Testing of antifungal natural products: Methodologies, comparability of results and assay choice

Phytochemical Analysis

Volumn 11, Issue 3, 2000, Pages 137-147

  Hadacek, Franz ^a   Greger, Harald ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

Antifungal bioassay; Bioautography on thin layer plates; Botrytis cinerea; Cladosporium herbarum; Disk diffusion; Falcarindiol; Fusarium avenaceum; Juglone; Microdilution; Radial growth

Indexed keywords

DIFFUSION; FUNGI; KETONES;

ANTIFUNGAL BIOASSAY; ANTIFUNGALS; BIOAUTOGRAPHY; BIOAUTOGRAPHY ON THIN- LAYER PLATE; BOTRYTIS CINEREA; CLADOSPORIUM HERBARUM; DISK DIFFUSION; FALCARINDIOL; FUSARIUM AVENACEUM; JUGLONE; MICRODILUTION; RADIAL-GROWTH; THIN LAYERS;

BIOASSAY;

ANTIFUNGAL AGENT; FALCARINDIOL; FLUORESCEIN DIACETATE; JUGLONE; NAPHTHOQUINONE; NATURAL PRODUCT; POLYACETYLENE;

ANTIFUNGAL ACTIVITY; ARTICLE; BIOASSAY; BOTRYTIS CINEREA; CLADOSPORIUM; CONTROLLED STUDY; DIFFUSION; DILUTION; FUSARIUM; GROWTH RATE; IMAGE ANALYSIS; INTERMETHOD COMPARISON; METHODOLOGY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; SCORING SYSTEM; THIN LAYER CHROMATOGRAPHY;

BOTRYOTINIA FUCKELIANA; BOTRYTIS; BOTRYTIS CINEREA; CLADOSPORIUM; CLADOSPORIUM HERBARUM; DAVIDIELLA TASSIANA; FUNGI; FUSARIUM; FUSARIUM AVENACEUM; GIBBERELLA AVENACEA;

EID: 0034101553     PISSN: 09580344     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1099-1565(200005/06)11:3<137::AID-PCA514>3.0.CO;2-I     Document Type: Article

References (79)

