DOI QR코드

DOI QR Code

Antifungal Activity of Bee Venom and Sweet Bee Venom against Clinically Isolated Candida albicans

  • Lee, Seung-Bae (Division of Animal Resources and Life Science, Sangji University)
  • Received : 2015.11.04
  • Accepted : 2016.12.21
  • Published : 2016.03.31

Abstract

Objectives: The purpose of this study was to investigate the antifungal effect of bee venom (BV) and sweet bee venom (SBV) against Candida albicans (C. albicans) clinical isolates. Methods: In this study, BV and SBV were examined for antifungal activities against the Korean Collection for Type Cultures (KCTC) strain and 10 clinical isolates of C. albicans. The disk diffusion method was used to measure the antifungal activity and minimum inhibitory concentration (MIC) assays were performed by using a broth microdilution method. Also, a killing curve assay was conducted to investigate the kinetics of the anti-fungal action. Results: BV and SBV showed antifungal activity against 10 clinical isolates of C. albicans that were cultured from blood and the vagina by using disk diffusion method. The MIC values obtained for clinical isolates by using the broth microdilution method varied from $62.5{\mu}g/mL$ to $125{\mu}g/mL$ for BV and from $15.63{\mu}g/mL$ to $62.5{\mu}g/mL$ for SBV. In the killing-curve assay, SBV behaved as amphotericin B, which was used as positive control, did. The antifungal efficacy of SBV was much higher than that of BV. Conclusion: BV and SBV showed antifungal activity against C. albicans clinical strains that were isolated from blood and the vagina. Especially, SBV might be a candidate for a new antifungal agent against C. albicans clinical isolates.

