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ORIGINAL • Rev Gaúch. Odontol. 71 • 2023 • https://doi.org/10.1590/1981-86372023000420210085 linkcopy

Open-access Effectiveness of ozone therapy in the treatment of periodontal diseases: a systematic review

Eficácia da ozonioterapia no tratamento de doenças periodontais: uma revisão sistemática

AuthorshipSCIMAGO INSTITUTIONS RANKINGS

    ABSTRACT

    The aim of this study was to evaluate the effectiveness of ozone as an adjuvant factor in the treatment of periodontal diseases. A systematic review was carried out using the PubMed, LILACS/BIREME, CoChrane, and Scielo databases and manual searches. Clinical studies published in English, Spanish, Portuguese, and French, between 1950 and 2020 that evaluated the effects of ozone in the treatment of periodontal diseases were included. The search resulted in 178 articles, of which 24 met the proposed eligibility criteria and were selected for this review. The risk of bias was assessed for each selected study in accordance with the Cochrane risk-of-bias tool - version 5.1.0. The selected studies evaluated the effect of ozone therapy on periodontitis, gingivitis, and peri-implant diseases. It was observed that the ozone in its oily form presented the best clinical results. In cases of periodontitis, it was concluded that ozone therapy in the gaseous form did not bring any additional benefit. With respect to gingivitis, ozone provided faster remission compared to the control group. And in peri-implant disease cases, ozone had the capacity to reduce the development of mucositis. Regarding microbiology, it was observed that ozone can continuously and significantly reduce periodontal microorganisms; however, with no difference from control groups. Further studies with adequate control of biases are suggested, using ozone in the oily or aqueous form, which are the most promising forms, also evaluating the possible effectiveness of ozone by-products.

    Indexing terms Ozone; Peri-implantitis; Periodontal diseases

    RESUMO

    O objetivo deste estudo foi avaliar a eficácia do uso do ozônio como fator adjuvante no tratamento das doenças periodontais. Foi realizada uma revisão sistemática utilizando as bases de dados PubMed, LILACS/BIREME, CoChrane, Scielo e pesquisa manual. Foram incluídos estudos clínicos publicados em inglês, espanhol, português e francês entre 1950 e 2020, que avaliaram os efeitos do ozônio no tratamento de doenças periodontais. A busca resultou em 178 artigos, destes 24 estudos atenderam aos critérios de elegibilidade propostos e foram selecionados para esta revisão. Foi realizada a avaliação do risco de viés em cada estudo selecionado de acordo com a ferramenta de avaliação de risco de viés Cochrane Risk of Bias Tool - versão 5.1.0. Os estudos selecionados avaliaram o efeito da ozonioterapia na periodontite, gengivite e em doenças peri-implantares. Observou-se que a utilização do ozônio na forma oleosa foi a que apresentou os melhores resultados clínicos. Nos casos de periodontite, concluiu-se que a ozonioterapia não trouxe nenhum benefício adicional sob a forma gasosa. Em relação à gengivite, o ozônio proporcionou uma remissão mais rápida do que do grupo controle. E nas doenças peri-implantares, o ozônio foi capaz de reduzir o desenvolvimento da mucosite. Com relação a microbiologia, foi observado que o ozônio pode reduzir contínua e significativamente os microorganismos periodontais, contudo, sem diferença para grupos controle. Sugerem-se mais estudos com controle adequado de vieses, utilizando o ozônio de forma oleosa ou aquosa, formas mais promissoras, além da avaliação de possível eficácia de subprodutos do ozônio.

    Termos de indexação Ozônio; Peri-Implantite; Doenças periodontais

    INTRODUCTION

    The development of periodontal diseases has been associated with anaerobic bacteria that initially affect the protective periodontium and can later reach the attachment periodontium, leading to bone destruction. As a result of this process, tooth mobility and even total tooth loss can be observed. Periodontitis is an inflammatory, chronic, multifactorial disease that begins with the accumulation of bacteria and their metabolic products. Thus, there is migration of the junctional epithelium in the apical direction, which promotes the deepening of the gingival sulcus and the formation of periodontal pockets associated with attachment loss [1].

