Microbial Biofilm Decontamination on Dental Implant Surfaces: A Mini Review

Abstract

Introduction:

After insertion into the bone, implants osseointegrate, which is required for their long-term success. However, inflammation and infection around the implants may lead to implant failure leading to peri-implantitis and loss of supporting bone, which may eventually lead to failure of implant. Surface chemistry of the implant and lack of cleanliness on the part of the patient are related to peri-implantitis. The only way to get rid of this infection is decontamination of dental implants.

Objective:

This systematic review intended to study decontamination of microbial biofilm methods on titanium implant surfaces used in dentistry.

Methods:

The electronic databases Springer Link, Science Direct, and PubMed were explored from their inception until December 2020 to identify relevant studies. Studies included had to evaluate the efficiency of new strategies either to prevent formation of biofilm or to treat matured biofilm on dental implant surfaces.

Results and Discussion:

In this systematic review, 17 different groups of decontamination methods were summarized from 116 studies. The decontamination methods included coating materials, mechanical cleaning, laser treatment, photodynamic therapy, air polishing, anodizing treatment, radiation, sonication, thermal treatment, ultrasound treatment, chemical treatment, electrochemical treatment, antimicrobial drugs, argon treatment, and probiotics.

Conclusion:

The findings suggest that most of the decontamination methods were effective in preventing the formation of biofilm and in decontaminating established biofilm on dental implants. This narrative review provides a summary of methods for future research in the development of new dental implants and decontamination techniques.

Introduction

Dental implants are number one choice for replacement of teeth. It is a valuable option in several treatment scenarios, e.g., (i) when teeth are lost to non-periodontal diseases, infection due to caries, traumatic injuries; (ii) loss of teeth due to periodontal diseases but the remaining teeth can be maintained; and (iii) combined scenarios requiring replacement of missing teeth (Greenwell et al., 2019). An implant is typically composed of titanium or titanium alloys because of its biocompatibility and mechanical properties. Recent studies show that titanium dental implants survived for more than 20 years, regardless of their long-term exposure to the oral environment (Chen et al., 2017; Albrektsson et al., 2019). After insertion into the bone, implant osseointegration is expected to occur and is fundamental for its long-term success (Alghamdi, 2018). However, dental implants cannot be used for treatment of periodontal or dental disease (Greenwell et al., 2019). In addition, inflammatory reaction and infection around the implants may occur and can lead to implant failure, a phenomenon called peri-implantitis (Berglundh et al., 2019). Peri-implantitis is caused by plaque bacteria, leading to inflammation of mucosa and subsequent bone loss surrounding the implant, which may ultimately result in total implant failure (Berglundh et al., 2019). Surface chemistry and lack of cleanliness are intimately associated with peri-implantitis (Rupp et al., 2018).

Implant loss often triggers a devastating psychological impact on patients’ lives, with significantly high financial losses to families and healthcare systems (Alzahrani and Gibson, 2018; Frazadmoghadam et al., 2018; Hoeksema et al., 2018). Peri-implantitis is reported to occur at different levels of severity, with about 10% of them being lost within a 5-year period (Koldsland et al., 2010; Caton J. et al., 2018). It has been reported that peri‐implantitis takes place in 3–47% of dental implants (Koldsland et al., 2010; Matarazzo et al., 2018; French et al., 2019). Peri-implantitis is frequently related to periodontal pathogens and usually treated with antibiotics (Ting et al., 2018; Hussain et al., 2018). Bacterial biofilm has been advocated to be the leading etiological factor in the causation of peri-implantitis. Biofilm is a highly structured, matrix-enclosed bacterial community in a sessile state (Magana et al., 2018). Biofilm formation is a typical feature of bacterial growth, causing evasion from host cells and avoiding competition with other microbial communities (Guilhen et al., 2017). Several steps are needed to form biofilms, which include (i) planktonic bacteria adhesion on the surface, (ii) adhesion on the surface to establish a firm platform, (iii) co-aggregation with other bacteria, which further stabilizes their buildup architecture, (iv) growth by absorbing nutrition from the environment until maturation phase, and (v) detachment of a portion of biofilms to invade another vulnerable site (Guilhen et al., 2017). It is more challenging to eradicate established biofilm colonization than to eradicate the circulating contamination itself (i.e., planktonic microbiota). This significantly increases resistance to antibiotic treatment (Arciola et al., 2018). Resident microbiota and matrix in biofilm may hinder access of antimicrobials locally, preventing their penetration into deeper layers of biofilm (Kuang et al., 2018). Therefore, it is deemed imperative that studies in the future focus on the prevention or reduction of biofilm formation.

Several techniques for decontamination of implants have been used over the years. However, none of them have successfully produced optimal results. Mechanisms underpinning these processes are still not understood fully and decontamination of implants remains challenging. A previous systematic review was performed a few years ago (Grischke et al., 2016). Thus, an updated review is necessary. Additionally, other systematic reviews have only evaluated the ability of a selected type of method for decontamination of the implant surface (Louropoulou et al., 2015; Chouirfa et al., 2018; Dutra et al., 2018; Mishra and Chowdhary, 2018). The primary objective of this systematic review was to study and report evidence on all currently investigated methods for decontaminating pathogenic microbiota on dental implant surfaces.

