The Open Dentistry Journal




ISSN: 1874-2106 ― Volume 13, 2019
REVIEW ARTICLE

In vitro Assessment of Peri-implantitis Treatment Procedures: A Review



Merve Benli1, 2, Catherine Petit2, 3, Henri Tenenbaum2, 3, Olivier Huck2, 3, *
1 Department of Prosthodontics, Faculty of Dentistry, Istanbul University, Istanbul, Turkey
2 Regenerative Nanomedicine , Fédération de Médecine Translationnelle de Strasbourg (FMTS), INSERM 1260, Strasbourg, France
3 Department of Periodontology, Faculté de Chirurgie-Dentaire, Université de Strasbourg, Strasbourg, France

Abstract

Background:

The prevalence of peri-implantitis is increasing continuously and such a biological complication significantly decreases implant survival and success. Although various treatment modalities have been identified for peri-implantitis, no completely efficient method has yet been established.

Objective:

The aim of this review was to evaluate the scientific literature regarding the in vitro effects of peri-implantitis treatment.

Methods:

A review of the literature was performed by using Google Scholar, PubMed/ MEDLINE and Science Direct databases. In vitro studies on peri-implantitis treatment modalities were selected. The search strategy identified 57 eligible studies. After selection, 21 articles met all the inclusion criteria and were included in the present review.

Results:

Included in vitro studies evaluated different types of peri-implantitis treatment modalities such as mechanical, chemical, combination and laser therapies. Combination therapies with the aid of adjuvants were found to be more effective compared to the studies that used only one type of treatment modality. Laser systems were also tested and displayed interesting results in terms of surface decontamination with a variability associated with selected parameters.

Conclusion:

This review was performed to evaluate the efficacy of the treatment modalities used for peri-implantitis in vitro. Although there are various effective treatment methods, none has been completely successful in removing the biofilms related to peri-implantitis. The findings imply the need for further studies to develop more effective antimicrobial treatment procedures.

Keywords: Biofilm, Peri-implantitis, Laser, Titanium, Implant, Mucositis.


Article Information


Identifiers and Pagination:

Year: 2019
Volume: 13
First Page: 267
Last Page: 273
Publisher Id: TODENTJ-13-267
DOI: 10.2174/1874210601913010267

Article History:

Received Date: 21/05/2019
Revision Received Date: 11/07/2019
Acceptance Date: 26/07/2019
Electronic publication date: 31/07/2019
Collection year: 2019

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© 2019 Benli et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Dental Faculty, Université de Strasbourg, 8 rue Sainte-Elisabeth, 67000 Strasbourg, France;
E-mail: huck.olivier@gmail.com






1. INTRODUCTION

Nowadays, dental implants are considered as a key therapeutic tool to replace missing teeth. This treatment procedure allows the restoration of oral function and esthetics. Even if their long-term success is high, complications of mechanical but mostly of biological origin might occur [1Tenenbaum H, Bogen O, Séverac F, Elkaim R, Davideau JL, Huck O. Long-term prospective cohort study on dental implants: Clinical and microbiological parameters. Clin Oral Implants Res 2017; 28(1): 86-94.
[http://dx.doi.org/10.1111/clr.12764] [PMID: 26773978]
]. Peri-implant diseases, such as mucositis and peri-implantitis, are considered leading causes of implant complications and implant loss [2Doornewaard R, Jacquet W, Cosyn J, De Bruyn H. How do peri-implant biologic parameters correspond with implant survival and peri-implantitis? A critical review. Clin Oral Implants Res 2018; 29(Suppl. 18): 100-23.
[http://dx.doi.org/10.1111/clr.13264] [PMID: 30306697]
]. Peri-implantitis is characterized by a progressive bone loss associated with inflammation induced by a microbial dysbiosis [3Zitzmann NU, Berglundh T. Definition and prevalence of peri-implant diseases. J Clin Periodontol 2008; 35(8)(Suppl.): 286-91.
[http://dx.doi.org/10.1111/j.1600-051X.2008.01274.x] [PMID: 1872 4856]
]. Indeed, this shift of composition within biofilms is concomitant with an increase in anaerobic bacterial species such as Porphyromonas gingivalis, Prevotella intermedia, Eikenella corrodens, Actinomyces naeslundi on the surface of the dental implants [1Tenenbaum H, Bogen O, Séverac F, Elkaim R, Davideau JL, Huck O. Long-term prospective cohort study on dental implants: Clinical and microbiological parameters. Clin Oral Implants Res 2017; 28(1): 86-94.
[http://dx.doi.org/10.1111/clr.12764] [PMID: 26773978]
, 4Kumar PS, Mason MR, Brooker MR, O’Brien K. Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants. J Clin Periodontol 2012; 39(5): 425-33.
[http://dx.doi.org/10.1111/j.1600-051X.2012.01856.x] [PMID: 2241 7294]
]. The prevalence of peri-implantitis ranges from 4% to 45% according to the definition used and sample population [5Derks J, Schaller D, Håkansson J, Wennström JL, Tomasi C, Berglundh T. Effectiveness of implant therapy analyzed in a swedish population: Prevalence of peri-implantitis. J Dent Res 2016; 95(1): 43-9.
[http://dx.doi.org/10.1177/0022034515608832] [PMID: 26701919]
].

