|
 
 |
| ORIGINAL ARTICLE |
|
| Year : 2022 | Volume
: 19
| Issue : 1 | Page : 36 |
|
Anti-adherence and anti-bacterial activities of Pistacia atlantica resin extract against strongly adherent Streptococcus mutans strains
Arezoo Tahmourespour1, Atousa Aminzadeh2, Iman Salehifard3
1 Department of Basic Medical Sciences and Medical Biotechnology, Isfahan (Khorasgan) Branch, Islamic Azad University, Isfahan, Iran
2 Department of Oral Pathology, School of Dentistry, Isfahan (Khorasgan) Branch, Islamic Azad University, Isfahan, Iran
3 Dentist, School of Dentistry, Isfahan (Khorasgan) Branch, Islamic Azad University, Isfahan, Iran
| Date of Submission | 26-May-2021 |
| Date of Acceptance | 16-Feb-2022 |
| Date of Web Publication | 27-Apr-2022 |
Correspondence Address:
Dr. Arezoo Tahmourespour
Department of Basic Medical Sciences and Medical Biotechnology, School of Dentistry, Isfahan (Khorasgan) Branch, Islamic Azad University, Isfahan
Iran
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/1735-3327.344159
Background: The reduction of Streptococcus mutans from the oral cavity or its adherence to tooth surfaces can prevent or decrease the progression of caries. In this study, the antimicrobial and anti-adherence properties of Pistacia atlantica (P. atlantica) resin (Essential oil [EO] and methanolic extract [ME]) were investigated on S. mutans strains.
Materials and Methods: In this in vitro experimental study, the growth rate, biofilm formation ability, and antibiotic susceptibility profile of S. mutans ATCC35668 and 3 strains isolated from caries lesions were studied. The EO and ME of P. atlantica resin were prepared. The anti-bacterial and anti-adherence properties of them were evaluated using microdilution and microplate adherence tests, respectively. The data were statistically analyzed using SPSS with one-way and two-way analysis variance. Direct comparisons between the groups were made using the Wilcoxon W-Mann–Whitney U-test. Statistical significance was set at P < 0.05.
Results: All target strains showed the same growth rate and antibiotic susceptibility profile and were found strongly adherent. Both EO and ME showed moderate anti-bacterial properties (growth reduction up to 47.1% and 39.1%, respectively) against S. mutans, while the anti-bacterial effect of EO was higher than ME, significantly (P < 0.05). In all tested concentrations, EO showed a significantly stronger anti-adherence activity (50%–80%) than ME.
Conclusion: The results showed an anti-cariogenic effect of EO extracted from P. Atlantica resin. Considering that S. mutans adhesion is a necessary step in the beginning and progression of dental caries, this study can suggest the use of such extract in mouthwashes or toothpaste as an alternative agent for preventing bacterial attachment and biofilm formation.
Keywords: Adherence, anti-bacterial agent, cariogenic, pistacia, Streptococcus mutans
How to cite this article:
Tahmourespour A, Aminzadeh A, Salehifard I. Anti-adherence and anti-bacterial activities of Pistacia atlantica resin extract against strongly adherent Streptococcus mutans strains. Dent Res J 2022;19:36 |
How to cite this URL:
Tahmourespour A, Aminzadeh A, Salehifard I. Anti-adherence and anti-bacterial activities of Pistacia atlantica resin extract against strongly adherent Streptococcus mutans strains. Dent Res J [serial online] 2022 [cited 2023 Mar 22];19:36. Available from: https://www.drjjournal.net/text.asp?2022/19/1/36/344159 |
| Introduction | |  |
Dental caries is the main public health concern ranked first for the permanent tooth decay of about 2.3 billion people.[1] Specific bacteria are related to dental caries initiation and progressions. Streptococcus mutans is considered the principal etiological agent of dental caries due to its adherence ability to tooth surface, sucrose fermentation, extracellular polysaccharides, and acid production.[2],[3] Hence, the reduction of S. mutans or its attachment to tooth surfaces can prevent or decrease caries development.[4]