    Tobacco smoking, diabetes, medication, age, hereditary, and obesity have been related to increased risk of periodontal diseases. Similarly, other studies have suggested association between periodontal diseases and other diseases such as diabetes, hypertension, asthma, liver diseases, among others [2]. Many studies have also suggested important association between periodontal disease and cardiovascular diseases, concluding that periodontal disease is a potential risk factor for cardiovascular events, such as stroke and coronary heart disease. Furthermore, it has been demonstrated that individuals with periodontitis have increased risk of developing cardiovascular diseases, including myocardial infarction, heart failure, peripheral artery disease, atherosclerosis and stroke [3].

    In addition, there are a number of factors that favor the accumulation of dental biofilm, such as crowding, unsatisfactory restorations, poor contact point, mouth breathing and caries [4]. For better control of the disease, periodontal treatment should be based on controlling the biofilm and the host response. The initial phase is the supra- and subgingival mechanical debridement, which, although being the most important part of the treatment, cannot completely eliminate periodontal microorganisms, especially in very deep pockets (greater than 5-6mm) and furcation lesions [5].

    Subgingival instrumentation failures reflected in periodontium with persistent inflammation can lead to indication of surgical procedure, which, in turn, can cause soft tissue recession and esthetic dissatisfaction [6]. To enhance mechanical debridement, topical or systemic antimicrobial agents have been developed. Long-term use of systemic antibiotics is not recommended, as bacterial resistance may develop, in addition to their undesired adverse effects. The topical use of mouthwashes has some limitations as they do not seem to penetrate more than 3mm into pockets and may have poor substantivity [5].

    In literature, there is controversy regarding the synergistic effect of subgingival irrigation combined with scaling and planing of root surfaces. Some authors believe that in this way, it is possible to release antimicrobial agents deep into pockets, thus being more effective in stopping the progression of the periodontal disease, reducing surgical interventions in the future [7,8].

    Subgingival irrigation with antiseptics is described in literature mainly with the use of water, saline solution, povidone iodine, hydrogen peroxide, and chlorhexidine gluconate. The latter is the substance most used for this purpose, as it is an antiseptic with broad bactericidal spectrum, with bacteriostatic and antifungal function, and is also effective against gram-positive and -negative aerobic and anaerobic bacteria, [9,10]. However, it also causes mucosal desquamation, damage to the healing of lesions, fixation of fibroblasts on root surfaces, changes in taste and tooth color [7]. Allergic reactions have also been described, especially using povidone-iodine [8].

    Recently, ozone has become an alternative antiseptic with good results in dentistry due to its strong action against bacteria, fungi, viruses, and protozoa, in addition to being a potent oxidant, acting as a metabolic and host response modulator [11]. There are various forms of using ozone, whether gaseous or aqueous, such as in the treatment of early caries lesions; in tooth hypersensitivity, in the disinfection of cavities, root canals, and periodontal pockets; in mouthwashes and also for cleaning full dentures [7]. Its use provides better healing of epithelial lesions such as canker sores and herpetic lesions, promotes hemostasis, and is also capable of sterilizing heat-sensitive medical and dental instruments [12].

    Thus, the aim of this work is to carry out a systematic review of the effects of ozone as an adjuvant factor in the treatment of periodontal diseases.

    METHODS

    To select studies to be included in this review, the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA-P) protocol was obtained as reference, registered in the PROSPERO platform (number CRD42020165351), with evaluation of the study design, population under study, types of intervention, presence of control group, and analyzed outcomes (PICO) [13].

    Clinical trials comparing the effectiveness of ozone as an auxiliary means of treatment for periodontal diseases in relation to other already established therapeutic modalities were selected.

    The population under study was composed of patients with some type of periodontal disease, whether gingivitis, chronic or aggressive periodontitis, and peri-implant diseases.

    Clinical trials evaluating the effects of ozone in the treatment of periodontal diseases were included.