Therefore, the elimination of dental plaque is the primary goal in peri-implantitis management and several treatment procedures have been suggested such as non-surgical approach with or without antimicrobials and surgical regenerative procedures [6Renvert S, Polyzois I. Treatment of pathologic peri-implant pockets. Periodontol 2000 2018; 76(1): 180-90.
[http://dx.doi.org/10.1111/prd.12149] [PMID: 29239086]
]. However, mechanical curettage has been found to be insufficient for implant surface decontamination due to the presence of bacteria in surface micro-irregularities, and new therapeutic strategies have been developed to improve treatment outcomes [7Esposito M, Hirsch J, Lekholm U, Thomsen P. Differential diagnosis and treatment strategies for biologic complications and failing oral implants: A review of the literature. Int J Oral Maxillofac Implants 1999; 14(4): 473-90.
[PMID: 10453661]
]. For instance, laser treatments, antiseptics, and antibiotics have been reported as curative alternatives [8Caccianiga G, Rey G, Baldoni M, Paiusco A. Clinical, radiographic and microbiological evaluation of high level laser therapy, a new photodynamic therapy protocol, in peri-implantitis treatment: A pilot experience. BioMed Res Int 2016; 2016: 6321906-8.
[http://dx.doi.org/10.1155/2016/6321906] [PMID: 27379251]
]. To develop and evaluate potential peri-implantitis treatment procedures, several in vitro studies have been and are still conducted. These studies evaluate the antibacterial, anti-inflammatory and also pro-regenerative effects of the tested procedures. This review aims to list the relevant in vitro models used and the outcomes of tested treatment procedures in the context of peri-implantitis management.

2. MATERIALS AND METHODS

2.1. Search Strategy, Eligibility, Inclusion and Exclusion Criteria

A review of the literature was performed using Google Scholar, PubMed/ MEDLINE and Science Direct databases, by searching for studies published after July 2012. Only in vitro studies assessing the treatment modalities of peri-implantitis were included. Additionally, a hand search was also carried out for cross-references of the selected articles. The keywords “peri-implantitis”, “treatment”, “in vitro”, “dental implant” were used on all databases in various combinations and alongside ‘and’, or, ‘not’.

The screening was performed by assessing the titles and abstracts of the research articles for initial analysis. Full-text of all relevant papers were obtained. The present review included papers based on the following inclusion criteria: 1)In-vitro studies including the types of treatments of peri-implantitis, 2) Studies including peri-implantitis and its microbiota, 3) Studies involving effective modalities or equipments as a treatment option for peri-implantitis, 4) Studies in English language, 5) Studies published in scientific journals. The exclusion criteria for this paper were as follows: 1)In- vivo studies, 2) Studies that did not present a compatible methodology, 3) Inadequate description of treatment modality for peri-implantitis, 4) Reviews and duplicates, 5) Studies with a lack of data regarding the extent of treatment modality or the method employed.

3. RESULTS

3.1. Study Selection

The search strategy identified 57 studies. After the screening procedure by reading abstracts and titles, 40 studies were found to be potentially eligible for this review. After full-text evaluation, 21 studies met all the selected criteria and were included. The flow diagram of article screening and selection process is shown in Fig. (1).

3.2. Study Characteristics

Among the selected in vitro studies, the authors evaluated the peri-implantitis treatment modalities using mainly titanium discs, dental implants and plan titanium specimens to mimic contaminated surfaces by different types of biofilms or planktonic bacteria including the main periodontal pathogens such as P.gingivalis, Treponema denticola, Aggregatibacter actinomycetemcomitans, Streptococcus oralis, Actinomyces viscosus, Veilloneilla parvula, Fusobacterium nucleatum and other species such as Escherichia coli, Staphyloccus epidermidis, Staphyloccus aureus or Candida albicans (Table 1).

3.3. Treatment Modalities

Several treatment modalities have been evaluated in vitro. These treatment modalities include mechanical procedures, chemical treatment through the use of antimicrobials and combinations (Table 1). Ultrasonic devices, manual curettes, air powder abrasion, titanium brush, implantoplasty, cold atmospheric pressure air plasma jet, electrolysis and laser have been assessed [9Sahrmann P, Zehnder M, Mohn D, Meier A, Imfeld T, Thurnheer T. Effect of low direct current on anaerobic multispecies biofilm adhering to a titanium implant surface. Clin Implant Dent Relat Res 2014; 16(4): 552-6.
[http://dx.doi.org/10.1111/cid.12018] [PMID: 23167678]
-12Yang Y, Guo J, Zhou X, et al. A novel cold atmospheric pressure air plasma jet for peri-implantitis treatment: An in vitro study. Dent Mater J 2018; 37(1): 157-66.
[http://dx.doi.org/10.4012/dmj.2017-030] [PMID: 29176301]
]. Regarding laser systems, diode, carbon dioxide, Er:YAG and GaAlAs lasers with different wavelengths, irradiation times and irradiation modes (pulsed and continuous) were tested [13Leja C, Geminiani A, Caton J, Romanos GE. Thermodynamic effects of laser irradiation of implants placed in bone: An in vitro study. Lasers Med Sci 2013; 28(6): 1435-40.
[http://dx.doi.org/10.1007/s10103-012-1215-z] [PMID: 23053251]
-17Huang TC, Chen CJ, Ding SJ, Chen CC. Antimicrobial efficacy of methylene blue-mediated photodynamic therapy on titanium alloy surfaces in vitro. Photodiagn Photodyn Ther 2019; 25: 7-16.
[http://dx.doi.org/10.1016/j.pdpdt.2018.11.008] [PMID: 30439531]
]. Photodynamic therapy (PDT) through the use of laser and LED has been a popular treatment modality and was carried out for the decontamination of dental implant surfaces [15Valente NA, Mang T, Hatton M, Mikulski L, Andreana S. Effects of two diode lasers with and without photosensitization on contaminated implant surfaces: An Ex vivo study. Photomed Laser Surg 2017; 35(7): 347-56.
[http://dx.doi.org/10.1089/pho.2016.4247] [PMID: 28253064]
, 18Widodo A, Spratt D, Sousa V, Petrie A, Donos N. An in vitro study on disinfection of titanium surfaces. Clin Oral Implants Res 2016; 27(10): 1227-32.
[http://dx.doi.org/10.1111/clr.12733] [PMID: 26863898]
-22Monzavi A, Fekrazad R, Chinipardaz Z, Shahabi S, Behruzi R, Chiniforush N. Effect of various laser wavelengths on temperature changes during periimplantitis treatment: An in vitro Study. Implant Dent 2018; 27(3): 311-6.
[http://dx.doi.org/10.1097/ID.0000000000000751] [PMID: 29489549]
].