Methods

Data Sources

A systematic search was performed in Science Direct, PubMed, and Springer Link from inception up until December 2020. The search was limited to studies published in the English language due to the authors’ inability to translate other published languages in the literature. The following search terms were used: “dental” AND “implant” AND “titanium” AND “bacteria” AND “biofilm” AND (“treatment” OR “decontamination” OR “eradication” OR “cleaning” OR “remove”). Wildcards, e.g., asterisk (*), a question mark ()?, or other symbols that designate the selected database, were applied. Original papers comprising of experimental studies that used titanium materials for the studies were included in the present review. The studies included should have reported the presence of microbial biofilm both by bacteria and fungi. After date was extracted, it was entered into Microsoft Excel in a data extraction form for enabling summarization of data and final report writing. Data analysis was completed using SPSS Software Version 23 and PRISM Software Version 7 (GraphPad Inc.).

Results and Discussion

The electronic exploration yielded six hundred and forty-three results (n = 643). Duplicates were removed, and on additional screening, one hundred and sixteen studies comprised this review (n =116) (Schwarz et al., 2005; Duarte et al., 2009; Ewald and Ihde, 2009; Größner-Schreiber et al., 2009; Sennhenn-Kirchner et al., 2009; Tamai et al., 2009; Gonçalves et al., 2010; Baffone et al., 2011; Ercan et al., 2011; Fröjd et al., 2011; Giordano et al., 2011; Mohn et al., 2011; Ntrouka et al., 2011; Bürgers et al., 2012; Cortizo et al., 2012; Lilja et al., 2012; Rehman et al., 2012; Subramanian et al., 2012; Trujillo et al., 2012; Alcheikh et al., 2013; Cochis et al., 2013; De Giglio et al., 2013; Diab Al-Radha et al., 2013; Eick et al., 2013; Holmberg et al., 2013; Idlibi et al., 2013; Roberts et al., 2013; Chen et al., 2014; Ciandrini et al., 2014; Drago et al., 2014; Godoy-Gallardo et al., 2014; Hauser-Gerspach et al., 2014; Kaliaraj et al., 2014; Kang et al., 2014; Lv et al., 2014; Massa et al., 2014; Sahrmann et al., 2014; Schmage et al., 2014; Schmidt et al., 2014; Yamada et al., 2014; Abdulkareem et al., 2015; Charalampakis et al., 2015; Cruz et al., 2015; de Avila et al., 2015; Duske et al., 2015; Janković et al., 2015; Jennings et al., 2015; Lewandowska et al., 2015; Narendrakumar et al., 2015; Park et al., 2015; Yucesoy et al., 2015; Wood et al., 2015; Zhang et al., 2015; Ayre et al., 2016; Chen et al., 2016; Ciandrini et al., 2016; Cochis et al., 2016; Cotolan et al., 2016; Cunha et al., 2016; Giannelli et al., 2016; Godoy-Gallardo et al., 2016; Gopal et al., 2016; Guan et al., 2016; John et al., 2016; Kuehl et al., 2016; Kotsakis et al., 2016; Mang et al., 2016; Preissner et al., 2016; Rodríguez-Contreras et al., 2016; Shi et al., 2016; Verardi et al., 2016; Al-Hashedi et al., 2017; Batsukh et al., 2017; Canullo et al., 2017; Ciandrini et al., 2017; Cometa et al., 2017; Dostie et al., 2017; Eick et al., 2017; Ferraris et al., 2017; Giannelli et al., 2017; Granick et al., 2017; Hirschfeld et al., 2017; Kim et al., 2017; Kulkarni Aranya et al., 2017; Li et al., 2017; Macpherson et al., 2017; Matthes et al., 2017; Prieto-Borja et al., 2017; Schmidt et al., 2017; Strever et al., 2017; Ramesh et al., 2017; Wang et al., 2017; Wiedmer et al., 2017; Ye et al., 2017; Zhang et al., 2017; Al-Hashedi et al., 2018; Akhavan et al., 2018; Atefyekta et al., 2018; Azizi et al., 2018; Ferraris et al., 2018; Fukushima et al., 2018; Hidalgo-Robatto et al., 2018; Hoyos-Nogués et al., 2018; Lee et al., 2018; Montelongo-Jauregui et al., 2018; Pantaroto et al., 2018; Pissinis et al., 2018; Santos-Coquillat et al., 2018; Schneider et al., 2018; Souza et al., 2018; Trobos et al., 2018; Vilarrasa et al., 2018; Wang et al., 2018; Zhang et al., 2018; Huang et al., 2019; Schmidt et al., 2019).

A flowchart (Supplementary Information 1) demonstrates the procedure of inclusion and exclusion of pertinent articles. We excluded review papers, non-English language studies, and those not relevant to the focus of this review. Our analysis revealed that the topic of our systematic review has been deeply researched for the previous 10 years, especially in the years 2017–2018. The interest on this topic is mainly because of titanium being an inert material with the properties of encouraging tissue healing and bacterial colonization resistance, as compared with other implant materials (Chen et al., 2017).

Numerous studies have attempted to evaluate different methods to decontaminate dental biofilms. The decontamination methods included in this systematic review were categorized into 19 groups, namely, the coating of titanium materials (47.4%), mechanical cleaning (10.3%), laser treatment (9.5%), photodynamic therapy (4.3%), air polishing (3.4%), anodizing treatment (3.4%), radiation (3.4%), sonication (0.9%), thermal treatment (0.9%), ultrasound (0.9%), chemical treatment (13.8%), electrochemical treatment (1.7%), antimicrobial drugs (0.9%), argon treatment (0.9%), and probiotics (0.9%). Table 1 presented the decontamination methods using specialized instruments and the findings of the respective studies. These decontamination methods were then divided into two types based on whether the biofilm was already established (biofilm-treatment) or not (biofilm-prevention). Supplementary Information 2 shows the coating of the titanium materials, method of decontamination, and type of decontamination method.

