Phenotypic Investigation of the Antimicrobial Effect of Organic and Hydro-Alcoholic Extracts of Boswellia serrata on Oral Microbiota
,
Abstract
Objectives: Considering the emergence of resistant microbes and side effects of chemical drugs, in this study, the inhibitory effect of organic and hydro-alcoholic extracts of Boswellia serrata (B. serrata) on some oral microbiota was investigated.
Materials and Methods: In this experimental study, standard strains of Candida albicans (C. albicans; PTCC 5027), Candida glabrata (C. glabrata; PTCC 5295), Candida krusei (C. krusei; PTCC 5297), and Streptococcus mutans (S. mutans; PTCC 1688) were collected from the Iranian Research Organization for Science and Technology (IROST). Then, the minimum inhibitory concentration (MIC) of organic and hydro-alcoholic extracts of B. serrata was determined based on the CLSI protocol and using the micro-dilution method. The contents of each well were subcultured in Müller-Hinton agar (Candida species) and blood agar (S. mutans). The lowest concentration with no growth was considered as the minimum fungicidal concentration (MFC) or bactericidal concentration (MBC). Statistical analyses were performed using Mann-Whitney test.
Results: Hydro-alcoholic extract of B. serrata at the concentration of 50 mg/ml inhibited the growth of C. albicans and S. mutans. It also inhibited the growth of C. krusei and C. glabrata at the concentration of 100 mg/ml. Organic extract of B. serrata at the concentration of 200 mg/ml only inhibited the growth of C. glabrata.
Conclusion: Hydro-alcoholic extract of B. serrata had a greater inhibitory effect on C. albicans and S. mutans compared to the organic extract.
1. Charushin AO, Elovikov AM, Charushina IP, Vorob'eva NN, Katretskaya GG. [The clinical and microbiological characteristics of oropharyngeal candidiasis in the HIV-infected patients at the late stages of the disease]. [Article in Russian; Abstract available in Russian from the publisher]. Vestn Otorinolaringol. 2017;82(6):7-10.
2. Lynch DP. Oral candidiasis. History, classification, and clinical progression. Oral Surg Oral Med Oral Pathol. 1994 Aug;78(2):189-93.
3. Taheri JB, Iman M, Mehdipour M, Bakhtiari S, Namazi F, Teheri Bayan M, et al. Study of Aqueous and Alcoholic Extract of the Melissa Officinalis Effect on Candida albicans,
4. Candida glabrata and Candida krusei. J Mil Med. 2018;19(5):505-512.
5. Krcmery V, Barnes AJ. Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistance. J Hosp Infect. 2002 Apr;50(4):243-60.
6. Fukuoka T, Johnson DA, Winslow CA, de Groot MJ, Burt C, Hitchcock CA, et al. Genetic basis for differential activities of fluconazole and voriconazole against Candida krusei. Antimicrob Agents Chemother. 2003 Apr;47(4):1213-9.
7. Lyu X, Zhao C, Yan ZM, Hua H. Efficacy of nystatin for the treatment of oral candidiasis: a systematic review and meta-analysis. Drug Des Devel Ther. 2016 Mar 16;10:1161-71.
8. Akhlaghi N, Mortazavi S, Akhlaghi N. Relationship between salivary Streptococcus mutans and Lactobacillus counts and caries in adults with a high level of dental care. J Isfahan Dent Sch. 2011;6(6):750-59.
9. Koga-Ito CY, Martins CA, Balducci I, Jorge AO. Correlation among mutans streptococci counts, dental caries, and IgA to Streptococcus mutans in saliva. Braz Oral Res. 2004 Oct-Dec;18(4):350-5.
10. Quirynen M, Soers C, Desnyder M, Dekeyser C, Pauwels M, Van Steenberghe D. A 0.05% cetyl pyridinium chloride/0.05% chlorhexidine mouth rinse during maintenance phase after initial periodontal therapy. J Clin Periodontol. 2005 Apr;32(4):390-400.
11. Berchier CE, Slot DE, Van der Weijden GA. The efficacy of 0.12% chlorhexidine mouthrinse compared with 0.2% on plaque accumulation and periodontal parameters: a systematic review. J Clin Periodontol. 2010 Sep;37(9):829-39.
12. Adelakun EA. Finbar EA, Agina SE. Makinele AA. Antimicrobial activity of Boswellia dalziellii stem bark. Fitoterapia. 2001 Nov;72(7):822-4.
13. Ammon HP, Safayhi H, Mack T, Sabieraj J. Mechanism of antiinflammatory actions of curcumine and boswellic acids. J Ethnopharmacol. 1993 Mar;38(2-3):113-9.