Studies assessing antimicrobial treatments used different kinds of antiseptics and antimicrobial agents [19Rismanchian M, Nosouhian S, Shahabouee M, Davoudi A, Nourbakhshian F. Effect of conventional and contemporary disinfectant techniques on three peri-implantitis associated microbiotas. Am J Dent 2017; 30(1): 23-6.
[PMID: 29178710]
, 23Bürgers R, Witecy C, Hahnel S, Gosau M. The effect of various topical peri-implantitis antiseptics on Staphylococcus epidermidis, Candida albicans, and Streptococcus sanguinis. Arch Oral Biol 2012; 57(7): 940-7.
[http://dx.doi.org/10.1016/j.archoralbio.2012.01.015] [PMID: 2236 5324]
, 24Astasov-Frauenhoffer M, Braissant O, Hauser-Gerspach I, et al. Microcalorimetric determination of the effects of amoxicillin, metronidazole, and their combination on in vitro biofilm. J Periodontol 2014; 85(2): 349-57.
[http://dx.doi.org/10.1902/jop.2013.120733] [PMID: 23594193]
]. These topical antiseptics used to treat the surfaces of the specimens were chlorhexidine gluconate 0.2%, hydrogen peroxide 3.0%, sodium hypochlorite 1.0%, cetylpyridinium chloride, essential oils or citric acid 40.0% [19Rismanchian M, Nosouhian S, Shahabouee M, Davoudi A, Nourbakhshian F. Effect of conventional and contemporary disinfectant techniques on three peri-implantitis associated microbiotas. Am J Dent 2017; 30(1): 23-6.
[PMID: 29178710]
, 23Bürgers R, Witecy C, Hahnel S, Gosau M. The effect of various topical peri-implantitis antiseptics on Staphylococcus epidermidis, Candida albicans, and Streptococcus sanguinis. Arch Oral Biol 2012; 57(7): 940-7.
[http://dx.doi.org/10.1016/j.archoralbio.2012.01.015] [PMID: 2236 5324]
]. Metronidazole, amoxicillin and the combination of these two antibiotics were used to treat titanium discs covered with bacterial biofilms [24Astasov-Frauenhoffer M, Braissant O, Hauser-Gerspach I, et al. Microcalorimetric determination of the effects of amoxicillin, metronidazole, and their combination on in vitro biofilm. J Periodontol 2014; 85(2): 349-57.
[http://dx.doi.org/10.1902/jop.2013.120733] [PMID: 23594193]
]. Additionally, some other molecules or compounds were tested such as grape seed extract, oligosaccharide nanomedicine OligoG and Triethoxysilylpropyl Succinic Anhydride (TESPSA) silane application to determine their antimicrobial properties [25Shrestha B, Theerathavaj MLS, Thaweboon S, Thaweboon B. In vitro antimicrobial effects of grape seed extract on peri-implantitis microflora in craniofacial implants. Asian Pac J Trop Biomed 2012; 2(10): 822-5.
[http://dx.doi.org/10.1016/S2221-1691(12)60236-6] [PMID: 23569 854]
-27Vilarrasa J, Delgado LM, Galofré M, et al. In vitro evaluation of a multispecies oral biofilm over antibacterial coated titanium surfaces. J Mater Sci Mater Med 2018; 29(11): 164.
[http://dx.doi.org/10.1007/s10856-018-6168-8] [PMID: 30392142]
].

3.4. Synthesis of the Results

In the study performed by Bürgers et al., six different topical antiseptics were tested where only sodium hypochlorite 1.0% exhibited a significant antimicrobial effect on all the tested microbes [23Bürgers R, Witecy C, Hahnel S, Gosau M. The effect of various topical peri-implantitis antiseptics on Staphylococcus epidermidis, Candida albicans, and Streptococcus sanguinis. Arch Oral Biol 2012; 57(7): 940-7.
[http://dx.doi.org/10.1016/j.archoralbio.2012.01.015] [PMID: 2236 5324]
]. In another study, hydrogen peroxide 3.0% and chlorhexidine 0.2% were tested and both were recommended for their antiseptic effect on three peri-implantitis associated microbiotas (S. aureus, S. epidermidis and C. albicans) [19Rismanchian M, Nosouhian S, Shahabouee M, Davoudi A, Nourbakhshian F. Effect of conventional and contemporary disinfectant techniques on three peri-implantitis associated microbiotas. Am J Dent 2017; 30(1): 23-6.
[PMID: 29178710]
].