    Studies that evaluated in vitro ozone therapy related to periodontal diseases or other outcomes (endodontics, periodontal disease not induced by biofilm, gingival graft hypersensitivity), review articles, other types of studies (case studies, quasi-experimental), without description of exposure, those performed with specific populations (pregnant women, diabetic patients), those with missing abstract or with unavailability of the full article, were excluded.

    The search strategy adopted was to include articles published in English, Spanish, Portuguese, and French between 1950 and 2020, in order to gather the largest number of scientific articles published in literature, within the inclusion and exclusion criteria.

    The following databases were searched: PubMed, LILACS/BIREME, Cochrane, and Scielo. To search the grey literature, the Open Grey platform was used, and a manual search for authors of selected articles was performed. The following Boolean expressions were used: “periodontal diseases” AND “ozone”; “gingivitis” AND “ozone”; “periodontitis” AND “ozone”.

    To search the articles in literature, three researchers reviewed titles and abstracts. After the first search, titles repeated in different databases were excluded. Finally, studies that did not meet the inclusion criteria were excluded. In cases of doubt, in order to decide whether a study should be included or excluded from this research, full reading was performed and, thus, it was decided by mutual agreement.

    The risk of bias was individually assessed for each study according to the Cochrane risk-of-bias tool (version 5.1.0) which determines low, high, or unclear risk of bias, according to the following possibilities: selection bias, performance bias, detection bias, attrition bias, reporting bias, and other biases not belonging to the aforementioned domains [14].

    RESULTS

    The database search strategy resulted in 168 articles. Of these, 81 were duplicates and 57 were excluded after analysis of titles and abstracts. Thus, 30 articles were read in full and, based on the proposed eligibility criteria, 24 articles were selected for this review (figure 1).

    Figure 1
    Article selection flowchart.

    Included articles were published between 2005 and 2020 and carried out in the following countries: India (7 studies), Turkey (6 studies), Cuba (4 studies), Egypt (2 studies), United Kingdom (1 study), Italy (1 study), Poland (1 study), Jordan (1 study), and Japan (1 study).

    Individual data for each study were obtained from publications, as well as from their protocols and registrations in clinical trials registry platforms (U.S. National Institutes of Health Clinical Trials Registry).

    Most included studies analyzed the relationship between ozone therapy and periodontitis. Only three studies evaluated gingivitis, one peri-implant mucositis, and one peri-implantitis. The follow-up time of studies ranged from 7 to 180 days, with wide variation within this range depending on the study.

    Interventions were performed with gaseous ozone in eight studies, topical in the oily form in seven studies, and liquid (ozonated water) in nine studies. In all cases, the manufacturer’s instructions regarding time, potency, pressure, and quantity were followed.

    In most studies, interventions performed were accompanied by hygiene instructions to participants, being well described in the articles, with the exception of seven studies [4,7,15-19], which did not provide information in this respect.

    In relation to the control group, in 33% of studies, only scaling and root planing were performed, without the use of any irrigation substance. In another 33%, isolated chlorhexidine gluconate was used. In addition, the use of common water, distilled water, oxygen, indocyanine green (photosensitizing agent), combined with laser, hydrogen peroxide, and saline solution was also observed.

    The general characteristics of studies in relation to intervention and control groups are described in table 1, which also show the main characteristics of the population of selected studies, the outcomes analyzed, and the results obtained.

    Thumbnail
    Table 1
    Characteristics of studies (population, interventions, and results).

    Table 2 shows the basic form of treatment for all subjects described in the studies, the clinical markers used to assess the disease, and the complementary exams performed.

    Thumbnail
    Table 2
    Type of standard treatment, clinical markers, and complementary exams performed in studies.

    Non-surgical supra- and subgingival scaling was performed in most studies, with mechanical and/or ultrasonic instrumentation without antibiotic prescription. Some studies reported the use of anesthesia for this procedure [8,23-25]. The duration and number of scaling sessions ranged from 1 to 7 sessions and from 30 min to 1 hour per patient. Irrigation time varied widely from seconds (20-45) to minutes (1-10). Only in the study by Isler et al. [29], surgical treatment for peri-implantitis was performed, and Amoxicillin (500mg) and Metronidazole (500mg) every 8 hours for 7 days were prescribed.