14. Saraswati S, Pandey M, Mathur R, Agrawal SS. Boswellic acid inhibits inflammatory angiogenesis in a murine sponge model. Microvasc Res. 2011 Nov;82(3):263-8.
15. Pungle P, Banavalikar M, Suthar A, Biyani M, Mengi S. Immunomodulatory activity of boswellic acids of Boswellia serrata Roxb. Indian J Exp Biol. 2003 Dec;41(12):1460-2.
16. Huang M-T, Badmaev V, Ding Y, Liu Y, Xie JG, Ho CT. Anti-tumor and anti-carcinogenic activities of triterpenoid, beta-boswellic acid. Biofactors. 2000;13(1-4):225-30.
17. Takada Y, Ichikawa H, Badmaev V, Aggarwal BB. Acetyl-11-keto-beta-boswellic acid potentiates apoptosis, inhibits invasion, and abolishes osteoclastogenesis by suppressing NF-kappa B and NF-kappa B-regulated gene expression. J Immunol. 2006 Mar 1;176(5):3127-40.
18. Bhushan S, Kumar A, Malik F, Andotra SS, Sethi VK, Kaur IP, et al. A triterpenediol from Boswellia serrata induces apoptosis through both the intrinsic and extrinsic apoptotic pathways in human leukemia HL-60 cells. Apoptosis. 2007 Oct;12(10):1911-26.
19. Liu JJ, Nilsson A, Oredsson S, Badmaev V, Zhao WZ, Duan RD. Boswellic acids trigger apoptosis via a pathway dependent on caspase-8 activation but independent on Fas/Fas ligand interaction in colon cancer HT-29 cells. Carcinogenesis. 2002 Dec;23(12):2087-93.
20. Park YS, Lee JH, Bondar J, Harwalkar JA, Safayhi H, Golubic M. Cytotoxic action of acetyl-11-keto-beta-boswellic acid (AKBA) on meningioma cells. Planta Med. 2002 May;68(5):397-401.
21. Pang X, Yi Z, Zhang X, Sung B, Qu W, Lian X, et al. Acetyl-11-keto-beta-boswellic acid inhibits prostate tumor growth by suppressing vascular endothelial growth factor receptor 2-mediated angiogenesis. Cancer Res. 2009 Jul 15;69(14):5893-900.
22. Kunnumakkara AB, Nair AS, Sung B, Pandey MK, Aggarwal BB. Boswellic acid blocks signal transducers and activators of transcription 3 signaling, proliferation, and
survival of multiple myeloma via the protein tyrosine phosphatase SHP-1. Mol Cancer Res. 2009 Jan;7(1):118-28.
23. Pandey RS, Singh BK, Tripathi YB. Extract of gum resins of Boswellia serrata L. inhibits lipopolysaccharide induced nitric oxide production in rat macrophages along with hypolipidemic property. Indian J Exp Biol. 2005 Jun;43(6):509-16.
24. Mahmoudi A, Hosseini-Sharifabad A, Monsef-Esfahani HR, Yazdinejad AR, Khanavi M, Roghani A, et al. Evaluation of systemic administration of Boswellia papyrifera extracts on spatial memory retention in male rats. J Nat Med. 2011 Jul;65(3-4):519-25.
25. Gerhardt H, Seifert F, Buvari P, Vogelsang H, Repges R. [Therapy of active Crohn disease with Boswellia serrata extract H 15]. [Article in German]. Z Gastroenterol. 2001 Jan;39(1):11-7.
26. Krieglstein CF, Anthoni C, Rijcken EJ, Laukötter M, Spiegel HU, Boden SE, et al. Acetyl-11-keto-beta-boswellic acid, a constituent of a herbal medicine from Boswellia serrata resin, attenuates experimental ileitis. Int J Colorectal Dis. 2001 Apr;16(2):88-95.
27. Kavitha JV, Rosario JF, Chandran J, Anbu P, Bakkiyanathan. Hypoglycemic and other related effects of Boswellia glabra in alloxan-induced diabetic rats. Indian J Physiol Pharmacol. 2007 Jan-Mar;51(1):29-39.
28. Borrelli F, Capasso F, Capasso R, Ascione V, Aviello G, Longo R, et al. Effect of Boswellia serrata on intestinal motility in rodents: inhibition of diarrhoea without constipation. Br J Pharmacol. 2006 Jun;148(4):553-60.
