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Journal of Periodontal & Implant Science logoLink to Journal of Periodontal & Implant Science
. 2022 Sep 7;53(2):110–119. doi: 10.5051/jpis.2200920046

In vitro investigation of the antibacterial and anti-inflammatory effects of LED irradiation

Jungwon Lee 1,2, Hyun-Yong Song 1, Sun-Hee Ahn 3, Woosub Song 3, Yang-Jo Seol 1, Yong-Moo Lee 1,✉, Ki-Tae Koo 1,✉
PMCID: PMC10133822  PMID: 36468477

Abstract

Purpose

This study aimed to investigate the proper wavelengths for safe levels of light-emitting diode (LED) irradiation with bactericidal and photobiomodulation effects in vitro.

Methods

Cell viability tests of fibroblasts and osteoblasts after LED irradiation at 470, 525, 590, 630, and 850 nm were performed using the thiazolyl blue tetrazolium bromide assay. The bactericidal effect of 470-nm LED irradiation was analyzed with Streptococcus gordonii, Aggregatibacter actinomycetemcomitans, Fusobacterium nucleatum, Porphyromonas gingivalis, and Tannerella forsythia. Levels of nitric oxide, a proinflammatory mediator, were measured to identify the anti-inflammatory effect of LED irradiation on lipopolysaccharide-stimulated inflammation in RAW 264.7 macrophages.

Results

LED irradiation at wavelengths of 470, 525, 590, 630, and 850 nm showed no cytotoxic effect on fibroblasts and osteoblasts. LED irradiation at 630 and 850 nm led to fibroblast proliferation compared to no LED irradiation. LED irradiation at 470 nm resulted in bactericidal effects on S. gordonii, A. actinomycetemcomitans, F. nucleatum, P. gingivalis, and T. forsythia. Lipopolysaccharide (LPS)-induced RAW 264.7 inflammation was reduced by irradiation with 525-nm LED before LPS treatment and irradiation with 630-nm LED after LPS treatment; however, the effects were limited.

Conclusions

LED irradiation at 470 nm showed bactericidal effects, while LED irradiation at 525 and 630 nm showed preventive and treatment effects on LPS-induced RAW 264.7 inflammation. The application of LED irradiation has potential as an adjuvant in periodontal therapy, although further investigations should be performed in vivo.

Keywords: Bacteria, Fibroblast, Inflammation, Osteoblast, Photobiology, Phototherapy

INTRODUCTION

Periodontal treatment has traditionally focused on the mechanical removal of local factors, bacteria and calculus [1], which are the causative factors of chronic periodontitis. Despite the positive clinical outcomes of scaling and root planing (SRP) as a nonsurgical treatment of choice for periodontitis treatment [2,3], the limited access to tissues during nonsurgical treatment has resulted in the necessity of adjunctive treatment, including phototherapy, local or systemic antibiotics, host modulation drugs, and probiotics before SRP to improve clinical outcomes [4,5,6,7,8,9,10]. Among them, phototherapy aims to promote the effect of periodontitis treatment by exerting a bactericidal effect on microorganisms or a photobiomodulation effect on host cells [4,11,12].

It has been reported that the biological effects of light irradiation, including bactericidal and photobiomodulation effects, are dependent on the wavelength of the light. Blue light has been reported to show bactericidal effects on various bacteria [13,14]. Meanwhile, a photobiomodulation effect can be obtained from longer wavelengths of light [11,12,15]. In this context, phototherapy using multiple wavelengths of light exhibiting bactericidal and photobiomodulation effects could be applied in periodontitis treatment. However, to date, there is little evidence regarding how to optimize the wavelengths to improve the combination of bactericidal and photobiomodulation effects.

In recent years, incoherent light sources such as light-emitting diodes (LEDs) have become increasingly common for low-energy phototherapy [16,17]. Recent advances in LED technology have exhibited several advantages over lasers. LED technology has the advantages of being relatively safe, being suitable for wearable devices and home use, and irradiating large tissue areas at one time; furthermore, LED-based irradiation devices are less costly than laser devices. As light sources have expanded, including lasers and LEDs, the term “low-level laser therapy” has also changed to “low-level light therapy” [18]. Although LED irradiation can affect both bacteria and the hosts, research aiming to understand the cellular responses of both the host and bacteria is still lacking.

The aim of this study was to investigate the optimal wavelengths of LED irradiation to safely produce bactericidal and photobiomodulation effects in vitro.