In this systematic review, 63 studies focused on biofilm-prevention methods (n = 63, 54.3%) (Duarte et al., 2009; Ewald and Ihde, 2009; Größner-Schreiber et al., 2009; Sennhenn-Kirchner et al., 2009; Tamai et al., 2009; Baffone et al., 2011; Ercan et al., 2011; Fröjd et al., 2011; Giordano et al., 2011; Cortizo et al., 2012; Rehman et al., 2012; Subramanian et al., 2012; Trujillo et al., 2012; Alcheikh et al., 2013; De Giglio et al., 2013; Holmberg et al., 2013; Roberts et al., 2013; Godoy-Gallardo et al., 2014; Lv et al., 2014; Kaliaraj et al., 2014; Kang et al., 2014; Massa et al., 2014; Yamada et al., 2014; Abdulkareem et al., 2015; de Avila et al., 2015; Janković et al., 2015; Jennings et al., 2015; Lewandowska et al., 2015; Narendrakumar et al., 2015; Wood et al., 2015; Yucesoy et al., 2015; Zhang et al., 2015; Ayre et al., 2016; Cochis et al., 2016; Cotolan et al., 2016; Cunha et al., 2016; Godoy-Gallardo et al., 2016; Gopal et al., 2016; Guan et al., 2016; Kuehl et al., 2016; Rodríguez-Contreras et al., 2016; Shi et al., 2016; Ciandrini et al., 2017; Cometa et al., 2017; Ferraris et al., 2017; Giannelli et al., 2017; Hirschfeld et al., 2017; Kulkarni Aranya et al., 2017; Macpherson et al., 2017; Schmidt et al., 2017; Ye et al., 2017; Akhavan et al., 2018; Atefyekta et al., 2018; Ferraris et al., 2018; Hidalgo-Robatto et al., 2018; Hoyos-Nogués et al., 2018; Pantaroto et al., 2018; Pissinis et al., 2018; Santos-Coquillat et al., 2018; Trobos et al., 2018; Vilarrasa et al., 2018; Wang et al., 2018; Zhang et al., 2018), whereas 51 studies focused on biofilm-treatment methods (n = 51, 44.0%) (Schwarz et al., 2005; Gonçalves et al., 2010; Mohn et al., 2011; Ntrouka et al., 2011; Bürgers et al., 2012; Cochis et al., 2013; Diab Al-Radha et al., 2013; Eick et al., 2013; Idlibi et al., 2013; Chen et al., 2014; Drago et al., 2014; Hauser-Gerspach et al., 2014; Sahrmann et al., 2014; Schmage et al., 2014; Schmidt et al., 2014; Charalampakis et al., 2015; Cruz et al., 2015; Duske et al., 2015; Park et al., 2015; Chen et al., 2016; Ciandrini et al., 2016; Mang et al., 2016; Giannelli et al., 2016; John et al., 2016; Kotsakis et al., 2016; Preissner et al., 2016; Verardi et al., 2016; Al-Hashedi et al., 2017; Batsukh et al., 2017; Canullo et al., 2017; Dostie et al., 2017; Eick et al., 2017; Granick et al., 2017; Kim et al., 2017; Li et al., 2017; Matthes et al., 2017; Prieto-Borja et al., 2017; Ramesh et al., 2017; Strever et al., 2017; Wang et al., 2017; Wiedmer et al., 2017; Zhang et al., 2017; Al-Hashedi et al., 2018; Azizi et al., 2018; Fukushima et al., 2018; Lee et al., 2018; Montelongo-Jauregui et al., 2018; Schneider et al., 2018; Souza et al., 2018; Huang et al., 2019; Schmidt et al., 2019), while two studies offered their novel method to work for both biofilm-prevention and biofilm-treatment measures (n = 2, 1.7%) (Lilja et al., 2012; Ciandrini et al., 2014).

