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Anti-Oral Microbial Effect of Ethanol Extract of Angelica gigas Nakai
J Dent Hyg Sci 2024;24:54-61
Published online March 31, 2024;  https://doi.org/10.17135/jdhs.2024.24.1.54
© 2024 Korean Society of Dental Hygiene Science.

Soon-Jeong Jeong

Department of Dental Hygiene and Institute of Basic Science for Well-Aging, College of Health Science, Youngsan University, Yangsan 50510, Korea
Correspondence to: Soon-Jeong Jeong, https://orcid.org/0000-0002-8959-4663
Department of Dental Hygiene and Institute of Basic Science for Well-Aging, College of Health Science, Youngsan University, Junam-ro 288, Yangsan 50510, Korea
Tel: +82-55-380-9453, Fax: +82-55-380-9453, E-mail: jeongsj@ysu.ac.kr
Received February 28, 2024; Revised March 12, 2024; Accepted March 15, 2024.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Background: The Korean name for Angelica gigas Nakai (AGN) is Cham-dang-gui, which grows naturally or is cultivated, and its dried roots are used in traditional herbal medicines. The AGN root exert various pharmacological effects. Despite the various pharmacological effects of the AGN root, there are no reports on its anti-oral microbial effects. The purpose of this study was to reveal the anti-oral microbial effect and the microbial and biochemical changes in oral microorganisms according to the concentration of the ethanol extract of AGN (EAGN) root, and to confirm the possibility of using EAGN as a plant-derived functional substance for controlling oral infectious microorganisms.
Methods: Disk diffusion test, growth measurement, biofilm formation assay, and measurements of acid production and buffering capacity were performed to confirm the antibacterial effect of EAGN.
Results: EAGN showed anti-oral bacterial effects against Streptococcus mutans and Aggregatibacter actinomycetemcomitans at all concentrations, with S. mutans showing a more susceptible effect at concentrations above 5.0 mg/ml and A. actinomycetemcomitans at 3.75 mg/ml. EAGN treatment significantly reduced A. actinomycetemcomitans growth at all concentrations tested. Biofilm formation was significantly reduced at concentrations above 3.75 mg/ml for S. mutans and 2.5 mg/ml for A. actinomycetemcomitans. Acid production in S. mutans and A. actinomycetemcomitans was significantly increased by treatment with EAGN, and the buffering capacities of S. mutans and A. actinomycetemcomitans increased from an EAGN concentration of 3.75 mg/ml and above.
Conclusion: EAGN showed anti-oral bacterial effects against both S. mutans and A. actinomycetemcomitans at concentrations above 3.75 mg/ml, which were thought to be related to the inhibition of their growth and biofilm formation. Therefore, EAGN can be used as a safe functional substance derived from medicinal plants owing to its antibacterial effects against S. mutans and A. actinomycetemcomitans.
Keywords : Aggregatibacter actinomycetemcomitans, Angelica gigas Nakai, Anti-oral bacterial effect, Cham-dang-gui, Streptococcus mutans
Introduction

1.Background

The inhibition of microbial growth and biofilm formation is important to reduce oral infectious diseases1). Antibiotics have been used to control infectious diseases, and their intensive use has led to the emergence of resistant bacterial strains2,3). Antibiotics have also been used to effectively control oral infectious diseases, however, they have many side effects4). Medicinal plants used in traditional medicine are known to have various biological activities and are safe with minimal or no side effects5,6). Research and interest in medicinal plants as a resource for finding safe substances to control new pathogenic microorganisms is growing2,3). The development of safe plant-derived medicinal substances is necessary to effectively control oral infectious microorganisms4).

Angelica is classified into three species: the Korean species is Angelica gigas Nakai (AGN), the Chinese species is Angelica sinensis, and the Japanese species is Angelica acutiloba7). The Korean name for AGN is Cham-dang-gui, which grows naturally or is cultivated, and the dried roots are used in traditional herbal medicine prescriptions8). The AGN root is known to have various pharmacological effects, including anticancer, neuroprotective, anti-inflammatory, anemia and cardiovascular system, antioxidant, and improving immunity9). In addition, there have been no reports of the side effects of AGN10), and its safety has already been confirmed in animal11) and clinical12) studies. Despite the various pharmacological effects and safety profiles of AGN, there are few reports on its antimicrobial effects. In particular, there are no reports on the anti-oral microbial effects of AGN.

2.Objectives

The purpose of this study was to reveal the anti-oral microbial effect and the microbial and biochemical changes in oral microorganisms according to the concentration of the ethanol extract of AGN (EAGN) root, and to confirm the possibility of using EAGN as a plant-derived functional substance for controlling oral infectious microorganisms.

