Comparison of the antimicrobial reduction effect of photodynamic inactivation with the addition of chlorophyll and curcumin photosensitizer in <i>Aggregatibacter actinomycetemcomitans</i> and <i>Enterococcus faecalis </i>

Deny Arifianto; Suryani Dyah Astuti; Sarah Ratri Medyaz; Septia Budi Lestari; Samian Samian; Dezy Zahrotul Istiqomah Nurdin; Dita Ayu Hariyani; Yunus Susilo; Ardiansyah Syahrom

doi:10.12688/f1000research.128483.1

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Research Article

Comparison of the antimicrobial reduction effect of photodynamic inactivation with the addition of chlorophyll and curcumin photosensitizer in Aggregatibacter actinomycetemcomitans and Enterococcus faecalis

[version 1; peer review: 1 approved with reservations]

Deny Arifianto¹, Suryani Dyah Astuti ², Sarah Ratri Medyaz², [...] Septia Budi Lestari², Samian Samian², Dezy Zahrotul Istiqomah Nurdin³, Dita Ayu Hariyani², Yunus Susilo⁴, Ardiansyah Syahrom⁵

Deny Arifianto¹, Suryani Dyah Astuti ², [...] Sarah Ratri Medyaz², Septia Budi Lestari², Samian Samian², Dezy Zahrotul Istiqomah Nurdin³, Dita Ayu Hariyani², Yunus Susilo⁴, Ardiansyah Syahrom⁵

PUBLISHED 07 Feb 2023

Author details Author details

¹ Doctoral Degree, Faculty of Science and Technology, Airlangga University, Surabaya, East Java, 60115, Indonesia
² Department of Physics, Faculty of Science and Technology, Airlangga University, Surabaya, East Java, 60115, Indonesia
³ Magister of Biomedical Engineering, Faculty of Science and Technology, Airlangga University, Surabaya, East Java, 60115, Indonesia
⁴ Faculty of Engineering, Dr Soetomo University, Surabaya, East Java, 60115, Indonesia
⁵ Medical Devices and Technology Centre, Universiti Teknologi Malaysia, Johor Bahru, Johor, 81310, Malaysia

Deny Arifianto
Roles: Data Curation, Methodology, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

Suryani Dyah Astuti
Roles: Conceptualization, Formal Analysis, Funding Acquisition, Methodology, Project Administration, Supervision, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

Sarah Ratri Medyaz
Roles: Conceptualization, Data Curation, Investigation, Methodology, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

Septia Budi Lestari
Roles: Conceptualization, Data Curation, Investigation, Methodology, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

Samian Samian
Roles: Conceptualization, Formal Analysis, Investigation, Methodology, Supervision, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

Dezy Zahrotul Istiqomah Nurdin
Roles: Conceptualization, Data Curation, Investigation, Methodology, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

Dita Ayu Hariyani
Roles: Conceptualization, Data Curation, Investigation, Methodology, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

Yunus Susilo
Roles: Conceptualization, Data Curation, Investigation, Methodology, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

Ardiansyah Syahrom
Roles: Conceptualization, Investigation, Methodology, Supervision, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

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This article is included in the Plant Science gateway.

Abstract

Background: Aggregatibacter actinomycetemcomitans and Enterococcus faecalis are pathogenic bacteria of the oral cavity that cause various diseases such as periodontitis and endodontics. These bacteria are easily resistant to antibiotics. Photodynamic inactivation (PDI) is a method of inactivating microorganisms that utilizes light to activate a photosensitizer agent (PS) that produces reactive oxygen species causing cell lysis.
Methods: This study used the PDI method with a 405 nm diode laser at various energy density with the addition PS curcumin or chlorophyll Alfalfa, as much as 1.6 mg/ml on A. actinomycetemcomitans and E. faecalis bacteria.
Results: The study on E. faecalis bacteria showed that the energy density diode laser irradiation of 1.59 J/cm² gave the percentage of E. faecalis bacteria death 36.7% without PS, 69.30% with the addition of chlorophyll Medicago sativa L and 89.42% with the addition of curcumin. Meanwhile, the bacteria A. actinomycetemcomitans showed that the energy density diode laser irradiation of 1.59 J/cm² gave the percentage of bacterial death 35.81% without PS, 64.39% with the addition of chlorophyll Medicago sativa L and 89.82% with the addition of curcumin. PS was critical to the success of the PDI.
Conclusions: The addition of PS curcumin increased the effectiveness of reducing bacteria E. faecalis and A. actinomycetemcomitans compared to chlorophyll Medicago sativa L.