In Vivo Studies

Twenty-two studies applied oral normal flora in human participants who were either healthy or diagnosed with peri-implantitis or periodontitis (n = 22, 19.0%) (Schwarz et al., 2005; Größner-Schreiber et al., 2009; Rehman et al., 2012; Diab Al-Radha et al., 2013; Cochis et al., 2013; Idlibi et al., 2013; Abdulkareem et al., 2015; Charalampakis et al., 2015; de Avila et al., 2015; Duske et al., 2015; Park et al., 2015; John et al., 2016; Kotsakis et al., 2016; Verardi et al., 2016; Al-Hashedi et al., 2017; Dostie et al., 2017; Li et al., 2017; Matthes et al., 2017; Al-Hashedi et al., 2018; Wang et al., 2018; Schmidt et al., 2019). One hundred and five studies performed in-vitro experiments (n = 105, 90.5%) (Duarte et al., 2009; Ewald and Ihde, 2009; Sennhenn-Kirchner et al., 2009; Tamai et al., 2009; Gonçalves et al., 2010; Baffone et al., 2011; Ercan et al., 2011; Fröjd et al., 2011; Mohn et al., 2011; Ntrouka et al., 2011; Bürgers et al., 2012; Cortizo et al., 2012; Lilja et al., 2012; Subramanian et al., 2012; Trujillo et al., 2012; Alcheikh et al., 2013; De Giglio et al., 2013; Diab Al-Radha et al., 2013; Eick et al., 2013; Holmberg et al., 2013; Roberts et al., 2013; Chen et al., 2014; Ciandrini et al., 2014; Drago et al., 2014; Godoy-Gallardo et al., 2014; Hauser-Gerspach et al., 2014; Kaliaraj et al., 2014; Kang et al., 2014; Lv et al., 2014; Massa et al., 2014; Sahrmann et al., 2014; Schmidt et al., 2014; Schmage et al., 2014; Yamada et al., 2014; Abdulkareem et al., 2015; Cruz et al., 2015; de Avila et al., 2015; Duske et al., 2015; Janković et al., 2015; Jennings et al., 2015; Lewandowska et al., 2015; Narendrakumar et al., 2015; Park et al., 2015; Wood et al., 2015; Yucesoy et al., 2015; Zhang et al., 2015; Ayre et al., 2016; Chen et al., 2016; Ciandrini et al., 2016; Cochis et al., 2016; Cotolan et al., 2016; Cunha et al., 2016; Giannelli et al., 2016; Godoy-Gallardo et al., 2016; Gopal et al., 2016; Guan et al., 2016; Kotsakis et al., 2016; Mang et al., 2016; Preissner et al., 2016; Rodríguez-Contreras et al., 2016; Shi et al., 2016; Verardi et al., 2016; Batsukh et al., 2017; Canullo et al., 2017; Ciandrini et al., 2017; Cometa et al., 2017; Dostie et al., 2017; Eick et al., 2017; Ferraris et al., 2017; Giannelli et al., 2017; Granick et al., 2017; Hirschfeld et al., 2017; Kim et al., 2017; Kulkarni Aranya et al., 2017; Li et al., 2017; Macpherson et al., 2017; Matthes et al., 2017; Prieto-Borja et al., 2017; Ramesh et al., 2017; Schmidt et al., 2017; Strever et al., 2017; Wang et al., 2017; Wiedmer et al., 2017; Ye et al., 2017; Zhang et al., 2017; Akhavan et al., 2018; Atefyekta et al., 2018; Azizi et al., 2018; Ferraris et al., 2018; Fukushima et al., 2018; Hidalgo-Robatto et al., 2018; Hoyos-Nogués et al., 2018; Lee et al., 2018; Montelongo-Jauregui et al., 2018; Pantaroto et al., 2018; Pissinis et al., 2018; Santos-Coquillat et al., 2018; Schneider et al., 2018; Souza et al., 2018; Trobos et al., 2018; Vilarrasa et al., 2018; Wang et al., 2018; Zhang et al., 2018; Huang et al., 2019), 11 studies performed in-vivo experiments on humans (n = 11, 9.5%) (Schwarz et al., 2005; Größner-Schreiber et al., 2009; Sennhenn-Kirchner et al., 2009; Baffone et al., 2011; Fröjd et al., 2011; Rehman et al., 2012; Cochis et al., 2013; Idlibi et al., 2013; Charalampakis et al., 2015; Cruz et al., 2015; John et al., 2016; Al-Hashedi et al., 2017; Al-Hashedi et al., 2018; Schmidt et al., 2019), while two studies performed both in-vitro and in-vivo experiments (n = 2, 1.7%) (Giordano et al., 2011; Kuehl et al., 2016). Amongst the in-vivo experiments which recruited human volunteers, 11 studies used titanium discs (n = 11, 9.5%) (Schwarz et al., 2005; Größner-Schreiber et al., 2009; Giordano et al., 2011; Rehman et al., 2012; Cochis et al., 2013; Idlibi et al., 2013; Charalampakis et al., 2015; Kuehl et al., 2016; Al-Hashedi et al., 2017; Al-Hashedi et al., 2018), while the other two studies used titanium implants (n = 2, 1.7%) (John et al., 2016; Schmidt et al., 2019).

In Vitro Studies

Out of 116 studies, some studies did not use discs (n = 13, 11.2%) (Gonçalves et al., 2010; Mohn et al., 2011; Subramanian et al., 2012; Kaliaraj et al., 2014; Lewandowska et al., 2015; Narendrakumar et al., 2015; Park et al., 2015; John et al., 2016; Preissner et al., 2016; Cometa et al., 2017; Schmidt et al., 2017; Azizi et al., 2018; Schmidt et al., 2019). One study performed on discs and other form of titanium (n = 1, 0.9%) (Kulkarni et al., 2017), four studies did not state whether they used discs (n = 4, 3.4%) (Cunha et al., 2016; Macpherson et al., 2017; Ramesh et al., 2017; Akhavan et al., 2018), while the others used discs (n = 98, 84.5%) (Schwarz et al., 2005; Duarte et al., 2009; Ewald and Ihde, 2009; Größner-Schreiber et al., 2009; Sennhenn-Kirchner et al., 2009; Tamai et al., 2009; Baffone et al., 2011; Ercan et al., 2011; Fröjd et al., 2011; Ntrouka et al., 2011; Bürgers et al., 2012; Cortizo et al., 2012; Lilja et al., 2012; Rehman et al., 2012; Trujillo et al., 2012; Alcheikh et al., 2013; Cochis et al., 2013; De Giglio et al., 2013; Diab Al-Radha et al., 2013; Eick et al., 2013; Holmberg et al., 2013; Idlibi et al., 2013; Roberts et al., 2013; Chen et al., 2014; Ciandrini et al., 2014; Drago et al., 2014; Godoy-Gallardo et al., 2014; Hauser-Gerspach et al., 2014; Kang et al., 2014; Lv et al., 2014; Massa et al., 2014; Sahrmann et al., 2014; Schmidt et al., 2014; Schmage et al., 2014; Yamada et al., 2014; Abdulkareem et al., 2015; Charalampakis et al., 2015; Cruz et al., 2015; de Avila et al., 2015; Duske et al., 2015; Janković et al., 2015; Jennings et al., 2015; Wood et al., 2015; Yucesoy et al., 2015; Zhang et al., 2015; Ayre et al., 2016; Chen et al., 2016; Cochis et al., 2016; Ciandrini et al., 2016; Cotolan et al., 2016; Giannelli et al., 2016; Godoy-Gallardo et al., 2016; Gopal et al., 2016; Guan et al., 2016; Kotsakis et al., 2016; Kuehl et al., 2016; Mang et al., 2016; Rodríguez-Contreras et al., 2016; Shi et al., 2016; Verardi et al., 2016; Al-Hashedi et al., 2017; Batsukh et al., 2017; Canullo et al., 2017; Ciandrini et al., 2017; Dostie et al., 2017; Eick et al., 2017; Ferraris et al., 2017; Granick et al., 2017; Giannelli et al., 2017; Hirschfeld et al., 2017; Kim et al., 2017; Kulkarni Aranya et al., 2017; Li et al., 2017; Matthes et al., 2017; Prieto-Borja et al., 2017; Strever et al., 2017; Wang et al., 2017; Wiedmer et al., 2017; Ye et al., 2017; Zhang et al., 2017; Al-Hashedi et al., 2018; Atefyekta et al., 2018; Ferraris et al., 2018; Fukushima et al., 2018; Hidalgo-Robatto et al., 2018; Hoyos-Nogués et al., 2018; Huang et al., 2019; Lee et al., 2018; Montelongo-Jauregui et al., 2018; Pantaroto et al., 2018; Pissinis et al., 2018; Santos-Coquillat et al., 2018; Schneider et al., 2018; Souza et al., 2018; Trobos et al., 2018; Vilarrasa et al., 2018; Wang et al., 2018; Zhang et al., 2018).