MATERIALS AND METHODS

Cytotoxicity assessment of LED irradiation

Human gingival fibroblast and human osteoblast cell culture

Human gingival fibroblasts (ScienCell Research Laboratories, Carlsbad, CA, USA) and human osteoblasts (ScienCell Research Laboratories) were cultivated in fibroblast medium and osteoblast medium, respectively. All media were supplemented with 2% fetal bovine serum (FBS), 1% fibroblast growth supplement, and 1% penicillin/streptomycin. The cells were incubated at 37°C in a humidified atmosphere and 5% CO2. The culture medium was exchanged once every 2 days, and the cell line used for the experiment was used at the third subculture.

LED irradiation source and exposure protocol

A customized LED device was fabricated with a 5-wavelength source (470, 525, 590, 630, and 850 nm) (Figure 1). The size of the LED was 1×0.5 mm (1005), and a total of 225 LEDs were arranged in a 15×15 pattern. The area of the optical module was 25 cm2 (5×5 cm), and the number of LEDs per area was 9/cm2. The energy density (energy per unit area) irradiated at each wavelength was kept constant at 10 J/cm2. The distance from the light to the cells was 1 cm. The irradiation time was different at each wavelength of LED, according to the power density (10, 8, 42, 30, and 6 minutes at 470, 525, 590, 630, and 850 nm, respectively).

Figure 1. Experimental light source module manufactured with wavelengths of (A) 470 nm, (B) 525 nm, (C) 560 nm, (D) 630 nm, and (E) 850 nm. (F) Light-emitting diode (LED) arrangement diagram. The size of the LEDs was 1×0.5 mm (1005), and a total of 225 LEDs were arranged in a 15×15 pattern. The area of the optical module was 25 cm2 (5×5 cm), and the number of LEDs per area was 9/cm2.

Figure 1

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Viability test

Human gingival fibroblasts and human osteoblasts were seeded in 96-well plates (200 µL/well at a density of 5×103 cells/mL) and incubated at 37°C in a 5% CO2 atmosphere for 24 hours. The cells were treated with LED light according to the aforementioned LED irradiation conditions. Thereafter, the cells were incubated at 37°C in a 5% CO2 atmosphere for another 1, 3, and 7 days. The supernatant was discarded, and 50 µL of thiazolyl blue tetrazolium bromide (MTT) solution (Thermo Fisher Scientific, Waltham, MA, USA) was added to each well. Then, 200 µL of cell medium was added to each well and incubated at 37°C for another 3 hours. After the medium was aspirated, the formazan crystals were solubilized with 50 µL of dimethyl sulfoxide and left for 30 minutes at room temperature. The absorbance of the formazan was reported as the optical density, which was read at 540 nm by a microplate reader (PowerWave X340; BioTek, Winooski, VT, USA). The cell viability for each LED wavelength was expressed as a percentage relative to the untreated control cells.

Antibacterial effect of 470-nm LED

Microbial strains and culture conditions

The strains used in this study were Streptococcus gordonii (ATCC 10558), Aggregatibacter actinomycetemcomitans (ATCC 43718), Fusobacterium nucleatum (ATCC 43718), Porphyromonas gingivalis (ATCC 33277), and Tannerella forsythia (ATCC 43037). S. gordonii was incubated with brain heart infusion broth (BHI). A. actinomycetemcomitans was incubated with BHI at 37°C in an anaerobic workstation (10% CO2, 10% H2, and 80% N2). F. nucleatum and P. gingivalis were incubated with BHI including 10 µg/mL hemin (Sigma, St. Louis, MO, USA) and 0.2 μg/mL vitamin K (Sigma) at 37°C in an anaerobic workstation (10% CO2, 10% H2, and 80% N2). T. forsythia was incubated with new oral spirochete broth (ATCC medium 1494) including 5 mg/mL hemin (Sigma), 1 mg/mL vitamin K (Sigma) and 0.01 mg/mL N-acetylmuramic acid (Sigma) at 37°C in an anaerobic workstation (10% CO2, 10% H2, and 80% N2).

LED irradiation source and exposure protocol

In the customized LED device used for the cytotoxicity assessment of LED irradiation, a 470 nm wavelength light source was used because previous studies reported that blue light showed a bactericidal effect [13,14]. The energy density irradiated at each wavelength was kept constant at 10 J/cm2. The distance from the light to the cells was 1 cm. The control group of each bacterium was not irradiated.