Materials and Methods

1.Study design

1) Preparation of EAGN

Dried AGN roots were purchased from Goodherb Co. (Seoul, Korea) and used for ethanol extract. AGN roots (500 g) were subjected to extraction with 70% ethanol according to a previous reported method1). The extracted solvent was soaked at room temperature for 48 hours, filtered with filter paper (Whatman No. 2; Whatman Inc., Maidstone, UK), concentrated with a rotary vacuum evaporator (Eyela A-1000; Eyela, Tokyo, Japan) and freeze-dried at −70°C. EAGN was dissolved in dimethyl sulfoxide (DMSO) (Sigma-Aldrich Chemical Co., St. Louis, MO, USA) to make a stock solution (250 mg/ml), and the stock solution of EAGN was diluted and used at concentrations 2.5 mg/ml, 3.75 mg/ml, 5.0 mg/ml, and 6.75 mg/ml.

2) Oral microbial culture

Streptococcus mutans, Lactobacillus casei, and Aggregatibacter actinomycetemcomitans, which are oral pathogenic bacteria, and Candida albicans, which is a fungus, were purchased from the Korea Microbiological Conservation Center and Korean Collection for Type Cultures (Table 1). S. mutans and A. actinomycetemcomitans were cultured with Brain Heart infusion agar and broth (MB cell Ltd., Seoul, Korea), L. casei was cultured with De Man–Rogosa–Sharpe (MRS) agar and broth (MB cell Ltd.), and C. albicans was cultured with Potato dextrose agar (PDA, MB cell Ltd.) and potato dextrose broth (MB cell Ltd.) in an incubator (Daihan Scientific Co., Daegu, Korea) at 36.5°C for 24 hours and were diluted to 5×106 CFU/ml according to a previous reported method13).

Oral Microbial Strains for Culture

Class name Strain Culture media Aero condition Staining
Bacteria Streptococcus mutans
KCCM 40105
Brain heart infusion (BHI) Agar and Broth Facultative anaerobic Gram positive
Bacteria Lactobacillus casei
KCCM 12452
De Man–Rogosa–Sharpe (MRS)
Agar and Broth
Facultative anaerobic Gram positive
Bacteria Aggregatibacter
actinomycetemcomitans
KCTC 2581
BHI Agar and Broth Microaerophilic Gram negative
Fungi Candida albicans
KCCM 11282
Potato dextrose agar (PDA) and
potato dextrose broth (PDB)
Aerobic Gram positive

KCCM: Korea Microbiological Conservation Center, KCTC: Korean Collection for Type Cultures.


3) Disk diffusion test

To confirm the anti-oral microbial activity according to the concentration of EAGN, oral microorganisms were cultured, diluted to 5×106 CFU/ml and smeared on agar plates. EAGN treated paper discs (Ф6 mm; Advantec Toyo Kaisha Ltd., Tokyo, Japan) and Penicillin G (10 mcg; Oxoid Ltd., Hampshire, UK) antibiotic discs were place on the prepared agar plates. After culturing for 24 hours, the diameter of the clear zone formed around the discs was measured using a vernier caliper (Mitutoyo Co., Kamagawa, Japan).

4) Measurement of growth and biofilm formation assay

The selective medium inoculated with diluted oral microorganisms was treated with EAGN at concentrations of 2.5 mg/ml, 3.75 mg/ml, 5 mg/ml, and 6.75 mg/ml and then cultured for 24 hours. The growth of oral microorganisms was measured at a wavelength of 600 nm using a UV-Vis spectrophotometer (X-ma 1200; Human Corp., Seoul, Korea). The biofilm formation of oral microorganisms was measured at 570 nm using microplate reader (Sunrise TM; Tecan, Grödig, Austria) after removing the medium, washing with DW, staining with 0.1% crystal violet (MB cell Ltd.) for 15 minutes, and treatment with 95% ethanol, according to a previously reported method14).

5) Measurement of acid production and buffering capacity

Oral microorganisms were diluted to 5×106 CF/ml and each concentration of EAGN was added to 5 ml selective medium and cultured for 24 hours. Acid production and buffering capacity were measured by the pH value using a pH meter (TTBH Pte Ltd., Petro Centre, Singapore), as previous reported14). Buffering capacity was measured as the amount of 1M NaOH required to bring the pH of the medium to 7, according to a previously reported method15).

2.Statistical analysis

The experiments were conducted three times and the results were presented as mean±standard deviation. The results were analyzed using IBM SPSS (version 25.0; IBM Corp., Amonk, NY, USA) and significant differences were determined using one-way analysis of variance.