Some natural compounds have also been evaluated. For instance, grape seed extract was tested firstly against peri-implantitis microflora. Interestingly, this extract inhibited S. aureus growth. However, modest or no effect against strains such as E. coli, C. albicans, C. parapsilosis, K. pneumonia was observed [25Shrestha B, Theerathavaj MLS, Thaweboon S, Thaweboon B. In vitro antimicrobial effects of grape seed extract on peri-implantitis microflora in craniofacial implants. Asian Pac J Trop Biomed 2012; 2(10): 822-5.
[http://dx.doi.org/10.1016/S2221-1691(12)60236-6] [PMID: 23569 854]
]. Another interesting study examined the potential role of oligosaccharide nanomedicine (OligoG), an antibiofilm adjuvant, and concluded that this agent was safe and non-toxic for clinical use and can help in preventing infection and attachment of P. gingivalis on implant surfaces [26Roberts JL, Khan S, Emanuel C, et al. An in vitro study of alginate oligomer therapies on oral biofilms. J Dent 2013; 41(10): 892-9.
[http://dx.doi.org/10.1016/j.jdent.2013.07.011] [PMID: 23907083]
]. The efficacy of the combination of amoxicilline/ metronidazole has also been advocated [24Astasov-Frauenhoffer M, Braissant O, Hauser-Gerspach I, et al. Microcalorimetric determination of the effects of amoxicillin, metronidazole, and their combination on in vitro biofilm. J Periodontol 2014; 85(2): 349-57.
[http://dx.doi.org/10.1902/jop.2013.120733] [PMID: 23594193]
, 28Walter C, Kulik EM, Weiger R, Zitzmann NU, Waltimo T. Additive or synergistic antimicrobial effects of amoxicillin and metronidazole on whole plaque samples: A preliminary report. J Int Acad Periodontol 2011; 13(1): 11-6.
[PMID: 21387982]
].

Fig. (1)
Flow diagram of the selection process.


Table 1
Summary of the descriptive characteristics of the included studies.


The study by Toma et al. evaluated four types of peri-implantitis treatment modalities: titanium brush (Ti-Brush), air-abrasive device (Perio-Flow), implantoplasty and plastic curette in terms of osteogenic effect and biocompatibility on titanium discs [11Toma S, Lasserre J, Brecx MC, Nyssen-Behets C. In vitro evaluation of peri-implantitis treatment modalities on Saos-2 osteoblasts. Clin Oral Implants Res 2016; 27(9): 1085-92.
[http://dx.doi.org/10.1111/clr.12686] [PMID: 26361088]
]. The authors found that although implantoplasty was the only treatment able to change the morphology of titanium surfaces, all modalities assessed in the study appeared to be valid in terms of biocompatibility and promoted mature osteoblastic phenotype as well as cell adhesion and proliferation. Sahrmann et al. evaluated the potential effect of decontamination of three different mechanical debridement modalities (ultrasonic device, air powder abrasive device and Gracey curette) and showed that airflow device was an efficient modality in peri-implantitis treatment with variable results according to the size of the defect [10Sahrmann P, Ronay V, Hofer D, Attin T, Jung RE, Schmidlin PR. In vitro cleaning potential of three different implant debridement methods. Clin Oral Implants Res 2015; 26(3): 314-9.
[http://dx.doi.org/10.1111/clr.12322] [PMID: 24373056]
]. Irradiation therapies with the use of laser systems are popular due to their decontamination efficiency on dental implant surfaces and in the treatment of peri-implant defects [29Stübinger S, Henke J, Donath K, Deppe H. Bone regeneration after peri-implant care with the CO2 laser: A fluorescence microscopy study. Int J Oral Maxillofac Implants 2005; 20(2): 203-10.
[PMID: 15839113]
]. Included studies showed high rates of sterilization for laser systems on implant surfaces [16Ghasemi M, Etemadi A, Nedaei M, Chiniforush N, Pourhajibagher M. Antimicrobial efficacy of photodynamic therapy using two different light sources on the titanium-adherent biofilms of Aggregatibacter actinomycetemcomitans: An in vitro study. Photodiagn Photodyn Ther 2019; 26: 85-9.
[http://dx.doi.org/10.1016/j.pdpdt.2019.03.004] [PMID: 30836212]
, 22Monzavi A, Fekrazad R, Chinipardaz Z, Shahabi S, Behruzi R, Chiniforush N. Effect of various laser wavelengths on temperature changes during periimplantitis treatment: An in vitro Study. Implant Dent 2018; 27(3): 311-6.
[http://dx.doi.org/10.1097/ID.0000000000000751] [PMID: 29489549]
, 30Kuo HN, Mei HI, Liu TK, Liu TY, Lo LJ, Lin CL. In vitro laser treatment platform construction with dental implant thread surface on bacterial adhesion for peri-implantitis. BioMed Res Int 2017; 2017: 4732302-7.
[http://dx.doi.org/10.1155/2017/4732302] [PMID: 28791302]
]. Additionally, changes in wavelengths and irradiation modes have been reported to influence the effectiveness of decontamination procedures [13Leja C, Geminiani A, Caton J, Romanos GE. Thermodynamic effects of laser irradiation of implants placed in bone: An in vitro study. Lasers Med Sci 2013; 28(6): 1435-40.
[http://dx.doi.org/10.1007/s10103-012-1215-z] [PMID: 23053251]
, 14Giannelli M, Landini G, Materassi F, et al. The effects of diode laser on Staphylococcus aureus biofilm and Escherichia coli lipopolysaccharide adherent to titanium oxide surface of dental implants. An in vitro study. Lasers Med Sci 2016; 31(8): 1613-9.
[http://dx.doi.org/10.1007/s10103-016-2025-5] [PMID: 27475996]
, 30Kuo HN, Mei HI, Liu TK, Liu TY, Lo LJ, Lin CL. In vitro laser treatment platform construction with dental implant thread surface on bacterial adhesion for peri-implantitis. BioMed Res Int 2017; 2017: 4732302-7.
[http://dx.doi.org/10.1155/2017/4732302] [PMID: 28791302]
].