References

  1. Odds FC. Candida species and virulence. Am Soc Microbiol News. 1994;60(6):313-8.
  2. Verduyn Lunel FM, Meis JF, Voss A. Nosocomial fungal infections: candidemia. Diagn Microbiol Infect Dis. 1999;34(3):213-20. https://doi.org/10.1016/S0732-8893(99)00035-8
  3. McNeil MM, Nash SL, Hajjeh RA, Phelan MA, Conn LA, Pilkaytis BD, et al. Trends in mortality due to invasive mycotic diseases in the United States, 1980-1997. Clin Infect Dis. 2001;33(5):641-7. https://doi.org/10.1086/322606
  4. Bodey GP. The emergence of fungi as major hospital pathogens. J Hosp Infect. 1988;11(Suppl A):411-26. https://doi.org/10.1016/0195-6701(88)90220-4
  5. Edwards JE Jr. Invasive candida infections-evolution of a fungal pathogen. N Engl J Med. 1991;324(15):1060-2. https://doi.org/10.1056/NEJM199104113241511
  6. Fisher-Hoch SP, Hutwagner L. Opportunistic candidiasis: an epidemic of the 1980s. Clin Infect Dis. 1995;21(4):897-904. https://doi.org/10.1093/clinids/21.4.897
  7. Edwards JE Jr, Bodey GP, Boeden RA, Buchner T, DePauw BE, Filler SG, et al. International conference for the development of a consensus on the management and prevention of severe candidal infections. Clin Infect Dis. 1997;25(1):43-59. https://doi.org/10.1086/514504
  8. Anttila VJ, Ruutus P, Bondestam S, Jansson SE, Nordling S, Farkkila M, et al. Hepatosplenic yeast infection in patients with acute leukemia: a diagnostic problem. Clin Infect Dis. 1994;18(6):979-81. https://doi.org/10.1093/clinids/18.6.979
  9. Gallis HA, Drew RH, Pickard WW. Amphotericin B: 30 years of clinical experience. Rev Infect Dis. 1990;12(2):308-29. https://doi.org/10.1093/clinids/12.2.308
  10. Hartsel S, Bolard J. Amphotericin B: new life for an old drug. Trends Pharmacol Sci. 1996;17(12):445-9. https://doi.org/10.1016/S0165-6147(96)01012-7
  11. Matsuoka S, Murata M. Cholesterol markedly reduces ion permeability induced by membrane-bound amphotericin B. Biochim Biophys Acta. 2002;1564(2):429-34. https://doi.org/10.1016/S0005-2736(02)00491-1
  12. Fonos V, Cataldi L. Amphotericin B-induced nephrotoxicity: a review. J Chemother. 2000;12(6):463-70. https://doi.org/10.1179/joc.2000.12.6.463
  13. Mayer J, Doubek M, Doubek J, Horky D, Scheer P, Stepanek M. Reduced nephrotoxicity of conventional amphotericin B therapy after minimal nephroprotective measures: animal experiments and clinical study. J Infect Dis. 2002;186(3):379-88. https://doi.org/10.1086/341662
  14. Chee HY, Kim H, Lee MH. In vitro antifungal activity of limonene against trichophyton rubrum. Microbiology. 2009;37(3):243-46.
  15. Kwon YB, Lee HJ, Han HJ, Mar WC, Kang SK, Yoon OB, et al. The water-soluble fraction of bee venom produces anti-nociceptive and antiinflammatory effects on rheumatoid arthritis in rats. Life Sci. 2002;71(2):191-204. https://doi.org/10.1016/S0024-3205(02)01617-X
  16. Kim HW, Kwon YB, Ham TW, Rho DH, Yoon SY, Lee JH, et al. Acupoint stimulation using bee venom attenuates formalin induced pain behavior and spinal cord fos expression in rats. J Vet Med Sci. 2003;65(3):349-55. https://doi.org/10.1292/jvms.65.349
  17. Han SM, Lee KG, Yeo JH, Kweon HY, Kim BS, Kim JM, et al. Antibacterial activity of the honey bee venom against bacterial mastitis pathogens infecting dairy cows. Int J Indust Entomol. 2007;14(2):137-42.
  18. Lee SM, Lim J, Lee JD, Choi DY, Lee S. Bee venom treatment for refractory postherpetic neuralgia: a case report. J Altern Complement Med. 2014;20(3):212-4. https://doi.org/10.1089/acm.2013.0130
  19. Choi SH, Cho SK, Kang SS, Bae CS, Bai YH, Lee SH, et al. Effect of apitherapy in piglets with preweaning diarrhea. Am J Chin Med. 2003;31(2):321-6. https://doi.org/10.1142/S0192415X03001004
  20. Park HJ, Lee SH, Son DJ, Oh KW, Kim KH, Song HS, et al. Anti-arthritic effect of bee venom: inhibition of inflammation mediator generation by suppression of NF-B through interaction with the p50 subunit. Arthritis Rheum. 2004;50(11):3504-15. https://doi.org/10.1002/art.20626
  21. Choi YG, Choi SH, Kwon KR. [Purification of peptide components including melitittin from bee venom using gel filtration chromatography and propionic acid/urea polyacrylamide gel electrophoresis]. J Pharmacopuncture. 2006;9(2):105-11. Korean. https://doi.org/10.3831/KPI.2006.9.2.105
  22. Eiseman JL, Von Bredow J, Alvares AP. Effect of honeybee (Apis mellifera) venom on the course of adjuvant-induced arthritis and depression of drug metabolism in the rat. Biochem Pharmacol. 1982;31(6):1139-46. https://doi.org/10.1016/0006-2952(82)90354-9