29. Gupta I, Gupta V, Parihar A, Gupta S, Lüdtke R, Safayhi H, et al. Effects of Boswellia serrata gum resin in patients with bronchial asthma: results of a double-blind, placebo-controlled, 6-week clinical study. Eur J Med Res. 1998 Nov 17;3(11):511-4.
30. Raja AF, Ali F, Khan IA, Shawl AS, Arora DS, Shah BA, et al. Antistaphylococcal and biofilm inhibitory activities of acetyl-11-keto-β-boswellic acid from Boswellia serrata. BMC Microbiol. 2011 Mar 16;11:54.
31. Schillaci D, Arizza V, Dayton T, Camarda L, Di Stefano V. In vitro anti-biofilm activity of Boswellia spp. oleogum resin essential oils. Lett Appl Microbiol. 2008 Nov;47(5):433-8.
32. Sabra SM, Al-Masoudi LM. The Effect of Using Frankincense (Boswellia sacra) Chewing Gum on the Microbial Contents of Buccal/Oral Cavity, Taif, KSA. J Dent Med Sci. 2014 Jan;13(4):77-82.
33. Patel NB, Patel KC. Antibacterial Activity of Boswellia serrata Roxb. ex Colebr. Ethnomedicinal Plant against Gram Positive UTI Pathogens. Life Sci Leafl. 2014 Jun;53:79-88.
34. Shareef AA. Evaluation of antibacterial activity of essential oils of Cinnamomum sp. and Boswellia sp. J Basra Res. 2011;37(5A):60-71.
35. Kasali AA, Adio AM, Kundaya OE, Oyedeji AO, Eshilokun AO, Adefenwa M. Antimicrobial activity of the essential oil of Boswellia serrata Roxb. J Essent Oil Bearing Plants. 2002;5(3):173-75.
36. Camarda L, Dayton T, Di Stefano V, Pitonzo R, Schillaci D. Chemical composition and antimicrobial activity of some oleogum resin essential oils from Boswellia spp. (Burseraceae). Ann Chim. 2007 Sep;97(9):837-44.
37. Hasson SS, Al-Balushi MS, Sallam TA, Idris MA, Habbal O, Al-Jabri AA. In vitro antibacterial activity of three medicinal plants- Boswellia (Luban) species. Asian Pac J Trop Biomed. 2011 Oct;1(2):S178-S182.
38. N9150 Sigma-Aldrich Nystatin Ready made solution suitable for cell culture. Available at: https://www.sigmaaldrich.com/catalog/product/sigma/n9150?lang=en®ion=IR / Accessed January 24, 2019.
39. M100 Performance Standards for Antimicrobial Susceptibility Testing. Clinical and Laboratory Standards Institute , 2017. Available at: https://clsi.org/media/1469/m100s27_sample.pdf /Accessed January 24, 2019.
40. Sharma R, Singh S, Singh GD, Khajuria A, Sidiq T, Singh SK, et al. In vivo genotoxicity evaluation of a plant based antiarthritic and anticancer therapeutic agent Boswelic acids in rodents. Phytomedicine. 2009 Dec;16(12):1112-8.
2. Lynch DP. Oral candidiasis. History, classification, and clinical progression. Oral Surg Oral Med Oral Pathol. 1994 Aug;78(2):189-93.
3. Taheri JB, Iman M, Mehdipour M, Bakhtiari S, Namazi F, Teheri Bayan M, et al. Study of Aqueous and Alcoholic Extract of the Melissa Officinalis Effect on Candida albicans,
4. Candida glabrata and Candida krusei. J Mil Med. 2018;19(5):505-512.
5. Krcmery V, Barnes AJ. Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistance. J Hosp Infect. 2002 Apr;50(4):243-60.
6. Fukuoka T, Johnson DA, Winslow CA, de Groot MJ, Burt C, Hitchcock CA, et al. Genetic basis for differential activities of fluconazole and voriconazole against Candida krusei. Antimicrob Agents Chemother. 2003 Apr;47(4):1213-9.
7. Lyu X, Zhao C, Yan ZM, Hua H. Efficacy of nystatin for the treatment of oral candidiasis: a systematic review and meta-analysis. Drug Des Devel Ther. 2016 Mar 16;10:1161-71.
8. Akhlaghi N, Mortazavi S, Akhlaghi N. Relationship between salivary Streptococcus mutans and Lactobacillus counts and caries in adults with a high level of dental care. J Isfahan Dent Sch. 2011;6(6):750-59.
9. Koga-Ito CY, Martins CA, Balducci I, Jorge AO. Correlation among mutans streptococci counts, dental caries, and IgA to Streptococcus mutans in saliva. Braz Oral Res. 2004 Oct-Dec;18(4):350-5.