Assessment of the antibacterial effect of 470 nm LED

The number of cells was adjusted with a microplate reader (PowerWave X340; BioTek) read at 600 nm. Each bacterium was seeded in 96-well plates (200 µL/well at a density of 1×107 CFU/mL) and subsequently treated with 470 nm wavelength LED light according to the aforementioned LED irradiation conditions for 10 minutes. Thereafter, the absorbance of each well was reported as the optical density read at 600 nm by a microplate reader (PowerWave X340; BioTek).

Anti-inflammatory effect of LED irradiation

Cell culture

Murine macrophage RAW 264.7 cells were used to investigate the anti-inflammatory effect of 525-nm and 630-nm wavelengths of LED irradiation. RAW 264.7 cells were cultured in Dulbecco’s modified Eagle’s medium supplemented with 10% FBS and 1% antibiotic-antimycotic solution (Thermo Fisher Scientific). The cells were incubated at 37°C in a humidified atmosphere and 5% CO2.

Experimental groups

RAW 264.7 cells were seeded in 96-well plates (200 µL/well at a density of 5×103 cells/mL) and incubated at 37°C in a 5% CO2 atmosphere for 24 hours. Lipopolysaccharide (LPS, 5 µg/mL, from Escherichia coli O111:B4; Sigma-Aldrich, St. Louis, MO, USA) was used for RAW 264.7 cell stimulation. LED light wavelengths of 525 nm and 630 nm were used to treat RAW 264.7 cells. The energy density at each wavelength was kept constant at 10 J/cm2. The irradiation time was 8, 42, 30, and 6 minutes at 525, 590, 630, and 850 nm, respectively. The experimental groups were as follows:

  • LED+/LPS+: LPS treatment 30 minutes after LED irradiation

  • LED−/LPS+: LPS treatment without LED irradiation

  • LPS+/LED+: LED irradiation 30 minutes after LPS treatment

  • LPS+/LED−: no LED irradiation 30 minutes after LPS treatment

  • LED+/LPS−: no LPS treatment but LED irradiation

  • LED−/LPS−: no LPS and no LED treatment

Measurement of nitric oxide production

Nitric oxide (NO) concentrations were measured in each experimental group to investigate the inflammatory reaction, since NO is a key mediator of the inflammatory response [19]. The amount of NO in the culture medium was measured using the Griess reagent (Promega, Madison, WI, USA). The standard curve was created using known concentrations of sodium nitrite (0–100 µM). Then, 100 µL of cell culture supernatant and 100 µL of the Griess reagent were mixed and reacted at room temperature in the dark for 10 minutes, and the absorbance was measured at 540 nm.

Statistical analysis

Fibroblast and osteoblast viability and NO production data were subjected to analysis of variance, followed by the Tukey test, and antibacterial data were analyzed with the t-test using statistical software (GraphPad; GraphPad LLC, San Diego, CA, USA). Data are expressed as the means and standard deviation and visualized using graphics. Statistical significance was set at 5% (P<0.05).

RESULTS

Cytotoxicity of LED irradiation on fibroblasts and osteoblasts

To identify whether LED irradiation is cytotoxic, LED irradiation at wavelengths of 470, 525, 590, 630, and 850 nm were compared with no LED irradiation. All of the viability data are presented in Figure 2.

Figure 2. Effect of each wavelength of LED irradiation on cell viability. (A) MTT assay of fibroblasts. (B) MTT assay of osteoblasts. Control: no LED irradiation; 470 nm: 470-nm LED irradiation; 525 nm: 525-nm LED irradiation; 590 nm: 590-nm LED irradiation; 630 nm: 630-nm LED irradiation; 850 nm: 850-nm LED irradiation. Data are presented as the mean ± standard deviation and bars. Asterisks indicate significant differences (P<0.05) compared to the control group during the same period.

Figure 2

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LED: light-emitting diode, MTT: thiazolyl blue tetrazolium bromide.

At day 1 and 3, fibroblasts did not show significant differences in absorbance (measured using optical density values). At day 7, the 630 and 850-nm groups presented significantly higher absorbance values than the control group (P=0.0060 and P=0.0032, respectively); however, the other wavelengths did not show any significant differences (Figure 2A). At day 1, 3, and 7, osteoblasts did not show significant differences in absorbance (Figure 2B).

Antibacterial effect of the 470-nm wavelength of LED irradiation

In a previous study, blue light was reported to show bactericidal effects on various bacteria [13,14]. In this study, we evaluated the antibacterial effect of 470-nm LED irradiation on S. gordonii, A. actinomycetemcomitans, F. nucleatum, P. gingivalis, and T. forsythia. As shown in Figure 3, 470-nm LED irradiation showed antibacterial effects on all bacteria. When irradiated with LED light at a wavelength of 470 nm, 71.0%, 94.7%, 95.4%, 76.9%, and 100% of S. gordonii, A. actinomycetemcomitans, F. nucleatum, P. gingivalis, and T. forsythia, respectively, were killed.