Studies With Development of Dental Biofilm

Forty-nine different types of microorganisms have been used for the development of dental biofilm in the included studies for this systematic review (n = 49, Table 2). The biofilm matrix was either in single species or mixed species. Seventy-eight studies performed on single-species biofilm (n = 78, 67.2%) (Duarte et al., 2009; Ewald and Ihde, 2009; Sennhenn-Kirchner et al., 2009; Tamai et al., 2009; Gonçalves et al., 2010; Ercan et al., 2011; Giordano et al., 2011; Trujillo et al., 2012; Bürgers et al., 2012; Lilja et al., 2012; Roberts et al., 2013; Holmberg et al., 2013; De Giglio et al., 2013; Alcheikh et al., 2013; Chen et al., 2014; Drago et al., 2014; Godoy-Gallardo et al., 2014; Hauser-Gerspach et al., 2014; Kaliaraj et al., 2014; Kang et al., 2014; Lv et al., 2014; Massa et al., 2014; Schmage et al., 2014; Yamada et al., 2014; Zhang et al., 2015; Jennings et al., 2015; Narendrakumar et al., 2015; Yucesoy et al., 2015; Wood et al., 2015; Janković et al., 2015; Lewandowska et al., 2015; Ayre et al., 2016; Chen et al., 2016; Ciandrini et al., 2016; Cotolan et al., 2016; Cunha et al., 2016; Giannelli et al., 2016; Godoy-Gallardo et al., 2016; Gopal et al., 2016; Guan et al., 2016; Kuehl et al., 2016; Mang et al., 2016; Preissner et al., 2016; Rodríguez-Contreras et al., 2016; Shi et al., 2016; Batsukh et al., 2017; Canullo et al., 2017; Ciandrini et al., 2017; Cometa et al., 2017; Eick et al., 2017; Ferraris et al., 2017; Giannelli et al., 2017; Granick et al., 2017; Hirschfeld et al., 2017; Kim et al., 2017; Kulkarni Aranya et al., 2017; Macpherson et al., 2017; Prieto-Borja et al., 2017; Strever et al., 2017; Zhang et al., 2017; Wang et al., 2017; Wiedmer et al., 2017; Ye et al., 2017; Akhavan et al., 2018; Atefyekta et al., 2018; Azizi et al., 2018; Ferraris et al., 2018; Fukushima et al., 2018; Hidalgo-Robatto et al., 2018; Hoyos-Nogués et al., 2018; Lee et al., 2018; Pissinis et al., 2018; Santos-Coquillat et al., 2018; Souza et al., 2018; Trobos et al., 2018; Zhang et al., 2018; Huang et al., 2019). Ten studies performed on mixed-species biofilm (n = 10, 8.6%) (Fröjd et al., 2011; Cortizo et al., 2012; Subramanian et al., 2012; Sahrmann et al., 2014; Schmidt et al., 2014; Cruz et al., 2015; Cochis et al., 2016; Ramesh et al., 2017; Schneider et al., 2018; Vilarrasa et al., 2018), while eight studies compared single-species and mixed species biofilm (n = 8, 6.9%) (Baffone et al., 2011; Ntrouka et al., 2011; Eick et al., 2013; Ciandrini et al., 2014; Annunziata et al., 2017; Schmidt et al., 2017; Montelongo-Jauregui et al., 2018; Pantaroto et al., 2018). Decontamination methods using antimicrobial drugs, chemical treatment, electrochemical treatment, probiotic, and the findings of the respective studies are presented in Supplementary Information 3.

In experiments that used bacteria or fungi either as single species or mixed species (without the exposure to normal flora), 143 experiments applied biofilm aged less or equal to 24 h (n = 143, 64.7%), 72 experiments applied biofilm aged more than 24 h or equal to 48 h (n = 72, 32.6%), 38 experiments applied biofilm aged more than 48 h or equal to 72 h (n = 38, 17.2%), while 23 experiments applied biofilm aged more than 72 h (n = 23, 10.4%) (Table 2). Table 2 shows the list of oral microbiota used for the development of biofilm on the titanium materials.