    Bacterial plaque samples were obtained for microbiological analysis in nine studies. Other complementary analyses carried out were blood samples, saliva samples, and gingival fluid samples. The collection frequency varied from before treatment (baseline=t0), the day after treatment, the 4th day, the 15th day, the 18th day, the 21st day, 1 month, 2 months, 3 months, up to 6 months.

    After treatment, subjects were recruited within a period of 1 week, 14 days, 1 month, 2 months, 3 months, 4 months, or up to 6 months for the evaluation of clinical parameters.

    Regarding methodological quality, the risk of bias results of selected studies are summarized in Figure 2.

    Figure 2
    Classification of the risk of bias of selected studies based on the Cochrane risk-of-bias tool - version 5.1.0.

    With regard to selection bias, low risk of bias was identified in 58% of studies in the random sequence domain and in 54% in the allocation concealment domain, as details about the randomization process were presented in these studies. As for performance bias, 62.5% of studies presented low risk, as blinding tools were well described in the methodology section. In 37.5% of studies; however, it was not possible to identify forms of blinding, being classified as undefined risk of bias. With regard to detection bias, 54% of studies had low risk of bias. Attrition bias was considered low in 62.5% of studies because, in these cases, when there was loss of follow-up, it was considered small and well justified. Regarding reporting bias, although some studies had not published a protocol, outcomes were reported as proposed in the methodology section and the treatment was well described and reproducible, and thus the probability of bias of this nature was considered low in 79% of studies.

    Another bias identified in most studies was the absence of sample calculation parameters, described in only seven studies [18,19,23,24,26-28].

    DISCUSSION

    It is known that ozone has several physicochemical properties such as immunostimulant and analgesic, anti-hypoxic and detoxifying, antimicrobial, bioenergetic and biosynthetic, by activating the metabolism of carbohydrates, proteins, and lipids [30].

    In periodontics, the therapeutic use of ozone has gained popularity due to the antimicrobial properties of ozone against gram-positive and -negative bacteria, viruses, and fungi [5,7,8,23,25], in addition to its ability to stimulate the circulatory system and modulate the immune response [28].

    Regarding gingivitis, only three studies were included, and in one of them, ozone provided faster remission compared to the control group [4]. However, these studies were classified as having undefined risk of bias, indicating the absence of relevant information to judge their validity.

    Based on articles with lower risk of bias in all six categories analyzed [22-25], it could be concluded that ozone therapy did not bring any additional benefit, nor any significant improvement in periodontal parameters in terms of periodontitis. On the other hand, in studies by Hayahumo et al. [8] and Yilmaz et al. [16], which were also classified as having lower risk of bias in five categories (lack of information on concordance for the assessment of clinical parameters), significant improvement was observed only in clinical parameters, for Hayahumo et al. [8], and in clinical and microbiological parameters for Yilmaz et al. [16]. The lack of standardization in the way ozone is applied for the treatment of periodontal diseases, length of use, and frequency could explain differences between results of these studies.

    Specifically for peri-implant diseases, two articles were identified [28,29] with low risk of bias in all categories. In both studies, the conclusion was that ozone can reduce the development of mucositis, significantly improving clinical parameters in addition to radiographic evidence of significant improvements. It is noteworthy that the inclusion of peri-implant conditions and diseases in the Classification of Periodontal Diseases and Conditions [31] is recent. Thus, further studies relating these diseases to ozone therapy are needed for a better understanding of its therapeutic effect.

    Regarding the form of ozone use, it could be concluded with studies by Skurska et al. [6], Uraz et al. [23], Dengizek et al. [24], and Tasdemir et al. [25] that gaseous ozone therapy does not lead to additional improvement in clinical and microbiological parameters. Only the study by Yilmaz et al. [16] found improvement in clinical parameters such as attachment gain and reduction in pocket depth with this form of administering ozone. This can be explained by the instability of ozone in the gaseous medium, which has half-life from 30 to 40 minutes at 20 °C [32,33].

