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 Table of Contents  
Year : 2020  |  Volume : 17  |  Issue : 1  |  Page : 31-36

Entrococcus faecalis elimination in retreatment cases using passive ultrasonic irrigation, manual dynamic activation and photodynamic therapy: a randomized clinical trial

1 Department of Endodontics, Faculty of Dentistry, Zonguldak Bülent Ecevit University, Zonguldak, Turkey
2 Microbiology Laboratory, Erzurum Region Training and Research Hospital, Erzurum, Turkey

Date of Submission10-Apr-2019
Date of Acceptance12-May-2019
Date of Web Publication20-Jun-2020

Correspondence Address:
Sevinç A. Türker
Department of Endodontics, Faculty of Dentistry, Bülent Ecevit University, Kozlu 67600, Zonguldak
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/tdj.tdj_42_19

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The aim of this in-vivo study was to compare the effect of passive ultrasonic irrigation, manual dynamic activation and photodynamic therapy in reducing Enterococcus faecalis load in retreatment cases by using PCR.
Materials and methods
Single-rooted, single-canalled 36 teeth with post-treatment apical periodontitis were selected for this study. Teeth were divided into three groups according to the disinfection methods: passive ultrasonic irrigation, manual dynamic activation, and photodynamic therapy (PDT). Microbiological samples were taken after removal of gutta-percha (S1), after preparation of the root canal (S2), and after disinfection method (S3) with sterile paper points. The E. faecalis amounts were measured by using PCR.
Intragroup analysis revealed that, all groups showed a significant decrease between S1 and S2 (P ≤ 0.05). However, a significant decrease between S2 and S3 was found only with PDT group (P ≤ 0.05). Intergroup analysis revealed that no significant differences were found among disinfection methods for bacterial load of S1, S2 and S3 (P ≥ 0.05). There were no significant differences among disinfection methods in terms of E. faecalis reduction percentages (from S2 to S3) (P ≥ 0.05).
PDT method significantly enhanced E. faecalis elimination after chemomechanical preparation. All disinfection methods were effective in reducing E. faecalis from infected root canals with no statistical differences.

Keywords: entrococcus faecalis, manual dynamic activation, passive ultrasonic irrigation, PCR, photodynamic therapy

How to cite this article:
Bilgin B, Türker SA, Aslan MH, Saǧlam BC, Koçak S, Koçak MM, Bodrumlu E. Entrococcus faecalis elimination in retreatment cases using passive ultrasonic irrigation, manual dynamic activation and photodynamic therapy: a randomized clinical trial. Tanta Dent J 2020;17:31-6

How to cite this URL:
Bilgin B, Türker SA, Aslan MH, Saǧlam BC, Koçak S, Koçak MM, Bodrumlu E. Entrococcus faecalis elimination in retreatment cases using passive ultrasonic irrigation, manual dynamic activation and photodynamic therapy: a randomized clinical trial. Tanta Dent J [serial online] 2020 [cited 2020 Sep 25];17:31-6. Available from: http://www.tmj.eg.net/text.asp?2020/17/1/31/287098

  Introduction Top

Nonsurgical root canal retreatment may become essential when the initial endodontic treatment fails. There are several causes of for failure such as, untreated root canals, inadequate cleaning, shaping, obturation procedures, and persistent intracanal or extracanal infections [1]. It has been stated that one of the main causes of post-treatment disease is persistent microorganism [2]. The infected root canals of endodontically treated teeth generally contain, gram positive, and facultative bacteria. Enterococcus faecalis, which has been shown to be resistant to root canal disinfection methods, is a commonly isolated facultative bacteria from infected endodontically treated root canals up to 77% [3].

Disinfection of root canals with root canal irrigants is an important step of endodontic treatment. Irrigants show antimicrobial activity by killing microorganism when in direct contact [4]. However, due to the complex root canal anatomy of none of the available irrigation solutions is sufficient to penetrate into depth areas where bacteria may remain and survive [4]. Therefore, irrigation agitation methods can help irrigation solutions to penetrate into deeper areas and eliminate bacteria from these complex canal systems. Manual and machine-assisted agitation techniques are commonly used as disinfection methods [5],[6].

Passive ultrasonic irrigation (PUI) is a machine-assisted activation technique. It enhances the irrigation solution properties by cavitation and acoustic streaming with the help of oscillating instrument [7]. The effectiveness of PUI on the reduction of E. faecalis from the infected root canals have shown in several in-vitro [8],[9],[10],[11] and an in-vivo studies [12].