The included studies in this systematic review applied several methods after decontamination of the titanium material either to quantify the microbial biofilm or to observe the morphological changes. Fifty-three studies used the number of colony forming unit (CFU) (n = 53, 45.7%) (Duarte et al., 2009; Ewald and Ihde, 2009; Tamai et al., 2009; Gonçalves et al., 2010; Giordano et al., 2011; Baffone et al., 2011; Mohn et al., 2011; Ntrouka et al., 2011; Cochis et al., 2013; Diab Al-Radha et al., 2013; Eick et al., 2013; Holmberg et al., 2013; Roberts et al., 2013; Chen et al., 2014; Ciandrini et al., 2014; Drago et al., 2014; Godoy-Gallardo et al., 2014; Hauser-Gerspach et al., 2014; Massa et al., 2014; Sahrmann et al., 2014; Abdulkareem et al., 2015; Charalampakis et al., 2015; Janković et al., 2015; Narendrakumar et al., 2015; Wood et al., 2015; Chen et al., 2016; Cochis et al., 2016; Giannelli et al., 2016; Guan et al., 2016; Kuehl et al., 2016; Mang et al., 2016; Preissner et al., 2016; Rodríguez-Contreras et al., 2016; Verardi et al., 2016; Ciandrini et al., 2017; Cometa et al., 2017; Dostie et al., 2017; Eick et al., 2017; Ferraris et al., 2017; Giannelli et al., 2017; Granick et al., 2017; Hirschfeld et al., 2017; Kim et al., 2017; Prieto-Borja et al., 2017; Wiedmer et al., 2017; Akhavan et al., 2018; Azizi et al., 2018; Ferraris et al., 2018; Pantaroto et al., 2018; Pissinis et al., 2018; Souza et al., 2018; Trobos et al., 2018; Vilarrasa et al., 2018). Fifty-eight studies used scanning electron microscopy (SEM) (n = 58, 50%) (Duarte et al., 2009; Sennhenn-Kirchner et al., 2009; Gonçalves et al., 2010; Ercan et al., 2011; Giordano et al., 2011; Trujillo et al., 2012; Cochis et al., 2013; Eick et al., 2013; Holmberg et al., 2013; Yamada et al., 2014; Duske et al., 2015; Godoy-Gallardo et al., 2014; Kaliaraj et al., 2014; Abdulkareem et al., 2015; Charalampakis et al., 2015; Cruz et al., 2015; de Avila et al., 2015; Lewandowska et al., 2015; Park et al., 2015; Zhang et al., 2015 ; Preissner et al., 2016; Chen et al., 2016; Cochis et al., 2016; Cotolan et al., 2016; Cunha et al., 2016; Giannelli et al., 2016; John et al., 2016; Kotsakis et al., 2016; Mang et al., 2016; Shi et al., 2016; Al-Hashedi et al., 2017; Batsukh et al., 2017; Canullo et al., 2017; Dostie et al., 2017; Giannelli et al., 2017; Kim et al., 2017; Kulkarni Aranya et al., 2017; Li et al., 2017; Matthes et al., 2017; Ramesh et al., 2017; Schmidt et al., 2017; Strever et al., 2017; Wang et al., 2017; Wiedmer et al., 2017; Zhang et al., 2017; Al-Hashedi et al., 2018; Atefyekta et al., 2018; Azizi et al., 2018; Hidalgo-Robatto et al., 2018; Lee et al., 2018; Montelongo-Jauregui et al., 2018; Pantaroto et al., 2018; Souza et al., 2018; Trobos et al., 2018; Vilarrasa et al., 2018; Wang et al., 2018; Zhang et al., 2018; Huang et al., 2019). Thirty-two studies used confocal laser scanning microscopy (CLSM) (n = 32, 27.6%) (Fröjd et al., 2011; Eick et al., 2013; Drago et al., 2014; Lv et al., 2014; Sahrmann et al., 2014; Schmidt et al., 2014; Abdulkareem et al., 2015; de Avila et al., 2015; Zhang et al., 2015; Guan et al., 2016; Kotsakis et al., 2016; Preissner et al., 2016; Dostie et al., 2017; Giannelli et al., 2017; Kim et al., 2017; Kulkarni Aranya et al., 2017; Li et al., 2017; Matthes et al., 2017; Strever et al., 2017; Wiedmer et al., 2017; Ye et al., 2017; Zhang et al., 2017; Al-Hashedi et al., 2018; Akhavan et al., 2018; Hoyos-Nogués et al., 2018; Montelongo-Jauregui et al., 2018; Souza et al., 2018; Trobos et al., 2018; Wang et al., 2018; Vilarrasa et al., 2018; Zhang et al., 2018). A few of the studies that reported the use of SEM disclosed that their SEM protocol was operated between 1 and 30 kV accelerating voltage (46.7%) (Sennhenn-Kirchner et al., 2009; Ercan et al., 2011; Trujillo et al., 2012; Cochis et al., 2013; ; Eick et al., 2013; Godoy-Gallardo et al., 2014; Cruz et al., 2015; Duske et al., 2015; Lewandowska et al., 2015; Park et al., 2015; Cotolan et al., 2016; Preissner et al., 2016; Al-Hashedi et al., 2017; Batsukh et al., 2017; Dostie et al., 2017; Kulkarni Aranya et al., 2017; Matthes et al., 2017; Ramesh et al., 2017; Al-Hashedi et al., 2018; Atefyekta et al., 2018; Lee et al., 2018; Pantaroto et al., 2018; Trobos et al., 2018; Wang et al., 2018).