Today, there are several mechanical, chemical, and biological preventive strategies to control the caries progression.[5] However, despite the progress in preventive methods, dental caries distribution in developed countries remains high. Hence, there is a great need to look for novel preventive methods. Besides, there are some well-known anti-microbial agents like chlorhexidine gluconate (CHX) which is very successful in reducing the salivary mutans Streptococci count, but it is not effective as a preventive agent due to its adverse effects like teeth and tongue discoloration and bacterial resistance.[6],[7]
However, biofilm elimination from teeth surfaces remains a challenge because the nature of structural and physiological properties of biofilm bacteria provides natural resistance to anti-bacterial agents.[8] Thus, further researches and development of alternative natural and safe antimicrobial agents for dental caries prevention are needed. In recent decades, much attention has been attracted to the use of traditional herbal agents due to exhibiting potent anti-bacterial, anti-cancer, anti-adhesion, or anti-cariogenic activities of plant-derived active compounds.[9],[10],[11]
One of the traditional plants is Pistacia atlantica (P. atlantica) which is called ”Banneh” in Iran. It is one of the most important tree species commonly distributed in different countries such as Iran, Iraq, Algeria, and turkey.[12] The resin of P. atlantica tree has various beneficial effects and it is traditionally used in Iran as peptic ulcer treatment, mouth freshener, antiseptic, gum tissue strengthener, appetizer, astringent, diuretic, gastrointestinal disorder treatment, etc.[13] Other studies have reported the anti-fungal, anti-parasite, and anti-bacterial activities of P. atlantica.[14],[15],[16],[17] So, this study aimed to investigate the anti-cariogenic efficacy of the essential oil (EO) and methanolic extract (ME) of P. atlantica resin through the investigation of their anti-bacterial, and anti-adhesion activities against strongly adherent (SA) S. mutans strains in vitro.
| Materials and Methods | | |
Bacterial strain and growth conditions
S. mutans ATCC 35668 and other SA strains, isolated from caries lesions, were provided from the Microbiology Laboratory of Isfahan branch, Azad University, and cultured in tryptic soy broth (TSB; Merck, Germany). The growth profile of the strains was recorded at time intervals. The antibiotic susceptibility of the strains was evaluated by the disc diffusion method (Kirby and Bauer) on Mueller Hinton agar (Merck Co. Germany).[18] The antibiotic discs (Padtan Teb Co. Iran) used were: Pencillin-G (P; 10 μg), Cefalothin (CF; 30 μg), Cefalexin (CN; 30 μg), Vancomycin (V; 30 μg), Gentamycin (GM; 10 μg) and Streptoomycin (S; 10 μg).
Biofilm formation ability
To select SA strains, the biofilm formation ability of strains was quantified by a microtiter plate method as previously described.[19] Briefly, overnight cultures of strains in TSB supplemented with and without substrates (Sucrose 1% and a mixture of 0.5% glucose and 0.5% fructose) were prepared. Their turbidity was adjusted to 0.5 on Mc Farland turbidity. Each bacterial suspension (250 μl) was transferred into wells of a microtiter plate, incubated (35 ° C, 24 h), the wells were emptied, and washed with sterile PBS solution. The remaining attached bacteria were fixed (96% methanol: 250 μl/well; 15 min), stained (2% crystal violet: 200 μl; 5 min), the excess stain was washed off, and the plates were left to dry. The formed biofilm was quantified by resolubilizing the stain in 200 μl of 33% (v/v) glacial acetic acid (Merck, Germany) per well. The optical density (OD) of the stain was measured at 492 nm by an ELISA reader (TECAN Co. Spectra SLT). Control wells only contained broth. According to the obtained ODs, strains can be classified into the different categories:
OD < ODC = nonadherent (NA); ODC < OD < 2ODC = Weakly adherent; 2ODC < OD < 4ODC = Moderatly adherent; 4ODC < OD = SA (or strong biofilm producer).
OD and ODC are the mean OD of wells with biofilm and the control wells, respectively.
