Int. J. Odontostomat., 7(2):267-278, 2013.

 

Ozone Therapy in Dentistry: A Systematic Review

 

Ozonoterapia en Odontología: Una Revisión Sistemática

 

Iris Jasmin Santos German*; Antonio de Castro Rodrigues*; Jesus Carlos Andreo*; Karina Torres Pomini*; Farooque Jamaluddin Ahmed*; Daniela Vieira Buchaim*; Geraldo Marco Rosa Júnior**; Jéssica Barbosa de Oliveira Gonçalves* & Rogério Leone Buchaim*

* Department of Biological Sciences, Bauru School of Dentistry, University of São Paulo, Bauru, Brazil.

** University of Sacred Heart, Bauru, São Paulo, Brazil.

Correspondence to:

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ABSTRACT: The purpose of this systematic review was to verify the literature available regarding the effectiveness and the biological effects of ozone therapy in periodontics, orthodontics and dental implants. Studies were searched in September 2012. Analyzed sources included the databases PubMed, Lilacs and SciELO, through a combination of key words, dental implants, periodontics, orthodontics, therapeutics. Studies between 2002 and 2012 were included. In vitro and in vivo studies English and Spanish language publications, excluding posters, letters to the editors and conferences. In Vitro and in Vivo studies showed the inactivation of the major periodontal pathogens by ozone. There were divergent results and lack of evidence for the activity of ozone on adhesion of orthodontic brackets, in implantology and orthodontics. Ozone could be considered as a promissory alternative therapy in dentistry. However, well-designed studies are needed to assess the application of ozone in order to evaluate its clinical effectiveness in the field of dentistry.

KEY WORDS: dental implants, periodontics, orthodontics, therapeutics.

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RESUMEN: El objetivo de esta revisión sistemática fue verificar la literatura disponible relacionada a la efectividad y efectos biológicos de la ozonoterapia en periodoncia, ortodoncia e implantes dentales. Se realizó una revisión sistemática en septiembre del 2012 en las bases de datos PubMed, LILACS and SciELO por medio de la combinación de las palabras clave dental implants, periodontics, orthodontics, therapeutics. Se evaluaron los artículos publicados entre los años 2002 y 2012. Fueron incluidos estudios In vitro e in vivo y publicaciones en Inglés y Español, excluyendo pósters, carta al editor y conferencias. Estudios in vitro e in vivo mostraron inactivación de los principales patógenos periodontais con el uso del ozono. Hubo resultados contradictorios y falta de evidencia sobre la acción del ozono en la adhesión de los brackets ortodónticos, así como también en la osteointegración de los implantes dentales. El ozono puede ser considerado como una terapia alternativa promisoria en la Odontología. Sin embargo, es necesaria la realización de estudios bien diseñados para, de ese modo, evaluar la aplicación del ozono y su efectividad clínica en el campo de la Odontología.

PALABRAS CLAVE: implantes dentales, periodoncia, ortodoncia, terapéutica.

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INTRODUCTION

Ozone is a gas with the chemical formula O3, and is the third most powerful oxidant. Medical ozone is produced by oxygen and its passage through a voltage gradient, using ozone generators that react to dioxygen molecules, forming ozone (O2 + OÆO3) (Ripamonti et al., 2011; Bocci, 2006; Swilling, 2004).

Several biological actions (Fig. 1) of medical ozone include the increase in the synthesis of biologically active substances such as interleukins, leukotrienes and prostaglandins that are beneficial in the reduction of inflammation and in cicatrization, the activation of aerobic processes (glycolysis, Krebs cycle, beta-oxidation of fatty acids), secretion of vasodilators (e.g. nitric oxide-NO), activation of the mechanism of protein synthesis and increase in the quantity of ribosome and mitochondria in the cells, thus raising the functional and potential activity of tissue regeneration (Seidler et al., 2008).

The ozone oxidant potential induces the destruction of cellular walls and cytoplasmatic membranes of bacteria (Thanomsub et al., 2002). The gas was named ozone (a Greek word that means "smell") by the German chemist Christian Frederick Schonbein of the University of Basel in Switzerland 1840 (Seidler et al.; Veranes et al., 1999).

During the First World War, ozone gas was used for the treatment of post-traumatic gangrene, infected wounds, burns and fistulas and other anaerobic infections, putrefied wounds, suppurations of bone fractures and various inflammations in German soldiers (Azarpazhooh & Limeback, 2008). By the middle of 1932, German dentist Edward A. Fisch, perceived the therapeutic possibilities of using ozone as a medical therapy (Altman, 2007; Bocci, 2005).