In this review, the most commonly employed oral microbiota for the study of dental biofilms were Staphylococcus aureus (15.9%) (Ewald and Ihde, 2009; Tamai et al., 2009; Baffone et al., 2011; Ercan et al., 2011; Giordano et al., 2011; Alcheikh et al., 2013; De Giglio et al., 2013; Drago et al., 2014; Lv et al., 2014; Yamada et al., 2014; Janković et al., 2015; Jennings et al., 2015; Lewandowska et al., 2015; Ayre et al., 2016; Cunha et al., 2016; Giannelli et al., 2016; Gopal et al., 2016; Kuehl et al., 2016; Shi et al., 2016; Cometa et al., 2017; Ferraris et al., 2017; Giannelli et al., 2017; Prieto-Borja et al., 2017; Wang et al., 2017; Ye et al., 2017; Akhavan et al., 2018; Atefyekta et al., 2018; Ferraris et al., 2018; Hidalgo-Robatto et al., 2018; Pissinis et al., 2018; Santos-Coquillat et al., 2018; Zhang et al., 2018), Porphyromonas gingivalis (9.5%) (Gonçalves et al., 2010; Giordano et al., 2011; Holmberg et al., 2013; Eick et al., 2013; Roberts et al., 2013; Ciandrini et al., 2014; Hauser-Gerspach et al., 2014; Kang et al., 2014; Sahrmann et al., 2014; Schmidt et al., 2014; Jennings et al., 2015; Zhang et al., 2015; Chen et al., 2016; Batsukh et al., 2017; Kulkarni Aranya et al., 2017; Schmidt et al., 2017; Strever et al., 2017; Azizi et al., 2018; Lee et al., 2018; Vilarrasa et al., 2018; Huang et al., 2019), Streptococcus sanguinis (7.3%) (Duarte et al., 2009; Fröjd et al., 2011; Bürgers et al., 2012; Godoy-Gallardo et al., 2014; Hauser-Gerspach et al., 2014; Schmidt et al., 2014; Narendrakumar et al., 2015; Chen et al., 2016; Godoy-Gallardo et al., 2016; Guan et al., 2016; Kim et al., 2017; Ramesh et al., 2017; Hoyos-Nogués et al., 2018; Pantaroto et al., 2018; Souza et al., 2018), and Streptococcus mutans (7.3%) (Baffone et al., 2011; Giordano et al., 2011; Ntrouka et al., 2011; Roberts et al., 2013; Schmage et al., 2014; Ciandrini et al., 2014; Cruz et al., 2015; Narendrakumar et al., 2015; Yucesoy et al., 2015; Zhang et al., 2015; Ciandrini et al., 2016; Ye et al., 2017; Ciandrini et al., 2017; Ramesh et al., 2017; Fukushima et al., 2018; Huang et al., 2019).

Cell Culture Studies

In addition, 37 of the included studies (n = 37, 31.9%) also performed cell culture in their methodology to study re-osseointegration (Schwarz et al., 2005; Ewald and Ihde, 2009; Giordano et al., 2011; Cortizo et al., 2012; Alcheikh et al., 2013; De Giglio et al., 2013; Eick et al., 2013; Holmberg et al., 2013; Godoy-Gallardo et al., 2014; Hauser-Gerspach et al., 2014; Duske et al., 2015; Janković et al., 2015; Lewandowska et al., 2015; Ayre et al., 2016; Cochis et al., 2016; Cotolan et al., 2016; Giannelli et al., 2016; Guan et al., 2016; Godoy-Gallardo et al., 2016; John et al., 2016; Kotsakis et al., 2016; Shi et al., 2016; Canullo et al., 2017; Cometa et al., 2017; Eick et al., 2017; Ferraris et al., 2017; Giannelli et al., 2017; Matthes et al., 2017; Ramesh et al., 2017; Wang et al., 2017; Ye et al., 2017; Zhang et al., 2017; Atefyekta et al., 2018; Hidalgo-Robatto et al., 2018; Hoyos-Nogués et al., 2018; Lee et al., 2018; Santos-Coquillat et al., 2018). The investigated cell types in this systematic review were osteogenic sarcoma (57.4%), epithelial (2.1%), fibroblast (17.0%), macrophages (4.3%), acute monocytic leukemia (2.1%), mesenchymal stem cells (4.3%), and stromal cells (2.1%).

This review has grouped the decontamination methods into two types: (i) biofilm-prevention method and (ii) biofilm-treatment method.

Biofilm-Prevention Methods

The studies focused on the modification of titanium implant surfaces. For example, one of the included studies focused on the type of instrument used to modify the surfaces, either to smooth or to roughen them (Schmidt et al., 2017). This biofilm-preventing step occurs before the development of assumed biofilm. In addition to the surface roughness, materials and surface treatment, too, have an impact on the early attachment of bacteria (Batsukh et al., 2017). Therefore, it is essential to assess the effect of various implant surfaces available on the attachment of initial and late colonizing bacteria. In biofilm-treatment method, biofilm development has already taken place. Most of the included studies were for biofilm-treatment.

The most common preventive method of decontamination used in the included studies was the application of a coating on the titanium implant or discs. The mechanism of decontamination did not completely rely on the physical separation of the titanium alloy and oral microbiota.

Biofilm-Treatment Methods

In a study using calcifying coating solutions (containing different ionic compositions of calcium, phosphate, and zinc), the degree of crystallinity was inversely proportional to antibacterial activity against Porphyromonas gingivalis in coated discs (Kulkarni Aranya et al., 2017). Lower the dissolution rate, lesser the antibacterial effect (Kulkarni Aranya et al., 2017). The addition of titanium dioxide nanoparticles boosted the antimicrobial efficacy of hydrogen peroxide solutions and delayed the redevelopment on surfaces which were previously contaminated by bacteria (Wiedmer et al., 2017).

