Anti-Aspergillus Activities of the Ligusticum chuanxiong Essential Oil Alone and in Combination with Antibiotics

  • Sim, Youn (College of Pharmacy, Duksung Women's University) ;
  • Shin, Seung-Won (College of Pharmacy, Duksung Women's University)
  • Received : 2010.08.10
  • Accepted : 2010.09.13
  • Published : 2010.09.30

Abstract

The present study aimed to assess the antifungal properties of the essential oil fraction from Ligusticum chuanxiong (Umbelliferae) and its components against five clinically important Aspergillus species. The essential oil fraction was extracted from the underground parts of the plant by steam distillation, and its main components, namely, Z-ligustilide, butylidene phthalide, and p-cresol were isolated by column chromatography. The antifungal activities of the essential oils were evaluated by the broth dilution method. Both the total essential oil fraction of L. chuanxiong and its components showed significant anti-Aspergillus activity against all five tested strains with MICs between 62.5 and 250 ${\mu}g$/ml, respectively. In a checkerboard microtiter assay, the combination of antibiotics, itraconazole with the essential oil fraction of L. chuanxiong or its main components exhibited synergistic or additive, and in some cases indifferent, effects against the tested Aspergillus species, resulting in FICIs (fractional inhibiting concentration indices) ranging from 0.12 to 2, while the combination of antibiotics, amphothericin B with L. chuanxiong essential oils mostly showed antagonistic effects.