Results

1.Anti-oral microbial activity of EAGN

The results of a disk diffusion test to confirm the anti-oral microbial activity of EAGN against S. mutans, L. casei, and A. actinomycetemcomitans belonging to bacteria and C. albicans belonging to fungi are shown in Fig. 1. EAGN showed anibacterial effects against S. mutans and A. actinomycetemcomitans at all concentration, and the antibacterial effects of S. mutans and A. actinomycetemcomitans increased with increasing EAGN concentrations. Especially, a more susceptible effect of EAGN concentration was seen above 5.0 mg/ml for S. mutans and above 3.75 mg/ml for A. actinomycetemcomitans (Table 2). However, EAGN had no effect on L. casei and C. albicans.

Comparison of Anti-oral Microbial Activity of 70% EAGN by Disk Diffusion Test

Strains DMSO EAGN (mg/ml) Penicillin G
(10 units)
2.5 3.75 5.0 6.75
Streptococcus mutans ++ ++ +++
Lactobacillus casei +++
Aggregatibacter actinomycetemcomitans ++ ++ ++ +++
Candida albicans

−: resistrant (<6 mm), +: susceptible (6∼10 mm), ++: more susceptible (11∼15 mm), +++: most susceptible (>16 mm).

DMSO: dimethyl sulfoxide, EAGN: ethanol extract of Angelica gigas Nakai.


Fig. 1. Anti-oral Microbial Activity of 70% ethanol extract of Angelica gigas Nakai (scare bar=6 mm). DMSO: dimethyl sulfoxide.

2.Inhibitory effect on growth and biofilm formation of oral microorganisms of EAGN

The effects of EAGN on the growth of oral microorganisms and biofilm formation were shown in Fig. 2. Regarding microbial growth (Fig. 2A), EAGN treatment reduced the growth of S. mutans, L. casei, and A. actinomycetemcomitans, in particular, the growth of A. actinomycetemcomitans and L. casei was significantly reduced. C. albicans increased with EAGN treatment. In the case of biofilm formation (Fig. 2B), S. mutans, L. casei and A. actinomycetemcomitans significantly decreased depending on EAGN concentration. A significant reduction in biofilm formation was seen at EAGN concentration above 3.75 mg/ml for S. mutans, at 6.75 mg/ml for L. casei, and above 2.5 mg/ml for A. actinomycetemcomitans (Table 2). The biofilm formation of C. albicans was significantly lower than that of other oral bacteria and was not affected by EAGN.

Fig. 2. Changes in growth (A) and biofilm formation (B) of oral microorganisms according to 70% ethanol extract of Angelica gigas Nakai treatment. OD: optical density, DMSO: dimethyl sulfoxide. **p<0.01, ***p<0.001 compared with DMSO of bacteria. ###p<0.001 compared with DMSO group.

3.Effect on acid production and buffering capacity of oral microorganisms of EAGN

The effects of EAGN on the acid production and buffering capacity of oral microorganisms are shown in Fig. 3. The pH was significantly reduced by treatment with EAGN in S. mutans, A. actinomycetemcomitans, and CC (Fig. 3A). In the case of S. mutans and A. actinomycetemcomitans, the pH increased slightly with 6.75 mg/ml EAGN. The pH of C. albicans decreased with EAGN treatment, whereas that of L. casei was unaffected by EAGN treatment. The value of 1M NaOH for S. mutans and A. actinomycetemcomitans decreased at an EAGN concentration of 3.75 mg/ml and above, and their buffering capacity increased. However, the buffering capacities of L. casei and C. albicans were not affected by EAGN treatment (Fig. 3B).

Fig. 3. Changes in acid production (A) and buffering capacity (B) according to 70% ethanol extract of Angelica gigas Nakai treatment. DMSO: dimethyl sulfoxide. *p<0.05, **p<0.01, ***p<0.001 compared with DMSO of bacteria. ##p<0.01 compared with DMSO group.
Discussion

1.Key results and interpretation

This study was conducted to reveal the anti-oral microbial effect and the microbial and biochemical changes in oral microorganisms according to the concentration of EAGN root, and to confirm the possibility of using EAGN as a functional substance derived from medicinal plants to control oral infectious microorganisms. EAGN showed anti-oral bacterial effects on S. mutans and A. actinomycetemcomitans at all concentration, and S. mutans showed a more susceptible effect at concentrations above 5.0 mg/ml and A. actinomycetemcomitans at 3.75 mg/ml (Table 2). However, EAGN had no effect on L. casei or C. albicans. These results indicate that EAGN has anti-oral bacterial effects against S. mutans, a dental caries-causing bacterium, and A. actinomycetemcomitans, a periodontal disease-causing bacterium, and has the potential to be used as a functional substance to control of these oral bacteria. EAGN treatment reduced the growth of S. mutans, L. casei, and A. actinomycetemcomitans. In particular, A. actinomycetemcomitans growth was significantly reduced at all concentrations tested. Biofilm formation was significantly reduced at concentrations greater than 3.75 mg/ml for S. mutans and 2.5 mg/ml for A. actinomycetemcomitans (Fig. 2). The acid production was significantly increased by treatment with EAGN in S. mutans, A. actinomycetemcomitans, and C. albicans, and the buffering capacity of S. mutans and A. actinomycetemcomitans increased from an EAGN concentration of 3.75 mg/ml and above (Fig. 3). These results indicate that EAGN induced changes were more sensitive to A. actinomycetemcomitans than to S. mutans, especially in terms of growth and biofilm formation.