1. Adam K, Sivropoulou A, Kokkini S, Lanaras T, Arsenakis M. 1998. Antifungal activities of Origanum vulgare subsp. hirtum, Mentha spicata, Lavandula angustifolia, and Salvia fruticosa essential oils against human pathogenic fungi. J Agric Food Chem 46: 1739-1745.
2. Barchiesi F, Del Poeta M, Morbiducci V, Ancarani F, Scalise G. 1993. Turbidimetric and visual criteria for determining the in vitro activity of six antifungal agents against Candida spp. and Cryptococcus neoformans. Mycopathologia 124: 19-25.
3. Bartley MR, Youle D. 1996. The use of in vitro and in vivo bioassays to screen for novel agrochemicals: approaches to experimental design. In Bioactive Compound Design: Possibilities for Industrial Use Ford MG, Greenwood R, Brooks GT and Franke R (eds), BIOS: Oxford; 15-35.
4. Bauer AW, Kirby WMM, Sherris JC, Turck M. 1966. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45: 493-496.
5. Betina V. 1973. Bioautography in paper and thin-layer chromatography and its scope in the antibiotic field. J Chromatogr 78: 41-51.
6. Bode HR. 1958. Beiträge zur Kenntnis allelopathischer Erscheinungen bei einigen Juglandaceen. Planta 51: 440-480.
7. Broekaert WF, Terras FRG, Cammue BPA, Vanderleyden J. 1990. An automated quantitative assay for fungal growth inhibition. FEMS Microbiol Lett 69: 55-60.
8. Brownlee HE, Hedger J, Scott IM. 1990. Host extracts cause morphological variation in germ-tubes of the cocoa pathogen, Crinipellis perniciosa. Mycol Res 94: 543-547.
9. Calhoun DL, Roberts GD, Galgiani JN, Bennett JE, Feingold DS, Jorgensen J, Kobayashi GS, Shadomy S. 1986. Results of a survey of antifungal susceptibility tests in the United States and interlaboratory comparison of broth dilution testing of flucytosine and amphotericin B. J Clin Microbiol 23: 298-301.
10. Chand S, Lusunzi I, Veal DA, Williams LR, Karuso P. 1994. Rapid screening of the antimicrobial activity of extracts and natural products. J Antibiot 47: 1295-1304.
11. Clancy CJ, Nguyen MH. 1997. Comparison of a photometric method with standardized methods of antifungal susceptibility testing of yeasts. J Clin Microbiol 35: 2878-2882.
12. Cole MD. 1994. Key antifungal, antibacterial and anti-insect assays - a critical review. Biochem Syst Ecol 22: 837-856.
13. Coleman T, Madassery JV, Kobayashi GS, Nahm MH, Little JR. 1989. New fluorescence assay for the quantitation of fungi. J Clin Microbiol 27: 2003-2007.
14. Cormican MG, Pfaller MA. 1996. Standardization of antifungal susceptibility testing. J Antimicrob Chemother 38: 561-578.
15. De Beer EJ, Sherwood MB. 1945. The paper-disk agar plate method for the assay of antibiotic substances. J Bacteriol 30: 459-468.
16. De Bolle MFC, Goderis IJ, Terras FRG, Cammue BPA, Broekaert WF. 1991. A technique for detecting antifungal activity of proteins separated by polyacrylamide gel electrophoresis. Electrophoresis 12: 442-444.
17. Del Poeta M, Barchiesi F, Arzeni D, Marinucci G, Scalise G. 1994. Turbidimetric and visual criteria for in vitro susceptibility testing of Cryptococcus neoformans clinical isolates. Mycoses 37: 411-416.
18. Dhingra OD, Sinclair JB. 1995. Basic Plant Pathology Methods. Lewis Publishers: Boca Raton, FL.
19. Elgersma DM, Weijman ACM, Roeymans HJ, van Eijk GW. 1984. Occurrence of falcarinol and falcarindiol in tomato plants after infection with Verticillium albo-atrum after characterization of four phytoalexins by capillary gas chromatography-mass spectroscopy. Phytopath Z 109: 237-240.
20. Ericson HM, Sherris JC. 1971. International collaborative study on antibiotic sensitivity testing. Acta Pathol Microbiol Scand Sect B (Suppl.) 217: 3-88.
21. Espinel-Ingroff A. 1998. In vitro activity of the new triazole voriconazole (UK-109,496) against opportunistic filamentous and dimorphic fungi and common and emerging yeast pathogens. J Clin Microbiol 36: 198-202.
22. Espinel-Ingroff A, Kerkering TM, Goldsom PR, Shadomy S. 1991. Comparison study of broth macrodilution and microdilution antifungal susceptibility tests. J Clin Microbiol 29: 1089-1094.
23. Espinel-Ingroff A, Dawson K, Pfaller M, Anaissie E, Breslin B, Dixon D, Fothergill A, Paetznick V, Peter J, Rinaldi M, Walsh T. 1995. Comparative and collaborative evaluation of standardization of antifungal susceptibility testing for filamentous fungi. Antimicrob Agents Chemother 39: 314-19.
24. Espinel-Ingroff A, Bartlett M, Bowden R, Chin NX, Cooper C, Fothergill A, McGinnis MR, Menezes P, Messer SA, Nelson PW, Odds FC, Pasarell L, Peter J, Pfaller MA, Rex JH, Rinaldi MG, Shankland GS, Walsh TJ, Weitzman I. 1997. Multicenter evaluation of proposed standardized procedure for antifungal susceptibility testing of filamentous fungi. J Clin Microbiol 35: 139-143.
25. Finney JD. 1971. Probit Analysis. Cambridge University Press: Cambridge.