Keywords

Aggregatibacter actinomycetemcomitans, Enterococcus faecalis, photodynamic inactivation, diode laser, diseases, periodontitis, curcumin, chlorophyll

Corresponding author: Suryani Dyah Astuti

Competing interests: No competing interests were disclosed.

Grant information: This work was supported by Grant Support International Collaborative Research Scheme [175/UN3.15/PT/2022].
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2023 Arifianto D et al. 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.

How to cite: Arifianto D, Astuti SD, Medyaz SR et al. Comparison of the antimicrobial reduction effect of photodynamic inactivation with the addition of chlorophyll and curcumin photosensitizer in Aggregatibacter actinomycetemcomitans and Enterococcus faecalis [version 1; peer review: 1 approved with reservations]. F1000Research 2023, 12:142 (https://doi.org/10.12688/f1000research.128483.1) First published: 07 Feb 2023, 12:142 (https://doi.org/10.12688/f1000research.128483.1) Latest published: 04 Apr 2025, 12:142 (https://doi.org/10.12688/f1000research.128483.4)

Introduction

The oral cavity is one of the most important parts of the body that must be maintained. Infectious diseases of the teeth and mouth that are often found are periodontitis and endodontics. Periodontitis is a bacterial infection of the teeth that causes inflammation of the supporting tissues of the teeth, which include the gingiva, ligaments, cement, and alveolar bone.¹ Periodontitis is caused by pathogenic bacteria, predominantly gram-negative, anaerobic, or microaerophilic in the subgingival area.² Aggregatibacter actinomycetemcomitans bacteria are found in dental plaque, periodontal pockets, and buccal mucosa in up to 36% of the normal population.³ Aggregatibacter actinomycetemcomitans bacteria can infect patients when the human immune system decreases and inhibits other organisms' growth in the oral mucosa, teeth, and nasopharynx.

In general, gram-positive bacteria, Enterococcus faecalis (E. faecalis), are found in the root canals of teeth. The bacterium Enterococcus faecalis is ovoid, with a diameter between 0.5 and 1 μm.⁴ These bacteria are facultative anaerobes and can survive in extreme environments such as highly alkaline pH and high salt concentration conditions. The number of these bacteria in the human body can be minimized by paying attention to the food consumed and environmental conditions such as humidity. Furthermore, E. faecalis bacteria resist calcium hydroxide and antibiotics such as tetracycline.⁵ Systemic treatment in the form of antibiotics has been widely used to treat periodontitis. However, several studies have reported cases of antimicrobial resistance to certain types of antibiotics. So alternative therapy is needed that is effective and does not cause antibiotic resistance.⁶ Therefore, the recommended alternative therapy in this study is photodynamic inactivation (PDI).

Photodynamic inactivation (PDI) is a method of inactivating microorganisms by utilizing light to activate a photosensitizer (PS) agent that produces reactive oxygen species (ROS), causing cell lysis.⁷^,⁸ The suitability of the light spectrum with the PS absorption spectrum is the key to photophysical reactions, namely the absorption of light energy by PS agents, which will trigger photochemical and photobiological reactions to produce antimicrobial effects⁹^,¹⁰ and biomodulation.¹¹ PS is a light-sensitive molecule that plays a role in absorbing light energy. PS is divided into two types, namely endogenous and exogenous photosensitizers. The addition of exogenous PS aims to increase the effectiveness of light energy absorption.¹² Some natural ingredients that are exogenous PS include chlorophyll and curcumin. Chlorophyll is a green substance found in green plants that photosynthesizes.¹³ In photosynthesis, chlorophyll acts as a light catcher, energy transfer, and light conversion and can absorb a maximum wavelength between 400-700 nm.¹⁴ Curcumin is a curcuminoid compound with yellow pigment in turmeric rhizome, which is antitumor, antioxidant, anticarcinogenic, anti-inflammatory, antiviral, antifungal, antispasmodic, and hepatoprotective.¹⁵ The absorption spectrum of curcumin is in the wavelength range of 375-475 nm.¹⁶

Previous studies have reported the effectiveness of using PS chlorophyll in alfalfa leaves with a blue LED activator of 20.48 J/cm2 for the inactivation of A. actinomycetemcomitans bacteria by 81%.¹⁷ The results of another study with the addition of PS curcumin and diode laser activator 403 nm 15.83 J/cm2 in Staphylococcus aureus resulted in a mortality rate of 85.48%.¹⁶ Then, another study using curcumin and blue LEDs on S. aureus bacteria resulted in a mortality rate of 91.49%.¹⁸ Continuing previous studies,¹⁵^,¹⁶^,¹⁸ this study aims to compare the effectiveness of antimicrobial reduction from photodynamic inactivation (PDI) on bacteria A. actinomycetemcomitans and E. faecalis with PS curcumin and chlorophyll Medicago sativa L. using a 405 nm diode laser. Diode laser irradiation was carried out at various lengths of irradiation time, namely (30, 60, 90, 120, 150, and 180) seconds.