Photodynamic therapy is another frequently suggested peri-implantitis treatment modality. PDT has been used alone and in combination with other treatment options [15Valente NA, Mang T, Hatton M, Mikulski L, Andreana S. Effects of two diode lasers with and without photosensitization on contaminated implant surfaces: An Ex vivo study. Photomed Laser Surg 2017; 35(7): 347-56.
[http://dx.doi.org/10.1089/pho.2016.4247] [PMID: 28253064]
-19Rismanchian M, Nosouhian S, Shahabouee M, Davoudi A, Nourbakhshian F. Effect of conventional and contemporary disinfectant techniques on three peri-implantitis associated microbiotas. Am J Dent 2017; 30(1): 23-6.
[PMID: 29178710]
, 21Rogers S, Honma K, Mang TS. Confocal fluorescence imaging to evaluate the effect of antimicrobial photodynamic therapy depth on P. gingivalis and T. denticola biofilms. Photodiagn Photodyn Ther 2018; 23: 18-24.
[http://dx.doi.org/10.1016/j.pdpdt.2018.04.015] [PMID: 29753881]
, 22Monzavi A, Fekrazad R, Chinipardaz Z, Shahabi S, Behruzi R, Chiniforush N. Effect of various laser wavelengths on temperature changes during periimplantitis treatment: An in vitro Study. Implant Dent 2018; 27(3): 311-6.
[http://dx.doi.org/10.1097/ID.0000000000000751] [PMID: 29489549]
]. In the study conducted by Widodo et al., the authors reported that the combination of PDT and titanium brush treatment was effective in reducing the number of selected bacteria [18Widodo A, Spratt D, Sousa V, Petrie A, Donos N. An in vitro study on disinfection of titanium surfaces. Clin Oral Implants Res 2016; 27(10): 1227-32.
[http://dx.doi.org/10.1111/clr.12733] [PMID: 26863898]
]. Rismanchian et al. showed that PDT provided better treatment results when it was applied with 0.2% chlorhexidine or hydrogen peroxide 3.0%, and they recommended this modality for the disinfection of dental implant surfaces [19Rismanchian M, Nosouhian S, Shahabouee M, Davoudi A, Nourbakhshian F. Effect of conventional and contemporary disinfectant techniques on three peri-implantitis associated microbiotas. Am J Dent 2017; 30(1): 23-6.
[PMID: 29178710]
]. Ghasemi et al. proposed another combination of PDT with LED and toluidine blue, while Huang et al. highlighted the use of methylene blue. According to the results of these recent studies, both PDT protocols were found to be efficient for the decontamination of implant surfaces [16Ghasemi M, Etemadi A, Nedaei M, Chiniforush N, Pourhajibagher M. Antimicrobial efficacy of photodynamic therapy using two different light sources on the titanium-adherent biofilms of Aggregatibacter actinomycetemcomitans: An in vitro study. Photodiagn Photodyn Ther 2019; 26: 85-9.
[http://dx.doi.org/10.1016/j.pdpdt.2019.03.004] [PMID: 30836212]
, 17Huang TC, Chen CJ, Ding SJ, Chen CC. Antimicrobial efficacy of methylene blue-mediated photodynamic therapy on titanium alloy surfaces in vitro. Photodiagn Photodyn Ther 2019; 25: 7-16.
[http://dx.doi.org/10.1016/j.pdpdt.2018.11.008] [PMID: 30439531]
].

4. DISCUSSION

The present review evaluated the treatment modalities for peri-implantitis and focused on their in vitro properties especially their antibacterial properties. Indeed, several modalities were proposed and tested with interesting outcomes and potential application in the management of peri-implantitis. However, significant differences in terms of the results were found according to the sample material, working mode, application time, type of system or combined usage.