10. Quirynen M, Soers C, Desnyder M, Dekeyser C, Pauwels M, Van Steenberghe D. A 0.05% cetyl pyridinium chloride/0.05% chlorhexidine mouth rinse during maintenance phase after initial periodontal therapy. J Clin Periodontol. 2005 Apr;32(4):390-400.
11. Berchier CE, Slot DE, Van der Weijden GA. The efficacy of 0.12% chlorhexidine mouthrinse compared with 0.2% on plaque accumulation and periodontal parameters: a systematic review. J Clin Periodontol. 2010 Sep;37(9):829-39.
12. Adelakun EA. Finbar EA, Agina SE. Makinele AA. Antimicrobial activity of Boswellia dalziellii stem bark. Fitoterapia. 2001 Nov;72(7):822-4.
13. Ammon HP, Safayhi H, Mack T, Sabieraj J. Mechanism of antiinflammatory actions of curcumine and boswellic acids. J Ethnopharmacol. 1993 Mar;38(2-3):113-9.
14. Saraswati S, Pandey M, Mathur R, Agrawal SS. Boswellic acid inhibits inflammatory angiogenesis in a murine sponge model. Microvasc Res. 2011 Nov;82(3):263-8.
15. Pungle P, Banavalikar M, Suthar A, Biyani M, Mengi S. Immunomodulatory activity of boswellic acids of Boswellia serrata Roxb. Indian J Exp Biol. 2003 Dec;41(12):1460-2.
16. Huang M-T, Badmaev V, Ding Y, Liu Y, Xie JG, Ho CT. Anti-tumor and anti-carcinogenic activities of triterpenoid, beta-boswellic acid. Biofactors. 2000;13(1-4):225-30.
17. Takada Y, Ichikawa H, Badmaev V, Aggarwal BB. Acetyl-11-keto-beta-boswellic acid potentiates apoptosis, inhibits invasion, and abolishes osteoclastogenesis by suppressing NF-kappa B and NF-kappa B-regulated gene expression. J Immunol. 2006 Mar 1;176(5):3127-40.
18. Bhushan S, Kumar A, Malik F, Andotra SS, Sethi VK, Kaur IP, et al. A triterpenediol from Boswellia serrata induces apoptosis through both the intrinsic and extrinsic apoptotic pathways in human leukemia HL-60 cells. Apoptosis. 2007 Oct;12(10):1911-26.
19. Liu JJ, Nilsson A, Oredsson S, Badmaev V, Zhao WZ, Duan RD. Boswellic acids trigger apoptosis via a pathway dependent on caspase-8 activation but independent on Fas/Fas ligand interaction in colon cancer HT-29 cells. Carcinogenesis. 2002 Dec;23(12):2087-93.
20. Park YS, Lee JH, Bondar J, Harwalkar JA, Safayhi H, Golubic M. Cytotoxic action of acetyl-11-keto-beta-boswellic acid (AKBA) on meningioma cells. Planta Med. 2002 May;68(5):397-401.
21. Pang X, Yi Z, Zhang X, Sung B, Qu W, Lian X, et al. Acetyl-11-keto-beta-boswellic acid inhibits prostate tumor growth by suppressing vascular endothelial growth factor receptor 2-mediated angiogenesis. Cancer Res. 2009 Jul 15;69(14):5893-900.
22. Kunnumakkara AB, Nair AS, Sung B, Pandey MK, Aggarwal BB. Boswellic acid blocks signal transducers and activators of transcription 3 signaling, proliferation, and
survival of multiple myeloma via the protein tyrosine phosphatase SHP-1. Mol Cancer Res. 2009 Jan;7(1):118-28.
23. Pandey RS, Singh BK, Tripathi YB. Extract of gum resins of Boswellia serrata L. inhibits lipopolysaccharide induced nitric oxide production in rat macrophages along with hypolipidemic property. Indian J Exp Biol. 2005 Jun;43(6):509-16.
24. Mahmoudi A, Hosseini-Sharifabad A, Monsef-Esfahani HR, Yazdinejad AR, Khanavi M, Roghani A, et al. Evaluation of systemic administration of Boswellia papyrifera extracts on spatial memory retention in male rats. J Nat Med. 2011 Jul;65(3-4):519-25.
25. Gerhardt H, Seifert F, Buvari P, Vogelsang H, Repges R. [Therapy of active Crohn disease with Boswellia serrata extract H 15]. [Article in German]. Z Gastroenterol. 2001 Jan;39(1):11-7.