Figure 3. Antibacterial effect of 470-nm LED irradiation. The test and control groups indicate 470-nm LED irradiation and no LED irradiation. Data are presented as the mean ± standard deviation and bars. Asterisks indicate significant differences at P<0.05.

Figure 3

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LED: light-emitting diode.

Anti-inflammatory effect of LED irradiation

The results of NO production are shown in Figure 4.

Figure 4. Effect of each wavelength of LED irradiation on NO production. Data are presented as the mean ± standard deviation and bars. Different letters indicate significant differences between groups at P<0.05 within each wavelength.

Figure 4

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LED: light-emitting diode, NO: nitric oxide, LPS: lipopolysaccharide.

At 525 nm, significantly lower NO concentrations were observed in the LED+/LPS+ group than in the LED−/LPS+ group. No significant difference between the LPS+/LED+ and LPS+/LED− groups was observed. Significantly lower NO values were observed in the LED+/LPS− and LED−/LPS− groups than in the LED+/LPS+, LED−/LPS+, LPS+/LED+, and LPS+/LED− groups.

At 630 nm, there was no significant difference in the NO concentration in the LED+/LPS+ group compared to the LED−/LPS+ and LPS+/LED+ groups. A significantly lower NO level was observed in the LPS+/LED+ group than in the LPS+/LED− group (Figure 4). Significantly lower levels of NO were observed in the LED+/LPS− and LED−/LPS− groups than in the LED+/LPS+, LED−/LPS+, LPS+/LED+, and LPS+/LED− groups.

At 590 nm and 850 nm, no significant differences among the LED+/LPS+, LED−/LPS+, LPS+/LED+, and LPS+/LED− groups were observed. Significantly lower levels of NO were observed in the LED+/LPS− and LED−/LPS− groups than in the LED+/LPS+, LED−/LPS+, LPS+/LED+, and LPS+/LED− groups.

DISCUSSION

The optimization of the appropriate wavelength of LED is fundamental for achieving desirable applications of LED in clinical situations. Previous studies have addressed the applicable results of LED irradiation in periodontitis, but without endeavoring to understand the host and bacterial cell reaction together [11,13,14,15]. The focus of this study was to investigate the most effective and safe wavelengths of LED irradiation with bactericidal and photobiomodulation effects in vitro.

In this study, cytotoxicity assessments of LED irradiation at wavelengths of 470, 525, 590, 630, and 850 nm were performed using the MTT assay. In the group irradiated with LEDs of each wavelength, the optical density value did not decrease compared to the control on day 1, 3, and 7, suggesting that none of the LED irradiation protocols showed any cytotoxic effects. Interestingly, the optical density values of fibroblasts increased at 630 and 850 nm compared to the control group on day 7. According to previous studies [20,21], the proliferation of fibroblasts irradiated with infrared or red LED was inhibited, which is inconsistent with our study. The difference in the results might be due to the energy density of the LED irradiation. In previous studies energy densities higher than the 10 J/cm2 used in this study, such as 160 or 320 J/cm2, were applied. Another study showed that fibroblasts proliferated after LED irradiation with a low energy level of 1 J/cm2 or less, which supports this reasoning [22].

After applying 10 J/cm2 to osteoblasts, there was no significant difference in optical density values on day 1, 3, and 7 compared with the control group. The outcome of this study is consistent with the results of a previous study demonstrating that the viability of osteoblasts was not significantly affected by a 635-nm wavelength of LED irradiation [23]. However, in a previous study that applied a 940-nm wavelength LED, the application of low energy densities of 1 and 5 J/cm2 did not affect cell viability, whereas the application of 7.5 J/cm2 negatively affected cell viability [24]. Taken together, the biological outcomes can be different depending on the LED wavelength, energy density, and cell types. At an energy density of 10 J/cm2 used in this study, wavelengths of 470, 525, 590, 630, and 850 nm can be safely used for fibroblasts and osteoblasts. In addition, photobiomodulation effects can be expected at 630 and 850-nm wavelengths of LED in fibroblasts, which are involved in wound healing.

