Korean Journal of Food Science and Technology (한국식품과학회지)

Korean Society of Food Science and Technology (한국식품과학회)
권호 표지
DOI QR코드

DOI QR Code

Synergistic Antimicrobial Effect of Sargassum serratifolium (C. Agardh) C. Agardh Extract against Human Skin Pathogens

피부 병원균에 대한 톱니모자반 추출물의 항균 시너지 효과

  • Kim, Yun Hye (Department of Food Science and Technology, Pukyong National University) ;
  • Kim, Ji-Hoon (Department of Food Science and Technology, Pukyong National University) ;
  • Kim, Deok-Hoon (Department of Food Science and Technology, Pukyong National University) ;
  • Kim, Song-Hee (Department of Food Science and Technology, Pukyong National University) ;
  • Kim, Hyeung-Rak (Department of Food Science and Nutrition, Pukyong National University) ;
  • Kim, Young-Mog (Department of Food Science and Technology, Pukyong National University)
  • Received : 2016.03.25
  • Accepted : 2016.05.02
  • Published : 2016.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

The object of this study was to develop an alternative way to treat human skin pathogens using marine algae. During this study, we observed that the ethanolic extract of the edible brown algae [Sargassum serratifolium (C. Agardh) C. Agardh] exhibited potential antimicrobial activity against pathogenic commensal bacteria related with acne vulgaris (Propionibacterium acnes, Staphylococcus epidermidis, Staphylococcus aureus and Pseudomonas aeruginosa), and Candida albicans which causes cutaneous candidiasis. Among the solvent-soluble fractions from the ethanolic extract, a hexane-soluble fraction showed the strongest antimicrobial activity against all tested human skin pathogens with MIC values ranging from 32 to $512{\mu}g/mL$. In addition, the hexane fraction exhibited a synergistic antimicrobial activity with commercial antibiotics used in the treatment of acne vulgaris or cutaneous candidiasis. Thus, this study suggests that S. serratifolium extract could be a potential source of natural antimicrobial agents or a pharmaceutical component against human skin pathogens.

S. aureus, S. epidermidis, P. aeruginosa, P. acnes와 C. albicans는 사람의 피부에서 발생하는 질병과 밀접한 관련을 가지는 대표적인 병원성 미생물로 알려져 있다. 본 연구에서는 해조류 중에서도 항균 활성에 대한 연구가 미미한 모자반을 대상으로 피부 병원균에 대한 항균 효과를 조사하였다. 국내의 연해에 자생하는 7종의 모자반 추출물 중에서 disc diffusion assay와 MIC assay를 통해 가장 뛰어난 항균 효과를 나타낸 톱니모자반을 후속 연구를 위한 후보 물질로 선정하고 연구를 진행하였다. 톱니모자반 추출물의 유기용매 분획층 중에서, 노말-헥세인 분획층이 S. aureus, S. epidermidis, P. aeruginosa, P. acnes 및 C. albicans에 대한 MIC값이 $32-256{\mu}g/mL$로 가장 뛰어난 항균 활성을 나타내었다. 이에 피부 병원균들에 대한 치료제로 사용되고 있지만 내성균의 출현으로 효능이 거의 없는 항생제들인 테트라사이클린, 에리트로마이신, 린코마이신과 플루코나졸과 항균 활성이 뛰어난 것으로 나타난 톱니모자반의 노말-헥세인 분획층과의 병용 사용에 의한 항균 시너지 효과를 조사하였다. 그 결과, 톱니모자반 노말-헥세인 분획층과 이들 항생제와의 병용 사용에 의해 피부 병원균에 대한 항생제와 톱니모자반 노말-헥세인 분획층의 MIC값이 4-32배 감소되었고, 톱니모자반 노말-헥세인 분획층과 이들 항생제와의 병용 시 median FIC값이 0.26-0.55로 항균 시너지 효과를 나타내었다. 즉, 항생제와 톱니모자반 노말-헥세인 분획층과의 병용 사용은 피부 병원균에 대한 이들 항생제의 감수성을 회복시키는데 크게 기여하는 것으로 나타났다.