Currently, there are divergences in the developed studies regarding ozone therapy action. Therefore, the studies available in the literature must be reviewed in order to evaluate the obtained results and estimate the effectiveness of ozone therapy and the methods used. The purpose of this study was to perform a review regarding the effectiveness of ozone therapy in the area of dentistry, with emphasis on the current uses, focusing on the areas of periodontics, orthodontics and dental implants. The authors aimed at answering the following questions: "What is the action of ozone on periodontal pathogens?" "What are the effects of ozone on the adhesion of brackets to dental enamel?" "How does ozone act in the bone integration of dental implants?"

These questions are important for future studies in order to understand the properties of ozone and its contribution in clinical uses.

Fig. 1. Major biological effects of ozone therapy.

MATERIAL AND METHOD

Data sources. The literature review included studies available in the databases, PubMed, LILACS and SciELO, utilizing the following descriptors: ozone, dentistry, periodontics, orthodontics and dental implants. Studies published between the years 2002 and 2012 were included. A combination of the key words was used, which helped to identify studies related to ozone therapy in dentistry. Books regarding ozone therapy were also referred to in order to obtain more information on the theme (Altman; Bocci, 2002, 2005). The search was limited to studies written in English and Spanish. Both in vitro and in vivo studies regarding ozone therapy in dentistry were selected (Fig. 2).

Fig. 2. Search strategy for literature review on the use of ozone therapy in dentistry.

Study selection. Letters to the editor, abstracts, conferences, comments, books and panels were not included; however all of them were reviewed in order to identify possible important data that could contribute to the development of this review.

Data extraction. After reviewing the titles of the researched studies, seven pertinent studies were found related to the study objectives (accessed on September 26, 2012). Several studies stemming from the search were read with the purpose of identifying relevant information on the theme in question.

RESULTS

Results are presented in three sections according to the purposes of the study.

Action of ozone on periodontal pathogens. Three in vivo (Kshitish & Laxman, 2010; Martinez Abreu & Abreu Sardinas, 2005; de Ramon et al., 2004) and one in vitro study (Huth et al., 2011) evaluating the action of ozone on periodontal microbiota were found.

In 2004, de Ramon et al., (Table IA) analyzed the periodontal responses in terms of the clinical, microbiological and immunologic aspects in patients with moderate and severe periodontal pockets, comparing the technique of scaling and root planning (control group) with the application of ozone (experimental group).

After 30 days, the average clinical evaluation showed the following data: in the experimental group, initial periodontal index (Russell's Index) was 5.72 and the final index was 5.59. Initial supragingival plaque index was 31.30 and the final index was 49.99. Initial gingival bleeding index was 62.43 and the final 26.29.

In the experimental group the microbiological analysis the reduction of periodontal pathogens (Aggregatibacter actinomycetencomitans (Aa), Bacteroides forsythus (Bf), and Porphyromonas gingivalis (Pg) was about 50%). In the immunologic analysis, the initial TNF-a was 101.23 and at the end it decreased to 36.01. Initial IL-1b also reported a decrease from an initial period of 96.12 to 34.28 after 30 days of treatment.

Martínez Abreu & Abreu Sardiñas (Table IA) developed a randomized controlled clinical study. The study was divided into two groups: the control (treated with 0.2% chlorhexidine) and the experimental group (treated with the ozonated oil Oleozon). A microbiological analysis was performed on the gingiva of the teeth with periodontitis after 21, 90 and 180 days respectively, during a nine-month postoperative period.

The microbiological and clinical evaluation was determined to be:

Satisfactory: Absence or lack of gram-negative microorganisms.

Unsatisfactory: Abundant presence or prevalence of gram-negative microorganisms.

After the postoperative period of 180 days, microbiological results were satisfactory in 98% of the patients in the experimental group and 78% in the control group. Regarding the clinical evaluation, satisfactory results after 180 days were present in 98% of the patients in the experimental group and 95% in the control group.

In 2010, Kshitish & Laxman (Table IB) developed a double-blind randomized study regarding the use of ozonated water in the treatment of periodontitis. The control group was irrigated with 0.2% chlorhexidine. Clinical parameters such as gingival index and gingival bleeding index were analyzed, in addition to the ozone activity on oral microorganisms: Aggregatibacter actinomycetemcomitans (Aa), Porphyromonas gengivalis (Pg), Tannerella forsythensis (Tf), Herpes Simplex virus (HSV-1 and HSV-2), Epstein Barr virus (EBV) human cytomegalovirus (HCMV) and Candida albicans.

Results of the ozone irrigations showed 12% of reduction of the plaque index. The gingival index decreased 29% and bleeding index 26%. After seven days, ozone showed presence of Aa in 25%, Pg 50%, Tf 25%, HSV-1 62.5%, HSV-2 0%, HCMV 25%, EBV 37.5% and Candida albicans 12.5% of the cases.