26. Finney JD. 1978. Statistical Methods in Biological Assay. Charles Griffin: London.
27. Forbes TL. 1993. The design and analysis of concentration-response experiments. In Handbook of Ecotoxicology, Vol. 1 Calow P (ed.), Blackwell Scientific: Oxford; 438-459.
28. Gadd GM. 1986. Toxicity screening using fungi and yeasts. In Toxicity Testing Using Microorganisms, Vol. II Dutka BJ and Bitton G (eds), CRC Press: Boca Raton, FL; 43-77.
29. Galgiani JN, Reiser J, Brass C, Espinel-Ingroff A, Gordon MA, Kerkering TM. 1987. Comparison of relative susceptibilities of Candida species to three antifungal agents as determined by unstandardized methods. Antimicrob Agents Chemother 31: 1343-1347.
30. Gehrt A, Peter J, Pizzo PA, Walsh TJ. 1995. Effect of increasing inoculum sizes of pathogenic filamentous fungi on MIC's of antifungal agents by broth microdilution method. J Clin Microbiol 33: 1302-1307.
31. Hansen MB, Nielsen SE, Berg K. 1989. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J Immunol Meth 119: 203-210.
32. Heaney SP, Knight SC. 1994. ICIA5504: A novel broad-spectrum systemic fungicide for use on fruit, nut and horticultural crops. Proceedings of Brighton Crop Protection Conference Pests and Diseases 2: 509-516.
33. Hector RF, Braun PC. 1986. A 96-well epifluorescence assay for rapid assessment of compounds inhibitory to Candida spp. J Clin Microbiol 24: 620-624.
34. Hedin PA, Collum DH, Langhans VE, Graves CH. 1980. Distribution of juglone and related compounds in pecan and their effect on Fusicladium effusum. J Agric Food Chem 28: 340-342.
35. Hilber UW, Schüepp H. 1992. Accurate and rapid measurement of lengths of fungal germ tubes by image analysis. Can J Plant Pathol 14: 185-186.
36. Homans AL, Fuchs A. 1970. Direct bioautography on thin-layer chromatograms for detecting fungitoxic substances. J Chromatogr 51: 325-327.
37. Howcroft D, Hector T, Rowell F. 1987. Quantitative Bioassay. Wiley: New York.
38. Ikekawa T, Wang EL, Hamada M, Takeuchi T, Umezawa H. 1967. Isolation and identification of the antifungal active substance in walnuts. Chem Pharm Bull 15: 242-245.
39. Jahn B, Martin E, Stueben A, Bhakdi S. 1995. Susseptibility testing of Candida albicans and Aspergillus species by a simple microtitre menadione-augmented 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazolium bromide assay. J Clin Microbiol 33: 661-667.
40. Janssen M, Scheffer JC, Svendsen AB. 1987. Antimicrobial activity of essential oils: a 1976-1986. literature review. Planta Med 53: 395-398.
41. Kato T. 1986. Methods for evaluating activities of disease control on plants in a model system - factors affecting activities. In In Vitro and In Vivo Evaluation of Antifungal Agents. Iwata K and Vanden Bossche H (eds), Elsevier: Amsterdam; 197-206.
42. Kemp MS. 1978. Falcarindiol: An antifungal polyacetylene from Aegopodium podagraria. Phytochemistry 17: 1002.
43. Kern JR, Cardellina JH. 1982. Native American medicinal plants; falcarindiol and 3-methylfalcarindiol from Osmorhiza occidentalis. J Nat Prod 45: 774-776.
44. Knight SCA, Anthony VM, Brady AM, Greenland AJ, Heaney SP, Murray DC, Powell KA, Schulz MA, Spinks CA, Worthington PA, Youle D. 1997. Rationale and perspectives on the development of fungicides. A Rev Phytopathol 35: 349-372.
45. Kobayashi H, Namikoshi M, Yoshimoto T, Yokochi T. 1996. A screening method for antimitotic and antifungal substances using conidia of Pyricularia oryzae, modification and application of tropical marine fungi. J Antibiot 49: 873-879.
46. Krajci WM, Lynch DL. 1977. The inhibition of various microorganisms by crude walnut hull extracts and juglone. Microbios Lett 4: 175-181.
47. Major JS. 1995. Current screening practices in the pharmaceutical industry. Proceedings of Brighton Crop Protection Conference on Weeds, 1: 89-96.
48. Mayfield CI. 1993. Microbial systems. In Handbook of Ecotoxicology, Calow P (ed.), vol. 1, Blackwell Scientific: Oxford; 9-27.
49. Mischke S. 1997. A quantitative bioassay for extracellular metabolites that antagonise growth of filamentous fungi, and its use with biocontrol fungi. Mycopathologia 137: 45-52.
50. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Meth 65: 55-63.
51. Muir AD, Cole ALJ, Walker JRL. 1982. Antibiotic compounds from New Zealand plants; falcarindiol, an anti-dermatophyte agent from Schefflera digitata. Planta Med 44: 129-133.
52. National Committee for Clinical Laboratory Standards 1997. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard M27-A. National Committee for Clinical Laboratory Standards: Villanova.
53. Nyholm N, Sørensen PS, Kusk O, Christensen ER. 1992. Statistical treatment of data from microbial toxicity tests. Environ Toxicol Chem 11: 157-167.
54. Oerke EC, Dehne HW, Schönbeck F, Weber A. 1994. Crop Protection and Crop Production. Elsevier: Amsterdam.