Photodynamic therapy (PDT) has been defined as the light induced inactivation of cells and microorganisms [13]. This technique is based on the activation of a photosensitizing agent with a specific wavelength of light in the presence of oxygen [13]. The antimicrobial effect of PDT on the microorganisms in root canal system has been assessed in several ex-vivo [14],[15],[16] and in-vivo [17],[18] studies.

Manual dynamic activation (MDA) is a simple manual agitation method that produces an effective hydrodynamic effect by push and pull movements of a well-fitting gutta-percha within a prepared root canal [19]. Several in-vitro studies have shown that activation of the irrigation solutions with MDA was effective in cleaning the root canal [19],[20],[21]. However, the efficacy of MDA on bacteria elimination is still not confirmed in vivo. Therefore, this in-vivo study was aimed to compare the efficacy of MDA, PDT, and PUI, in reducing E. faecalis load during root canal retreatment. The null hypothesis tested was that there is no significant difference among disinfection methods.

  Materials and Methods Top

This study was approved by the clinical trials ethics committee of university (protocol number 2016–80–29/06). The project was registered at http://www.clinicaltrial.gov (ClinicalTrials.gov ID: XXX03750162). Forty patients older than 18 years old with no existing systemic disease attending endodontic department were assessed for eligibility. A total of 36 endodontically treated teeth (≥2 years previously) and no clinical symptoms (pain or swelling) with a single root and a single canal with post-treatment apical periodontitis were included. Exclusion criteria included teeth with periodontal pockets deeper than 4 mm and failures such as, fractured instrument, resorption, perforation, ledge, over fillings, and transportation. The patients enrolled in the clinical trial are presented in the flow diagram [Figure 1].
Figure 1: The CONSORT flow diagram of patients enrolled in the clinical trial.

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Sample taking and treatment procedures

The study was explained to the participants, and informed written consent was obtained from all participants. Randomization and blinding: The participants had randomized into three groups according to disinfection methods using the Research Randomizer Program (available at http://www.randomizer.org) by one of the investigators. Because of the nature of the interventions, the other clinician who performed the endodontic treatment procedures was not blinded to the interventions. However, data analysis was performed by an external person who was blind to the treatment group. Blinding of patients is not relevant as this is not a patient-reported outcome measure.

Aseptic techniques were used strictly during sampling from root canals. After an oral rinse with 0.12% chlorhexidine for 1 min tooth was isolated with a rubber dam. 3% hydrogen peroxide and 2.5% NaOCl were used to clean the tooth, clamp, and rubber dam. Then access cavity preparation was performed with sterile burs under sterile saline irrigation. Before entrance to the root canal, the tooth was disinfected once again as described previously [12].

Previous obturation materials were removed by using D1, D2, and D3 files of the ProTaper Universal Retreatment system (Dentsply Sirona, Ballaigues, Switzerland) according to the manufacturer's recommendation using an endodontic motor (X-Smart; Denstply Maillefer, Ballaigues, Switzerland). To avoid any potential antimicrobial activity of the solvent, sterile saline solution was used as irrigant in this step. The working length (WL) of the root canal was determined via an apex locator (Root ZX mini, Morita, Kyoto, Japan) and confirmed by periapical radiographs. To take bacterial sample root canal was filled with sterile saline. A size 10 K-type file was inserted into the root canal and was gently moved on the canal walls. Three sterile paper points were used to take samples. Each paper points left for about one minute and an initial bacterial sample (S1) was taken from the root canal as described in a previous study [12]. Paper points were put into cryotubes containing RNA later (RiboSaver; Geneall Biotechnology Co., Seoul, Korea), and stored at 4°C for 12 h. Then, samples were frozen at − 20°C. Patients with E. faecalis positive S1 according to the qPCR assay results were included in the study.

Chemomechanical preparation was completed at a single visit in all cases using ProTaper Next system (Dentsply Maillefer) up to size X3. The sequence of instruments was used according to the manufacturer's directions. 2 ml of 2.5% NaOCl was used with a 30-G needle after each instrument change. 2 ml 2.5% NaOCl and 3 ml 17% EDTA for 1 min were used for removing smear layer. To inactivate any residual effect of NaOCl, each canal was flushed with 1 ml 10% sodium thiosulfate for 1 min. A postinstrumentation sample (S2) was taken from the root canal as described previously.

Following the chemomechanical preparation disinfection methods were applied to the participants.

Passive ultrasonic irrigation group

A volume of 2 ml 2.5% NaOCl was ultrasonically activated in root canal for 1 min by using IrriSafe tip with an ultrasonic device (VDW ULTRA; VDW GmbH, Munich, Germany). Then, the canal was flushed with 1 ml 10% sodium thiosulfate for 1 min and S3 sample was taken as described previously.

