relat. Res. 2012, 14 (2), 170–183.
[6]Pontoriero, R.; Tonelli, M.P.; Carnevale, G.; Mombelli, A; Nyman, S.R.; Lang, N. P. Experimentally Induced Peri-Implant Mucositis. A Clinical Study in Humans. Clin. Oral Implants Res. 1994, 5 (4), 254–259.
[7] Valderrama P, Gonzalez MG, Cantu MG, Wilson TG. Detoxification of Implant Surfaces Affected by Peri-Implant Disease: An Overview of Non-surgical Methods. Open Dent J. 2014;8(1):77-84. doi:10.2174/1874210601408010077.
[8] Subramani, K. & Wismeijer, D. (2012) Decontamination of titanium implant surface and re osseointegration to treat peri-implantitis: a literature review. International Journal of Oral Maxillofacial Implants 27: 1043–1054.
[9] Finnegan, M., Linley, E., Stenyer, S.P., Mcdonnell, G., Simons, C. & Maillard, J.Y. (2010) Mode of action of hydrogen peroxide and other oxidizing agents: differences between liquid and gas forms.Journal of Antimicrobial Chemotherapy 65:2108–2115.
[10] Gosau, M., Hahnel, S., Schwarz, F., Gerlach, T., Reichert, T.E. & B€urger, R. (2010) Effect of six different peri-implantitis disinfection methods on in vivo human oral biofilm. Clinical Oral Implants Research 21: 866–872.
[11] De Waal, Y.C.M., Raghoebar, G.M., Meijer, H.J., Winkel, E.G. & van Winkelhoff, J. (2014) Implant decontamination with 2% chlorhexidine during surgical peri-implantitis treatment: a randomized, double-blind, controlled trial. Clinical Oral Implants Research 1–9. doi:10.1111/ clr.12419.
[12] Wheelis SE, Gindri IM, Valderrama P, Wilson TG, Huang J, Rodrigues DC. Effects of decontamination solutions on the surface of titanium: Investigation of surface morphology, composition, and roughness. Clin Oral Implants Res. 2016;27(3):329-340. doi:10.1111/clr.12545.