55. Oh KB, Chen YS, Matsuoka H, Yamamoto A, Kurata H. 1996. Morphological recognition of fungal spore germination by a computer-aided image analysis and its application to antifungal activity evaluation. J Biotechnol 45: 71-79.
56. Pagé B, Pagé M, Noel C. 1993. A new fluorometric assay for cytotoxic measurements in vitro. Int J Oncol 3: 473-476.
57. Paxton JD. 1991. Assays for antifungal activity. In Methods in Plant Biochemistry, Vol. 6 Assays for Bioactivity. Hostettmann K (ed.), Academic Press: London; 33-46.
58. Paxton JD, Wilson EE. 1965. Anatomical and physiological aspects of branch wilt disease of Persian walnut. Phytopathology 55: 21-26.
59. Pelloux-Prayer AL, Priem B, Joseleau JP. 1998. Kinetic evaluation of conidial germination of Botrytis cinerea by a spectrofluorometric method. Mycol Res 102: 320-322.
60. Pfaller MA, Messer SA, Coffmann S. 1995. Comparison of visual and spectrophotometric methods of MIC endpoint determinations by using broth microdilution methods to test five antifungal agents, including the new triazole D0870. J Clin Microbiol 33: 1094-1097.
61. Pfaller MA, Rex JH, Rinaldi MG. 1997. Antifungal susceptibility testing: technical advances and potential clinical applications. Clin Infect Dis 24: 776-784.
62. Pujol I, Guarro J, Llop C, Soler L, Fernandez-Ballart J. 1996. Comparison study of broth macrodilution and microdilution antifungal susceptibility tests for the filamentous fungi. Antimicrob Agents Chemother 40: 2106-2110.
63. Pujol I, Guarro J, Gene J, Sala J. 1997a. In-vitro antifungal susceptibility of clinical and environmental Fusarium spp. strains. J Antimicrob Chemother 39: 163-167.
64. Pujol I, Guarro J, Sala J, Riba MD. 1997b. Effects of incubation temperature, inoculum size, and time of reading on broth microdilution susceptibility test results for amphotericin B against Fusarium. Antimicrobl Agents Chemother 41: 808-811.
65. Rahalison L, Hamburger M, Hostettmann K, Monod M, Frenk E. 1991. A bioautographic agar overlay method for the detection of antifungal compounds from higher plants. Phytochem Anal 2: 199-203.
66. Rahalison L, Hamburger M, Monod M, Frenk E, Hostettmann K. 1994. Antifungal tests in photochemical investigations: comparison of bioautographic methods using phytopathogenic and human pathogenic fungi. Planta Med 60: 41-44.
67. Rex JH, Pfaller MA, Rinaldi MG, Polak A, Galgiani JN. 1993. Antifungal susceptibility testing. Clin Microbiol Rev 6: 367-381.
68. Rex JH, Pfaller MA, Galgiani JN, Bartlett MS, Espinel-Ingroff A, Ghannoum MA, Lancaster M, Odds FC, Rinaldi MG, Walsh TG, Barry AL. 1997. Development of interpretative breakpoints for antifungal susceptibility testing: conceptual framework and analysis of in vitro-in vivo correlation data forfluconazole, itraconazole, and candida infections. Clin Infect Dis 24: 235-247.
69. Rios JL, Recio MC, Villar A. 1988. Screening methods for natural products with antimicrobial activity: a review of the literature. J Ethnopharmac 23: 127-149.
70. Roberts M, Boyce CBC. 1972. Principles of biological assay. In Methods in Microbiology, Vol. 7A Norris JR, Ribbons DW (eds), Academic Press: New York; 153-190.
71. Rodríguez-Tudela JL, Berenguer J, Martínez-Suárez JV, Sanchez R. 1996. Comparison of a spectrophotometric microdilution method with RPMI-2% glucose with the National Committee for Clinical Laboratory Standards Reference Macrodilution Method M27-P for in vitro susceptibility testing of amphotericin B, flucytosine, and fluconazole against Canadida albicans. Antimicrob Agents Chemother 40: 1998-2003.
72. Shephard MC. 1987. Screening for fungicides. A Rev Phytopathol 25: 189-206.
73. Singleton LL, Mihail JD, Rush CM. 1992. Methods for Research on Soilborne Phytopathogenic Fungi. APS Press: St Paul, MN.
74. Stratton CW. 1993. Bactericidal testing. Infect Dis Clin N Am 7: 445-449.
75. Trancassini M, Ghezzi MC, Cipriani P, Mancini C, Brenciaglia MI. 1986. Susceptibility of Candida species strains to five antifungal agents: comparison between agar dilution and disk diffusion tests. Chemioterapia 5: 14-17.
76. Villegas M, Vargas D, Msonthi JD, Marston A, Hostettmann K. 1987. Isolation of the antifungal compounds falcarindiol and sarisan from Heteromorpha trifoliata. Planta Med 54: 36-37.
77. Weidenbörner M, Hindorf H, Chandra Jha H, Tsotsonos P, Egge H. 1989. Antifungal activity of isoflavonoids against storage fungi of the genus Aspergillus. Phytochemistry 28: 3317-3319
78. Wilson CL, Solar JM, Elghaouth A, Wisniewski ME. 1997. Rapid evaluation of plant extracts and essential oils for antifungal activity against Botrytis cinerea. Plant Dis 81: 204-210.
79. World Health Organisation 1977. Report of the WHO Expert Committee on Antibiotics. Inform no. 26. Technical Report series no. 610. WHO: Geneva.