Blue light was explored in this study to investigate the bactericidal effect on S. gordonii, A. actinomycetemcomitans, F. nucleatum, P. gingivalis, and T. forsythia based on previous studies [13,14]. The 470-nm LED showed a bactericidal effect ranging from 71.0% to 100% on the 5 species in this study (Figure 3). Bacterial death through light irradiation was originally carried out with an exogenous photosensitizer. However, it has been reported that pigments such as porphyrin or other tetrapyrrole molecules in bacteria could act as endogenous photosensitizers, causing bacterial death only with light irradiation [25,26,27]. The bactericidal effect was confirmed in all included bacteria in this study following 470-nm LED irradiation with an energy density of 10 J/cm2. Endogenous porphyrin or other tetrapyrrole molecules seem to be photosensitizers, and blue-light LED exhibited a bactericidal effect by producing bactericidal reactive oxygen species, as in previous studies [28,29]. However, additional experiments will be needed in the future to determine whether the bactericidal effect is simply due to light irradiation or specifically due to LED irradiation at a wavelength of 470 nm.

Based on the significantly lower production of NO in RAW 264.7 cells in the LED+/LPS+ group than in the LED−/LPS+ group at 525 nm of LED irradiation, 525-nm LED irradiation might have a preventive effect on the process of LPS-induced inflammation. However, other wavelengths, including 590, 630, and 850 nm, did not show any difference in NO production between the LED+/LPS+ and LED−/LPS+ groups, suggesting that these wavelengths of LED had no preventive effect on LPS-induced inflammation. However, 630-nm LED irradiation resulted in significantly lower NO production in RAW 264.7 cells in the LPS+/LED+ group than in the LPS+/LED− group, suggesting that 630-nm LED irradiation might alleviate LPS-induced inflammation. However, other wavelengths, including 525, 590, and 850 nm, of LED irradiation did not show a treatment effect. However, the preventive effect of 525-nm LED irradiation and the treatment effect of 630-nm LED irradiation should be considered limited in their effectiveness, as the NO production was still higher than that in the control group (LED−/LPS−). Therefore, when trying to apply these wavelengths to elicit an anti-inflammatory response, they should be considered as an adjunct therapy in periodontal treatment. No significant differences were found between the LED+/LPS− and LED−/LPS− groups under any conditions; therefore, LED irradiation does not seem to induce inflammation.

Within these limitations, LED irradiation at wavelengths of 470, 525, 590, 630, and 850 nm showed no cytotoxic effects on fibroblasts or osteoblasts. LED irradiation at 630 and 850 nm might promote fibroblast proliferation. LED irradiation at 470 nm resulted in bactericidal effects on S. gordonii, A. actinomycetemcomitans, F. nucleatum, P. gingivalis, and T. forsythia. A preventive and treatment effect at 525 and 630-nm wavelengths of LED irradiation was observed in LPS-induced RAW 264.7 macrophages, although the effects were limited. The outcome of this study suggest the possibility of applying a combination of 525, 630, and 470-nm wavelengths of LED for the treatment of periodontitis.

This study has some limitations. First, only NO concentrations were measured to evaluate the anti-inflammatory effect. If pro-inflammatory mediators, including prostaglandin E2, tumor necrosis factor-α, or interleukin-6, were measured, the conclusions of this study could have been further strengthened. Second, since this study only involved in vitro experiments, there is a limitation in terms of interpreting the findings as applicable for real-world periodontitis treatment. It is necessary to further prove the biological efficacy and safety of LED irradiation at various wavelengths through in vivo experiments.

Footnotes

Funding: This work was supported by the Development of Advanced Technology for Electronic Systems Program – Optical Convergence for Human Care Technology Development Project (20010763, Development of oral care device with LED standard light source for oral health improvement) funded by the Ministry of Trade, Industry & Energy (MOTIE, Korea).

Conflict of Interest: No potential conflict of interest relevant to this article was reported.

Author Contributions:
  • Conceptualization: Ki-Tae Koo.
  • Data curation: Jungwon Lee, Hyung-Yong Song.
  • Formal analysis: Yang-Jo Seol, Yong-Moo Lee.
  • Investigation: Hyung-Yong Song, Sun-Hee Ahn, Woosub Song.
  • Methodology: Yang-Jo Seol, Yong-Moo Lee.
  • Project administration: Ki-Tae Koo.
  • Software: Jungwon Lee.
  • Validation: Jungwon Lee.
  • Writing - original draft: Jungwon Lee.
  • Writing - review & editing: Hyung-Yong Song, Sun-Hee Ahn, Woosub Song, Yang-Jo Seol, Yong-Moo Lee, Ki-Tae Koo.

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