Methods

Bacterial culture

Bacteria A. actinomycetemcomitans ATCC 43718 and E. faecalis ATCC 29212 were cultured in Tryptone Soy Broth (TSB). Then, they were incubated for 24 hours at 37^oC until the colonies reached ~108 CFU/mL or 1.0 McFarland standard. The culture was placed 100 L on 96-well microplates and incubated for 48 hours.

Photosensitizer (PS)

Chlorophyll was extracted from Medicago sativa L (K-Link liquid, Indonesia) and Curcuma standard (Sigma Aldrich) with a concentration of 1.6 mg/ml diluted with sterile normal saline. The absorption spectrum of chlorophyll was measured using Shimadzu UV-VIS 1800 spectrometer.

Light source

The light source of a laser diode is 405 nm, and characterization was carried out using Jasco CT–10 monochromators to determine the peak wavelength. The power output was 2.49 mW, measured with power meter OMM-6810B-220V. The spot beam area size was 0.28 cm². Diode laser irradiation was carried out with variations in the length of the irradiation time of 30, 60, 90, 120, 150, and 180 seconds. The energy density value can be calculated using equation 1⁹:

(1)

Energy Density (J . {cm}^{- 2}) = Intensity (W . m^{- 2}) \times Irradiation Time (s)

PDI treatment

The treatment samples consisted of two types of bacteria, A. actinomycetemcomitans and E. faecalis. The bacterial PDI treatment consisted of a negative control group without treatment (T0), a positive control group with the addition of chlorophyll and curcumin (T1), a 405 nm diode laser treatment group at various energy densities of 0.26; 0.53; 0.79; 1.06; 1.32; 1.59 J/cm² (S1), a 405 nm diode laser treatment group with the addition of chlorophyll Medicago sativa L 1.6 mg/ml (S2), and a 405 nm diode laser treatment group with the addition of curcumin PS 1.6 mg/ml (S3). In groups S2 and S3, samples were given chlorophyll or curcumin and they were incubated for 10 minutes, then irradiated with 405 nm diode laser with an exposure time (30, 60, 90, 120, 150, and 180 seconds). The treated samples were grown on TSA media, incubated for 24 hours at 37C, and the number of bacterial colonies grown was counted by the Total Plate Count method.

Statistical analysis

Each treatment was calculated as CFU/ml using equation 2. Next, the percentage of bacterial reduction was calculated using equation 3 based on the control group. The results of bacterial reduction were statistically analyzed by ANOVA test using IBM SPSS Statistics Version 21.

(2)

\frac{CFU}{ml} = \frac{number of colonies \times dilution factor}{volume of culture plate}

(3)

%Viability reduction of bacteria = [\frac{\sum \frac{CFU}{ml} (control) - \sum \frac{kCFU}{ml} (treatment)}{\sum \frac{CFU}{ml} (control)}] \times 100 %

Results

The chlorophyll and curcumin extracts were tested using UV-Vis at a wavelength range of 325 nm to 705 nm to determine the absorption spectrum of light. Then, the results of the characterization of the absorption spectrum of chlorophyll and curcumin to light are obtained, as shown in Figures 1 and 2. Based on Table 1, the characterization results show the peak wavelength of the laser diode at 405 nm with the stability of the output power at a distance of 1 cm (2.49 ±0.07) mW. The temperature characterization showed the optimum temperature stability (26.60±0.01)^oC for bacterial growth. Thus, the irradiation energy density of the laser diode is 405 nm with an output power of 2.49 mW and a beam area of 0.28 at various exposure times (30, 60, 90, 120, 150, 180) seconds are 0.26; 0.53; 0.79; 1.06; 1.32 and 1.59 J/cm².

Figure 1. Graph of curcumin absorption spectrum.

Figure 2. Graph of Chlorophyll Absorption Spectrum.