In an in vitro study, Huth et al. (2011) (Table IB) determined the efficacy of the use of gaseous/aqueous ozone in the reduction of several periodontal pathogens (Aa, Pg, Tannerella forsythia (Tf) and Parvimonas micra (Pm) in both planktonic state and biofilm. Aqueous ozone in a concentration of 20 mg ml-1 resulted in the reduction of approximately 99% of the total A. actinomycetencomitans in planktonic state, and 70% in biofilm. Gaseous ozone (concentration of 1, 2, 4, 8, 16 g m-3) was capable of reducing this pathogen by 99.7% in isolated state, and by approximately 70% in biofilm at a concentration of 53 g m-3.

The complete elimination of P. gingivalis and T. forsythia in planktonic state was obtained through the concentrations of gaseous ozone of 8 and 16 g m-3 and 2% chlorhexidine; in biofilm gaseous ozone of 53 g m-3 and 2% chlorhexidine showed effectiveness of 100%. Even in low concentrations (1, 2 and 4 g m-3), gaseous ozone reduced the levels of these pathogens by 99.7% in planktonic state.

Parvimonas micron, in isolated state, was totally eliminated by all agents, with the exception of low concentrations of aqueous ozone at 1.25 mg ml-1 (reduction of 78% in planktonic state). However, in biofilm, P. micra presented greater susceptibility to ozone gas (53 g m -3) and 2% chlorhexidine.

Ozone effects on the adhesion of brackets to dental enamel. Two in vitro studies evaluating the effects of ozone application on the adhesion of orthodontic brackets were found.

In a randomized in vitro study, Cehreli et al., (2010) (Table II) evaluated prophylactic pretreatment with ozone, applying shear tension to the bonding of orthodontic brackets. Moreover, it analyzed the bonding failures in the interface using the modified adhesive remnant index (ARI).

Vertical force was applied to the bracket base (1N/mm2=1MPa) at a speed of 1mm/min. Each tooth was washed, and polished with pumice and rubber cups for 10 seconds. The results of the shear bond strength were: Group 1: 10.48 MPa; Group 2: 8.89 MPa; Group 3: 9.41MPa; Group 4: 9.82 MPa.

The results of modified adhesive remnant index ARI (0-3) were: Group 1: 2.38; Group 2: 1.31; Group 3: 3.00; Group 4: 1.92.

Groups that were pretreated with ozone showed greater shear strength over the bracket. The lowest shear strength was obtained in Group 2. Pretreatment with ozone in the enamel did not affect the adhesive system used to attach the brackets.

Pithon & dos Santos (2010) (Table II) determined whether aqueous ozone reduces the bond strength of orthodontic adhesives. In total, 120 bovine mandibular incisor teeth were selected randomly and divided into 4 groups. Groups 1 and 3 were cleaned with pumice and washed with water; groups 2 and 4 were washed with ozonated water before adhesion to stainless orthodontic brackets with resin Transbond XT, 3M Unitek, Monrovia, CA, USA (Group 1 and 2;) and a modified resin of glass ionometer cement (Groups 3 and 4; Fuji Ortho LC, Japan).

Results showed, on average, shear bond strength (SBS) of 22.07 Mpa for Group 1; 20.21 Mpa in Group 2; approximately 20.06 Mpa in Group 3 and over 18.73 Mpa in Group 4. In terms of the adhesive remnant index ARI (0-3), results showed: Absence of adhesive remnant in the tooth (0): Group 1=3, Group 2=9, Group 3=0, Group 4=0; less than half of the adhesive remnant in the tooth (1): Group 1=3, Group 2=6, Group 3=3, Group 4=12; more than half of the adhesive remnant in the tooth (2): Group 1=15, Group 2=12, Group 3=15, Group 4=18; total presence of adhesive in the tooth (3): Group 1=9, Group 2=3, Group 3=12, Group 4=0. Results showed that the SBS of the groups washed with ozone (Group 2 and 4) were slightly less than the brackets washed with tap water (Group 1 and 3) but with no significant differences related to the shear bond strength in both groups. Ozone did alter the sites of the resin fracture when Fuji Ortho LC was used. The adhesive remnant index (ARI) in Groups 2 and 3 was significantly different from Groups 3 and 4. Ozone did not reduce the shear strength in orthodontic bracket debonding.

Ozone action on the bone integration of dental implants. The search method used allowed us to find one in vivo study regarding the effects of ozonated oil on the bone integration of implants:

El Hadary et al. (2011) (Table III) evaluated ozonated oil (sunflower oil, 0.55 ml) under the influence of cyclosporine A in the bone integration of dental implants. In total, 20 adult New Zealand rabbits aged 9-12 months and weighing between 3 and 3.5 kg, were administered a subcutaneous daily dose of 10 mg of cyclosporine per kg for a period of fourteen days.