Resin collection, essential oil and methanolic extract preparation
P. atlantica resin was gathered from the Zagros Mountains of Iran. ME and EO were obtained from P. atlantica resin. The EO was extracted by hydrodistillation method (150 g; with 3 L water) and pale yellow oil (12 g) was obtained (8% v/w).[20]
Anti-bacterial activity assay
Anti-bacterial activity of EO and ME was evaluated by the microdilution method as described previously.[21] The crude EO and ME of P. atlantica were used as stock solutions with the concentration of 300 mg/ml in DMSO which was nontoxic to bacteria. The S. mutans suspension (20 μl equal to 0.5 Mc Farland suspension.), diluted extracts at different concentrations (30 μl of 60%-100%), and BHI broth (200 μl) were added to each well of 96-well microtiter plates. Wells containing CHX (0.65 mg/ml) and bacterial suspension without any inhibitory compound (non-treated) were considered as the positive and negative controls, respectively. Then, plates were incubated (37 °C, 18 h) and the optical densities of wells were read by the ELISA reader at 620 nm and compared. Each control or treatment was tested in 8 replicates.
Anti-adhesion activity assay
The anti-adhesion assay was performed according to Tahmourespour et al.(2019) with some modifications as follows:[21] Each column of a 96-well microplate was filled with 200 μl/well of each EO and ME concentration. The plate was shaken (1 h) and the wells were emptied. S. mutans suspension (20 μl) along with TSB containing 1% sucrose (200 μl) were added to them and incubated (4 h, 37°C). The unattached cells were rinsed then adhered S. mutans cells were fixed, stained and the optical density of every well was read as described above. This assay can estimate the microbial adhesion reduction percentage versus the control wells. Control wells contained PBS buffer instead of ME or EO.
Statistical analysis
Each experiment was done in triplicate. The obtained data were statistically analyzed using a software package SPSS-20 (SPSS Inc., Chicago, IL, USA) with one-way and two-way analysis variance. Direct comparisons between the two groups were made using the Wilcoxon W-Mann–Whitney U-test. Statistical significance was set at P < 0.05.
| Results | | |
[Figure 1] shows the optical densities obtained from the growth of S. mutans strains after 24 h of incubation in the same medium and condition which did not show any significant difference using the Kruskal–Wallis test (P > 0.05). The results of in vitro antibiotic susceptibility tests of selected strains are summarized in [Table 1]. No significant differences (P > 0.05) in antibiotic-resistance rates between the tested strains were found. The resistance prevalence against the tested antibiotics was relatively low, ranging from 0% (Vancomycin) to 100% (Streptomycin). | Figure 1: The comparison between the growth rate of Streptococcus mutans strains after 24 h incubation in same condition. (OD: Optical density; STD: Standard strain of S. mutans ATCC35668; SM: Streptococcus mutans).
Click here to view |
 | Table 1: The antibiotic susceptibility profile of Streptococcus mutans strains based on zone of growth inhibition diameter in millimeter
Click here to view |
According to determining the biofilm formation ability of tested S. mutans strains in the existence of different substrates [Figure 2], it was clear that, all of the strains were classified as (SA) and (NA) in the existence of sucrose and no sugar, respectively. The adherence ability of SM1 was significantly higher (P < 0.001) than other tested strains in presence of sucrose as a carbohydrate source while there was no significant difference between SM2, SM3 and STD strains. | Figure 2: The biofilm formation ability of tested strains in the existence of different substrates. SA: Strongly adherent; MA: Moderately adherent; WA: Weakly adherent; NA: Nonadherent.
Click here to view |
Anti-bacterial activity
According to the results of the microdilution assay [Figure 3], it was clear that the growth reduction percentages of S. mutans strains in the presence of both EO and ME were under 50%, while, CHX could cause up to 98.7% reduction in the growth of testing strains with a significant difference, according to the KW test and Chi-square (P < 0.001). | Figure 3: The antibacterial activity of Pistacia atlantica resin, essential oil and methanolic extract against Streptococcus mutans strains using microdillution method.