An effective peri-implantitis treatment requires the following conditions: (1) Removing biofilm from the implant surfaces and (2) Promoting the adhesion of osteoblasts [31Claffey N, Clarke E, Polyzois I, Renvert S. Surgical treatment of peri-implantitis. J Clin Periodontol 2008; 35(8)(Suppl.): 316-32.
[http://dx.doi.org/10.1111/j.1600-051X.2008.01277.x] [PMID: 1872 4859]
]. However, effective debridement of oral biofilms on dental implant surfaces is difficult to achieve due to the rough surface and the design of dental implants in contrast to the surfaces of natural teeth [32Renvert S, Roos-Jansåker AM, Claffey N. Non-surgical treatment of peri-implant mucositis and peri-implantitis: A literature review. J Clin Periodontol 2008; 35(8)(Suppl.): 305-15.
[http://dx.doi.org/10.1111/j.1600-051X.2008.01276.x] [PMID: 18724 858]
]. Therefore, several approaches have been developed to treat peri-implantitis [33Heitz-Mayfield LJA, Salvi GE, Mombelli A, et al. Supportive peri-implant therapy following anti-infective surgical peri-implantitis treatment: 5-year survival and success. Clin Oral Implants Res 2018; 29(1): 1-6.
[http://dx.doi.org/10.1111/clr.12910] [PMID: 27335316]
, 34Smeets R, Henningsen A, Jung O, Heiland M, Hammächer C, Stein JM. Definition, etiology, prevention and treatment of peri-implantitis: A review. Head Face Med 2014; 10: 34.
[http://dx.doi.org/10.1186/1746-160X-10-34] [PMID: 25185675]
]. In some studies, contradictory results have been found. For instance, studies comparing several treatment procedures did not have the same conclusion. The differences between them may be due to the equipment used or sample materials.

Mechanical therapy induces significant changes in the composition and microstructure of titanium and implant surfaces as they might be damaged during treatment [11Toma S, Lasserre J, Brecx MC, Nyssen-Behets C. In vitro evaluation of peri-implantitis treatment modalities on Saos-2 osteoblasts. Clin Oral Implants Res 2016; 27(9): 1085-92.
[http://dx.doi.org/10.1111/clr.12686] [PMID: 26361088]
]. To reduce surface damage originated from metal-to-metal contact, a non-metallic instrument could be used [35Gantes BG, Nilvéus R. The effects of different hygiene instruments on titanium surfaces: SEM observations. Int J Periodontics Restorative Dent 1991; 11(3): 225-39.
[PMID: 1666395]
]. However, these instruments have been shown to inadequately remove microorganisms from rough surfaces, and air-powder abrasive systems might be an interesting option. Implantoplasty also appeared to be a promising treatment because of inducing surface smoothness, surface hydrophily and purity [11Toma S, Lasserre J, Brecx MC, Nyssen-Behets C. In vitro evaluation of peri-implantitis treatment modalities on Saos-2 osteoblasts. Clin Oral Implants Res 2016; 27(9): 1085-92.
[http://dx.doi.org/10.1111/clr.12686] [PMID: 26361088]
]. Special attention should be paid to mechanical therapy because of the difficulty in visualizing the surface and to eliminate microorganisms [36Chan Y, Lai C-H. Bactericidal effects of different laser wavelengths on periodontopathic germs in photodynamic therapy. Lasers Med Sci 2003; 18(1): 51-5.
[http://dx.doi.org/10.1007/s10103-002-0243-5] [PMID: 12627274]
]. Therefore, antibiotics or antiseptic agents have also been proposed to improve peri-implantitis treatment outcomes [15Valente NA, Mang T, Hatton M, Mikulski L, Andreana S. Effects of two diode lasers with and without photosensitization on contaminated implant surfaces: An Ex vivo study. Photomed Laser Surg 2017; 35(7): 347-56.
[http://dx.doi.org/10.1089/pho.2016.4247] [PMID: 28253064]
, 19Rismanchian M, Nosouhian S, Shahabouee M, Davoudi A, Nourbakhshian F. Effect of conventional and contemporary disinfectant techniques on three peri-implantitis associated microbiotas. Am J Dent 2017; 30(1): 23-6.
[PMID: 29178710]
, 23Bürgers R, Witecy C, Hahnel S, Gosau M. The effect of various topical peri-implantitis antiseptics on Staphylococcus epidermidis, Candida albicans, and Streptococcus sanguinis. Arch Oral Biol 2012; 57(7): 940-7.
[http://dx.doi.org/10.1016/j.archoralbio.2012.01.015] [PMID: 2236 5324]
, 37Schwarz F, Bieling K, Bonsmann M, Latz T, Becker J. Nonsurgical treatment of moderate and advanced periimplantitis lesions: A controlled clinical study. Clin Oral Investig 2006; 10(4): 279-88.
[http://dx.doi.org/10.1007/s00784-006-0070-3] [PMID: 16969659]
].