Table 1. Laser energy density at various time exposure.

Laser parameters
Parameter	Value
Emitter type	Laser Diode
Center wavelength	405 ± 0,02 nm
Operating mode	Continuous wave (CW)
Polarization	Linear
Beam spot size at target	≈ 2.80 ± 0.01 mm²
Beam divergence	≈ 12^o parallel to beam ≈ 26^o perpendicular to the beam
Application technique	Distance 1 cm
Aperture diameter	1.89 mm
Power	2.49 ± 0,01 mW
Beam shape	elliptical
Variation in laser exposure time	30; 60; 90; 120; 150 and 180 s
Spectral bandwidth	10 nm
Average radiant power	2.49 ± 0,01 mW
Variation in radiant exposure/energy density	0.26; 0.53; 0.79; 1.06; 1.32; 1.59 J/cm²
Area irradiated	2.80 mm²
Variation in radiant energy	0.075; 0.15; 0.22; 0.29; 0.37; 0.45 J

After that, antibacterial tests were carried out on Aggregatibacter actinomycetemcomitans and Enterococcus faecalis bacteria, which were exposed to a diode laser with and without a photosensitizer. The viability of the bacteria Aggregatibacter actinomycetemcomitans and Enterococcus faecalis are shown in Figures 3 and 4. Based on bacterial viability, the percentages of death of A. actinomycetemcomitans and E. faecalis bacteria by diode laser irradiation with the addition of curcumin photosensitizer and Medicago sativa L chlorophyll treatment are shown in Figures 5 and 6.

Figure 3. Graph of bacterial viability of A. actinomycetemcomitans in various treatments with and without the addition of curcumin and chlorophyll Medicago sativa L.

Figure 4. Graph of bacterial viability of E. faecalis in various treatments with and without the addition of curcumin and chlorophyll Medicago sativa L.

Figure 5. Graph of the percentage of death of A. actinomycetemcomitans bacteria in various treatments with and without the addition of curcumin and chlorophyll Medicago sativa L.

Figure 6. Graph of the percentage of death of E. faecalis bacteria in various treatments with and without the addition of curcumin and chlorophyll Medicago sativa L.

Based on the results of statistical tests, it was shown that diode laser irradiation with an energy density of 1.59 J/cm² gave a percentage of E. faecalis bacteria death of 36.7% without adding a photosensitizer. Then, the percentage of death of E. faecalis bacteria was 69.30% with the addition of PS chlorophyll Medicago sativa L. and 89.42% with the addition of PS curcumin. Meanwhile, the results of statistical tests on bacteria A. actinomycetemcomitans with diode laser irradiation at an energy density of 1.59 J/cm² gave the percentage of bacterial death of 35.81% without the addition of PS. Then, the death of A. actinomycetemcomitans was 64.39% with the addition of PS chlorophyll Medicago sativa L and 89.82% with the addition of PS curcumin.was 64.39% with the addition of PS chlorophyll Medicago sativa L and 89.82% with the addition of PS curcumin.

Discussion

This research was conducted using the PDI technique using a blue diode laser as a light source, chlorophyll Medicago sativa L and curcumin as PS to reduce bacteria E. faecalis and A. actinomycetemcomitans. The wavelength of light is an important factor in the photoinactivation process. The laser diode used in this study has a wavelength of 405 nm and output power of 2.49 mW. The results of the characterization of power against time and temperature show the stability of power and temperature so that the temperature factor does not cause the death of bacteria.

PS is a light-sensitive molecule. Exogenous PS is PS that is added to assist the photoinactivation process. This study used exogenous PS chlorophyll Medicago sativa L and curcumin. Medicago sativa L chlorophyll absorbance used for a laser wavelength of 405 nm was 85.1% and for curcumin was 80.64%.¹⁸ The photoinactivation process occurs due to a photophysical mechanism initiated by the absorption of light by PS. The energy of the absorbed photon will cause the excitation of the electron to increase to a higher energy level. If the energy excitation state overlaps with the triplet excitation state, an intersystem crossing occurs, a spin reversal that places the electron in a triplet excited state and triggers a photochemical reaction.

Photochemical reactions are divided into two types. The first type is the transfer of electrons to a biological substrate in the form of a redox reaction and produces singlet oxygen. The second type is the transfer of energy to the triplet electrons to produce singlet oxygen. Singlet oxygen is radical. If attached to lipids and membrane proteins, it will cause peroxidation and damage cell membranes, causing leakage and cell lysis.¹⁸ The photochemical reactions in PDI are generally of the second type.