Click here to view |
Two-way analysis of variance (Wilcoxon W-Mann–Whitney U-test) did not show any significant difference between the EO and ME inhibitory effects (P > 0.05) concerning the CHX effect. Without considering the effect of CHX, the anti-bacterial effect of EO was higher than ME, significantly (P < 0.05).
Anti-adherence activity
The anti-adherence activity was observed in presence of both herbal agents (EO and ME). However, EO showed the highest and the lowest anti-adherence activity of about 81% and 54% at concentrations of 100% and 60%, respectively. Meanwhile, the highest and the lowest anti-adherence activity of 22.9% and 2.07% at concentrations of 100% and 60% of ME were observed. Hence, according to the statistical analysis, the P. atlantica resin EO showed significantly higher anti-adherence activity than ME (P < 0.05) [Figure 4]. | Figure 4: The anti-adherence activity of essential oil and methanolic extract of Pistacia atlantica resin.
Click here to view |
| Discussion | | |
As S. mutans is the main bacterium responsible for early colonizing the oral cavity, it is necessitated in caries progression from its initiation. Dental caries is an important oral health problem that needs more investigation. In this regard, the use of different mouthwashes with anti-microbial activity is increased, but most of their major components (e.g., CHX) can cause various side effects.[4] Hence, to overcome and reduce such side effects, different studies have been evaluated the anti-microbial and anti-biofilm effects of various herbal extracts.[6],[7],[21],[22] Since dental plaque formation as a biofilm initiates with the adherence of bacteria (S. mutans) to the pellicle and in situ growth of attached cells, finding herbal agents with the anti-adherence activity along with anti-microbial property can possess a beneficial role in preventing biofilm and caries development. Although P. atlantica species are considered the best known and one of the most appreciated medicinal plants in countries like Iran, Turkey, etc., still very few studies regarding its anti-cariogenic potential are available in literatures. Hence, in this study, the anti-bacterial and anti-adherence potential of EO and ME derived from P. atlantica resin was investigated, because the resin has been utilized for 5000 years ago for a wide range of purposes.[23]
The target strains of this research were selected with the aim of inhibition or suppression of growth and biofilm formation by the EO and ME of P. atlantica resin. At first, the properties of target strains such as their planktonic growth rate, antibiotic susceptibility profile, and biofilm formation ability were investigated. According to the results, no statistically significant difference in each of the examining properties was observed between the selected strains. Hence that, all 4 strains showed the same growth rate and antibiotic susceptibility profile. Also, all were found SA in the existence of sucrose (1%) while they were NA in no sugar condition.
According to the results, P. atlantica resin showed moderately anti-bacterial activity against S. mutans strains. Furthermore, it is observed that its EO possesses significantly higher anti-bacterial activity than the ME. The EO could reduce the growth of S. mutans cells up to 47.1%, while the S. mutans growth reduction in the existence of ME reached up to 39.1%. Mohamed et al.(2007) also showed that the EO of the Pulicaria crispa (Forsk.) Oliv., and Pulicaria undulata had better antimicrobial activity on most of the microorganisms than the ME.[24]