Several classical antiseptic agents have been proposed for the management of peri-implantitis and peri-implant mucositis. Sodium hypochlorite, a strong disinfecting agent, has been tested but was not highly recommended due to its cytotoxicity [19Rismanchian M, Nosouhian S, Shahabouee M, Davoudi A, Nourbakhshian F. Effect of conventional and contemporary disinfectant techniques on three peri-implantitis associated microbiotas. Am J Dent 2017; 30(1): 23-6.
[PMID: 29178710]
, 23Bürgers R, Witecy C, Hahnel S, Gosau M. The effect of various topical peri-implantitis antiseptics on Staphylococcus epidermidis, Candida albicans, and Streptococcus sanguinis. Arch Oral Biol 2012; 57(7): 940-7.
[http://dx.doi.org/10.1016/j.archoralbio.2012.01.015] [PMID: 2236 5324]
]. Common concentrations of hydrogen peroxide and non-toxic chemicals, provide rapid bactericidal effects and antimicrobial action [38Zablotsky MH, Diedrich DL, Meffert RM. Detoxification of endotoxin-contaminated titanium and hydroxyapatite-coated surfaces utilizing various chemotherapeutic and mechanical modalities. Implant Dent 1992; 1(2): 154-8.
[http://dx.doi.org/10.1097/00008505-199205000-00009] [PMID: 1288 809]
, 39Quirynen M, Teughels W, De Soete M, van Steenberghe D. Topical antiseptics and antibiotics in the initial therapy of chronic adult periodontitis: Microbiological aspects. Periodontol 2000 2002; 28: 72-90.
[http://dx.doi.org/10.1034/j.1600-0757.2002.280104.x] [PMID: 1201 3349]
]. Chlorhexidine gluconate was assessed in many studies and showed broad antimicrobial activity by changing the bacterial membrane and resulting in cell destruction [19Rismanchian M, Nosouhian S, Shahabouee M, Davoudi A, Nourbakhshian F. Effect of conventional and contemporary disinfectant techniques on three peri-implantitis associated microbiotas. Am J Dent 2017; 30(1): 23-6.
[PMID: 29178710]
, 23Bürgers R, Witecy C, Hahnel S, Gosau M. The effect of various topical peri-implantitis antiseptics on Staphylococcus epidermidis, Candida albicans, and Streptococcus sanguinis. Arch Oral Biol 2012; 57(7): 940-7.
[http://dx.doi.org/10.1016/j.archoralbio.2012.01.015] [PMID: 2236 5324]
, 39Quirynen M, Teughels W, De Soete M, van Steenberghe D. Topical antiseptics and antibiotics in the initial therapy of chronic adult periodontitis: Microbiological aspects. Periodontol 2000 2002; 28: 72-90.
[http://dx.doi.org/10.1034/j.1600-0757.2002.280104.x] [PMID: 1201 3349]
]. Citric acid has also been utilized as an antibacterial agent in detoxification of plaque infected implant surfaces and its efficacy has been proved [40Mouhyi J, Sennerby L, Pireaux JJ, Dourov N, Nammour S, Van Reck J. An XPS and SEM evaluation of six chemical and physical techniques for cleaning of contaminated titanium implants. Clin Oral Implants Res 1998; 9(3): 185-94.
[http://dx.doi.org/10.1034/j.1600-0501.1998.090306.x] [PMID: 1053 0133]
, 41Meffert RM. Treatment of failing dental implants. Curr Opin Dent 1992; 2: 109-14.
[PMID: 1520919]
]. Essential oil (Listerine) also displayed antibacterial activity with enzymatic inhibition and cell wall destruction of microorganisms [42Cortelli SC, Cortelli JR, Holzhausen M, et al. Essential oils in one-stage full-mouth disinfection: Double-blind, randomized clinical trial of long-term clinical, microbial and salivary effects. J Clin Periodontol 2009; 36(4): 333-42.
[http://dx.doi.org/10.1111/j.1600-051X.2009.01376.x] [PMID: 1942 6180]
]. Triclosan served as an inhibitor of oral biofilm and is an effective antimicrobial product [43Arweiler NB, Henning G, Reich E, Netuschil L. Effect of an amine-fluoride-triclosan mouthrinse on plaque regrowth and biofilm vitality. J Clin Periodontol 2002; 29(4): 358-63.
[http://dx.doi.org/10.1034/j.1600-051X.2002.290412.x] [PMID: 1196 6934]
].