Manuel dynamic activation group

F4 Pro-Taper Gutta-Percha Point (Dentsply Maillefer) placed to WL was then moved in push–pull motions for 30 s at an approximate frequency of 100 times per minute.

Root canals were filled with 2 ml 2.5% NaOCI, and a well-fitting X3 ProTaper Next gutta-percha point (Dentsply Maillefer) placed to WL. Then, gutta-percha was moved in up and down motions at a rate of 100 strokes per minute [19] and S3 sample was taken as described previously.

Photodynamic therapy group

A volume of 0.5 ml of 0.01% methylene blue (MB) was left in the root canal for 5 min, then radiated by the light supply of diode laser AMD Picasso (ABD; Indianapolis, Indiana, USA) with a wavelength of 810 nm for 40 s (0.2 W) [18]. Laser beam was directed into the canal by the fiber optic cone with a diameter of 200 μm. The tip of the fiber optic cone was placed at 1 mm short from WL. After radiation for 10 s, the tissues relaxed for 10 s. The final microbiological sample S3 was obtained described as previously after washing the MB solution from the root canal with sterile saline.

Following disinfection methods, 2% chlorhexidine gluconate was used for final irrigation of root canals. Then, the root canals were dried and obturated with X3 gutta percha in conjuction with Adseal (Metabiomed, Seoul, South Korea) root canal sealer. Final coronal restorations were performed at the same appointment.

DNA extraction and quantitative real-time PCR analysis

The frozen samples were thawed to room temperature and vortexed, and the microbial suspension was washed three times in ultrapure water by centrifugation. Pellets were resuspended in 100 μl of ultrapure water, and DNA was extracted using the QIAamp DNA mini-kit (QIAGEN Inc., GmbH, Hilden, Germany) following the protocol recommended by the manufacturer. To quantify the total bacterial load and levels of E. faecalis before and after treatment procedures, 16S ribosomal RNA gene-targeted qPCR was used. The qPCR was performed with Power SYBR Green PCR Master Mix (Applied Biosystems, Foster City, California, USA) on a Step OnePlus real-time PCR (Applied Biosystems). Total reaction volume was 20 μl. Each reaction included 10 μl of Power SYBR Green PCR Master Mix, 3.5 μl of sterile distilled water, 1 μl primer, and 4-μl DNA template. 16S rRNA-directed species-specific primers were a forward 5'–3' ATCAAGTACAGTTAGTCT and a reverse 5'–3' ACGATTCAAAGCTAACTG. All measurements were taken in triplicate for samples and standards. Fluorescence measurements were taken and StepOne Software v2.3 (Applied Biosystems) was used to acquire and analyze the data.

Statistical analysis

Comparison of the bacterial reduction was analyzed for intragroups and intergroups. Comparisons among the disinfection groups (PUI, MDA, and PDT) were performed by using Kruskal–Wallis test. Friedman test was performed to compare the amount of microorganisms at different sampling times. Wilcoxon test was used when significant differences were found between different sampling times. Significance level was set at 5% (P ≤ 0.05).

  Results Top

Obtained data are shown in [Table 1]. Changes in bacterial load in all sampling times (S1, S2, and S3) are shown in [Figure 2].
Table 1: Mean±SS, median, and percentage reductions of Entrococcus faecalis in different sampling times (CFU/ml) (S1, S2, and S3)

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Figure 2: Bacterial load change at different sampling times in experimental groups.

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Intragroup analysis

A significant decrease was found between S1 and S2 considering bacterial load in all experimental groups (P ≤ 0.05). A decrease in bacterial load between S2 and S3 was found in all experimental groups. However, this was significant for only PDT group (P ≤ 0.05).

Intergroup analysis

No significant differences were found among groups at the three sampling times (S1, S2, and S3) considering bacterial load. No significant differences were found among groups in terms of E. faecalis reduction percentages (from S1 to S2 and from S2 to S3) (P ≥ 0.05).

  Discussion Top

This clinical study evaluated the effect of different disinfection methods on the elimination of E. faecalis in teeth with post-treatment apical periodontitis by using PCR. Findings revealed that in all experimental groups, samples taken after chemomechanical preparation (S2 samples) showed a significant reduction in the levels of E. faecalis compared to S1 samples. This means that chemomechanical preparation along with irrigation of 2.5% NaOCl was effective in reducing the initial bacterial load regardless of the disinfection methods. This result is consonance with a previous study that has shown the effectiveness of preparation procedures in reducing E. faecalis from previously treated teeth [22]. Ferrer-Luque et al. [22] reported that reduction of E. faecalis from infected root canals by mechanical debridement along with irrigation is ranged from 95.9 to 100% by using nickel titanium rotary files.