Such anti-microbial activity is not supported by other researches as they reported complete growth inhibitory activity or higher anti-microbial activity on S. mutans; Hosseini et al.(2013) showed that the diethyl ether extracts of P. athlatica possess stronger inhibitory activity compared to aqueous extracts, although the bacterial cells in the biofilm were not affected by the extracts.[25] Najafi et al. (2014) also observed the anti-microbial effect of P. atlantica (var. mutica) against Bacillus cereus, Staphylococcus aureus, and Escherichia More Details coli (O157 H7) by the method of disc diffusion which can be attributed to the high content of α-pinene. They also indicated that in the case of Pseudomonas aeroginosa no clear zone was formed.[26] Roozegar et al.(2016) showed the anti-microbial effect of the leaf extract P. atlantica on S. mutans.[27] These differences are possibly due to qualitative and quantitative variations between the content of the EO which are related to several parameters such as plant species and part, cultivars sex, harvesting time, climatic conditions, geographical origin, microbial species and their resistance ability, and methods used to investigate their activity.[28],[29],[30],[31] In general, EO is one of the major constituents of various parts of Pistacia species which contains various types of phytochemical agents such as terpenoids, fatty acids, phenolic compounds, and sterols.[23] Golestannejad et al.(2020) also showed that olive leaf methanolic, ethanolic, and hydroalcoholic extracts have appropriate anti-bacterial activities due to their high phenolic content but they did not study the antibacterial activity of its EO.[32]
The inhibition of S. mutans adherence onto the polystyrene microtiter plate by different concentrations of the extract and EO was also observed in this study. In all tested concentrations of EO, a significantly stronger anti-adherence activity (50%–80%) than ME (up to 22%) was seen. It is probably due to EO constituent effects on hydrophobic interactions, which were reported to be significant in bacterial adhesion onto tooth surfaces. Thus, the surface hydrophobicity modification could be used as an anti-adherence strategy.[33] As S. mutans adherence to surfaces is mediated by glucan, the product of glucosyltransferases, the anti-adherence property of EO probably could be associated with the anti-glucosyltransferases activity of compounds such as flavonoids and tannins. Hence, the inhibition of such enzymes can be used as another anti-adherence or anti-biofilm formation strategy. The cariostatic efficacy of flavonoids and tannins (a kind of polyphenole) relates to their anti-microbial activity against S. mutans planktonic and biofilms cells; effects on acidogenic or aciduric characteristics, and down-regulating gtf gene expression.[34] Zeng et al.(2019) also demonstrated the anti-biofilm effect of flavonoids, quercetin, and kaemferol against S. mutans.[35] Yoo et al. (2018) showed the anti-microbial activity of β-caryophyllene, EO from clove, against S. mutans biofilm and planktonic cells. They concluded that such EO can decrease S. mutans count, inhibit biofilm formation also decrease Gtfs expression.[36] As the resin of P. atlantica is composed of different substances, it is better to isolate and purify them and evaluate their anti-cariogenic potential one by one, which was the limitation of the present study.
| Conclusion | | |
Overall, the growth of SA S. mutans strains was inhibited moderately in presence of EO and ME of P. atlantica resin. The EO exhibited a significantly higher anti-adherence (anti-biofilm) activity than ME against the S. mutans strains. Hence, this compound with anti-bacterial and anti-adherence activities without drug resistance induction potential can serve as a key component of mouthwashes and toothpaste formulations facilitating the prevention of dental caries or other biofilm-related oral diseases. Hence, each of the different herbal extracts or their mixture can be a promising part of an ideal caries management program and still needs additional researches.
Acknowledgment
The authors would like to thank Mr. Khalkhali (Microbiology lab assistant) and Ayla Hoodaji (a student) who helped for this research progression.
Financial support and sponsorship
Nil.
Conflicts of interest
The authors of this manuscript declare that they have no conflicts of interest, real or perceived, financial or nonfinancial in this article.