Keywords

References

  1. Farrar MD, Ingham E. Acne: Inflammation. Clin. Dermatol. 22: 380-384 (2004). https://doi.org/10.1016/j.clindermatol.2004.03.006
  2. Lee JH, Eom SH, Lee EH, Jung YJ, Kim HJ, Jo MR, Son KT, Lee HJ, Kim JH, Lee MS, Kim YM. In vitro antibacterial and synergistic effect of phlorotannins isolated from edible brown seaweed Eisenia bicyclis against acne-related bacteria. Algae 29: 47-55 (2014) https://doi.org/10.4490/algae.2014.29.1.047
  3. Yamaguchi N, Satoh-Yamaguchi K, Ono M. In vitro evaluation of antibacterial, anticollagenase, and antioxidant activities of hop components (Humulus lupulus) addressing acne vulgaris. Phytomedicine 16: 369-376 (2009) https://doi.org/10.1016/j.phymed.2008.12.021
  4. Eom SH, Kang SK, Lee DS, Myeong JI, Lee J, Kim HW, Kim KH, Je JY, Jung WK, Kim YM. Synergistic antibacterial effect and antibacterial action mode of chitosan-ferulic acid conjugate against methicillin-resistant Staphylococcus aureus. J. Microbiol. Biotechnol. 26: 784-789 (2016) https://doi.org/10.4014/jmb.1511.11046
  5. Kim SY, Kim YM, Kim EJ, Lee MS. Synergistic antibacterial activity of Ecklonia cava extract against antibiotic resistant Enterococcus faecalis. Korean J. Fish. Aquat. Sci. 48: 51-57 (2015) https://doi.org/10.5657/KFAS.2015.0051
  6. Ravenscroft J. Evidence based update on the management of acne. Arch. Dis. Child. Educ. Pract. Ed. 90: ep98-ep101 (2005)
  7. Abad MJ, Bedoya LM, Bermejo P. Natural marine anti-inflammatory products. Mini Rev. Med. Chem. 8: 740-754 (2008) https://doi.org/10.2174/138955708784912148
  8. Gupta S, Abu-Ghannam N. Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci. Technol. 22: 315-326 (2011) https://doi.org/10.1016/j.tifs.2011.03.011
  9. Choi JS, Bae HJ, Kim SJ, Choi IS. In vitro antibacterial and antiinflammatory properties of seaweed extracts against acne inducing bacteria, Propionibacterium acnes. J. Environ. Biol. 32:313-318 (2011)
  10. Choi JS, Lee K, Lee BB, Kim YC, Kim YD, Hong YK, Cho KK, Choi IS. Antibacterial activity of the phlorotannins dieckol and phlorofucofuroeckol-A from Ecklonia cava against Propionibacterium acnes. Bot. Sci. 92: 425-431 (2014)
  11. Oak JH, Lee IK. Taxonomy of the genus Sargassum (Fucales, Phaeophyceae) from Korea II. subgenus Bactrophycus section Halochloa and Repentia. Algae 21: 393-405 (2006) https://doi.org/10.4490/ALGAE.2006.21.4.393
  12. Ahn SM, Hong YK, Kwon GS, Sohn HY. Evaluation of antioxidant and nitrite scavenging activity of seaweed extracts. J. Life Sci. 21: 576-583 (2011) https://doi.org/10.5352/JLS.2011.21.4.576
  13. Bae SJ. Anticarcinogenic effects of Sargassum fulvellum fractions on several human cancer cell lines in vitro. J. Korean Soc. Food Sci. Nutr. 33: 480-486 (2004) https://doi.org/10.3746/jkfn.2004.33.3.480
  14. Kim JY, Lee JA, Kim KN, Yoon WJ, Lee WJ, Park SY. Antioxidative and antimicrobial activities of Sargassum muticum extracts. J. Korean Soc. Food Sci. Nutr. 36: 663-669 (2007) https://doi.org/10.3746/jkfn.2007.36.6.663
  15. Joung EJ, Lee MS, Choi JW, Kim JS, Shin TS, Jung BM, Yoon NY, Lim CW, Kim JI, Kim HR. Anti-inflammatory effect of ethanolic extract from Myagropsis myagroides on murine macrophages and mouse ear edema. BMC Complement. Altern. Med. 12:171 (2012) https://doi.org/10.1186/1472-6882-12-171
  16. Kang CW, Park MS, Kim NH, Lee JH, Oh CW, Kim HR, Kim GD. Hexane extract from Sargassum serratifolium inhibits the cell proliferation and metastatic ability of human glioblastoma U87MG cells. Oncol. Rep. 34:2602-268 (2015) https://doi.org/10.3892/or.2015.4222
  17. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Forth Informational Supplement. CLSI document M100-S24, Wayne, PA, USA. (2014)