Keywords

References

  1. Beck, J.J. and Chou, S.C., The Structural diversity of phthalides from the apiaceae J. Nat. Prod., 70, 891-900 (2007). https://doi.org/10.1021/np0605586
  2. Beernaert, L.A., Pasmans, F., Waeyenberghe, L., Dorrestein, G.M., Verstappen, F., Vercammen, F., Haesebrouck, F., and Martel, A., Avian Aspergillus fumigatus strains resistant to both itraconazole and voriconazole. Antimicrob. Agents Chemother. 53, 2199-2201 (2009). https://doi.org/10.1128/AAC.01492-08
  3. Bidlack, W.R., Omaye, S.T., Meskin, M.S., and Topham, D., Phytochemicals as bioactive agents. Technomic Publishing Company, Lancaster, pp. 106-110, 2000.
  4. Cuenca-Estrella, M., Gomez-Lopez, A., Garcia-Effron, G., Alcazar-Fuoli, L., Mellado, E., Buitrago, M.J., and Rodriguez-Tudela, J.L., Combined Activity In Vitro of Caspofungin, Amphotericin B, and Azole Agents against Itraconazole-Resistant Clinical Isolates of Aspergillus fumigates. Antimicrob. Agents Chemother. 49, 1232-1235 (2005). https://doi.org/10.1128/AAC.49.3.1232-1235.2005
  5. Dagenais, T.R.T. and Keller, N.P., Pathogenesis of Aspergillus fumigatus in invasive Aspergillosis. Clin. Microbiol. Rev. 22, 447-465 (2009). https://doi.org/10.1128/CMR.00055-08
  6. Davidson, P.M. and Parish, M.E., Methods for testing the efficacy of food antimicrobials. Food Technol. 43, 148-155 (1989).
  7. Denning, D. W., Aspergillosis: diagnosis and treatment. Int. J. Antimicrob. Agents 6, 161-168 (1996). https://doi.org/10.1016/0924-8579(95)00042-9
  8. Engelhart, S., Loock, A., Skutlarek, D., Sagunski, H., Lommel, A., Färber, H., and Exner, M., Occurrence of toxigenic Aspergillus versicolor isolates and sterigmatocystin in carpet dust from damp indoor environments. Appl. Env. Microbiol. 68, 3886-3890 (2002). https://doi.org/10.1128/AEM.68.8.3886-3890.2002
  9. Hachem, R., Kontoyiannis, D., Boktour, M.R., Afif, C., Cooksley, C., Bodey, G.P., Chatzinikolaou, I., Perego, C., Kantarjian, H.M., and Raad, I.I., Aspergillus terreus: an emerging amphotericin B-resistant opportunistic mold in patients with hematologic malignancies. Cancer, 101, 1594-1600 (2004). https://doi.org/10.1002/cncr.20554
  10. Ibrahim, A.S, Gebremariam, T., French, S.W., Edwards, J.E., and Spellberg, B., The iron chelator deferasirox enhances liposomal amphotericin B efficacy in treating murine invasive pulmonary aspergillosis. J. Antimicrob. Chemother. 65, 289-292 (2010). https://doi.org/10.1093/jac/dkp426
  11. Lee, Y.M., Dang, H.D., Hong, J., Lee, C.-O., Bae, K.S., Kim, D.-K., and Jung, J.H., A Cytotoxic Lipopeptide from the Sponge-Derived Fungus Aspergillus versicolor. Bull. Korean Chem. Soc. 31, 205-208 (2010). https://doi.org/10.5012/bkcs.2010.31.01.205
  12. Lestner, J., Howard, S.J., Goodwin, J., Gregson, L., Majithiya, J., Walsh, T.J., Jensen, G. M., and Hope, W.W., Pharmacokinetics and pharmacodynamics of amphotericin B deoxycholate, liposomal amphotericin B, and amphotericin B lipid complex in an in vitro model of invasive pulmonary aspergillosis. Antimicrob. Chemother. 54, 3432-3441 (2010). https://doi.org/10.1128/AAC.01586-09
  13. Lin, C.M., Tsai, Y.H., Huang, C.C., Lee, C.H., Chiang, P.C., Huang, S.F., and Liu, H.P., Invasive pulmonary aspergillosis and pulmonary cryptococcosis really coexist in immunocompromised host. J. Infec. 53, 55-58 (2006). https://doi.org/10.1016/j.jinf.2005.10.017
  14. Otsubo, T., Maesaki, S., Hossain, M.A., Yamamoto, Y., Tomono, K., Tashiro, T., Seki, J., Tomii, Y., Sonoke, S., and Kohno, S., In vitro and in vivo activities of NS-718, a new lipid nanosphere incorporating amphotericin B against Aspergillus fumigatus. Antimicrob. Agents Chemother. 43, 471-475 (1999).
  15. Packer, L., Ong, C.N., and Halliwell, B., Herbal and traditiional medicne, Marcel Dekker, New York, pp.247-254, 2004.
  16. Scholar, E.M. and Pratt, W.B., Animicrobial Drugs. Oxford Press, New York, pp. 336-353, 2000.
  17. Shin, S., Anti-Aspergillus activities of plant essential oils and their combination effects with ketoconazole or amphotericin B. Arch. Pharm. Res. 26, 389-393 (2003). https://doi.org/10.1007/BF02976696
  18. Shin, S. and Lim, S., Antifungal effects of herbal essential oils alone and in combination with ketoconazole against Trichophyton spp. J. Appl. Mirobiol. 97, 1289-1296 (2004). https://doi.org/10.1111/j.1365-2672.2004.02417.x
  19. Sim, Y. and Shin, S., Combinatorial anti-Trichophyton effects of Ligusticum chuanxiong essential oil components with antibiotics. Arch. Pharm. Res. 31, 497-502 (2008). https://doi.org/10.1007/s12272-001-1184-7
  20. Srebrnik, A., Levtov, S., Ben-Ami, R., and Brenner, S., Liver failure and transplantation after itraconazole treatment for toenail onychomycosis. J. Eur. Acad. Derm. Venereol. 19, 205-207 (2005). https://doi.org/10.1111/j.1468-3083.2005.00943.x
  21. Vanhee, L.M.E., Perman, D., Nelis, H. J., and Coenye, T., Rapid quantification of itraconazole-resistant Aspergillus fumigates in air. J. Microbiol. Meth. 81, 197-199 (2010). https://doi.org/10.1016/j.mimet.2010.02.012
  22. Veraldi, S., Chiaratti, A., and Harak, H., Onychomycosis caused by Aspergillus versicolor. Mycoses 53, 363-365 (2010).
  23. Wang, J., Du., J.-R., Wang, Y., Kuang, X., and Wang, C.-Y., Z-ligustilide attenuates lipopolysaccharide-induced proinflammatory response via inhibiting NF-kB pathway in primary rat microglia. Acta Pharmacol. Sin. 31, 791-797 (2010). https://doi.org/10.1038/aps.2010.71
  24. Winterstein, A., Bohndorf, K., Vollert, K., Wagner, T., Gnekow, A., and Roemer, F., Invasive aspergillosis osteomyelitis in children-a case report and review of the literature. Skeletal Radiol. 39, 827-831 (2010). https://doi.org/10.1007/s00256-010-0967-4
  25. Xavier, M.O., Pasqualotto, A.C. Sales, M.D.P.U., Severo, C.B., Camargo, J.J.P., and Severo, L.C., Invasive pulmonary aspergillosis due to a mixed infection caused by Aspergillus flavus and Aspergillus fumigates. Rev. Iberoam. Micol. 25, 176-178 (2008). https://doi.org/10.1016/S1130-1406(08)70041-X
  26. Xu, H., Chen, W., Li, L., Wan, Z., Li, R., and Liu, W., Clinical itraconazole-resistant strains of Aspergillus fumigates, isolated serially from a lung aspergilloma patient with pulmonary tuberculosis, can be detected with real-time PCR method. Mycopathologia 169, 193-199 (2010). https://doi.org/10.1007/s11046-009-9249-x
  27. Yuchong, C., Dingheng, Z., Zhizhong, Y., Hongyu, Y., Jing, H., and Jianghan, C., Aspergillosis of biliary tract after liver transplantation: a case report. Mycopathologia 170, 117-121 (2010). https://doi.org/10.1007/s11046-010-9300-y
  28. Zhang, C., Qi, M., Shao, Q., Zhou, S., and Fu, R., Analysis of the volatile compounds in Ligusticum chuanxiong Hort. using HS-SPME-GC-MS. J. pharmaceut. Biomed,, 44, 464-470 (2007). https://doi.org/10.1016/j.jpba.2007.01.024
  29. Zhirong, Y., Wanqing, L., and Weihua, P., Invasive pulmonary aspergillosis in non-neutropenic patients treated with liposomal amphotericin B. Mycoses, 42, 679-682 (1999). https://doi.org/10.1046/j.1439-0507.1999.00508.x