| References | | |
| 1. | World Health Organization. Sugars and Dental Caries. Geneva, Switzerland: World Health Organization; 2017. License: CC BY-NC-SA 3.0 IGO: 4. Doc no. WHO/NMH/NHD/17.12. Available from October 2017: https://apps.who.int/iris/handle/10665/259413.  |
| 2. | Selwitz RH, Ismail AI, Pitts NB. Dental caries. Lancet 2007;369:51-9. |
| 3. | Yadav K, Prakash S. Dental caries: A review. Asian J Biomed Pharm Sci 2016;6:01. |
| 4. | Scharnow AM, Solinski AE, Wuest WM. Targeting S. mutans biofilms: A perspective on preventing dental caries. MedChemComm 2019;10:1057-67. |
| 5. | Lee Y. Diagnosis and prevention strategies for dental caries. J Lifestyle Med 2013;3:107-9. |
| 6. | Islam B, Khan SN, Naeem A, Sharma V, Khan AU. Novel effect of plant lectins on the inhibition of Streptococcus mutans biofilm formation on saliva-coated surface. J Appl Microbiol 2009;106:1682-9. |
| 7. | Ramalingam K, Amaechi BT. Antimicrobial effect of herbal extract of Acacia arabica with triphala on the biofilm forming cariogenic microorganisms. J Ayurveda Integr Med 2020;11:322-8. |
| 8. | Gebreyohannes G, Nyerere A, Bii C, Sbhatu DB. Challenges of intervention, treatment, and antibiotic resistance of biofilm-forming microorganisms. Heliyon 2019;5:e02192. |
| 9. | Heana NY, Othmanb S, Basarb N, Jemona K. Antibiofilm and antiadhesion activities of Phaleria macrocarpa against oral Streptococcus mutans. J Teknol 2015;77:31-5. |
| 10. | Santos MM, Vieira-da-Motta O, Vieira IJ, Braz-Filho R, Gonçalves PS, Maria EJ, et al. Antibacterial activity of Capsicum annuum extract and synthetic capsaicinoid derivatives against Streptococcus mutans. J Nat Med 2012;66:354-6. |
| 11. | Liu C, Li XT, Cheng RR, Han ZZ, Yang L, Song ZC, et al. Anti-oral common pathogenic bacterial active acetylenic acids from Thesium chinense Turcz. J Nat Med 2018;72:433-8. |
| 12. | Minaiyan M, Karimi F, Ghannadi A. Anti-inflammatory effect of Pistacia atlantica subsp. kurdica volatile oil and gum on acetic acid-induced acute colitis in rat. Res J Pharmacogn 2015;2:1-12. |
| 13. | Shrafkandi A. Avicenna: The Canon. Tehran, Iran: Soroush Press; 2008. |
| 14. | Amini K, Bahramian S. Antifungal activity of Pistacia eurycarpa Yalt. Essential oil on Aspergillus flavus by direct addition and vapor contact. J Agric Sci Technol 2019;21:323-30. |
| 15. | Boukaew S, Prasertsan P, Sattayasamitsathit S. Evaluation of antifungal activity of essential oils against aflatoxigenic Aspergillus flavus and their allelopathic activity from fumigation to protect maize seeds during storage. Ind Crops Prod 2017;97:558-66. |
| 16. | Ghalem B, Mohamed B. Essential oil from gum of Pistacia atlantica Desf.: Screening of antimicrobial activity. Afr J Pharm Pharmacol 2009;3:087-91. |
| 17. | Rezaie M, Farhoosh R, Sharif A, Asili J, Iranshahi M. Chemical composition, antioxidant and antibacterial properties of Bene ( Pistacia atlantica subsp. mutica) hull essential oil. J Food Sci Technol 2015;52:6784-90. |
| 18. | Wayne P. Performance Standards for Antimicrobial Susceptibility Testing. 20 th Informational Supplement. CLSI Document M100-S20. USAClinical and Laboratory Standards Institute; 2011. |
| 19. | Tahmourespour A, Kermanshahi RK, Salehi R, Pero NG. Biofilm formation potential of oral streptococci in related to some carbohydrate substrates. Afr J Microbiol Res 2010;4:1051-6. |
| 20. | Pharmacopoeia B. British Pharmacopoeia. 2015 ed. London, UK: Stationery Office; 2016. |
| 21. | Liu Y, Xu Y, Song Q, Wang F, Sun L, Liu L, et al. Anti-biofilm activities from Bergenia crassifolia leaves against Streptococcus mutans. Front Microbiol 2017;8:1738. |