PUI is one of the most preferred irrigation activation technique to improve removal of bacteria [23], smear layer [24], and calcium hydroxide [25] from root canal walls. Present study results showed that PUI did not significantly succeeded in reduction of E. faecalis after chemomechanical preparation (S2–S3 count). The mean percentage reduction of S2–S3 was 19% in the present study. This reduction in bacterial counts was statistically lower than chemomechanical preparation (65%) and this result is in consonance with other studies [26],[27].

Sampling method may be the one of the reasons for insignificant improvement in disinfection after PUI, because it only provides information about the bacterial load of the main canal [26]. In the present study to standardize the potential effect of chemomechanical preparation on the bacterial reduction, root canals were prepared up to size #30 at the WL in all experimental groups. It may be concluded that this apical enlargement did not allow enough space for free displacement amplitude of the ultrasonic instrument.

MDA depends on the up and down movements of a well-fitting gutta-percha point inside the root canal. Several studies reported the effectiveness of MDA in cleaning of the root canal walls [19],[20],[21]. However, its effectiveness in elimination of bacteria has not been studied yet. Due to the lack of studies evaluating the effectiveness of MDA on bacterial elimination, the results of this in-vivo study were compared with the findings of in-vitro studies investigating its cleaning efficiency of root canal walls.

Results of the present study revealed that MDA technique did not significantly reduce E. faecalis counts after chemomechanical preparation. The percentage reduction was 19% in MDA group as obtained in PUI group. Data from ex-vivo studies evaluating the cleaning effectiveness of MDA have been inconclusive [28],[29]. In a previous report, MDA showed better results than conventional needle irrigation in terms of cleaning root canal [28]. In another previous research, no significant differences were found between manual dynamic agitation and PUI in terms of penetration of sodium hypochlorite into dentinal tubules [29]. The activation time and total volume of irrigant and root morphology may have led to the differences in effectiveness of MDA shown in these studies.

According to the results of intragroup analysis, PDT was the only disinfection methods that was significantly succeeded in reduction of bacterial counts after chemo-mechanical preparation (S2-–S3). The protocol for PDT application was based on the reaction of photosensitizer agent with molecular oxygen. The production of reactive oxygen species that formed at the end of reaction induces death of E. faecalis. In several in-vitro studies, wavelengths of diode laser were ranged between 625 and 805 nm [30],[31],[32]. However, recently, an 810 nm diode laser was used in an in-vivo study by Asnaashari et al. [18]. They reported that PDT with diode laser 810 nm could evidently decrease the amount of E. faecalis in root canals [18].

In a previous research, Carvalho Edos et al. [33] showed that even low concentrations of MB were able to penetrate into the dentinal tubules after PDT. Therefore, in the present study, a low concentration (0.01%) MB was used as a photosensitizer agent with 810 nm diode laser with an optical fiber with a diameter of 200 μm.

According to the results of the present study the percentage reduction of S2–S3 was 46% in PDT. PDT has been reported as a promising approach and excellent bactericidal potential against E. faecalis in several studies [34],[35],[36],[37]. Garcez et al. [34] reported that E. faecalis was significantly reduced following chemomechanical treatment with adjunct PDT compared to chemomechanical treatment alone.

Percentage reductions from S2 to S3 and from S1 to S3 in PUI, MDA, and PDT groups showed that all techniques provided reduction in E. faecalis load, however any of these techniques were not able to eliminate E. faecalis completely. These results revealed that bacteria were still in root canal even though disinfection approaches were used. However, it is important to point out that to achieve an optimal outcome, maximal reduction of the bacterial load is necessary to be compatible with periradicular tissue healing [26].

Within the limitation of this in-vivo study, results revealed that all disinfection methods were effective in reducing E. faecalis from infected root canals with no statistical differences. PDT could evidently decrease the amount of E. faecalis in root canals after chemomechanical preparation.

  Conclusion Top

Photodynamic therapy (PDT) significantly enhanced E. faecalis elimination after chemomechanical preparation. All disinfection methods were effective in reducing E. faecalis from infected root canals with no statistical differences.


This study was supported by the funds of Scientific Research and Project Unit of Zonguldak Bülent Ecevit University (grant number: 2016–27194235–02).

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2]

  [Table 1]


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