Two groups were formed: Group A: ozonated and Group B: non-ozonated (Control group). After eight weeks, in the ozonated group (A) the microscopic exam showed organization of the mature bone with intimate contact between the implant surface and new bone with numerous haversian systems. In group A, bone density values (± SD) was initially 126.7 ± 3.3; and after eight weeks bone density was 134.1 ± 5.0; for Group B (non-ozonated) bone density was initially 117.7 ± 8.4; after eight weeks bone density was 124.0 ± 5.6. The study demonstrated that the application of cyclosporine for short term in combination with the topical application of ozonated oil may significantly influence bone density and bone integration quality around dental implants. No statistically significant differences were found related to bone density in both groups.

DISCUSSION

The present literature review analyzed the effects of ozone on periodontal pathogens, bone integration of dental implants and adhesion of orthodontic brackets.

The literature available related to ozone therapy in dentistry showed relevance in terms of the properties of ozone therapy, namely: therapeutic action through the distribution of oxygen, expression of growth factors and cytokines and reduction of oxidative stress and acting as modifier of the biological response (Seidler et al.; Bocci, 2006; Estrela et al., 2006; Valacchi et al., 2002).

Only one in vivo study (Martínez Abreu & Abreu Sardiñas) regarding the action of ozone against periodontal pathogens was performed for a larger period (six months), which represents a fragility of the studies already developed. Additionally, the results of this article also showed reduction of 98% of gram-negative microorganisms in the group treated with ozone.

There was remarkable inactivation of the major periodontal pathogens, in both the analyzed in vivo and in vitro studies. The results obtained by de Ramon et al., confirm the effective action of ozone on gingival bleeding, with a decrease of over 50% of the main periodontal pathogens: Aggregatibacter actinomycetencomitans, Bacteroides forsythus and Porphyromonas gingivalis. It showed a significant reduction of TNF-a and IL-1b. Furthermore, there was no variation in the pocket depth, or the level of periodontal insertion, which reinforces the need for mechanical removal of plaque for gingival control and periodontal maintenance (Müller et al., 2007; Lindhe & Nyman, 1975).

Nevertheless, ozone had significantly effectiveness in eliminating gram-negative microorganisms, reducing periodontal pathogens, bleeding on probing (Kshitish & Laxman).

In one study (de Ramon et al.), ozone reduced plaque index over 25%. However in another article (Kshitish & Laxman) results demonstrated that dental plaque was reduced by 12%.

Although therapeutic ozone is applied in several forms, including aqueous, gaseous and oil, there is evidence of better biocompatibility in the cell with the use of aqueous ozone (Huth et al., 2006). Ozone gas had greater antimicrobial activity in terms of the total elimination of pathogens (Aa, Pg, Tf and Pm) in planktonic state than in biofilm.

Regarding the effects of ozone therapy on the adhesion of orthodontic brackets, the results of the study of Cehreli et al., demonstrated that groups pretreated with ozone presented greater shear strength. Although Pithon and dos Santos found that the shear bond strength of the brackets washed with ozone were slightly less than the brackets washed with tap water after debonding but with no significant differences.

According to the search strategy used, the only study found about ozone activity on bone integration of dental implants (El Hadary et al.) demonstrated an increase in bone density around dental implants in the ozonated group, but no significant differences regarding the non-ozonated group were noticed. Nevertheless, the study was carried out only for two months, under the influence of an immunosuppressive drug and it also did not report the concentration and time of application of ozone, which renders the research irreproducible.

Ozone's biological and stimulatory effects could be useful in periodontal therapeutics, in orthodontics and dental implants.

In conclusion, the studies analyzed showed several biological properties of ozone and could be considered as a promising therapy. Further studies are needed for the analysis of the application of ozone in dentistry, in order to assess its clinical effectiveness in the field of dentistry.

ACKNOWLEDGEMENTS

The authors express their thanks to the Anatomy Department of the University of São Paulo (USP), Bauru, São Paulo, Brazil, for the additional information offered for the development of this review. The authors received no financial support and declare no conflicts of interest related to the authorship of this study.

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Correspondence to:

Iris Jasmin Santos German

Department of Biological Sciences (Anatomy)
Bauru School of Dentistry
Al. Dr. Octávio Pinheiro Brisola, 9-75
Postal code: 17012-901
University of São Paulo
FOB-USP
Bauru - BRAZIL
Phone: +55 14 3235-8226
Fax: +55 14 3235-8223

Email: irisgerman@usp.br

Received: 27-04-2013
Accepted: 15-06-2013