Based on these results, EAGN showed anti-oral bacterial effects on S. mutans and A. actinomycetemcomitans, which are thought to be related to the inhibition of their growth and biofilm formation. The concentration of EAGN for effective antibacterial effects against both S. mutans and A. actinomycetemcomitans was confirmed to be 3.75 mg/ml and above. Therefore, EAGN can be used as a safe functional substance derived from medicinal plants owing to its antibacterial effects against S. mutans and A. actinomycetemcomitans.

2.Comparison with previous studies

There are abundant studies on the various pharmacological effects of AGN9), however, studies on its antibacterial effects are rare, and these studies have reported that EAGN has antibacterial effects against Bacillus subtilis, Bacillus cereus, Staphylococcus aureus, Escherichia coli, and Pseudomonas fluorescens16). This is the first study to investigate the anti-oral microbial effects of EAGN. In this study, S. mutans, L. casei, and A. actinomycetemcomitans, which are pathogenic oral bacteria and C. albicans, which is fungus were used in the experiments. S. mutans causes dental caries and forms biofilms on the tooth surface17). L. casei causes advanced dental caries14), and colonizes oral tissues to form biofilm18). A. actinomycetemcomitans causes aggressive periodontal disease and colonizes dental plaque19,20). C. albicans is a normal flora in the non-pathogenic state, but attaches to oral epithelial cells or dentures of patients with weakened immune systems and causes opportunistic infections and candidiasis21). The main components of AGN are coumarin, a lipid-soluble substance, and polysaccharide, a water-soluble substance22). Cumarin includes pyranocoumarins (decursin and decursinol algelate), umbelliferone, nodakenin, peucedanone, marmesin, demethylsuberosin and isoimperatorin23). Decursin and decursinol algelate are the main active components of the biological effects of AGN23,24). AGN root contains more than 6% of the active components, decursin, decursinol angelate and nodakenin, in particular, decursin and decursinol angelate are not found in Chinese and Japanese Angelica species25). AGN roots extracted with water did not show an antibacterial effect, but only EAGN roots showed an effect26). In addition, among lipid-soluble cumarins, decursin and decursinol angelate have six-membered rings and senecioylic acid-type side chain that show antibacterial properties in structure, and decursin and decursinol angelate showed antibacterial activity against Bacillus subtilis16). Therefore, the antibacterial effect and inhibition of growth and biofilm formation of EAGN against S. mutans and A. actinomycetemcomitans observed in this study were also thought to be caused by decursin and decursinol angelate. There was a study in which decursin and decursinol angelate showed antifungal effects on the pathogenic fungi Magonaporthe oryzae27), but in another study using EAGN, it did not show an effect on Sacchromyces cerevisiae26), and this study also had no antifungal effect on C. albicans.

3.Limitations

A limitation of this study is that we could not identify substances with antibacterial effects against S. mutans and A. actinomycetemcomitans, because used crude extracts of EAGN. Future studies are needed to identify the components and mechanisms of EAGN root showing antibacterial effects against S. mutans and A. actinomycetemcomitans, and to confirm the effectiveness of EAGN root through clinical application.

4.Conclusion

EAGN showed anti-oral bacterial effects against both S. mutans and A. actinomycetemcomitans at concentrations above 3.75 mg/ml, and these effects are thought to be related to the inhibition of their growth and biofilm formation. Therefore, EAGN can be used as a safe functional substance derived from medicinal plants owing to its antibacterial effects against S. mutans and A. actinomycetemcomitans.

Acknowledgements

None.

Conflict of interest

Soon-Jeong Jeong has been serving as an editor-in-chief of the Journal of Dental Hygiene Science since January 2023. She was not involved in the review process of this editorial. So, there was no conflict of interest.

Ethical approval

Not applicable.

Funding

This work was supported by Youngsan University Research Fund of 2023.

Data availability

The data supporting the findings of this study are available from the corresponding author upon reasonable request.

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