| 22. | Karadağlıoğlu Öİ, Ulusoy N, Başer KH, Hanoğlu A, Şık İ. Antibacterial activities of herbal toothpastes combined with essential oils against Streptococcus mutans. Pathogens 2019;8:20. |
| 23. | Bozorgi M, Memariani Z, Mobli M, Salehi Surmaghi MH, Shams-Ardekani MR, Rahimi R. Five pistacia species ( P. vera, P. atlantica, P. terebinthus, P. khinjuk, and P. lentiscus): A review of their traditional uses, phytochemistry, and pharmacology. ScientificWorldJournal 2013;2013:219815. |
| 24. | Mohamed EA, Muddathir AM, Osman MA. Antimicrobial activity, phytochemical screening of crude extracts, and essential oils constituents of two Pulicaria spp. growing in Sudan. Sci Rep 2020;10:17148. |
| 25. | Hosseini F, Adlgostar A, Sharifnia F. Antibacterial activity of Pistacia atlantica extracts on Streptococcus mutans biofilm. Int Res J Biol Sci 2013;2:1-7. |
| 26. | Najafi MH, Farimani RH, Tavakoli J, Madayeni S. GC-MS analysis and antimicrobial activity of the essential oil of trunk exudates of Pistacia atlantica var. mutica. Chem Nat Compd 2014;50:376-8. |
| 27. | Ali Roozegar M, Azizi Jalilian F, Reza Havasian M, Panahi J, Pakzad I. Antimicrobial effect of Pistacia atlantica leaf extract. Bioinformation 2016;12:19-21. |
| 28. | Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils – A review. Food Chem Toxicol 2008;46:446-75. |
| 29. | Benamar H, Rached W, Derdour A, Marouf A. Screening of Algerian medicinal plants for acetylcholinesterase inhibitory activity. J Biol Sci 2010;10:1-9. |
| 30. | Bluma RV, Etcheverry MG. Application of essential oils in maize grain: Impact on Aspergillus section flavi growth parameters and aflatoxin accumulation. Food Microbiol 2008;25:324-34. |
| 31. | Tajkarimi M, Ibrahim SA, Cliver D. Antimicrobial herb and spice compounds in food. Food Control 2010;21:1199-218. |
| 32. | Golestannejad Z, Khozeimeh F, Abtahi R, Zarei Z, Sadeghalbanaei L, Sadeghian R. Inhibitory effects of ethanolic, methanolic, and hydroalcoholic extracts of olive ( Olea europaea) leaf on growth, acid production, and adhesion of Streptococcus mutans. Dent Res J (Isfahan) 2020;17:179-85. |
| 33. | Hu J, Lin J, Zhang Y, Lin Z, Qiao Z, Liu Z, et al. A new anti-biofilm strategy of enabling arbitrary surfaces of materials and devices with robust bacterial anti-adhesion via a spraying modified microsphere method. J Mater Chem A 2019;7:26039-52. |
| 34. | Ren Z, Chen L, Li J, Li Y. Inhibition of Streptococcus mutans polysaccharide synthesis by molecules targeting glycosyltransferase activity. J Oral Microbiol 2016;8:31095. |
| 35. | Zeng Y, Nikitkova A, Abdelsalam H, Li J, Xiao J. Activity of quercetin and kaemferol against Streptococcus mutans biofilm. Arch Oral Biol 2019;98:9-16. |
| 36. | Yoo HJ, Jwa SK. Inhibitory effects of β-caryophyllene on Streptococcus mutans biofilm. Arch Oral Biol 2018;88:42-6. |
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1]
| This article has been cited by | | 1 |
Synthesize of Pluronic-based Nanovesicular Formulation Loaded with Pistacia atlantica Extract for Improved Antimicrobial Efficiency |
|
| Mushtak T.S. Al-Ouqaili, Raed Obaid Saleh, Hawraz Ibrahim M. Amin, Zanko Hassan Jawhar, Majid Reza Akbarizadeh, Mahin Naderifar, Kovan Dilawer Issa, Juan Carlos Orosco Gavilán, Marcos Augusto Lima Nobre, Abduladheem Turki Jalil, Reza Akhavan-Sigari | | Arabian Journal of Chemistry. 2023; : 104704 | | [Pubmed] | [DOI] | | | 2 |
Chemical composition, pharmaceutical potential and toxicity of the essential oils extracted from the leaves, fruits and barks of Pistacia atlantica |
|
| Hannou Zerkani, Smail Amalich, Imane Tagnaout, Rachid Bouharoud, Touriya Zair | | Biocatalysis and Agricultural Biotechnology. 2022; : 102431 | | [Pubmed] | [DOI] | |
|
 |
|
|
|
Search Pubmed for