26. Krieglstein CF, Anthoni C, Rijcken EJ, Laukötter M, Spiegel HU, Boden SE, et al. Acetyl-11-keto-beta-boswellic acid, a constituent of a herbal medicine from Boswellia serrata resin, attenuates experimental ileitis. Int J Colorectal Dis. 2001 Apr;16(2):88-95.
27. Kavitha JV, Rosario JF, Chandran J, Anbu P, Bakkiyanathan. Hypoglycemic and other related effects of Boswellia glabra in alloxan-induced diabetic rats. Indian J Physiol Pharmacol. 2007 Jan-Mar;51(1):29-39.
28. Borrelli F, Capasso F, Capasso R, Ascione V, Aviello G, Longo R, et al. Effect of Boswellia serrata on intestinal motility in rodents: inhibition of diarrhoea without constipation. Br J Pharmacol. 2006 Jun;148(4):553-60.
29. Gupta I, Gupta V, Parihar A, Gupta S, Lüdtke R, Safayhi H, et al. Effects of Boswellia serrata gum resin in patients with bronchial asthma: results of a double-blind, placebo-controlled, 6-week clinical study. Eur J Med Res. 1998 Nov 17;3(11):511-4.
30. Raja AF, Ali F, Khan IA, Shawl AS, Arora DS, Shah BA, et al. Antistaphylococcal and biofilm inhibitory activities of acetyl-11-keto-β-boswellic acid from Boswellia serrata. BMC Microbiol. 2011 Mar 16;11:54.
31. Schillaci D, Arizza V, Dayton T, Camarda L, Di Stefano V. In vitro anti-biofilm activity of Boswellia spp. oleogum resin essential oils. Lett Appl Microbiol. 2008 Nov;47(5):433-8.
32. Sabra SM, Al-Masoudi LM. The Effect of Using Frankincense (Boswellia sacra) Chewing Gum on the Microbial Contents of Buccal/Oral Cavity, Taif, KSA. J Dent Med Sci. 2014 Jan;13(4):77-82.
33. Patel NB, Patel KC. Antibacterial Activity of Boswellia serrata Roxb. ex Colebr. Ethnomedicinal Plant against Gram Positive UTI Pathogens. Life Sci Leafl. 2014 Jun;53:79-88.
34. Shareef AA. Evaluation of antibacterial activity of essential oils of Cinnamomum sp. and Boswellia sp. J Basra Res. 2011;37(5A):60-71.
35. Kasali AA, Adio AM, Kundaya OE, Oyedeji AO, Eshilokun AO, Adefenwa M. Antimicrobial activity of the essential oil of Boswellia serrata Roxb. J Essent Oil Bearing Plants. 2002;5(3):173-75.
36. Camarda L, Dayton T, Di Stefano V, Pitonzo R, Schillaci D. Chemical composition and antimicrobial activity of some oleogum resin essential oils from Boswellia spp. (Burseraceae). Ann Chim. 2007 Sep;97(9):837-44.
37. Hasson SS, Al-Balushi MS, Sallam TA, Idris MA, Habbal O, Al-Jabri AA. In vitro antibacterial activity of three medicinal plants- Boswellia (Luban) species. Asian Pac J Trop Biomed. 2011 Oct;1(2):S178-S182.
38. N9150 Sigma-Aldrich Nystatin Ready made solution suitable for cell culture. Available at: https://www.sigmaaldrich.com/catalog/product/sigma/n9150?lang=en®ion=IR / Accessed January 24, 2019.
39. M100 Performance Standards for Antimicrobial Susceptibility Testing. Clinical and Laboratory Standards Institute , 2017. Available at: https://clsi.org/media/1469/m100s27_sample.pdf /Accessed January 24, 2019.
40. Sharma R, Singh S, Singh GD, Khajuria A, Sidiq T, Singh SK, et al. In vivo genotoxicity evaluation of a plant based antiarthritic and anticancer therapeutic agent Boswelic acids in rodents. Phytomedicine. 2009 Dec;16(12):1112-8.
| Files | ||
| Issue | Vol 16, No 5 (2019) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/fid.v16i5.2287 | |
| Keywords | ||
| Candida albicans Candida glabrata Streptococcus mutans Boswellia serrata Minimum Inhibitory Concentration | ||
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How to Cite
1.
Bakhtiari S, Nematzade F, Hakemi-Vala M, Talebi G. Phenotypic Investigation of the Antimicrobial Effect of Organic and Hydro-Alcoholic Extracts of Boswellia serrata on Oral Microbiota. Front Dent. 2020;16(5):386-392.