GaAlAs diode, Er:YAG, diode and carbon dioxide lasers have been used to treat peri-implantitis [13Leja C, Geminiani A, Caton J, Romanos GE. Thermodynamic effects of laser irradiation of implants placed in bone: An in vitro study. Lasers Med Sci 2013; 28(6): 1435-40.
[http://dx.doi.org/10.1007/s10103-012-1215-z] [PMID: 23053251]
-16Ghasemi M, Etemadi A, Nedaei M, Chiniforush N, Pourhajibagher M. Antimicrobial efficacy of photodynamic therapy using two different light sources on the titanium-adherent biofilms of Aggregatibacter actinomycetemcomitans: An in vitro study. Photodiagn Photodyn Ther 2019; 26: 85-9.
[http://dx.doi.org/10.1016/j.pdpdt.2019.03.004] [PMID: 30836212]
, 21Rogers S, Honma K, Mang TS. Confocal fluorescence imaging to evaluate the effect of antimicrobial photodynamic therapy depth on P. gingivalis and T. denticola biofilms. Photodiagn Photodyn Ther 2018; 23: 18-24.
[http://dx.doi.org/10.1016/j.pdpdt.2018.04.015] [PMID: 29753881]
, 30Kuo HN, Mei HI, Liu TK, Liu TY, Lo LJ, Lin CL. In vitro laser treatment platform construction with dental implant thread surface on bacterial adhesion for peri-implantitis. BioMed Res Int 2017; 2017: 4732302-7.
[http://dx.doi.org/10.1155/2017/4732302] [PMID: 28791302]
]. According to study protocols, treatment outcomes vary between studies. For instance, Kuo et al. recommended the use of Er:YAG lasers in pulsed mode for peri-implantitis treatment [30Kuo HN, Mei HI, Liu TK, Liu TY, Lo LJ, Lin CL. In vitro laser treatment platform construction with dental implant thread surface on bacterial adhesion for peri-implantitis. BioMed Res Int 2017; 2017: 4732302-7.
[http://dx.doi.org/10.1155/2017/4732302] [PMID: 28791302]
]. In the study performed by Leja et al., diode lasers in pulsed mode were found to be efficient, while Giannelli et al. reported continuous mode of diode lasers as more efficient than pulsed mode [13Leja C, Geminiani A, Caton J, Romanos GE. Thermodynamic effects of laser irradiation of implants placed in bone: An in vitro study. Lasers Med Sci 2013; 28(6): 1435-40.
[http://dx.doi.org/10.1007/s10103-012-1215-z] [PMID: 23053251]
, 14Giannelli M, Landini G, Materassi F, et al. The effects of diode laser on Staphylococcus aureus biofilm and Escherichia coli lipopolysaccharide adherent to titanium oxide surface of dental implants. An in vitro study. Lasers Med Sci 2016; 31(8): 1613-9.
[http://dx.doi.org/10.1007/s10103-016-2025-5] [PMID: 27475996]
]. The main risk of laser treatment is the extra heat generation in bone structures [44Monteiro JSC, de Oliveira SCPS, Pires Santos GM, Pires Sampaio FJ, Pinheiro Soares LG, Pinheiro AL. Effectiveness of antimicrobial photodynamic therapy (AmPDT) on Staphylococcus aureus using phenothiazine compound with red laser. Lasers Med Sci 2017; 32(1): 29-34.
[http://dx.doi.org/10.1007/s10103-016-2079-4] [PMID: 27677473]
]. Contrary to this, laser treatment outcomes may change with the use of combination therapies such as PDT. The study conducted by Valente et al. showed that diode lasers have been useful regardless of the aid of photosenzitation, while others reported Er:YAG and diode lasers as effective treatment modalities with photosenzitation and highlighted efficient combination on implant decontamination [15Valente NA, Mang T, Hatton M, Mikulski L, Andreana S. Effects of two diode lasers with and without photosensitization on contaminated implant surfaces: An Ex vivo study. Photomed Laser Surg 2017; 35(7): 347-56.
[http://dx.doi.org/10.1089/pho.2016.4247] [PMID: 28253064]
, 17Huang TC, Chen CJ, Ding SJ, Chen CC. Antimicrobial efficacy of methylene blue-mediated photodynamic therapy on titanium alloy surfaces in vitro. Photodiagn Photodyn Ther 2019; 25: 7-16.
[http://dx.doi.org/10.1016/j.pdpdt.2018.11.008] [PMID: 30439531]
, 21Rogers S, Honma K, Mang TS. Confocal fluorescence imaging to evaluate the effect of antimicrobial photodynamic therapy depth on P. gingivalis and T. denticola biofilms. Photodiagn Photodyn Ther 2018; 23: 18-24.
[http://dx.doi.org/10.1016/j.pdpdt.2018.04.015] [PMID: 29753881]
, 22Monzavi A, Fekrazad R, Chinipardaz Z, Shahabi S, Behruzi R, Chiniforush N. Effect of various laser wavelengths on temperature changes during periimplantitis treatment: An in vitro Study. Implant Dent 2018; 27(3): 311-6.
[http://dx.doi.org/10.1097/ID.0000000000000751] [PMID: 29489549]
]. PDT has also been carried out in conjunction with different mechanical treatment, chemical agents, LED and laser systems. Only in the study performed by Valente et al., PDT was found to give a modest improvement regarding the surface decontamination and it was not statistically significant when compared to the group of diode laser treatment [15Valente NA, Mang T, Hatton M, Mikulski L, Andreana S. Effects of two diode lasers with and without photosensitization on contaminated implant surfaces: An Ex vivo study. Photomed Laser Surg 2017; 35(7): 347-56.
[http://dx.doi.org/10.1089/pho.2016.4247] [PMID: 28253064]
]. Other studies in the literature reported advanced treatment efficacy for PDT when it is performed as a combination therapy [15Valente NA, Mang T, Hatton M, Mikulski L, Andreana S. Effects of two diode lasers with and without photosensitization on contaminated implant surfaces: An Ex vivo study. Photomed Laser Surg 2017; 35(7): 347-56.
[http://dx.doi.org/10.1089/pho.2016.4247] [PMID: 28253064]
-19Rismanchian M, Nosouhian S, Shahabouee M, Davoudi A, Nourbakhshian F. Effect of conventional and contemporary disinfectant techniques on three peri-implantitis associated microbiotas. Am J Dent 2017; 30(1): 23-6.
[PMID: 29178710]
, 21Rogers S, Honma K, Mang TS. Confocal fluorescence imaging to evaluate the effect of antimicrobial photodynamic therapy depth on P. gingivalis and T. denticola biofilms. Photodiagn Photodyn Ther 2018; 23: 18-24.
[http://dx.doi.org/10.1016/j.pdpdt.2018.04.015] [PMID: 29753881]
, 22Monzavi A, Fekrazad R, Chinipardaz Z, Shahabi S, Behruzi R, Chiniforush N. Effect of various laser wavelengths on temperature changes during periimplantitis treatment: An in vitro Study. Implant Dent 2018; 27(3): 311-6.
[http://dx.doi.org/10.1097/ID.0000000000000751] [PMID: 29489549]
].

CONCLUSION

The present review was conducted to evaluate the in vitro effects of commonly used peri-implantitis treatment modalities. Although there is a wide range of treatment options, none of these modalities were able to completely remove peri-implantitis related biofilms in any of the affected surfaces. Further studies are needed to identify a capable and suitable treatment or combined modality treatment for peri-implantitis therapy. The impact of each treatment modality should also be take into account as, even minimal, surface modifications will increase the risk of bacterial recontamination.

CONSENT FOR PUBLICATION

Not applicable.

FUNDING

None.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

Declared none.

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