    In the study by Kshitish & Laxman [9], good results using ozonated water under pressure from 350 to 500kPa were obtained. On the other hand, in the study by Pandya et al. [5], chlorhexidine was more effective than ozonated water produced at 0.595-350kPa, suggesting that the absence of pressure standardization interferes with the result obtained. Hayakumo et al. [8] used nanobubbles as alternative, with significant results for clinical and microbiological parameters.

    The oily form of ozone was the form that presented the best clinical results in the evaluated studies [1,4,11,15,17,27]. The advantage of this method is that the oil remains in contact with the surface for longer period of time, performing its functions. In addition, it can be stored under refrigeration for several months, eliminating the need for generator. This characteristic is opposed to that of gaseous ozone, which needs to be generated and used immediately, since when exposed to air, the gas decomposes quickly.

    On the other hand, the chemical evaluation of the ozonation of some types of oils such as sunflower, castor, olive, almond, and propylene glycol was carried out. The absence of ozone percentages and the presence of formaldehyde were observed in all analyzed samples. It is known that the hydrolysis of ozonated oils can generate hydrogen peroxide, aldehyde, and ketones, which are antimicrobial. This suggests that the bactericidal and curative results of ozonated oils may be related to their by-products rather than to the ozone itself [34].

    Regarding microbiology, it was observed in studies by Yilmaz et al. [16], Saeed et al. [1], Verma & Indurkar [18], Hayakumo et al. [8], Shoukheba & Ali [11], Pandya et al. [5], and Uraz et al. [23] that ozone can continuously and significantly reduce periodontal microorganisms. However, there were no significant differences between intervention groups and their controls, indicating that the antimicrobial effect between groups was similar.

    In the study by Uraz et al. [23], reduction of potent pathogens of the orange and red complexes such as Porphyromonas gingivalis (Pg) was observed in the first month and Tannerella forsythia (Tf) and Prevotella intermedia (Pi) in three months. Shoukheba & Ali [11] observed significant reduction in Pg and Actinobacillus actinomycetemcomitans (Aa) between 1 and 3 months in the ozone group; however between 3 and 6 months, no significant differences between groups were observed. In the study by Saeed et al. [1], reduction in Pg was observed for three months and Hayakumo et al. [8] also reported a more than 95% reduction in all sites under study. Verma & Indurkar [18] observed reduction in the four periodontal pathogens (Aa, Pg, Pi, and Tf) in both groups, which can be attributed to the fact that repeated subgingival irrigations were performed, interfering with the recolonization of the subgingival microflora. In the work by Kshitish & Laxman [9], percentage reduction was only observed in Actinobacillus actinomycetemcomitans, with no antibacterial effect on Porphyromonas gingivalis and Tannerella forsythensis, using ozone or chlorhexidine.

    Two studies [6,27] evaluated the presence of high MMP-8 levels (metalloproteinases) in saliva and gingival fluid. In the study by Nardi et al. [27], it was observed that scaling and root planing, accompanied by subgingival irrigation with ozone in the oily form, was more effective in reducing this metalloproteinase in saliva than scaling and root planing alone, with significant difference between groups. MMP-8 levels are associated with the disease severity and help understanding the pathogenesis, diagnosis, and treatment of periodontal diseases.

    CONCLUSION

    Works that discuss the use of ozone as a therapeutic alternative in periodontics do not reach any conclusion regarding a protocol to be used. It could be inferred that the antimicrobial effectiveness of ozone is related to the form of presentation, concentration (dose), exposure time, and microorganism evaluated. Thus, well-defined criteria must be implemented to provide the quality and reliability of the ozone produced in any of its forms.

    Further studies with adequate control of biases are suggested, using ozone in the oily or aqueous form, as the most promising forms, also evaluating the possible effectiveness of ozone by-products.

    How to cite this article

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    Edited by

    • Assistant editor: Luciana Butini Oliveira

    Publication Dates

    • Publication in this collection
      13 Mar 2023
    • Date of issue
      2023

    History

    • Received
      28 July 2021
    • Reviewed
      02 Feb 2022
    • Accepted
      16 Mar 2022
    Creative Common - by 4.0
    This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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