The second most common biofilm-treatment method of decontamination in this review is by chemical treatment. However, similar to the previous findings, their results showed that not all of the agents used for disinfection in the clinic are effective in the removal of the biofilm. Some of the agents left behind live bacteria on the surface (Dostie et al., 2017). With regards to mechanical cleaning, a complete decontamination of a surface will not be possible as certain bacteria will continue to reside in “valleys and undercuts” (Schmage et al., 2014). In general, removal of greater than 96% biofilm was reported as satisfactory for clinical health, and this was achieved by the oscillating instruments and air polishing (Schmage et al., 2014). One study focused on the application of a direct contact ultrasound at low frequency (Granick et al., 2017). They described that the ultrasound biocidal activity occurred due to acoustic microstreaming and bubble cavitation, releasing considerable energy and damaging bacterial cell walls. In another study, implants were used as cathodes to generate an alkaline environment and reactive oxygen species, and showed a twofold reduction of bacteria compared with the untreated controls (Mohn et al., 2011). Mechanisms are similar to chemical treatments. For example, the ability of hydrogen peroxide to cause bacterial biofilm disruption is associated with oxidation of a number of cellular components and production of gas (Wiedmer et al., 2017).

Staphylococcus aureus, Porphyromonas gingivalis, Streptococcus sanguinis, and Streptococcus mutans are the commonly used oral microbiota for the study of dental biofilms reported in the included studies of this review. These bacteria are all responsible for peri-implantitis (Lavere et al., 2018). They can also exist in the oral saliva of healthy adults and later transform into opportunistic pathogens to become the main cause of the host diseases (Gao et al., 2018). S. aureus is a Gram-positive, aerobic cocci and may cause infections ranging from minor skin infections to pneumonia, bacteremia, and infective endocarditis (Oliveira et al., 2018). P. gingivalis is a Gram-negative anaerobic bacteria and has a strong positive correlation with periodontal diseases (Rafiei et al., 2017). S. sanguinis, previously known as S. sanguis, is a Gram-positive, non-spore-forming, facultative anaerobe and is typically found in a healthy plaque (Zhu et al., [[NoYear]]). S. mutans is a Gram-positive cocci, a facultative anaerobe responsible for the initiation of dental caries, which may lead to the formation of dental plaque and endocarditis (Daboor et al., 2015).

An important question for surface decontamination studies is whether the different patterns of biofilm play a clinical role (Trobos et al., 2018). Biofilm‐associated antimicrobial resistance is related to a number of factors. Established biofilms are resistant to antimicrobial agents as compared with planktonic bacteria which are attributed to biofilm properties, including nature and structure, poor antibiotic penetration, bacterial cells metabolic state, nutrient and oxygen availability, and antimicrobial resistance acquired by gene transfer and mutation (Arciola et al., 2018).

There are many other factors to consider if the decontamination method is successful or not. The first is the age of the biofilm. Half of the included studies in this review evaluated on biofilm aged less or equal to 24 h. However, this may also depend on the type of resident microbiota, maturity of the biofilm, and the number of bacterial cell clusters and micro colonies (Cao et al., 2018). This is a crucial factor especially for those treatment methods aimed at established biofilms, such as in clinically diagnosed peri-implantitis. Additionally, in-vitro developed biofilm is easily affected by surface configuration than biofilm that forms in the mouth (Bevilacqua et al., 2018). Nutrients and mixed bacterial species present in more favorable environment will encourage biofilm formation (Bevilacqua et al., 2018). Quantitative differences detected in-vitro amongst surfaces with dissimilar features might not predict the rate of in-vivo colonization. Various studies analyzed the efficacy of their decontamination methods using a scanning electron microscopy (SEM). However, the energy beam by SEM on its own can be a potential decontamination strategy as the high energy (in kV) can cause bacterial cell wall destruction and internal reversible changes to genetic materials (Ghomi et al., 2005). Therefore, when a high-energy SEM captured the images of bacterial matrix for quantification, their image analysis may introduce inaccuracies.

Re-osseointegration is also an important issue taken into account when decontamination methods are performed. About one-third of the included studies in this review investigated the cell adherence on the titanium implants with biofilm contamination. This phenomenon is described as “the race for the surface,” wherein bacterial and host cells compete in colonizing implant surface (Hoyos-Nogués et al., 2018). Previous systematic review on re-osseointegration has reported that the application of single decontamination measure was not sufficient to get a desirable treatment outcome for peri-implantitis (Madi et al., 2018). Therefore, further studies must be conducted to focus on the dual mechanism (or more) to encourage re-osseointegration after biofilm decontamination. So far, there is no “gold standard” that has been specified in the decontamination of dental implants. A decontamination treatment will need to be combined with mechanical therapy for a successful outcome (Prathapachandran and Suresh, 2012).

Conclusion

In conclusion, this review found that the commonly used decontamination methods of microbial biofilm on dental implant surfaces focused on the addition of surface coating and chemical treatment. Further efforts should be aimed at finding the optimal implant surface property that features antimicrobial treatment that is effective and does not compromise osseointegration.

Funding

The work was supported by the University Research Council grant under Universiti Brunei Darussalam (grant number: UBD/RSCH/URC/RG (b)/2018/004). Allied Grant-Universiti Brunei Darusslam for Publication Cost.

Publisher’s Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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