  18. Hsieh MH, Yu CM, Yu VL, Chow JW. Synergy assessed by checkerboard: A critical analysis. Diagn. Microbiol. Infect. Dis. 16: 343-349 (1993) https://doi.org/10.1016/0732-8893(93)90087-N
  19. Choi JG, Kang OK, Brice OO, Lee YS, Chae HS, Oh YC, Sohn DH, Park Y, Choi HG, Kim SG, Shin DW, Kwon DY. Antibacterial activity of Ecklonia cava against methicillin-resistant Staphylococcus aureus and Salmonella spp. Foodborne Path. Dis. 7:435-441(2010) https://doi.org/10.1089/fpd.2009.0434
  20. Gollnick H, Cunliffe W, Berson D, Dreno B, Finlay A, Leyden JJ, Shalita AR, Thiboutot D. Management of acne: A report from a global alliance to improve outcomes in acne. J. Am. Acad. Dermatol. 49: S1-S37 (2003) https://doi.org/10.1067/mjd.2003.618
  21. Han SM, Lee KG, Yeo JH, Baek HJ, Park KK. Antibacterial and anti-inflammatory effects of honeybee (Apis mellifera) venom against acne-inducing bacteria. J. Med. Plants Res. 4: 459-464 (2010)
  22. Pfaller MA, Diekema DJ, Sheehan DJ. Interpretive breakpoints for fluconazole and Candida revisited:a blueprint for the future of antifungal susceptibility testing. Clin. Microbiol. Rev. 19: 435-447 (2006) https://doi.org/10.1128/CMR.19.2.435-447.2006
  23. Soussy CJ, Cluzel R, Courvalin P. Definition and determination of in vitro antibiotic susceptibility breakpoints for bacteria in France. Eur. J. Clin. Microbiol. Infect. Dis.13: 238-246 (1994) https://doi.org/10.1007/BF01974543
  24. Fothergill AW, Sutton DA, McCarthy DI, Wiederhold NP. Impact of new antifungal breakpoints on antifungal resistance in Candida species. J. Clin. Microbiol. 52: 994-997 (2014) https://doi.org/10.1128/JCM.03044-13
  25. Eady EA, Farmery MR, Ross JI, Cove JH, Cunliffe WJ. Effects of benzoyl peroxide and erythromycin alone and in combination against antibiotic-sensitive and -resistant skin bacteria from acne patients. Br. J. Dermatol. 131: 331-336 (1994) https://doi.org/10.1111/j.1365-2133.1994.tb08519.x
  26. Eady EA, Bojar RA, Jones CE, Cove JH, Holland KT, Cunliffe WJ. The effects of acne treatment with a combination of benzoyl peroxide and erythromycin on skin carriage of erythromycin resistant propionibacteria. Br. J. Dermatol. 134: 107-113 (1996) https://doi.org/10.1111/j.1365-2133.1996.tb07847.x
  27. Eom SH, Kim DH, Lee SH, Yoon NY, Kim JH, Kim TH, Chung YH, Kim SB, Kim YM, Kim HW, Lee MS, Kim YM. In vitro antibacterial activity and synergistic antibiotic effects of phlorotannins isolated from Eisenia bicyclis against methicillin-resistant Staphylococcus aureus. Phytother. Res. 27: 1260-1264 (2013) https://doi.org/10.1002/ptr.4851
  28. Nshimiyumukiza O, Kang SK, Kim HJ, Lee EH, Han HN, Kim YH, Kim DH, Kim JH, Eom SH, Kim YM. Synergistic antibacterial activity of Ecklonia cava (Phaeophyceae: Laminariales) against Listeria monocytogenes (Bacillales: Listeriaceae). Fish. Aquat. Sci. 18: 1-6 (2015)

Cited by

  1. Anti-inflammatory Effects of Chitosan-phytochemical Conjugates against Propionibacterium acnes-induced Inflammation vol.49, pp.5, 2016, https://doi.org/10.5657/KFAS.2016.0589
  2. Synergistic Antibacterial Effects of Chitosan-Caffeic Acid Conjugate against Antibiotic-Resistant Acne-Related Bacteria vol.15, pp.6, 2017, https://doi.org/10.3390/md15060167
  3. Antibacterial Property of Ecklonia cava Extract against Marine Bacterial Pathogens vol.31, pp.5, 2016, https://doi.org/10.13103/JFHS.2016.31.5.380
  4. BACE1 inhibitory activity and molecular docking analysis of meroterpenoids from Sargassum serratifolium vol.25, pp.15, 2017, https://doi.org/10.1016/j.bmc.2017.05.033
  5. α-Glucosidase and Protein Tyrosine Phosphatase 1B Inhibitory Activity of Plastoquinones from Marine Brown Alga Sargassum serratifolium vol.15, pp.12, 2017, https://doi.org/10.3390/md15120368