The study's results on E. faecalis bacteria showed a significant difference between treatments. Diode laser irradiation with an energy density of 1.59 J/cm² gave the percentage of bacterial death of E. faecalis 36.7% without the addition of PS, 69.30% with the addition of PS chlorophyll Medicago sativa L and 89.42% with the addition of PS curcumin. Meanwhile, in A. actinomycetemcomitans bacteria with energy density diode laser irradiation 1.59 J/cm², the percentage of bacterial death was 35.81% with the addition of PS, 64.39% with the addition of PS chlorophyll Medicago sativa L and 89.82% with the addition of PS curcumin.

The results showed that adding PS curcumin increased the effectiveness of reducing E. faecalis and A. actinomycetemcomitans bacteria. PDI with PS curcumin was effectively used to reduce bacteria because its absorption followed endogenous porphyrins.¹⁹ The addition of energy density will increase the reduction effect without and with the addition of PS Medicago sativa L¹⁷ and curcumin.¹⁸

Conclusion

Based on statistical tests, the results of research on E. faecalis bacteria showed that laser irradiation with an energy density of 1.59 J/cm² gave a percentage of E. faecalis bacteria mortality of 36.7% without the addition of PS, 69.30% with the addition of PS chlorophyll Medicago sativa L and 89.42% with the addition of PS curcumin. Meanwhile, A. actinomycetemcomitans showed that the energy density diode laser irradiation of 1.59 J/cm² gave the percentage of bacterial death 35.81% without the addition of PS, 64.39% with the addition of PS chlorophyll Medicago sativa L and 89.82% with the addition of PS curcumin. So it can be concluded that the role of PS is significant for the success of PDI. The addition of PS curcumin increased the effectiveness of reducing bacteria E. faecalis and A. actinomycetemcomitans compared to chlorophyll Medicago sativa L.

Author contributions

DA contributes to the data curation, methodology, validation, original draft preparation of the work and editing of the work. SDA contributes to the conception, methodology, analysis, funding acquisitions, project administration, supervision, validation, review, original draft preparation of the work and editing of the work. SRM, SBL, DZIN, and DAH contribute to the conception, data curation, methodology, investigation, validation, original draft preparation of the work and editing of the work. S contributes to the conception, methodology, investigation, analysis, supervision, validation, review, original draft preparation of the work and editing of the work. YS contributes to the conception, data curation, methodology, investigation, validation, original draft preparation of the work and editing of the work. AS contributes to the conception, methodology, analysis, supervision, validation, review, original draft preparation of the work and editing of the work.

Data availability

Underlying data

Open Science Framework: Antimicrobial Reduction Effect of Photodynamic Inactivation with The Addition Photosensitizer. https://doi.org/10.17605/OSF.IO/BEZ2R.²⁰

This project contains the following files:

- Table 1. Laser energy density at various time exposure.docx (The laser parameters used in this research)
- Bacterial Treatment Group Aggregatibacter actinomycetemcomitant
- • CFU Calculation Aggregatibacter actinomycetemcomitant.xlsx
- • Excel of Bacterial Viability.xls
- • Graph of Bacterial Viability.jpg
- Bacterial Treatment Group Enterococcus faecalis
- • CFU Calculation Bacterial Treatment Group Enterococcus faecalis.xlsx
- • Excel of Bacterial Viability.xls
- • Graph of Bacterial Viabilty.jpg

Extended data

Open Science Framework: Antimicrobial Reduction Effect of Photodynamic Inactivation with The Addition Photosensitizer. https://doi.org/10.17605/OSF.IO/BEZ2R.²⁰

This project contains the following extended data:

- Figure 1. Graph of curcumin absorption spectrum.jpg
- Figure 2. Graph of Chlorophyll Absorption Spectrum.jpg.
- Figure 3. Graph of bacterial viability of A. actinomycetemcomitans in various treatment.jpg.
- Figure 4. Graph of bacterial viability of E. faecalis in various treatment.jpg.
- Figure 5. Graph of the percentage of death of A. actinomycetemcomitans.jpg.
- Figure 6. Graph of the percentage of death of E. faecalis.jpg
- Equipment used during the research.docx
- The materials used during the research.docx
- Treatment process.docx

Data are available under the terms of the Creative Commons Attribution 4.0 International license (CC-BY 4.0).

Acknowledgements

We would like to thank Dr Riries Rulaningtyas for providing advice and supervision for this manuscript.

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