  23. Akdis CA, Akdis M, Blesken T, Wymann D, Alkan SS, Muller U, et al. Epitope-specific T cell tolerance to phospholipase A2 in bee venom immunotherapy and recovery by IL-2 and IL-15 in vitro. J Clin Invest. 1996;98(7):1676-83. https://doi.org/10.1172/JCI118963
  24. Kwon YB, Lee JD, Lee HJ, Han HJ, Mar WC, Kang SK, et al. Bee venom injection into an acupuncture point reduces arthritis associated edema and nociceptive responses. Pain. 2001;90(3):271-80. https://doi.org/10.1016/S0304-3959(00)00412-7
  25. Espinel-Ingroff A, Barchiesi F, Cuenca-Estrella M, Pfaller MA, Rinaldi M, Rodriguez-Tudela JL, et al. International and multicenter comparison of EUCAST and CLSI M27-A2 broth microdilution methods for testing susceptibilities of Candida spp. to fluconazole, itraconazole, posaconazole, and voriconazole. J Clin Microbiol. 2005;43(8):3884-9. https://doi.org/10.1128/JCM.43.8.3884-3889.2005
  26. Klepser ME, Ernst EJ, Lewis RE, Ernst ME, Pfaller MA. Influence of test conditions on antifungal time-kill curve results: proposal for standardized methods. Antimicrob Agents Chemother. 1998;42(5):1207-12.
  27. Owens WE, Nickerson SC, Boddie RL, Tomita GM, Ray CH. Prevalence of mastitis in dairy heifers and effectiveness of antibiotic therapy. J Dairy Sci. 2001;84(4):814-7. https://doi.org/10.3168/jds.S0022-0302(01)74538-9
  28. Pitkala A, Haveri M, Pyorala S, Myllys V, Honkanen-Buzalski T. Bovine mastitis in Finland 2001-prevalence, distribution of bacteria, and antimicrobial resistance. J Dairy Sci. 2004;87(8):2433-41. https://doi.org/10.3168/jds.S0022-0302(04)73366-4
  29. Nair MK, Joy J, Vasudevan P, Hinckley L, Hoagland TA, Venkitanarayanan KS. Antibacterial effect of caprylic acid and monocaprylin on major bacterial mastitis pathogens. J Dairy Sci. 2005;88(10):3488-95. https://doi.org/10.3168/jds.S0022-0302(05)73033-2
  30. Komine Y, Komine K, Kai K, Itagaki M, Kuroishi T, Aso H, et al. Effect of combination therapy with lactoferrin and antibiotics against staphylococcal mastitis on drying cows. J Vet Med Sci. 2006;68(3):205-11. https://doi.org/10.1292/jvms.68.205
  31. Fennell JF, Shipman WH, Cole LJ. Antibacterial action of melittin, a polypeptide from the venom. Proc Soc Exp Biol Med. 1968;127(3):707-10. https://doi.org/10.3181/00379727-127-32779
  32. Somerfield SD, Stach JL, Mraz C, Gervais F, Skamene E. Bee venom inhibits superoxide production by human neutrophils. Inflammation. 1984;8(4):385-91. https://doi.org/10.1007/BF00918214
  33. Saini SS, Peterson JW, Chopra AK. Melittin binds to secretory phospholipase A2 and inhibits its enzymatic activity. Biochem Biophys Res Commun. 1997;238(2):436-42. https://doi.org/10.1006/bbrc.1997.7295
  34. Stocker JF, Traynor JR. The action of various venoms on Escherichia coli. J Appl Bacteriol. 1986;61(5):383-8. https://doi.org/10.1111/j.1365-2672.1986.tb04300.x
  35. Perumal Samy R, Gopalakrishnakone P, Thwin MM, Chow TK, Bow H, Yap EH, et al. Antibacterial activity of snake, scorpion and bee venoms: a comparison with purified venom phospholipase A2 enzymes. J Appl Microbiol. 2007;102(3):650-9. https://doi.org/10.1111/j.1365-2672.2006.03161.x
  36. Nakatuji T, Kao MC, Fang JY, Zouboulis CC, Zhang L, Gallo RL, et al. Antimicrobial property of lauric acid against Propionibacterium acnes: Its therapeutic potential for inflammatory acne vulgaris. J Invest Dermatol. 2009;129(10):2480-8. https://doi.org/10.1038/jid.2009.93
  37. 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. 2010;4(6):459-64.
  38. Yu AR, Kim JJ, Park GS, Oh SM, Han CS, Lee MY. The antifungal activity of bee venom against dermatophytes. J Appl Biol Chem. 2012;55(1):7-11. https://doi.org/10.3839/jabc.2011.052
  39. Seoung IW. Antifungal activity of the extracts from Galla rhosis against Candida albicans. Korean J Med Mycol. 2007;12(4):175-9.
  40. Seoung IW. Antifungal activity of the extracts from Paeonia japonica against Candida albicans. Korean J Med Mycol. 2006;11(1):19-26.

Cited by

  1. Synergistic antimicrobial activity ofBoswellia serrataRoxb. ex Colebr. (Burseraceae) essential oil with various azoles against pathogens associated with skin, scalp and nail infections vol.63, pp.6, 2016, https://doi.org/10.1111/lam.12683
  2. Honeybee venom: influence of collection on quality and cytotoxicity vol.47, pp.10, 2017, https://doi.org/10.1590/0103-8478cr20160486
  3. : A Novel Approach of Bee Venom Study for Possible Emerging Antifungal Agent vol.30, pp.2, 2018, https://doi.org/10.5021/ad.2018.30.2.202